0% found this document useful (0 votes)
47 views28 pages

The Physiology of Female Sexual Function

The document summarizes a review on the physiology of female sexual function and pathophysiology of female sexual dysfunction. It covers six sections on topics such as female genital anatomy, physiology of arousal and orgasm, psychological aspects, and laboratory assessments. The review aims to provide recommendations based on levels of evidence where relevant, despite limitations of applying this to basic scientific research.

Uploaded by

костя
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
0% found this document useful (0 votes)
47 views28 pages

The Physiology of Female Sexual Function

The document summarizes a review on the physiology of female sexual function and pathophysiology of female sexual dysfunction. It covers six sections on topics such as female genital anatomy, physiology of arousal and orgasm, psychological aspects, and laboratory assessments. The review aims to provide recommendations based on levels of evidence where relevant, despite limitations of applying this to basic scientific research.

Uploaded by

костя
Copyright
© © All Rights Reserved
We take content rights seriously. If you suspect this is your content, claim it here.
Available Formats
Download as PDF, TXT or read online on Scribd
You are on page 1/ 28

See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/301624706

The physiology of female sexual function and the pathophysiology of female


sexual dysfunction

Article  in  Journal of Sexual Medicine · April 2016

CITATIONS READS

12 1,188

6 authors, including:

Roy Jerome Levin Stephanie Both Phd


The University of Sheffield Leiden University Medical Centre
243 PUBLICATIONS   4,349 CITATIONS    71 PUBLICATIONS   1,270 CITATIONS   

SEE PROFILE SEE PROFILE

Janniko R Georgiadis Tuuli Kukkonen


University of Groningen University of Guelph
45 PUBLICATIONS   1,231 CITATIONS    20 PUBLICATIONS   323 CITATIONS   

SEE PROFILE SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Book chapters from 'The Living Barrier' View project

All content following this page was uploaded by Stephanie Both Phd on 09 May 2016.

The user has requested enhancement of the downloaded file.


INTERNATIONAL CONSULTATION ON SEXUAL MEDICINE REPORTS

The Physiology of Female Sexual Function and the Pathophysiology


of Female Sexual Dysfunction (Committee 13A)
Roy J. Levin, PhD,1,* Stephanie Both, PhD,2 Janniko Georgiadis, PhD,3 Tuuli Kukkonen, PhD,4
Kwangsung Park, MD, PhD,5 and Claire C. Yang, MD6

ABSTRACT

Introduction: The article consists of six sections written by separate authors that review female genital anatomy,
the physiology of female sexual function, and the pathophysiology of female sexual dysfunction but excluding
hormonal aspects.
Aim: To review the physiology of female sexual function and the pathophysiology of female sexual dysfunction
especially since 2010 and to make specific recommendations according to the Oxford Centre for evidence based
medicine (2009) “levels of evidence” wherever relevant.
Conclusion: Recommendations were made for particular studies to be undertaken especially in controversial
aspects in all six sections of the reviewed topics. Despite numerous laboratory assessments of female sexual
function, genital assessments alone appear insufficient to characterise fully the complete sexual response.
J Sex Med 2016;13:733e759. Copyright  2016, International Society for Sexual Medicine. Published by Elsevier
Inc. All rights reserved.
Key Words: Genital Anatomy; Physiology of Arousal and Orgasm; Brain Imaging; Psychological Function
and Dysfunction; Laboratory Assessments of Sexual Function and Dysfunction; Pathophysiology of Sexual
Function

INTRODUCTION that the Oxford level of evidence assessment system does not
The title of the review for Committee 13A was “The apply to basic scientific research publications; thus, its absence
Anatomy and Physiology of Female Sexual Function and the on various references is intentional and not an oversight. A
Pathophysiology of Female Sexual Dysfunction.” With such a much longer and more detailed report of each section is to be
wide-ranging remit that included anatomy, physiology, clin- found in the Proceedings of the Fourth International
ical functional assessments, brain imaging, non-neurologic Consultation of Sexual Medicine, Committee 13A Chapter:
pathology, and psychosexual function and dysfunction, a The Anatomy and Physiology of Female Sexual Function and
composite review containing six separate sections, each written the Pathophysiology of Female Sexual Dysfunction, published
by a committee member, was appropriate. It should be noted online.1

Received October 26, 2015. Accepted February 24, 2016. SECTION 1. ANATOMY OF THE FEMALE SEX
1
Reader in Physiology (Retired), Department of Biomedical Science, ORGANS
University of Sheffield, Sheffield, UK: Section 2;
2
Department of Psychosomatic Gynecology and Sexology, Leiden University Recommendation
Medical Center, Leiden, The Netherlands: Section 3;
3
1. Despite recent claims, characterization of the anatomy and
Department of Neuroscience, University Medical Center, Groningen,
University of Groningen, The Netherlands: Section 4;
function of the putative G-spot remains controversial and
4 requires more robust and stringent examination.
College of Social and Applied Human Science, University of Guelph, Guelph,
ON, Canada: Section 6;
5
Department of Urology, Chonnan National University Medical School,
Gwangju, Korea: Section 5;
Introduction
6
This section is a brief presentation of the anatomy and his-
Department of Urology, University of Washington, Seattle, WA, USA:
Section 1; tology of the female sex organs from the perspective of under-
*Committee 13A chair.
standing the physiology of the female genital response to sexual
arousal. The external genital structures are emphasized, because
Copyright ª 2016, International Society for Sexual Medicine. Published by
Elsevier Inc. All rights reserved. those are the ones about which most physiologic research has
http://dx.doi.org/10.1016/j.jsxm.2016.02.172 been conducted.
J Sex Med 2016;13:733e759 733
734 Levin et al

Figure 1. Female external genitalia (premenopausal woman).


Image from: http://commons.wikimedia.org/wiki/File:Womans_
vulva.jpg. Under GNU Free Documentation License.

Anatomy
The external genitalia, referred to collectively as the vulva,
Figure 2. Genital structures below the surface of the skin. Clitoral
consist of the mons pubis, clitoris and bulbs, labia majora, and complex (1 ¼ body, 2 ¼ glans, 3 ¼ crura) in an inverted wishbone
labia minora (Figure 1). The mons pubis is an area of fatty tissue formation with the body in midline and crura extending posteriorly.
overlying the pubic symphysis and covered by pubic hair. The Bulbar tissue (6) is draped over the urethra (4) and vaginal introitus
body of the clitoris extends into the mons for several centimeters (5). The bony pelvis (7) is shown.
before bifurcating into the crura (singular ¼ crus), which run
bilaterally under the inferior pubic rami. Between the crura lie two histologically distinct types of vascular tissue. Trabeculated
the clitoral bulbs, draped over the urethra, with the bulk of the erectile tissue is found in the clitoris and the bulbs. The erectile
bulbar tissue lateral to the vaginal walls (Figure 2). Usually, only tissue of the clitoris and bulbs is very similar to that of the male
the glans clitoris is visible externally, approximately 1 cm anterior corpora cavernosa and corpus spongiosum. The trabecular nature
to the urethral meatus, and the glans is often covered by the of the erectile tissue allows for engorgement with blood and
clitoral hood (or prepuce; Figure 1). The labia majora are fatty, volume expansion during sexual arousal. In contrast to the
elongated, hair-bearing folds of tissue forming the lateral clitoral and bulbar erectile tissue, the labia minora and glans
boundaries of the vulva. The medial aspects of the labia majora clitoris are composed of non-erectile vascular tissue, in which the
fuse with the labia minora, which are thin folds of skin outlining blood vessels are dispersed within a fibrous matrix, with only a
the introitus, or entry to the vagina. The anterior aspects of the minimal amount of smooth muscle. Non-erectile, sexually
labia minora split and fuse with the frenulum of the glans clitoris responsive vascular tissue also is found surrounding the urethral
on its ventral aspect and unite over the glans as the hood. The lumen and within the walls of the vagina. These tissues also
posterior aspects of the labia minora fuse in the midline at the respond during sexual arousal with increases in blood flow, but
lower aspect of the introitus. the structure of the tissues does not accommodate vascular
Gross anatomic and histologic study of the clitoris, clitoral engorgement as in the erectile tissues.
bulbs, labia minora, and urethra show them to contain special- The urethra is a midline structure and sits toward the apex of
ized vascular tissues that are sexually responsive2 and consist of the introitus. Although not classically described as a sex organ, it

J Sex Med 2016;13:733e759


Female Sexual Function and Dysfunction 735

does demonstrate changes in blood flow during arousal. The distal section on anatomy (Section 1). Because space is limited, only
urethra is flanked by the erectile tissue of the clitoral bulbs. There controversial aspects of arousal and orgasm are highlighted. A
are paraurethral glands along the length of the lumen. Some of fuller account of the physiology of female sexual arousal is
these glands stain positively for prostate-specific antigen,3 leading detailed in online.1
some to state that this area is homologous to the male prostate. Human female sexual arousal encompasses a mental state
However, the glands are isolated and do not seem to have any (emotional and cognitive) and a physical state induced by various
recognizable endocrine or exocrine function in women. A region stimuli that usually produce feelings of pleasure and initiate a
of the anterior wall of the vagina overlying the midurethra has desire to continue the activity often to orgasm.1 Changes in the
been identified as the Grafenberg spot (or G-spot), an area that, in physical state involve increases in heart rate, blood pressure,
some women, is particularly sensitive to tactile stimulation. Gra- respiration, genital blood flow and vasocongestion, vaginal
fenberg’s original article identified the erogenous area as arising lubrication, and nipple erection.7 However, there are conditions
from the urethra.4 Controversy still exists over the possible in which mental arousal can occur without genital physical
anatomic structure and site of the G-spot5,6 (see also Section 2). changes8 and physical changes can occur without mental
The vagina is considered an internal genital structure. It is a changes.9 Any or all of the senses (vision, hearing, taste, smell,
potential space consisting of a flattened fibromuscular tube with and touch) and fantasy can be involved in creating the
anterior and posterior walls collapsed onto each other, extending arousal.10,11 However, touch is of great importance, because
from the introitus to the fornices that surround the cervix. The most intrapersonal sexual scenarios involve this sense. Many sites
vaginal wall consists of three layers: (i) the stratified squamous on the female body can evoke arousal when caressed—for
non-keratinized epithelium and an underlying lamina propria of example, the lips, nape and back of neck, ears, underarms, breasts
connective tissue; (ii) the muscular layer, composed of smooth and nipples,12,13 pubic hairline, inside of thighs, buttocks, anus,
muscle fibers disposed longitudinally and circularly; and (iii) the and perineum—but the most sensitive structures lie in and
adventitia, a dense connective tissue that blends with the sur- around the genitalia.14 The sites can be stimulated by different
rounding fascia. The lamina propria and connective tissue layers means (vibrators, dildoes, digitally, and lingually) and by PVI.
contain a rich supply of vascular channels. During sexual stim- One major difference of PVI from the other stimulations is that
ulation, the marked increase in fluid production in the vagina is it is uniquely a multisite stimulus capable of activating some
caused by transudation across the vaginal wall, providing the of—or all—the sites listed in Table 1.4,7,10,15e39 Because of this,
lubrication needed for non-painful and non-traumatic vaginal it would be expected that the neural inputs from PVI-stimulated
intercourse. There are no glands in the vaginal wall. multiple sites would facilitate rapidly induced sexual arousal
leading to orgasm more quickly than that from the stimulation of
a single site, such as the clitoral shaft and glans. In fact, when
SECTION 2. THE PHYSIOLOGY OF FEMALE
questioned, women find that the latter stimulation needs less
SEXUAL AROUSAL AND ORGASM
energy, creates arousal faster, and yields more intense or-
Recommendations gasms,7,15 although these are not always the most satisfying.7
1. No published data show that efforts to facilitate or augment
G-spot function by medical or surgical interventions are
Vaginal Anterior Wall and G-Spot
The so-called G-spot has been the focus of much controversy
effective or that any dysfunctional condition is specific to the
and dissent. First described by Grafenberg4 in an obscure
lack of its functioning.
journal in the 1950s, it was rediscovered and especially pro-
2. The vestibular bulbs and the clitoral crura become vaso-
moted by Ladas et al38 in an non-refereed, popular book. Since
congested on sexual arousal, but evidence for their erotic
then, numerous articles have been published, some describing
functionality has not been proved.
anecdotal reports and even a few claiming to have identified the
3. No robust method of quantifying vaginal lubrication as a
structure in the anterior wall of the vagina from the dissections
clinical index of sexual arousal has been developed.
of cadavers,37 by ultrasound and histology,35,36 and in cadaver
4. Perception problems involved in women self-reporting their
dissections and ultrasound in live subjects.40 Unfortunately,
specific site for the induction of orgasm during penile-vaginal
none of these have confirmed that the subjects studied specif-
intercourse (PVI) include clouding or loss of conscious focus
ically had G-spot orgasms. Moreover, the dissection studies
during sexual arousal (obnubilation), misinterpretation of the
have identified different sites and structures as the organ in
site by inadequate specific signals (sexual pareidolia), igno-
question. Some investigators believe that the structure is
rance of erotic genital sites (lack of sexual and anatomic lit-
functionally difficult to identify as in and attached to the
eracy), and questionnaire bias.
vaginal anterior wall or in excitatory structures such as the
urethra,25 the internal crus of the clitoris (Table 1), or the
Introduction clitoris activated by its ligament attachments.41 Little stringency
This section covers the physiology of sexual arousal and has been applied in the various studies, and unfortunately some
orgasm and should be read in conjunction with the previous brief farfetched and illusory functions have been suggested.42 No

J Sex Med 2016;13:733e759


736 Levin et al

Table 1. Female genital-pelvic erotogenic and putative erotogenic sites*


Site Studies (PRO and CON) Controversy Physiology
7
Clitoris (hood, Masters and Johnson, Universally accepted Dorsal nerve of clitoris
shaft, glans) Puppo,16 Shafik et al17
Clitoral crus Buisson and Jannini,18 Foldes Varied opinions for and against Dorsal nerve of clitoris (somatic)
(internal)? and Buisson,19 Buisson et al20 cavernous nerve (autonomic)
Clitoral bulbs Puppo16 Suggested but no published evidence Visceral afferents from Pelvic
(internal)? plexus (autonomic)
Labia (minora) Masters and Johnson,7 Levin,21 Universally accepted Perineal nerve (somatic)
Ginger et al,22 Martin-Alguacil
et al23
Periurethral glans Sevely,24 Levin25,26 Erotogenic but nomenclature disputed Perineal nerve (somatic)
Halban fascia Minh et al,27 Battaglia et al28 Part of vaginal anterior wall erotic Perineal nerve (somatic)
(vaginal-bladder complex
septum)
Anus-perineum Komisaruk and Whipple,10 Universally accepted Perineal nerve
Masters and Johnson,7
Kinsey et al29
Urethral meatus Eichel et al30 Generally ignored Pudendal nerve (somatic)
Cervix? Komisaruk et al,31 Brody,32 Controversial due to cervico-uterine Visceral afferents from lower
Levin15,33,34 elevation (vaginal tenting) thoracic segments/hypogastric
preventing penile contact plexus vagus?
G-spot? Grafenberg,4 Thabet,35,36 Controversial site despite claims of No published studies?
Ostrezenski et al,37 anatomic identification
Ladas et al,38 Levin33,39
Urethra Levin25 Serotonin released by penile thrusting Pudendal nerve and nerves from
sensitizing nerves? vesical plexus
*The question marks indicate possible uncertainty in sexual function. The references listed support (PRO) or call into question (CON) the function of the
site. See text for details.

published data have shown that efforts to facilitate or augment The Cervix
G-spot function by medical or surgical interventions are During sexual arousal, the cervical-utero complex is elevated up
effective43e45 or that any dysfunctional condition is specific to into the false pelvis away from the thrusting penile axis and the
the lack of its function. ejaculated semen.7,33 The sensory innervation of the cervix is
It is often assumed that the facilitation of sexual arousal by limited; some surgical treatments can be applied without
stimulating the anterior vaginal wall is due to the action of the anesthesia.33 Evidence from women with spinal cord injury (SCI)
G-spot per se. However, as Hoch46 and Levin39 pointed out, the suggests a possible vagal innervation,31 but its relevance in able
anterior wall contains several structures that can cause arousal, women during coitus is not fully established. Whether the cervix is
namely the urethra,25 the Halban fascia in the vaginal-urethral involved in creating sexual arousal during PVI remains conten-
septum,27 the internal clitoral structures (Table 1), and the lig- tious. Although some women claim to experience arousal from
aments attached to the clitoris.41 Levin39 suggested that the sites cervical buffeting, the reports are not robust and do not exclude
should be named “the anterior wall erogenous complex,” and a conditions such as uterine prolapse, damaged pelvic musculature
much later review47 called it the “clitorourethral complex”—a from childbirth, especially short vaginas or long cervices, and
designation that unfortunately does not include the possible inadequate arousal leading to poor vaginal tenting.49
function of the Halban fascia. Because of this aggregation of
erotic sites, it is impossible to ascribe the sexual arousal from the Vestibular Bulbs and Clitoral Crura
These internal structures are described in Section 1. They
stimulation of the anterior vaginal wall to any one specific
become vaso-congested on arousal, but whether they are func-
structure. According to Burri et al,48 if G-spot activity is the
tionally erotic from friction or pressure remains undecided
physiologic activity of an anatomic structure, then it should show
because no empirical studies have been published (Table 1).
indications of heritability. However, in a study of 1,804 twins,
the researchers reported that despite the claim by 56% to have a
G-spot, there was no detectable genetic influence. This lack of Vaginal Lubrication
heritability was controversially suggested to occur because there The non-aroused vagina is a potential space and its epithelial
was no physiologic or experimental basis for it. surfaces are covered by a film of fluid that prevents the opposing

J Sex Med 2016;13:733e759


Female Sexual Function and Dysfunction 737

surfaces from creating adhesions. This “just moist” condition is in other aspects remain obvious. Unlike men, women lack a post-
insufficient to allow painless penile penetration and thrusting. orgasmic refractory period. After orgasm, women’s subjective
Successful sexual stimulation leads to an increase in vaginal blood sexual arousal and desire can be maintained,66 and they can have
flow mediated by arterial dilatation and a decrease in vasomotion serial, multiple orgasms.7 The subjective pleasure of orgasm does
with its opening of all the capillaries.50 Increased capillary surface not appear to be related to its duration.67
area and vasocongestion enhance the production of a plasma
transudate (neurogenic) that percolates through the vaginal
Summary
epithelium, saturating its limited reabsorptive ion-transfer ca-
Although anatomic descriptions of different structures in the
pacity51 and greatly increasing the surface lubrication. This fa-
human female genitalia indicate possible functionality in sexual
cilitates painless penile penetration and thrusting. In the Western
arousal and orgasm (Table 1), definitive empirical physiologic
world, such lubrication is regarded as an exemplary index of
studies and evidence are wanting for some of these structures.
successful female sexual arousal, but it can occur even in forced
or non-consensual sex.52 In certain states in Africa, men prefer a
dry, tight vagina for coitus, influencing women to use methods of SECTION 3. LABORATORY ASSESSMENT OF
drying up their fluids.53 Vaginal lubrication is decreased in FEMALE SEXUAL FUNCTION AND DYSFUNCTION
several conditions (menopause, diabetes, and atrophic vaginitis).
Although quantification of the vaginal lubrication as an index of Recommendations
successful arousal has been attempted, no published study has 1. Studies assessing genital response in somatically healthy
been successful or robust enough to be useful for diagnosis in the women reporting sexual problems do not indicate an impaired
clinical context.54 A robust, quantitative method of assessing genital responsiveness (level 3 evidence).
vaginal lubrication is sorely needed. 2. Somatic diseases that involve damage to blood vessels or
nerves, such as diabetes, SCI, and pelvic surgery, are associ-
ated with impaired genital response compared with healthy
Female Emission
controls (level 4 evidence). However, this is not necessarily
Women can have an emission (often described as an ejacula-
associated with the experience of sexual problems.
tion) of a small volume of fluid from their urethra at high sexual
3. The genital and sensory components of the female sexual
arousal or at orgasm.55 This is likely to be the discharge of se-
response are loosely coupled; in general, the correlation be-
cretions from the paraurethral glands lining the urethra (female
tween genital response measured with vaginal photo-
prostate), but the much larger volumes released in spurts are
plethysmography and sensations of sexual arousal is low (level
almost certainly urine due to coital incontinence. According to
3 evidence). Therefore, genital assessment alone is not suffi-
Pastor,56 the incidence range of small volume emission is 10% to
cient to characterize female sexual responsiveness.
54% and that of coital incontinence is 0.2% to 66%.
4. Female genital response appears to be a reflexive reaction to
sexually relevant stimuli whether or not these stimuli are
Orgasm preferred by the individual (level 3 evidence).
No other topic of women’s sexual arousal has created con-
troversy comparable to that over the female orgasm. Many as-
pects of the orgasm are still highly contentious and a consensus is Introduction
not available. The controversial issues include (i) the anatomic After the discussion of the bases of the physiology of female sexual
identification of its induction site(s) during PVI by women from arousal, in this section, laboratory assessment of female sexual
self-reports and questionnaires15,49,57,58 because of clouding or response is described. Methods to test genital sensory function,
loss of conscious focusing (obnubilation) or misinterpreting the pelvic floor muscle function, and genital and subjective sexual
induction site because of inadequate specific signals and igno- arousal and studies using these methods in women with sexual
rance of genital erotic anatomy (poor anatomic literacy); (ii) dysfunction are discussed. Opportunities and limitations of these
whether orgasmic induction comes from PVI alone or from methods in the assessment of female sexual function are described.
clitoral stimulation, specifically relating to claims that the former
creates better psychological, social, and physiologic aspects of the Genital Sensory Function
health of women15,21,49,55,58,59; (iii) claimed orgasm involvement Disturbed genital sensitivity can play a role in female sexual
in enhancing sperm transport and thus “reproductive fitness” by dysfunction (FSD). Hyposensitivity might be a cause of low sexual
its release of systemic oxytocin33; (iv) its relevance to female and arousal and orgasmic problems, whereas hypersensitivity might be
male sexual satisfaction60e62; and (v) the complete lack of involved in sexual pain disorders. Gruenwald et al68 developed a
consensus on the brain’s pattern of activity and inhibition during test for genital sensitivity and observed vaginal and clitoral hypo-
arousal to orgasm63,64 (see Orgasm in Section 4). sensitivity in women with multiple sclerosis and an association
Although there is a strong indication that the mental (erotic) with orgasmic problems. Using comparable methods, studies
changes are similarly perceived by men and women,65 differences found evidence that multiple sclerosis, diabetes, and vaginal

J Sex Med 2016;13:733e759


738 Levin et al

surgery affect genital sensitivity (level 4 evidence). However, in with women without sexual problems (Table 3). This indicates
most studies, genital sensitivity was not associated with sexual that physically healthy women with sexual problems can equally
complaints.69e71 In the context of sexual pain disorders, calibrated achieve genital sexual response as women without such problems
spring-loaded devices have been developed to correlate pain with (level 3 evidence). However, they do experience less subjective
precise mechanical forces on the vulvar tissue. Women with pro- sexual arousal or positive affect. Therefore, in these women,
voked vestibulodynia have shown significantly lower vestibular sexual arousal problems seem more related to inadequate erotic
pressure-pain thresholds and increased numbers of vestibular stimulation in everyday life or to negative evaluations of the
nociceptors compared with control women (level 3 evidence).72 sexual stimulus or the context than to disturbances in genital
responsiveness.99
Pelvic Floor Function The failure to find differences in genital response between
Studies monitoring pelvic floor musculature (PFM) activity by women with and without sexual problems has raised questions
electromyography have shown some evidence for deviant PFM about the sensitivity of VPA to detect impaired genital respon-
tone or strength in women with sexual pain disorders (level 4 siveness. However, studies of women with medical disorders that
evidence), but the results are mixed. Increased resting electromy- are likely to impair sexual response owing to disease-related
ography and stronger contractile responses to vestibular pressure neuronal or vascular damage have shown lower VPA in
have been observed,73,74 but some studies have reported lower response to sexual stimulation (level 4 evidence; Table 3). Also,
muscle strength.75,76 Studies in women with and without sexual studies comparing pre- and postmenopausal women have shown
pain disorder have shown increased PFM activity when in a fear lower basal postmenopausal VPA.69,100,101 These observations
state.77,78 This suggests involuntary defensive PFM contraction, prove the sensitivity of VPA measurement to detect differences in
which is in line with research showing indirect PFM innervation by basal vaginal blood flow and in responsiveness to sexual stimu-
the limbic system and high reactivity to emotional states.79 lation (level 4 evidence). However, lower VPA in women with
medical disorders is not necessarily related to weaker sensations
of sexual arousal or to sexual complaints.69,101e104
Genital Sexual Response
In the development of laboratory assessment of genital sexual Also, methods that assess vulvar blood flow have been used to
response, the focus has been on vaginal blood flow. More compare women with and without sexual dysfunction. Com-
recently, techniques to measure vulvar changes have been bined clitoral and vaginal photoplethysmography in women with
developed. Sexual response in the laboratory can differ from real- sexual desire disorder and/or arousal disorder showed similar
world experience. However, substantial levels of sexual arousal increases in clitoral and vaginal blood flow as the control
and even orgasm can be elicited in a laboratory setting using group.98,105 A study using thermal imaging in women with
sexual stimuli such as erotic pictures, erotic film, or genital sexual pain disorder showed similar increases in vulvar temper-
vibration. Important methodologic issues in the assessment of ature during erotic film viewing compared with controls.106 Laser
genital response include specificity of the measurements— Doppler imaging in women with provoked vestibulodynia and
whether the observed genital changes are specific for sexual controls showed a significant difference between groups in vulvar
arousal or appear during other emotional states, whether the blood flow in response to erotic film viewing; however, these
assessments can be experienced as uncomfortable, which can results are difficult to interpret because the difference was
hamper sexual response in the laboratory, and the ability to observed only in women with a high baseline blood flow.107
measure responses using an absolute scale. Measuring responses Other studies using Doppler imaging showed decreased clitoral
on an ordinal scale, rather than an interval or ratio scale, impedes blood flow in women with systemic sclerosis—a disease charac-
the use of a measurement as an individual diagnostic method of terized by endothelial dysfunction and fibrosis of the skin and
genital responsiveness. Table 2 presents an overview of various internal organs—and in women with diabetes.108e110
methods and their (dis)advantages.50,67,80e98 Unfortunately, to Taken together, several techniques have been used to examine
date, none of the available methods are suitable for diagnosis. differences in genital response between women with and without
Vaginal photoplethysmography, the most widely used method to sexual problems. In general, the results do not point to an
assess changes in vaginal blood flow, lacks an absolute scale, impaired genital response in somatically healthy women report-
which hampers the establishment of diagnostic criteria. Owing to ing sexual problems. However, in women with somatic diseases
a lack of data regarding normal values, no method allows for involving pathophysiology that is likely to affect sexual function,
evaluation on an individual level about whether genital responses such as damage to blood vessels or nerves, impaired genital
are abnormal or disturbed. response has been observed.69,99,101e104,111e121
Most studies comparing genital responses of women with and
without sexual dysfunction have used vaginal photo- Discordance Between Genital and Subjective Sexual
plethysmography that measures vaginal pulse amplitude (VPA). Responses
In most of these studies, women who met the criteria for sexual A robust finding in psychophysiologic research on female
dysfunction showed no difference in genital response compared sexual response is the low concordance between reported feelings

J Sex Med 2016;13:733e759


Table 2. Methods to assess female genital response
J Sex Med 2016;13:733e759

Female Sexual Function and Dysfunction


Technique Advantages Disadvantages
Methods for assessment of vaginal blood flow
Oxygen perfusion and heat Heated electrode (with or without a po2 Fixation prevents movement artifacts and Device has to be attached by the
dissipation in vaginal wall67,80,81 sensor) held by a suction cup onto the allows po2 measurements during orgasm; experimenter, which might be less
vaginal wall; the more blood in the vaginal blood flow calibrated in absolute terms comfortable for subjects;
wall, the greater the amount of oxygen (ml/100 g tissue/min) measurement of blood flow takes
diffusion and heat clearance from the 3e5 min
electrode
Vaginal photoplethysmograph50,82e85 Menstrual tampon-size probe with light Placed by the subject herself; depth and Signal can be disturbed by movement
source (infrared diode) and photo orientation of diode and photo transistor artifacts; lacks an absolute scale
transistor; diode illuminates vaginal tissue are standardized; VPA showed specificity
and photo transistor picks up light that is to sexual stimulation and sensitivity to
backscattered from the vaginal wall and distinct levels of intensity of erotic
the blood circulating within it; amount of stimulation
light backscattered is dependent on the
volume of blood within the vaginal wall; AC
signal assesses VPA, reflecting changes in
blood volume at each heartbeat; in
addition, recording of vasomotion seems
to enhance sensitivity of measurements
for changes in vaginal microcirculation
Methods for assessment of vulvar blood flow
Oxygen perfusion in minor labia86 Device consisting of heated oxygen electrode Fixation prevents movement artifacts, Device has to attached by experimenter,
attached by single-sided adhesive ring on enabling measurements during orgasm; which might be less comfortable for
minor labia; the more blood present, the calibrated in terms of absolute blood flow subjects
greater the amount of perfused oxygen
Labial photoplethysmograph87 Light source and photo transistor built in a Can be placed by the subject herself; showed Subjects reported more discomfort
plastic clip that is attached to labia majora specificity to sexual stimulation compared with vaginal probe
Thermistor clip88,89 Labial temperature is assessed using a Can be placed by the subject herself; less Requires control of temperature in
thermistor clip attached to labia minora; sensitive to movement artifacts; absolute laboratory room; variation in body
temperature is assumed to be related to unit of measurement temperature during menstrual phases
blood flow is a potential confounder
Thermal imaging90e92 Human skin emits electrochemical energy, Assessment of very small changes in Participant has to be undressed with her
including infrared radiation, which is temperature; absolute unit of legs spread apart; high costs; regions
registered with thermal imaging; genital measurement; showed specificity to of interest can be difficult to track
temperature is assumed to be related to erotic stimulation owing to movement of participant
blood flow
Doppler ultrasonography93,94 Pulse of ultrasound is sent into tissue using Morphologic, volumetric, and hemodynamic No discrimination between sexual
ultrasound transducer; sound echoes from changes can be assessed arousal and humor condition;
parts of the tissue and these echoes are assessment has to be performed by
recorded and displayed as an image ultrasound technician holding the
probe
(continued)

739
740 Levin et al

of sexual arousal and changes in genital vasocongestion.122

undressed with her legs spread apart;


Measurements have to take place in the
dark; high sensitivity for movement;
Correlations between genital and subjective sexual arousal in

room temperature needs to remain

High sensitivity to motion; high costs


women are generally non-significant or low, whereas correla-

No absolute unit of measurement


constant; participant has to be
tions in men are usually significantly positive. Based on these
observations, it has been stated that, in women, subjective
sexual experience is determined more strongly by contextual
factors than by their genital response.85 In contrast, others
have attributed the low correlations in women to the various
ways subjective arousal was assessed, how correlations were
Disadvantages

high costs

calculated, or to a measurement error of the vaginal


photoplethysmograph.90,123
To examine whether the lower concordance in women is
the result of methodologic issues, Chivers et al122 conducted a
internally or deep within the pelvis are visible
anatomic structures; genital organs that lie

meta-analysis including 132 studies in men and women. An


Provides high-resolution images of detailed
Showed specificity to erotic stimulation;

difference detected between separate

overall sex difference in concordance was found, with men


absolute unit of measurement; no

Can be placed by the woman herself

showing higher subjective-genital correlation than women.


sessions, indicating reliability of

Moderators associated with methodologic variation could not


account for this sex difference. However, most studies in the
meta-analysis measured female genital response by vaginal
photoplethysmography, and it has been argued that because
changes in vaginal blood flow might not be perceptible to
measurements

women, this might result in lower concordance. Changes in


genital temperature measured by, for example, thermography
Advantages

can yield stronger concordance.90 The meta-analysis and


more recent data support this hypothesis, and concordance
estimates obtained using thermography are higher.124 How-
ever, the number of studies using thermography is small and
changes when it interacts with an object in
on the principle that the frequency of light

silicon shield attached to the lower side of


of light are converted in an electric signal
Measures superficial skin blood flow; based

motion (eg, blood); changes in frequency

further research is needed to determine whether thermog-


Clitoral photoplethysmograph is built into a

raphy yields similar concordance estimates in women and


Detects changes in tissue engorgement,
which is reflected as increased signal

men.
that is processed to an image

Based on the low concordance of subjective-genital sexual


vaginal photoplethysmograph

arousal in women, it has been speculated that female genital


arousal is an automatic response.125,126 This hypothesis of
reflexive genital response is supported by the intriguing
observation that women respond genitally even when they are
exposed to non-preferred sexual stimuli. Heterosexual women
show similar genital response to homosexual and heterosexual
intensity
Technique

erotic stimuli, whereas men respond specifically to stimuli that


match their sexual orientation.125 It has been suggested that
the reflexive activation of vaginal vasocongestion and lubrica-
tion by sexual cues could serve a protective function by
decreasing discomfort and the possibility of injury during
vaginal penetration.125,126 Reports of women responding
Magnetic resonance imaging97

genitally during sexual assault52 and studies showing genital


Combined clitoral and vaginal
95,96

photoplethysmography98

responses to sexual threat stimuli9,78,83,127e129 suggest that, in


VPA ¼ vaginal pulse amplitude.
Laser Doppler imaging

women, genital responses do occur under conditions of sexual


threat.
Table 2. Continued

Taken together, these observations indicate that women’s


vaginal vasocongestion response is automatically initiated by
exposure to sexual stimuli, whether or not these stimuli are
preferred, and whether or not the processing of these stimuli
results in the experience of sexual arousal or positive
affect (level 3 evidence). Moreover, the low concordance of

J Sex Med 2016;13:733e759


Table 3. Studies using vaginal photoplethysmography measuring VPA in somatically healthy women with sexual dysfunction and in women with medical conditions
J Sex Med 2016;13:733e759

Female Sexual Function and Dysfunction


Study Participants Stimuli and conditions Results
Studies in somatically healthy women with sexual dysfunction
Heiman et al,111 2011 HSDD (n ¼ 46), controls (n ¼ 47) Sexual fantasy, erotic film VPA—no significant difference between groups
Subjective response—significantly lower sexual desire in HSDD but only in
women not using oral contraceptives
Brotto and Yule,112 2011 Asexual women (n ¼ 7), Erotic film VPA—no significant difference between groups
heterosexual (n ¼ 10),
bisexual (n ¼ 10),
homosexual (n ¼ 11) controls
Subjective response—significantly lower sensual feelings and positive affect
in asexual women
Meston et al,113 2010 Orgasm disorder (n ¼ 12), Erotic film VPA—no significant difference between women with sexual dysfunction and
sexual arousal disorder controls
(n ¼ 38), controls (n ¼ 12)
Subjective response—significantly lower sexual arousal in women with sexual
arousal disorder
Brauer et al,114 2009 Dyspareunia (n ¼ 50), controls Erotic film with pain vs Sexual VPA—no significant difference between groups
(n ¼ 25) pleasure attribution
instruction
Subjective response—higher negative affect in pain attribution condition and
trend for stronger negative affect in women with dyspareunia
Laan et al,99 2008 Sexual arousal disorder Erotic film VPA—no significant difference between groups
(n ¼ 29), controls (n ¼ 30)
Subjective response—significantly lower sexual arousal and positive affect and
significantly higher negative affect in women with sexual arousal disorder
Brauer et al,115 2007 Dyspareunia (n ¼ 48), controls Erotic film in pain vs no-pain VPA—significantly lower in pain condition, no significant difference between
(n ¼ 48) threat condition groups
Subjective response—lower positive affect and higher negative affect in pain
threat condition, significantly higher negative affect in dyspareunia group
Meston,116 2006 Sexual arousal disorder (n ¼ 16), Erotic film in self-focus vs no VPA—no significant differences between groups
controls (n ¼ 16) self-focus condition
Subjective response—significantly lower feelings of sexual arousal in women
with sexual arousal disorder
Brauer et al,117 2006 Dyspareunia (n ¼ 50), controls Erotic film with and without VPA—no significant difference between groups
(n ¼ 25) coitus scene
Subjective response—significantly lower positive affect and higher negative
affect in women with dyspareunia
Brotto et al,118 2004 Sexual arousal disorder (n ¼ 31), Erotic film VPA—no significant difference between groups
controls (n ¼ 30)
Subjective response—significantly lower genital sensations and positive
affect in women with sexual arousal disorder
(continued)

741
742
Table 3. Continued
Study Participants Stimuli and conditions Results
Meston and Gorzalka, 119
Sexual arousal (n ¼ 12), Erotic film in exercise vs no- VPA—no significant difference between groups in no-exercise condition; in
1996 orgasmic disorder (n ¼ 12), exercise condition exercise condition, women with orgasmic disorder had significantly lower
controls (n ¼ 12) VPA
Subjective response—no significant difference between groups
Studies in women with medical conditions
Both et al,69 2015 Diabetes mellitus (n ¼ 42), Erotic film, clitoral vibration VPA—no significant differences between women with diabetes and controls;
controls (n ¼ 46) significantly lower VPA in women with diabetes and retinopathy
Subjective response—no significant differences between groups
Vlug et al,103 2010 Pre- and post-restorative Erotic film with and without VPA—significantly lower postoperatively
proctocolectomy with ileal clitoral vibration
pouch anal anastomosis
(n ¼ 30)
Subjective response—no significant changes
Pieterse et al,101 2008 Radical hysterectomy (n ¼ 13), Erotic film VPA—lower basal and responsive VPA in women with radical hysterectomy
nerve-sparing radical vs nerve-sparing and control groups
hysterectomy (n ¼ 10),
controls (n ¼ 14)
Subjective response—no significant differences between groups
Maas et al,102 2004 Radical hysterectomy (n ¼ 12), Erotic film VPA—significantly lower in women with radical hysterectomy vs controls
simple abdominal
hysterectomy (n ¼ 12),
controls (n ¼ 17)
Subjective response—significantly lower feelings of sexual arousal in women
with simple hysterectomy vs controls
Sipski et al,120 2001 SCI (n ¼ 68), controls (n ¼ 21) Erotic film with and without VPA—significantly lower in women with SCI
additional manual stimulation
Subjective response—significantly lower feelings of sexual arousal in women
with SCI during erotic film with manual stimulation
Wincze et al,104 1993 Diabetes mellitus (n ¼ 7), Erotic film VPA—significantly lower in women with diabetes
controls (n ¼ 7 )
Subjective response—no significant differences in sexual arousal
Sipski et al,121 1995 Complete SCI (n ¼ 13), controls Erotic film with and without VPA—significantly lower in women with SCI during erotic film, no significant
(n ¼ 8) additional manual stimulation difference during film plus manual stimulation
Subjective response—no significant differences between groups during erotic
J Sex Med 2016;13:733e759

film, lower sexual arousal in women with SCI during film plus manual
stimulation
HSDD ¼ hypoactive sexual desire disorder; SCI ¼ spinal cord injury; VPA ¼ vaginal pulse amplitude.

Levin et al
Female Sexual Function and Dysfunction 743

subjective-genital sexual arousal in women shows that the techniques131 (for detailed discussion, see Yang et al2). By and
physical and subjective-experiential components of sexual large, women activate the following areas of the brain when they
response can be loosely coupled, and that genital signs alone are watch erotica (“VSS brain network”; Table 4, Figure 3): occi-
not sufficient to conclude that a woman is sexually aroused pitotemporal cortex, superior parietal lobule, orbitofrontal cor-
(level 3 evidence). Sexual experience consists of awareness of tex, inferior frontal gyrus, anterior cingulate cortex, anterior
bodily responses plus information about stimulus and context insula, ventral striatum, amygdala, thalamus, and hypothal-
that is stored in memory and that can be more or less posi- amus.132e150 Interestingly, pheromone stimulation, used in a
tive.130 Therefore, a complete picture of sexual response is best few studies,22e24,151e153 activates very similar areas of the brain
provided by assessing genital and subjective sexual arousal and despite the different sensory modality and the fact that subjects
affect. did not report being aware of the pheromone stimulation. Some
VSS studies use relatively brief VSS trials with erotic photos
SECTION 4. CENTRALLY BASED PHYSIOLOGY OF (mostly single nudes). This stimulation mode catches early
WOMEN’S SEXUAL FUNCTION AND phases of sexual responsiveness, which are characterized by
DYSFUNCTION saliency detection, sexual interest, attraction, and expectancy.1
Exposure to longer periods (>1 minute) of video VSS is likely
Recommendations to have different affective and behavioral consequences, to elicit
1. Results from brain imaging studies indicate clearly distinct bodily responses such as genital engorgement, and therefore
neural networks for visually induced sexual interest and desire activates a different brain network. In fact, this is what happens
and genitally induced sexual arousal and orgasm (level 2, in men131,154; however, in women, this more vivid type of VSS
grade B). activates largely the same brain network as photo VSS
2. Contrary to what is suggested in many textbooks, the location does.97,140e143 One might think that this is due to ineffective
of the female genitalia on the brain’s main body map is VSS; yet, the use of validated, female-friendly pornographic
subject to considerable debate (level 5). movie excerpts is quite common,11,27,140,155 and enhanced
3. The induction of sexual arousal and orgasm create very perceived sexual arousal is usually reported.139,140,142,143 Indeed,
different activation patterns depending on whether the stim- activity in most of the VSS brain network has been shown to
ulation is clitoral or vaginal, but this divergence is most likely correlate with subjective sexual arousal.139,140 Interestingly,
due to large differences among studies in their methodologic genital arousal (inferred from VPA) has shown no relation with
approach and scrutiny (level 5). brain responses.139 A possible explanation is that women perceive
4. Brain imaging has been unable to show the effects of men- genital engorgement differently than men.
strual cycle phase on sexual cue-induced brain activity (level 4,
grade D). Ovarian Hormone Effects on VSS-Induced Brain
5. Brain imaging is not a proven diagnostic tool for FSD, with Responses
the possible exception of prefrontal hyperactivity in women Regarding the modulating effect of menstrual cycle phase on
with hypoactive sexual desire disorder (HSDD; level 4, (parts of) the VSS brain network, consistency across studies is
grade D). lacking. Studies have found VSS-induced brain activity to be
6. The research field of brain imaging for female sexual response strongest during the follicular phase156 and during menses.157
is underdeveloped and in need of better designed studies, One study found that brain activity only related to anticipa-
especially regarding sexual performance (level 5). tion or expectancy was dependent on the menstrual cycle phase,
such that the strongest anticipatory brain responses were
recorded in women who were in their luteal phase; women in
Introduction
their follicular phase or women on oral contraceptives showed
This section reviews neuroimaging studies on women’s sexual
less modulation.135
response to propose functional brain networks involved in the
control of female sexual responsiveness, with comments on their Two studies investigated the effect of sex steroid administra-
relevance to dysfunction. The studies on which these networks tion on VSS-induced brain activity and suggested that testos-
are based are described in more detail online.1 terone is the primary hormone modulating the strength of brain
responses to VSS.146,158
Brain Networks for Desire and Arousal
Most neuroimaging studies of sexual response use visual sexual VSS-Induced Brain Responses in HSDD
stimulation (VSS), and as a result, VSS-induced brain activity Arnow et al139 found that although women with HSDD
provides the most important central proxy of sexual desire and reported much lower sexual arousal than asymptomatic women,
arousal. The impetus for researchers to use VSS is twofold: vision their vaginal vasocongestion response was very similar, which
is a dominant sensory modality for most humans and visual supports the subjective nature of HSDD. Indeed, compared
paradigms generally work well with all available neuroimaging with sexually asymptomatic women, in women with HSDD,

J Sex Med 2016;13:733e759


744 Levin et al

Table 4. Summary of female brain responses to visual sexual stimulation*


Brain areas Known functions
Cortical areas
Anterior cingulate cortex Incentive salience detection; attention; changing behavior; reward processing
Anterior insula Interoception; attention; switching mindset; reward processing
Inferior frontal gyrus Premotor cortex; understanding actions of others
Occipitotemporal cortex Processing bodily shapes; sensory integration; understanding actions of others
Orbitofrontal cortex Incentive salience detection; reward processing; behavioral control
Superior parietal lobule Vigilance; attention; location of body in space
Subcortical areas
Amygdala Incentive salience detection; vigilance
Hypothalamus Genital arousal; autonomic control
Thalamus Somatosensory, motor, visceral, cognitive, and emotional relay center
Ventral striatum Incentive salience detection; reward processing
*A brief description of the generally accepted functions of the respective areas is provided. Brain areas associated with genital stimulation and orgasm
are not included because of the paucity of studies and inconsistent effects. Mixed men-women studies were included in this review only when they
involved a separate analysis on the data on women.

VSS-induced brain activity is weaker in some areas of the brain Brain Areas Activated During Genital Stimulation
and enhanced in others. HSDD is characterized by less activity and Orgasm
in parts of the VSS brain network,159 which is supported by
Central Representation of the Female Genitalia
structural data from magnetic resonance imaging showing
Somatosensory brain areas tend to be topographically organized,
significantly less gray matter density in parts of the VSS brain
but because of different methodologic issues, no consensus has been
network.160 Enhanced brain activity in women with HSDD is
reached regarding the location of the genitalia on these body
most typically seen in the prefrontal cortex.139,159,161,162
maps.164,165 The most detailed body map is located in the primary
Additional evidence was recently provided by a genetic func-
somatosensory cortex, for which two locations have been
tional magnetic resonance imaging study in carriers of different
proposed.166e171 The brain also possesses body maps in the oper-
serotonin alleles (serotonin release in the prefrontal cortex is
culum (secondary somatosensory cortex) and in the posterior part of
assumed to promote behavioral inhibition).163 Central inhibi-
the insula.172,173 The location of the genitalia in these areas has not
tion also is believed to play a role in female penetration disor-
been systematically mapped, but a study of women with vulvar
ders, but a functional magnetic resonance imaging study with
vestibular pain suggested that these areas are important for pro-
women with lifelong vaginismus could not substantiate this
cessing the emotional meaning of the genital stimulation.174
theory.133

Figure 3. Summary of female brain responses to visual sexual stimulation schematically represented by three different views of the brain
(from left to right ¼ lateral, mesial, basal). Neuroimaging studies presenting subjects with visual erotica consistently find enhanced activity
(indicated by red shading) in a network of brain areas, including the orbitofrontal cortex (OFC), the hypothalamus (HT), the ventral striatum
(VS), the inferior and superior parietal lobules (IPL and SPL), the insula, the amygdala (Amy), the anterior cingulate cortex (ACC), and the
occipitotemporal cortex (OT). Decreased activity (indicated by blue shading) is occasionally seen in parts of the medial temporal lobe,
including the parahippocampal gyrus (med. temp.), but only when more vivid visual sexual stimuli (erotic movies instead of pictures) are
used.

J Sex Med 2016;13:733e759


Female Sexual Function and Dysfunction 745

Persistent genital arousal disorder, also known as restless genitals on orgasm induced by clitoral vs penile stimulation, women did
syndrome,175,176 is a condition that can affect the somatosensory not show significantly different activity in cortical areas.186
body maps, but so far brain research into this condition has been However, results from another study suggested that the pitui-
limited to case studies.177e179 tary gland was active during orgasm in women but not in
men,187 presumably owing to enhanced oxytocin or prolactin
Sexual Arousal Induced by Genital Stimulation release from the pituitary in women during orgasm. Although
Sexual genital stimulation alters VSS-related brain activity. Two interesting, this result requires independent verification.
types of genital stimulation have been used: partnered clitoral
stimulation171 and penetrative (vaginal) self-stimulation.180,181 Summary
These studies have produced very different findings. Partnered The introduction and increased use of neuroimaging methods
clitoral stimulation resulted in increased activity in (mainly) have enabled exploration of the functional and structural brain
cortical somatosensory areas and decreased activity in prefrontal correlates of female sexual response. VSS has been the most
areas and medial temporal areas (including the amygdala). Indeed, widely used stimulation, which leads to a rather fixed activation
the more pleasure was perceived, the stronger the activity decrease pattern, with no clear or consistent modulation by female sex
in these areas. This phenomenon of decreased brain activity could steroids. Some indications support that HSDD relates to pre-
mediate the disinhibition necessary to engage in intense sexual frontal hyperactivity, but localizing it to a distinct prefrontal
activity or intense sexual feelings.171,182,183 region is not possible. For sexual performance, the most effort
Brain responses to sexual-intended vaginal self-stimulation has been put into locating the representation of the female
have been studied in women with SCI180,181 following the genitalia on the main brain body map, although studies on
clinical observation that genital sensitivity can be (partly) rescued genitally induced sexual arousal and orgasm are very few and
(ie, can reach the brain) by virtue of the autonomic innervation have produced almost opposing results. It is clear is that this
of the internal genitalia. Indeed, many parts of the research is in need of more studies.
brain—subcortical and cortical—were activated in response to
vaginal-cervical stimulation, but no decreased activity was re-
ported. The reasons for these opposing findings between clitoral SECTION 5. NON-NEUROLOGIC PATHOLOGY
studies and vaginal studies are potentially manifold and, besides (VASCULAR, UROLOGIC, AND PELVIC FLOOR
the obvious difference of healthy women from women with SCI, DYSFUNCTIONS) THAT PREDISPOSE FSD
include somatic versus visceral sensory inflow to the brain and
Recommendations
the use of different control stimuli and arousal validation
methods, among other methodologic issues.63 1. Vasculogenic FSD results from vascular insufficiency of
female genital tissue that is caused by structural and functional
changes. The risk factors of vasculogenic FSD include hy-
Orgasm pertension, hyperlipidemia, smoking, and diabetes mellitus
These studies also registered orgasm-related brain activity, and (level 3, grade B).
the divergences between the studies are striking. For women with 2. Urinary incontinence is a prevalent disorder that negatively
SCI who had their orgasm induced by vaginal stimulation, the affects female sexual function and women’s quality of life.
pattern of orgasm-related brain activity was an expansion of that Surgery for stress incontinence can improve sexual function
found for stimulation alone, with many areas of the (level 3, grade C).
brain—cortical and subcortical—showing activation.182 Unfor- 3. Pelvic radiotherapy and surgery, including radical cystectomy
tunately, because only three of five women actually achieved and rectal cancer surgery, can influence FSD (level 3, grade B).
orgasm, this study could not provide meaningful group effects
with good predictive validity about the brain control of orgasm in
women. The results on partnered clitoral orgasm were based on Introduction
brain activity recorded in 12 women.171 In that study, orgasm This section reviews the non-neurologic pathology of FSD,
caused a clear switch in brain activity. The few areas that showed which includes pathophysiologic mechanisms of vasculogenic
enhanced activity relative to sexual clitoral stimulation alone were FSD with its risk factors and FSD in the context of various
nearly all in the cerebellum. A strong positive association was diseases and conditions such as urinary incontinence, lower tract
found between activity of the left vermis of the cerebellum and urinary symptoms (LUTS), radical hysterectomy, and pelvic
rectal pressure fluctuations, a measurement of pelvic and surgery and radiation.
abdominal muscular contractions.184 Decreased activity was
much more widespread than during genital stimulation and Pathophysiologic Mechanisms of Vasculogenic FSD
included larger areas of the temporal lobe and prefrontal cortex, Sexual arousal disorder is defined as the “persistent or recur-
which could underlie the substantial changes in cognitive and rent inability to attain or maintain sufficient sexual excitement
moral functioning during orgasm.185 In direct sex comparisons that causes personal distress.”188,189 Women with sexual arousal

J Sex Med 2016;13:733e759


746 Levin et al

disorder report less vaginal lubrication, a longer time to become peripheral tissue perfusion and increase the risks of genital
aroused, lowered sensations of vaginal tissues and clitoris, and vessel stiffness and impaired sexual performance.198 In pre-
problems achieving orgasm. menopausal women, current smoking was reported to be an
In vasculogenic sexual arousal disorder, the major contributing independent risk factor for FSD,199 and cumulative smoking
factor is decreased arterial inflow after sexual stimulation.190 dose and nicotine dependency might be associated with higher
Cardiovascular risk factors such as hypertension, hypercholes- risk of FSD.199
terolemia, smoking, and diabetes mellitus can cause structural
and functional changes in female genital tissues.191 Atheroscle- Diabetes Mellitus
rotic blood vessels might not maintain sufficient perfusion, FSD is common in women with diabetes mellitus. In women
which results in chronic ischemia and hypoxia of the female with type 1 diabetes, the prevalence of FSD totaled 35.4%, and
genital tissues. In addition, vascular endothelial dysfunction is a depression and marital status were significant predictors of
major contributor to vascular insufficiency of female genital tis- FSD.200 Therefore, the researchers suggested that women with
sues.190 Therefore, structural and functional changes in female type 1 diabetes should be routinely checked for the presence of
genital tissues result in vascular insufficiency, which causes sexual dysfunction and possible co-association with depression.
decreased genital arousal and lubrication and leads to vasculo- For women with type 2 diabetes, the prevalence of FSD reached
genic FSD. 53.4% and was significantly higher in menopausal women
(63.9%) than in premenopausal women (41%).201 In this study,
independent predictors of FSD included age, metabolic syn-
Risk Factors of Vasculogenic FSD drome, and atherogenic dyslipidemia. In a systematic review and
Hypertension meta-analysis about FSD and diabetes, the frequency of FSD was
The prevalence of FSD in women with hypertension is higher higher in women with type 1 or 2 diabetes than in controls for
than in women with normal blood pressure, with one study any duration of diabetes.202,203 The risk for FSD was 2.27 and
reporting FSD in 42.1% of women with hypertension compared 2.49 in type 1 and 2 diabetes, respectively. In addition, FSD was
with 19.4% of women without hypertension.192 Adequate control more evident in premenopausal than in menopausal women202
of hypertension can have a great impact on the quality of life of (Table 5).
women with hypertension. Age, systolic blood pressure, duration
of hypertension, and use of b-blockers also are associated with an Urinary Incontinence and FSD
increased prevalence of FSD.192 The duration of hypertension and Urinary incontinence is a prevalent disorder that affects
some antihypertensive drugs, such as b-blockers and diuretics, women’s sexual health.204 According to a recent report, the
have been shown to affect FSD,193 such that the researchers rec- prevalence of sexual dysfunction in women with urinary incon-
ommended that clinicians should be familiar with antihypertensive tinence ranges from 19% to 68%.205
medications with the least influence on the female sexual response
Women can expel various kinds of fluids during sexual
cycle.193 Another study reported that compared with women with
activity.56 Coital incontinence is an involuntary leakage of urine
no hypertension, women with treated or untreated hypertension
during coitus.206 Two kinds of coital urinary incontinence have
were significantly less sexually active.194
been identified based on the timing of its occurrence during
intercourse: incontinence at penetration and incontinence during
Hyperlipidemia
orgasm.205 The pathophysiologic mechanism of urinary leakage
In addition, women with hyperlipidemia have higher preva-
during vaginal penetration could be caused by displacement of
lence of FSD. One study reported that 51% of women with
the bladder neck or the anterior vaginal wall or by decreased
hyperlipidemia had FSD compared with 21% of women without
tension in the PFM. Incontinence during orgasm could result
hyperlipidemia, and that high-density lipoprotein cholesterol and
from simultaneous detrusor contraction.207
triglyceride levels were independently associated with scores on the
Female Sexual Function Index.195 In obese women, high-density Penetration incontinence has been mostly associated with
lipoprotein cholesterol positively correlated with global Female stress urinary incontinence, whereas orgasmic incontinence oc-
Sexual Function Index score and low-density lipoprotein choles- curs more commonly in women with detrusor overactivity.208
terol predicted a lower Female Sexual Function Index score.196 Women with coital incontinence always have pathologic find-
ings on urodynamic studies.209 Therefore, urodynamic exami-
Smoking nation could help differentiate orgasmic incontinence from other
Cigarette smoking also can impair female sexual arousal types of incontinence.56
responses. In healthy non-smoking women, acute nicotine Surgical treatment of urinary incontinence can improve female
intake was shown to significantly attenuate physiologic sexual sexual function. Surgery for stress incontinence has been reported
arousal and decrease genital arousal responses in women by up to have a two to three times greater likelihood of improvement
to 30%.197 Cigarette smoking also can decrease central and compared with deterioration in sexual function.210

J Sex Med 2016;13:733e759


Table 5. Risk factors for vasculogenic female sexual dysfunction
J Sex Med 2016;13:733e759

Female Sexual Function and Dysfunction


Risk factor Study, Year N Methods Summary of results LOE

Hypertension Doumas et al,192 2006 417 FSFI 42.1% of women with FSD had HTN, 19.4% did 3
not have HTN; predictor of FSD: age, systolic
blood pressure, and use of b-blocker
Latif et al,193 2014 355 FSFI Duration of HTN and type of antihypertensive 3
drugs can affect female sexual response cycle
Spatz et al,194 2013 1,390 Self-administered Women with treated and untreated HTN were 3
questionnaire significantly less sexually active than women
with no HTN
Hyperlipidemia Esposito et al,195 2009 115 FSFI 51% of women with FSD had hyperlipidemia, 3
32% did not have hyperlipidemia
Veronelli et al,196 2009 91 FSFI LDL cholesterol affected FSD, whereas HDL 3
cholesterol was protective
Smoking Harte and Meston,197 2008 25 FSFI, vaginal Acute nicotine intake significantly attenuated 2
photoplethysmography physiologic sexual arousal in healthy non-
smoking women
Battaglia et al,198 2011 137 MFSQ, Doppler US Clitoral and labial vascular indexes minus blood 3
flow were worst in heavy smokers
Choi et al,199 2015 900 FSFI Current smoking was independent risk factor for
FSD; cumulative smoking dose and nicotine
dependency were associated with higher risk
of FSD
Diabetes Enzlin et al,200 2009 424 FSFI 35% of women with FSD had type 1 DM, 2
possible co-association with depression
Esposito et al,201 2010 595 FSFI 53.4% of women with FSD had type 2 DM, 3
significantly higher in menopausal women
Pontiroli et al,202 2013 26 studies, 3,168 DM, FSFI, patients’ details FSD was higher in women with DM than in 2
2,823 control controls for any duration of DM; lower FSFI
score was associated with high BMI
BMI ¼ body mass index; DM ¼ diabetes mellitus; FSD ¼ female sexual dysfunction; FSFI ¼ Female Sexual Function Index; HDL ¼ high-density lipoprotein; HTN ¼ hypertension; LDL ¼ low-density
lipoprotein; LOE ¼ level of evidence; MFSQ ¼ McCoy Female Sexuality Questionnaire; US ¼ ultrasonography.

747
748 Levin et al

LUTS and FSD SECTION 6. PSYCHOSOCIAL DETERMINANTS OF


LUTS are another independent risk factor for FSD.211 The SEXUAL FUNCTION AND DYSFUNCTION
potential mechanisms of FSD in women with LUTS can be
related to atrophy in the epithelium of the vagina, urethra, trigon Recommendations
of the bladder, and in the PFM. Compared with women without 1. Clinical levels of anxiety and depression are significantly
urinary complaints, women with LUTS significantly complained associated with sexual dysfunction; more general negative and
of sexual dysfunction.212 Sexual pain disorders can result from positive mood states also have a significant impact on physi-
vaginal atrophy, bacterial vaginitis, vulvar vestibulitis syndrome, ologic and subjective sexual arousal (grade B, level 3).
and vaginal candidiasis. 2. Persistent and daily stressors have a significant impact on
physiologic sexual functioning (grade B, level 3).
3. Individual and partner variables, such as history of abuse, self-
Radical Hysterectomy and FSD esteem, relationship conflict, and the propensity for sexual
Radical hysterectomy can affect female sexual function as a excitation and inhibition, have been related to sexual
result of anatomic disruption in the pelvis.213,214 However, there dysfunction (grade C, level 4).
has been little relevant data comparing postoperative sexual
dysfunction between classic hysterectomy and nerve-sparing
hysterectomy.215 Conventional laparoscopic radical hysterec- Introduction
During the past 10 years, several studies have highlighted the
tomy and nerve-sparing laparoscopic radical hysterectomy
significant interaction between psychosocial variables and sexual
negatively affect patients’ sexual function; however, the nerve-
functioning in women. In particular, mood states, history of
sparing approach has resulted in less sexual dysfunction
trauma, relational factors, and personality variables have been
compared with conventional laparoscopic radical hysterec-
linked to significant impairments in sexual functioning.224e226
tomy.216 The pathophysiology of FSD in patients with hyster-
However, the existing literature is largely correlational and re-
ectomy can stem from anatomic changes in the vagina, such as
lies heavily on self-report, with very few studies examining
shortening or decreased elasticity, pelvic nerve and vessel injury,
physiologic measurements of sexual response. As such, there is a
and removal of the ovaries.216,217
lack of high-level evidence-based research on the relation be-
tween women’s physiologic sexual functioning and psychosocial
Pelvic Surgery, Radiotherapy, and FSD variables. Any discussion of findings and recommendations must
Major pelvic surgery can influence FSD. Radical cystectomy be considered within this limited scope. What follows is a brief
and urinary diversion affect female sexual function. Of patients summary of each category of psychosocial variables and its
who underwent radical cystectomy, 39% complained of impact on female sexual function.
worsening relations with their partners and decreased sexual
function postoperatively.218 The researchers suggested that Affect and Sexual Response: Recommendation
radical cystectomy influenced several physical and psychologi- Level 4, Grade C
cal factors, including loss of reproductive organs, resultant Self-reported positive mood has been shown to be significantly
neurovascular damage, remaining narrow dry vagina, large positively related to sexual functioning.227,228 Laboratory-induced
abdominal scar, presence of stoma, or complications of the positive emotions have led to increased subjective sexual arousal;
mode of diversion. however, this rarely extends to significant differences in physio-
Sexual dysfunction also is a common complication of surgery logic sexual arousal.9,229e232 Similarly, negative affect has consis-
for rectal cancer. After surgery for rectal cancer, 93% of women tently been linked to sexual dysfunction in women. An established
patients reported FSD.219 The researchers asserted that nerve body of research highlights the significant relations among
preservation is generally ignored during surgery in women, and depression, anxiety, and sexual dysfunction.225,233 Although
early menopause resulting from related chemoradiotherapy can studies show a strong correlation among these variables, the data
lead to sexual dysfunction after treatment. However, another are largely self-report and cross-sectional, which does not allow for
study reported that 29% of women still complained of FSD even causality, and the few studies that report on physiologic mea-
though nerve-sparing surgery had been performed for the treat- surements of sexual response show mixed results.226,229,232,234
ment of rectal cancer.220
In addition, pelvic radiotherapy has a significant effect on FSD Depression: Recommendation Level 3, Grade B
because of multiple organic changes, such as excessive pelvic Levels of depression are significantly correlated with
fibrosis, and psychological issues. Women who have undergone self-reported sexual functioning. In one population-based
pelvic radiotherapy have reported feelings of lack of femininity, prevalence study in the United States of more than 31,000
sexual attractiveness, and confidence and distress from vaginal respondents,235 approximately 40% of individuals with sexual
bleeding, vaginal pain, vaginal dryness, and decreased elasticity, arousal disorders also reported having concurrent depression.
resulting in a fear of having sex and less sexual enjoyment.221e223 This relation remains significant after controlling for

J Sex Med 2016;13:733e759


Table 6. Psychosocial variables and their association with women’s sexual dysfunction
J Sex Med 2016;13:733e759

Female Sexual Function and Dysfunction


Psychosocial variable Summary of findings References Recommendation

Affect Positive affect associated with higher levels of sexual functioning, negative affect 227e234 grade C: evidence suggests that affect
with lower levels of sexual functioning; mixed evidence for impact of affect on can impact female sexual response
physiologic sexual response, with some research reporting affect as predictive though level 2, 3 studies are small
of physiologic sexual response and others not in number
Depression Significant relation between depression and self-reported sexual dysfunction 234e246 Grade B: number of level 2 and 3
studies highlight significant
relation
Anxiety High or clinical levels of anxiety typically associated with sexual dysfunction 224, 225, 231, 242, Grade B: number of level 2 and 3
though some reports of anxiety increasing sexual interest; moderate levels of 247e250 studies note significant relation
anxiety facilitate physiologic sexual response
Stress Chronic and acute stress impact self-reported sexual functioning and physiologic 238, 251e259 Grade B: number of recent level 2 and
sexual response 3 studies found significant relation
Attention vs distraction High-level distraction during sexual arousal in laboratory settings significantly 116, 260e266 Grade B: consistent evidence from
inhibits genital response, low- or moderate-level distraction does not level 2 and 3 studies
CSA CSA significantly associated with sexual dysfunction although some studies 234, 267e273 Grade B: number of level 2 and 3
report no differences from individuals without history of CSA; mixed results studies found relation
regarding impact of CSA on physiologic measurements of sexual arousal
Personality characteristics Body image, sexual excitation, inhibition, self-schemas, and adult attachment 231, 242, 274e279 Grade C: small number of level 2 and
related to sexual functioning 3 studies examining each variable
Relationship variables Relationship factors such as duration, communication issues, partner 93, 280, 281 Grade C: small number of level 2 and
dysfunction, and relationship satisfaction related to sexual functioning; no 3 studies
studies examining direct impact on physiologic response
Conditioned learning Appetitive and aversive learning paradigms significantly affect genital response in 282e285 Grade C: small number of level 2 and
women; evidence of extinction for aversive stimulus 3 studies
CSA ¼ childhood-adolescent sexual abuse.

749
750 Levin et al

antidepressant medication use236,237 and has been found in Childhood Sexual Abuse and Early Negative
clinical and non-clinical samples of participants across the life- Experiences: Recommendation Level 3, Grade B
span.238e246 Although increased levels of depression are typically The literature on childhood-adolescent sexual abuse and sexual
associated with decreased sexual functioning, one recent study of functioning in adulthood indicate that this early trauma is
663 female college students demonstrated that approximately significantly associated with sexual dysfunction in wom-
10% of participants reported increased desire and sexual interest en231,267e269 and with lower genital responses in a laboratory
when depressed and 40% of participants reported that depressive environment.234,270 Although the relation between childhood-
mood had no impact on their self-reported sexual functioning.242 adolescent sexual abuse and female sexual difficulties is fairly
consistent across studies, some have found no differences in sexual
functioning scores269,271 or genital responses272,273 between
Anxiety: Recommendation Level 3, Grade B women with a history of childhood-adolescent sexual abuse and
Anxiety disorders also have a significant relation to self- those without, suggesting some variability in this relation.
reported sexual functioning in women.224,225 In a recent study
examining the impact of state-trait anxiety and anxiety sensitivity
to sexual responding, women with anxiety disorders reported Personality Variables: Recommendation Level 4,
significantly worse sexual functioning than those without, and Grade C
state and trait anxiety were related to global reports of sexual Many personality variables have been examined with regard
function.247 However, several studies have suggested anxiety also to physiologic sexual response. In particular, sexual excitation and
can facilitate sexual response. In a sample of 606 women, inhibition have emerged as important in predicting
approximately 20% indicated increased sexual interest when sexual functioning in women.274 The examination of these concepts
anxious,242 and self-reported state anxiety levels demonstrated a in a laboratory setting has shown that sexual excitation scores predict
curvilinear relation with genital response.248 In addition, in increases in genital change and that sexual inhibition scores nega-
healthy women, self-reported anxiety was found to be a signifi- tively predict genital change.229 In addition, researchers have shown
cant positive predictor of genital sexual response229 and activa- that these factors can moderate the relation between sexual response
tion of the sympathetic nervous system was found to have a and mood.229,242 Body image and appreciation,231,275e277 negative
curvilinear relation with sexual response.249,250 self-schemas,278 and adult attachment279 also have been linked to
decreases in sexual functioning.

Stress: Recommendation Level 3, Grade B Relationship Variables: Recommendation Level 4,


Acute and long-term stressors have been significantly associ- Grade C
ated with poorer sexual functioning.238,251e255 Specifically, re- Relationship difficulties and partner variables have been
sults from survey research have suggested that daily life stressors related to self-reported sexual arousal difficulties in
are correlated with self-reported sexual problems and lower sexual women.226,280,281 Specifically, relational conflict, longer rela-
satisfaction in women.238,251e253 In addition, laboratory studies tionship duration, general dissatisfaction or distress, desire or
on stress and sexual functioning have demonstrated significantly sexual script discrepancies, lack of intimacy or trust, in-
lower genital responses during a sexual stimulus in women with compatibility, poor sexual stimulation, or an otherwise inap-
higher levels of chronic stress compared with low or average levels propriate or non-optimal sexual context have been found to
of chronic stressors.254,255 Furthermore, studies examining relate to sexual arousal problems.280 Partner variables have
cortisol levels as an indicator of stress have shown that higher included a partner’s sexual dysfunction and inadequate sexual
levels of cortisol are significantly related to poorer self-reported knowledge of and/or poor sexual stimulation techniques.280
sexual functioning256e258 and less genital response during sex- However, it should be noted that these associations are based
ual arousal in a laboratory setting.258,259 on self-report and no laboratory studies have been conducted to
investigate the impact of partner and relationship variables on
Attention and Distraction: Recommendation Level physiologic sexual response.
3, Grade B
Several recent studies have shown the impact of attention and Learning and Physiologic Sexual Response:
distraction on physiologic sexual response. Studies have shown Recommendation Level 4, Grade C
that self-focused attention during sexual arousal significantly When examining the physiologic sexual response in women,
decreases physiologic sexual response in healthy women,116,260 conditioned learning has been shown to have a significant impact
although one study demonstrated that body awareness had no on genital response in a laboratory environment, which high-
impact.261 In addition, the inclusion of highly distracting stimuli lights the importance of understanding the mind-body connec-
during sexual arousal in a laboratory setting has consistently been tion when assessing female sexual arousal.282e285 Physiologic
shown to decrease sexual response in healthy women and those responses, as measured through vaginal photoplethysmography,
reporting sexual dysfunction.262e266 are amenable to conditioned learning in a laboratory

J Sex Med 2016;13:733e759


Female Sexual Function and Dysfunction 751

environment282e285 and aversive conditioned responses can be (c) Analysis and Interpretation of Data
extinguished,283 which highlights the potential of treatments Not applicable
targeting negative learned responses and introducing new appe- Category 2
titive learning experiences to improve physiologic functioning.
(a) Drafting the Article
Roy J. Levin; Stephanie Both; Janniko Georgiadis; Tuuli Kukkonen;
Summary
Kwangsung Park; Claire C. Yang
Overall, different psychosocial variables are associated with
(b) Revising It for Intellectual Content
physiologic sexual functioning in women. Although the evidence is Roy J. Levin; Stephanie Both; Janniko Georgiadis; Tuuli Kukkonen;
largely based on level 2 and 3 studies, enough research suggests that Kwangsung Park; Claire C. Yang
clinicians should assess for issues with mood, particularly anxiety
Category 3
and depression, daily stressors, and histories of childhood sexual
abuse when evaluating FSD. In addition, health practitioners (a) Final Approval of the Completed Article
should keep in mind that relationship variables and personality Roy J. Levin; Stephanie Both; Janniko Georgiadis; Tuuli Kukkonen;
Kwangsung Park; Claire C. Yang
characteristics can significantly affect sexual response and should
be accounted for accordingly. A growing number of studies sup-
REFERENCES
port the importance of examining the mind-body relation when 1. Levin RJ, Yang CC, Both S, et al. Committee 13A: the anatomy
assessing physiologic sexual functioning. The grade of recom- and physiology of female sexual function and the patho-
mendation for each of the variables is presented in Table 6. physiology of female sexual dysfunction. In: Sexual medicine.
Proceedings of the 4th International Consultation of Sexual
LAST WORDS Medicine, 2015, in press.
A concluding section can only briefly highlight just a few 2. Yang CC, Cold CJ, Yilmaz U, et al. Sexually responsive vascular
important aspects of the individual sections. In relation to female tissue of the vulva. BJU Int 2006;97:766-772.
anatomy, the outstanding unanswered question is still the localiza- 3. Tepper SL, Jagirdar J, Heath D, et al. Homology between the
tion and functionality of the postulated G-spot. In the physiology of female paraurethral (Skene’s) glands and the prostate.
Immunohistochemical demonstration. Arch Pathol Lab Med
sexual arousal, the functionality of the cervix, clitoral (vestibular)
1984;108:423-425.
bulbs, and orgasm are still sub judice. Despite numerous laboratory
assessments of female sexual function, it appears that genital as- 4. Grafenberg E. The role of urethra in female orgasm. Int J
Sexol 1950;3:145-148.
sessments alone are insufficient to characterize the complete female
sexual response. Although brain imaging has opened up the “black 5. Hines TM. The G-spot: a modern gynecologic myth. Am J
box” of the brain for study, it has not yet become a diagnostic tool for Obstet Gynecol 2001;185:359-362.
routine clinical use. FSD resulting from vascular insufficiency of the 6. Pan S, Leung C, Shah J, et al. Clinical anatomy of the G-spot.
genital tissues can occur from a wide range of risk factors (hyper- Clin Anat 2015;28:363-367.
tension, hyperlipidemia, smoking, diabetes, LUTS, and major pel- 7. Masters WH, Johnson VE. Human sexual response. Boston:
vic surgery). Psychosocial determinants such as persistent stress, Little, Brown & Co.; 1966. p. 185.
abuse, relationship conflict, and general negative mood states have 8. Levin R, Wagner G. Self-reported central sexual arousal
been significantly associated with FSD. without vaginal arousal-duplicity or veracity revealed by
objective measurement? J Sex Res 1987;23:540-544.
Corresponding Author: Roy J. Levin, PhD, 145 Dobcroft 9. Suschinsky KD, Lalumiere ML. Prepared for anything? An
Road, Sheffield, UK. Tel: 0114-236-2987; E-mail: r.j.levin@ investigation of female genital arousal in response to rape
sheffield.ac.uk cues. Psychol Sci 2011;22:159-165.
10. Komisaruk BR, Whipple B. Non-genital orgasms. Sex Relatsh
Conflict of Interest: Stephanie Both, Janniko Georgiadis, Tuuli Kuk- Ther 2011;26:356-372.
konen, Kwansung Park, and Claire Yang report no conflicts of in-
11. Herbenick D, Fortenberry JD. Exercise-induced orgasm and
terest. Roy Levin has acted as an advisor to Pastorus Pharma, New
pleasure among women. Sex Relatsh Ther 2011;26:373-388.
York.
12. Levin R, Meston C. Nipple/breast stimulation and sexual arousal
Funding: None. in young men and women. J Sex Med 2006;3:450-454.
13. Levin RJ. The breast/nipple/areola complex and human
STATEMENT OF AUTHORSHIP sexuality. Sex Relatsh Ther 2006;21:237-249.
Category 1 14. Turnbull OH, Lovett VE, Chaldecott J, et al. Reports of inti-
mate touch: erogenous zones and somatosensory cortical
(a) Conception and Design
organization. Cortex 2014;53:146-154.
Roy J. Levin; Stephanie Both; Janniko Georgiadis; Tuuli Kukkonen;
Kwangsung Park; Claire C. Yang 15. Levin RJ. Should the clitoris become a vestigial organ by
(b) Acquisition of Data personal ‘psychological clitoridectomy’? A critical examination
Not applicable of the literature. J Womens Health Issues Care 2014;3:1-14.

J Sex Med 2016;13:733e759


752 Levin et al

16. Puppo V. Anatomy of the clitoris: revision and clarifications 36. Thabet SM. New findings and concepts about the G-spot in
about the anatomical terms for the clitoris proposed (without normal and absent vagina: precautions possibly needed for
scientific bases) by Helen O’Connell, Emmanuele Jannini, and preservation of the G-spot and sexuality during surgery.
Odile Buisson. ISRN Obstet Gynecol 2011;2011:261464. J Obstet Gynaecol Res 2013;39:1339-1346.
17. Shafik A, El-Sibai O, Mostafa R, et al. Response of the internal 37. Ostrezenski A, Krajewski P, Ganjei-Azar P, et al. Verification of
reproductive organs to clitoral stimulation: the clitorouterine the anatomy and newly discovered histology of the G-spot
reflex. Int J Impot Res 2005;17:121-126. complex. BJOG 2014;121:1333-1339.
18. Buisson O, Jannini EA. Pilot echographic study of the dif- 38. Ladas AK, Whipple B, Perry JD. The G spot: and other dis-
ferences in clitoral involvement following clitoral or vaginal coveries about human sexuality. New York: Macmillan; 2005.
sexual stimulation. J Sex Med 2013;10:2734-2740. 39. Levin RJ. The G-spot—reality or illusion? Sex Relatsh Ther
19. Foldes P, Buisson O. The clitoral complex: a dynamic sono- 2003;18:117-119.
graphic study. J Sex Med 2009;6:1223-12231. 40. Lenck LC, Vanneuville G, Monnet JP, et al. [Urethral sphincter
20. Buisson O, Foldes P, Jannini E, et al. Coitus as revealed (G point). Anatomo-clinical correlations]. Rev Fr Gynecol
by ultrasound in one volunteer couple. J Sex Med 2010; Obstet 1992;87:65-69 [in French].
7:2750-3754. 41. Ingelman-Sundberg A. The anterior vaginal wall as an organ for
21. Levin RJ. The human female orgasm: a critical evaluation of the transmission of active forces to the urethra and the clitoris.
its proposed reproductive functions. Sex Relatsh Ther 2011; Int Urogynecol J Pelvic Floor Dysfunct 1997;8:50-51.
26:301-314. 42. Ostrzenski A. Anatomic documentation of the G-spot com-
22. Ginger VA, Cold CJ, Yang CC. Structure and innervation of the plex role in the genesis of anterior vaginal wall ballooning. Eur
labia minora: more than minor skin folds. Female Pelvic Med J Obstet Gynecol Reprod Biol 2014;180:186-191.
Reconstr Surg 2011;17:180-183. 43. Herold C, Motamedi M, Hartmann U, et al. G-spot augmen-
23. Martin-Alguacil N, Schober J, Kow LM, et al. Arousing tation with autologous fat transplantation. J Turk Ger
properties of the vulvar epithelium. J Urol 2006;176: Gynecol Assoc 2015;16:187-188.
456-462. 44. ACOG Committee Opinion No. 378: Vaginal “rejuvenation”
24. Sevely JL. Eve’s secrets: a new perspective on human sexu- and cosmetic vaginal procedures. Obstet Gynecol 2007;
ality. London: Bloomsbury; 1987. 110:737-738.

25. Levin RJ. The mechanisms of human female sexual arousal. 45. Shaw D, Lefebvre G, Bouchard C, et al. Female genital
Annu Rev Sex Res 1992;3:1-48. cosmetic surgery. J Obstet Gynaecol Can 2013;35:1108-1114.

26. Levin RJ. VIP, vagina, clitoral and periurethral glans—an up- 46. Hoch Z. Vaginal erotic sensitivity by sexological examination.
Acta Obstet Gynecol Scand 1986;65:767-773.
date on human female genital arousal. Exp Clin Endocrinol
1991;98:61-69. 47. Jannini EA, Buisson O, Rubio-Casillas A. Beyond the G-spot:
27. Minh H, Smadja A, Herve de Sigalony J. Le fascia de Halban: clitourethrovaginal complex anatomy in female orgasm. Nat
Son role dans la physiologie sexuelle. Gynecologie 1979; Rev Urol 2014;11:531-538.
30:267-273. 48. Burri AV, Cherkas L, Spector TD. Genetic and environmental
28. Battaglia C, Nappi RE, Mancini F, et al. 3-D volumetric and influences on self-reported G-spots in women: a twin study.
vascular analysis of the urethrovaginal space in young women J Sex Med 2010;7:1842-1852.
with or without vaginal orgasm. J Sex Med 2010;7:1445-1453. 49. Levin RJ. The deadly pleasures of the clitoris and the con-
29. Kinsey A, Pomeroy W, Martin C, et al. Sexual behaviour in the dom—a rebuttal of Brody, Costa and Hess (2012). Sex
human female. Philadelphia: WB Saunders; 1953. Relatsh Ther 2012;27:272-295.

30. Eichel EW, Eichel JD, Kule S. The technique of coital alignment 50. Levin RJ, Wylie K. Vaginal vasomotion—its appearance,
and its relation to female orgasmic response and simulta- measurement, and usefulness in assessing the mechanisms
neous orgasm. J Sex Marital Ther 1988;14:129-141. of vasodilatation. J Sex Med 2008;5:377-386.

31. Komisaruk BR, Beyer C, Whipple B. The science of orgasm. 51. Levin RJ. Actions of spermicidal and virucidal agents on
Baltimore: Johns Hopkins University Press; 2006. electrogenic ion transfer across human vaginal epithelium
in vitro. Pharmacol Toxicol 1997;81:219-225.
32. Brody S. The relative health benefits of different sexual ac-
tivities. J Sex Med 2010;7:1336-1361. 52. Levin RJ, van Berlo W. Sexual arousal and orgasm in subjects
who experience forced or non-consensual sexual stim-
33. Levin RJ. Recreation and procreation: a critical view of sex in ulation—a review. J Clin Forensic Med 2004;11:82-88.
the human female. Clin Anat 2015;28:339-354.
53. Levin RJ. Wet and dry sex—the impact of cultural influence in
34. Levin RJ. The involvement of the human cervix in reproduc- modifying vaginal function. Sex Relatsh Ther 2005;20:
tion and sex. Sex Relatsh Ther 2005;20:251-260. 465-474.
35. Thabet SM. Reality of the G-spot and its relation to female 54. Levin R. Measuring the menopause genital changes—a critical
circumcision and vaginal surgery. J Obstet Gynaecol Res account of laboratory procedures past and for the future.
2009;35:967-973. Menopause Rev 1999;1:49-57.

J Sex Med 2016;13:733e759


Female Sexual Function and Dysfunction 753

55. Wimpissinger F, Springer C, Stackl W. International online 74. Glazer HI, Jantos M, Hartmann EH, et al. Electromyographic
survey: female ejaculation has a positive impact on women’s comparisons of the pelvic floor in women with dysesthetic
and their partners’ sexual lives. BJU Int 2013;112:E177-E185. vulvodynia and asymptomatic women. J Reprod Med 1998;
56. Pastor Z. Female ejaculation orgasm vs coital incontinence: a 43:959-962.
systematic review. J Sex Med 2013;10:1682-1691. 75. White G, Jantos M, Glazer H. Establishing the diagnosis of
57. Prause N. The human female orgasm: critical evaluations of vulvar vestibulitis. J Reprod Med 1997;42:157-160.
proposed psychological sequelae. Sex Relatsh Ther 2011; 76. Engman M, Lindehammar H, Wijma B. Surface electro-
26:315-328. myography diagnostics in women with partial vaginismus
58. Prause N. A response to Brody, Costa and Hess (2012): theo- with or without vulvar vestibulitis and in asymptomatic
retical, statistical and construct problems perpetuated in the women. J Psychosom Obstet Gynecol 2004;25:
study of female orgasm. Sex Relatsh Ther 2012;27:260-271. 281-294.

59. Laan E, Rellini AH. Can we treat anorgasmia in women? The 77. van der Velde J, Laan E, Everaerd W. Vaginismus, a
challenge to experiencing pleasure. Sex Relatsh Ther 2011; component of a general defensive reaction. an investigation
26:329-341. of pelvic floor muscle activity during exposure to emotion-
inducing film excerpts in women with and without vagi-
60. Meston CM, Levin RJ, Sipski ML, et al. Women’s orgasm. nismus. Int Urogynecol J Pelvic Floor Dysfunct 2001;
Annu Rev Sex Res 2004;15:173-257. 12:328-331.
61. Waterman CK, Chiauzzi EJ. The role of orgasm in male and 78. Both S, van Lunsen R, Weijenborg P, et al. A new device for
female sexual enjoyment. J Sex Res 1982;18:146-159. simultaneous measurement of pelvic floor muscle activity
62. Higgins JA, Mullinax M, Trussell J, et al. Sexual satisfaction and vaginal blood flow: a test in a nonclinical sample. J Sex
and sexual health among university students in the United Med 2012;9:2888-2902.
States. Am J Public Health 2011;101:1643-1654. 79. Blok BF, Holstege G. The neuronal control of micturition and
63. Georgiadis JR. Exposing orgasm in the brain: a critical eye. its relation to the emotional motor system. Prog Brain Res
Sex Relatsh Ther 2011;26:342-355. 1996;107:113-126.
64. Komisaruk BR, Whipple B. Functional MRI of the brain during 80. Levin RJ, Wagner G. Haemodynamic changes of the human
orgasm in women. Annu Rev Sex Res 2005;16:62-86. vagina during sexual arousal assessed by a heated oxygen
65. Vance EB, Wagner NN. Written descriptions of orgasm: a electrode [proceedings]. J Physiol 1978;275:23P-24P.
study of sex differences. Arch Sex Behav 1976;5:87-98. 81. Levin RJ. Blood flow: heated electrodes. In: Goldstein I,
66. Paterson LQ, Jin ES, Amsel R, et al. Gender similarities and Meston CM, Davis SR, et al, eds. Women’s sexual function
differences in sexual arousal, desire, and orgasmic pleasure in and dysfunction, study, diagnosis, and treatment. London:
the laboratory. J Sex Res 2014;51:801-813. Taylor & Francis; 2006: pp 391-398.
67. Levin RJ, Wagner G. Orgasm in women in the laboratory— 82. Sintchak G, Geer JH. A vaginal plethysmograph system.
quantitative studies on duration, intensity, latency, and Psychophysiology 1975;12:113-115.
vaginal blood flow. Arch Sex Behav 1985;14:439-449. 83. Laan E, Everaerd W, Evers A. Assessment of female sexual
68. Gruenwald I, Vardi Y, Gartman I, et al. Sexual dysfunction in arousal: response specificity and construct validity. Psycho-
females with multiple sclerosis: quantitative sensory testing. physiology 1995;32:476-485.
Mult Scler 2007;13:95-105. 84. Both S, Boxtel G, Stekelenburg J, et al. Modulation of spinal
69. Both S, Ter Kuile M, Enzlin P, et al. Sexual response in women reflexes by sexual films of increasing intensity. Psycho-
with type 1 diabetes mellitus: a controlled laboratory study physiology 2005;42:726-731.
measuring vaginal blood flow and subjective sexual arousal. 85. Laan E, Everaerd W, van der Velde J, et al. Determinants of
Arch Sex Behav 2015;44:1573-1587. subjective experience of sexual arousal in women: feedback
70. Lakeman MME, Laan E, Roovers JPWR. The effects of pro- from genital arousal and erotic stimulus content. Psycho-
lapse surgery on vaginal wall sensibility, vaginal vaso- physiology 1995;32:444-451.
congestion, and sexual function: a prospective single centre 86. Sommer F, Caspers HP, Esders K, et al. Measurement of
study. Neurourol Urodyn 2014;33:1217-1224. vaginal and minor labial oxygen tension for the evaluation of
71. Lowenstein L, Yarnitsky D, Gruenwald I, et al. Does hyster- female sexual function. J Urol 2001;165:1181-1184.
ectomy affect genital sensation? Eur J Obstet Gynecol 87. Prause N, Cerny J, Janssen E. The labial photoplethysmo-
Reprod Biol 2005;119:242-245. graph: a new instrument for assessing genital hemodynamic
72. Basson R. The recurrent pain and sexual sequelae of provoked changes in women. J Sex Med 2005;2:58-65.
vestibulodynia: a perpetuating cycle. J Sex Med 2012; 88. Henson DE, Rubin HB, Henson C. Consistency of the labial
9:2077-2092. temperature change measure of human female eroticism.
73. Gentilcore-Saulnier E, McLean L, Goldfinger C, et al. Pelvic Behav Res Ther 1978;16:125-129.
floor muscle assessment outcomes in women with and 89. Slob AK, Ernste M, van der Werff ten Bosch JJ. Menstrual
without provoked vestibulodynia and the impact of a physical cycle phase and sexual arousability in women. Arch Sex
therapy program. J Sex Med 2010;7:1003-1022. Behav 1991;20:567-577.

J Sex Med 2016;13:733e759


754 Levin et al

90. Kukkonen TM, Binik YM, Amsel R, et al. Thermography as a 106. Cherner RA, Reissing ED. A psychophysiological investigation
physiological measure of sexual arousal in both men and of sexual arousal in women with lifelong vaginismus. J Sex
women. J Sex Med 2007;4:93-105. Med 2013;10:1291-1303.
91. Kukkonen TM, Binik YM, Amsel R, et al. An evaluation of the 107. Boyer SC, Pukall CF, Chamberlain SM. Sexual arousal in
validity of thermography as a physiological measure of sexual women with provoked vestibulodynia: the application of laser
arousal in a non-university adult sample. Arch Sex Behav Doppler imaging to sexual pain. J Sex Med 2013;10:
2010;39:861-873. 1052-1064.
92. Huberman JS, Chivers ML. Examining gender specificity of 108. Caruso S, Rugolo S, Mirabella D, et al. Changes in clitoral
sexual response with concurrent thermography and plethys- blood flow in premenopausal women affected by type 1 dia-
mography. Psychophysiology 2015;52:1382-1395. betes after single 100-mg administration of sildenafil. Urol-
93. Garcia S, Talakoub L, Maitland S, et al. Genital duplex ogy 2006;68:161-165.
Doppler ultrasonography before and after sexual stimula- 109. Caruso S, Rugolo S, Agnello C, et al. Sildenafil improves
tion in women with sexual dysfunction: gray scale, volu- sexual functioning in premenopausal women with type 1
metric, and hemodynamic findings. Fertil Steril 2005; diabetes who are affected by sexual arousal disorder: a
83:995-999. double-blind, crossover, placebo-controlled pilot study. Fertil
94. Kukkonen TM, Paterson L, Binik YM, et al. Convergent and Steril 2006;85:1496-1501.
discriminant validity of clitoral color Doppler ultrasonography 110. Rosato E, Gigante A, Barbano B, et al. Clitoral blood flow in
as a measure of female sexual arousal. J Sex Marital Ther systemic sclerosis women: correlation with disease clinical
2006;32:281-287. variables and female sexual dysfunction. Rheumatology
95. Styles SJ, Maclean AB, Reid WM, et al. Laser Doppler (Oxford) 2013;52:2238-2242.
perfusion imaging: a method for measuring female sexual 111. Heiman JR, Rupp H, Janssen E, et al. Sexual desire, sexual
response. BJOG 2006;113:599-601. arousal and hormonal differences in premenopausal US and
96. Waxman SE, Pukall CF. Laser Doppler imaging of genital Dutch women with and without low sexual desire. Horm
blood flow: a direct measure of female sexual arousal. J Sex Behav 2011;59:772-779.
Med 2009;6:2278-2285. 112. Brotto LA, Yule MA. Physiological and subjective sexual
97. Maravilla KR, Yang CC. Magnetic resonance imaging and the arousal in self-identified asexual women. Arch Sex Behav
female sexual response: overview of techniques, results, and 2011;40:699-712.
future directions. J Sex Med 2008;5:1559-1571. 113. Meston CM, Rellini AH, McCall K. The sensitivity of contin-
98. Gerritsen J, van der Made F, Bloemers J, et al. The clitoral uous laboratory measures of physiological and subjective
photoplethysmograph: a new way of assessing genital sexual arousal for diagnosing women with sexual arousal
arousal in women. J Sex Med 2009;6:1678-1687. disorder. J Sex Med 2010;7:938-950.

99. Laan E, van Driel EM, van Lunsen RH. Genital responsiveness 114. Brauer M, ter Kuile MM, Laan E. Effects of appraisal of sexual
in healthy women with and without sexual arousal disorder. stimuli on sexual arousal in women with and without super-
J Sex Med 2008;5:1424-1435. ficial dyspareunia. Arch Sex Behav 2009;38:476-485.
100. Laan E, van Lunsen RHW. Hormones and sexuality post- 115. Brauer M, ter Kuile MM, Janssen SA, et al. The effect of pain-
menopausal women: a psychophysiological study. related fear on sexual arousal in women with superficial
J Psychosom Obstet Gynecol 1997;18:126-133. dyspareunia. Eur J Pain 2007;11:788-798.
101. Pieterse QD, Ter Kuile MM, Deruiter MC, et al. Vaginal blood 116. Meston CM. The effects of state and trait self-focused
flow after radical hysterectomy with and without nerve attention on sexual arousal in sexually functional and
sparing. A preliminary report. Int J Gynecol Cancer 2008; dysfunctional women. Behav Res Ther 2006;44:515-532.
18:576-583. 117. Brauer M, Laan E, ter Kuile MM. Sexual arousal in women with
102. Maas CP, ter Kuile MM, Laan E, et al. Objective assessment of superficial dyspareunia. Arch Sex Behav 2006;35:191-200.
sexual arousal in women with a history of hysterectomy. 118. Brotto LA, Basson R, Gorzalka BB. Psychophysiological
BJOG 2004;111:456-462. assessment in premenopausal sexual arousal disorder. J Sex
103. Vlug MS, Laan ET, van Lunsen RH, et al. Genital and Med 2004;1:266-277.
subjective sexual response in women after restorative proc- 119. Meston CM, Gorzalka BB. Differential effects of sympathetic
tocolectomy with ileal pouch anal anastomosis—a prospective activation on sexual arousal in sexually dysfunctional and
clinical trial. J Sex Med 2010;7:2509-2520. functional women. J Abnorm Psychol 1996;105:582-591.
104. Wincze JP, Albert A, Bansal S. Sexual arousal in diabetic fe- 120. Sipski ML, Alexander CJ, Rosen R. Sexual arousal and
males: physiological and self-report measures. Arch Sex orgasm in women: effects of spinal cord injury. Ann Neurol
Behav 1993;22:587-601. 2001;49:35-44.
105. Bloemers J, Gerritsen J, Bults R, et al. Induction of sexual 121. Sipski ML, Alexander CJ, Rosen RC. Physiological-parameters
arousal in women under conditions of institutional and associated with psychogenic sexual arousal in women with
ambulatory laboratory circumstances: a comparative study. complete spinal-cord injuries. Arch Phys Med Rehabil 1995;
J Sex Med 2010;7:1160-1176. 76:811-818.

J Sex Med 2016;13:733e759


Female Sexual Function and Dysfunction 755

122. Chivers ML, Seto MC, Lalumiere ML, et al. Agreement of self- 140. Karama S, Lecours AR, Leroux JM, et al. Areas of brain
reported and genital measures of sexual arousal in men and activation in males and females during viewing of erotic film
women: a meta-analysis. Arch Sex Behav 2010;39:5-56. excerpts. Hum Brain Mapp 2002;16:1-13.
123. Rellini AH, McCall KM, Randall PK, et al. The relationship 141. Park K, Kang HK, Seo JJ, et al. Blood-oxygenation-lev-
between women’s subjective and physiological sexual arousal. eledependent functional magnetic resonance imaging for
Psychophysiology 2005;42:116-124. evaluating cerebral regions of female sexual arousal response.
124. Huberman JS, Chivers ML. Examining sexual concordance and Urology 2001;57:1189-1194.
the time course of sexual response with concurrent thermog- 142. Kim TH, Kang HK, Jeong GW. Assessment of brain metab-
raphy and plethysmography. Presented at: 41th Annual Meeting olites change during visual sexual stimulation in healthy
of the International Academy of Sex Research. 2015; Toronto. women using functional MR spectroscopy. J Sex Med 2013;
125. Chivers ML, Bailey JM. A sex difference in features that elicit 10:1001-1011.
genital response. Biol Psychol 2005;70:115-120. 143. Gizewski ER, Krause E, Karama S, et al. There are differences
126. Laan E, Everaerd W, van Bellen G, et al. Women’s sexual and in cerebral activation between females in distinct menstrual
emotional responses to male- and female-produced erotica. phases during viewing of erotic stimuli: a fMRI study. Exp
Arch Sex Behav 1994;23:153-169. Brain Res 2006;174:101-108.
127. Both S, Everaerd W, Laan E. Modulation of spinal reflexes by 144. Gizewski ER, Krause E, Schlamann M, et al. Specific cerebral
aversive and sexually appetitive stimuli. Psychophysiology activation due to visual erotic stimuli in male-to-female
2003;40:174-183. transsexuals compared with male and female controls: an
fMRI study. J Sex Med 2009;6:440-448.
128. Both S, Laan E. Simultaneous measurement of pelvic floor
muscle activity and vaginal blood flow: a pilot study. J Sex 145. Hamann S, Herman RA, Nolan CL, et al. Men and women
Med 2007;4:690-701. differ in amygdala response to visual sexual stimuli. Nat
Neurosci 2004;7:411-416.
129. Stock WE, Geer JH. A study of fantasy-based sexual arousal
in women. Arch Sex Behav 1982;11:33-47. 146. Hamann S, Stevens J, Vick JH, et al. Brain responses to
sexual images in 46,XY women with complete androgen
130. Everaerd W, Both S, Laan E. The experience of sexual emo-
insensitivity syndrome are female-typical. Horm Behav 2014;
tions. J Sex Res 2006;43:3-23.
66:724-730.
131. Georgiadis JR, Kringelbach ML. The human sexual response
147. Demos KE, Heatherton TF, Kelley WM. Individual differences
cycle: brain imaging evidence linking sex to other pleasures.
in nucleus accumbens activity to food and sexual images
Prog Neurobiol 2012;98:49-81.
predict weight gain and sexual behavior. J Neurosci 2012;
132. Borg C, de Jong PJ, Georgiadis JR. Subcortical BOLD re- 32:5549-5552.
sponses during visual sexual stimulation vary as a function of
implicit porn associations in women. Soc Cogn Affect Neu- 148. Gillath O, Canterberry M. Neural correlates of exposure to
rosci 2014;9:158-166. subliminal and supraliminal sexual cues. Soc Cogn Affect
Neurosci 2012;7:924-936.
133. Borg C, Georgiadis JR, Renken RJ, et al. Brain processing of
visual stimuli representing sexual penetration versus core and 149. Rupp HA, James TW, Ketterson ED, et al. The role of the
animal-reminder disgust in women with lifelong vaginismus. anterior cingulate cortex in women’s sexual decision making.
PLoS One 2014;9:e84882. Neurosci Lett 2009;449:42-47.

134. Ponseti J, Bosinski HA, Wolff S, et al. A functional endo- 150. Rupp HA, James TW, Ketterson ED, et al. Lower sexual in-
phenotype for sexual orientation in humans. Neuroimage terest in postpartum women: relationship to amygdala acti-
2006;33:825-833. vation and intranasal oxytocin. Horm Behav 2013;63:114-121.
135. Abler B, Kumpfmuller D, Gron G, et al. Neural correlates of 151. Berglund H, Lindstrom P, Savic I. Brain response to putative
erotic stimulation under different levels of female sexual pheromones in lesbian women. Proc Natl Acad Sci U S A
hormones. PLoS One 2013;8:e54447. 2006;103:8269-8274.
136. Wehrum S, Klucken T, Kagerer S, et al. Gender commonalities 152. Burke SM, Veltman DJ, Gerber J, et al. Heterosexual men and
and differences in the neural processing of visual sexual women both show a hypothalamic response to the chemo-
stimuli. J Sex Med 2013;10:1328-1342. signal androstadiene. PLoS One 2012;7:e40993.
137. Wehrum-Osinsky S, Klucken T, Kagerer S, et al. At the second 153. Zhou W, Chen D. Encoding human sexual chemosensory cues
glance: stability of neural responses toward visual sexual in the orbitofrontal and fusiform cortices. J Neurosci 2008;
stimuli. J Sex Med 2014;11:2720-2737. 28:14416-14421.
138. Klucken T, Schweckendiek J, Merz CJ, et al. Neural activations of the 154. Poeppl TB, Langguth B, Laird AR, et al. The functional
acquisition of conditioned sexual arousal: effects of contingency neuroanatomy of male psychosexual and physiosexual
awareness and sex. J Sex Med 2009;6:3071-3085. arousal: a quantitative meta-analysis. Hum Brain Mapp
2014;35:1404-1421.
139. Arnow B, Millheiser L, Garrett A, et al. Women with hypo-
active sexual desire disorder compared to normal females: a 155. Huynh HK, Beers C, Willemsen A, et al. High-intensity erotic
functional magnetic resonance imaging study. Neuroscience visual stimuli deactivate the primary visual cortex in women.
2009;158:484-502. J Sex Med 2012;9:1579-1587.

J Sex Med 2016;13:733e759


756 Levin et al

156. Rupp HA, James TW, Ketterson ED, et al. Neural activation in 172. Bjornsdotter M, Loken L, Olausson H, et al. Somatotopic
the orbitofrontal cortex in response to male faces increases organization of gentle touch processing in the posterior
during the follicular phase. Horm Behav 2009;56:66-72. insular cortex. J Neurosci 2009;29:9314-9320.
157. Zhu X, Wang X, Parkinson C, et al. Brain activation evoked by 173. Eickhoff SB, Jbabdi S, Caspers S, et al. Anatomical and
erotic films varies with different menstrual phases: an fMRI functional connectivity of cytoarchitectonic areas within the
study. Behav Brain Res 2010;206:279-285. human parietal operculum. J Neurosci 2010;30:6409-
158. Archer JS, Love-Geffen TE, Herbst-Damm KL, et al. Effect of 6421.
estradiol versus estradiol and testosterone on brain-activation 174. Pukall CF, Strigo IA, Binik YM, et al. Neural correlates of
patterns in postmenopausal women. Menopause 2006; painful genital touch in women with vulvar vestibulitis syn-
13:528-537. drome. Pain 2005;115:118-127.
159. Bianchi-Demicheli F, Cojan Y, Waber L, et al. Neural bases of 175. Waldinger MD, Schweitzer DH. Persistent genital arousal
hypoactive sexual desire disorder in women: an event-related disorder in 18 Dutch women: part II. A syndrome clustered
fMRI study. J Sex Med 2011;8:2546-2559. with restless legs and overactive bladder. J Sex Med 2009;
160. Bloemers J, Scholte HS, van Rooij K, et al. Reduced gray 6:482-497.
matter volume and increased white matter fractional 176. Facelle TM, Sadeghi-Nejad H, Goldmeier D. Persistent genital
anisotropy in women with hypoactive sexual desire disorder. arousal disorder: characterization, etiology, and management.
J Sex Med 2014;11:753-767. J Sex Med 2013;10:439-450.
161. Woodard TL, Nowak NT, Balon R, et al. Brain activation 177. Korda JB, Pfaus JG, Kellner CH, et al. Persistent genital
patterns in women with acquired hypoactive sexual desire arousal disorder (PGAD): case report of long-term symp-
disorder and women with normal sexual function: a cross- tomatic management with electroconvulsive therapy. J Sex
sectional pilot study. Fertil Steril 2013;100:1068-1076.e5. Med 2009;6:2901-2909.
162. Versace F, Engelmann JM, Jackson EF, et al. Brain responses 178. Korda JB, Pfaus JG, Goldstein I. Case reports: persistent
to erotic and other emotional stimuli in breast cancer survi- genital arousal disorder: a case report in a woman with life-
vors with and without distress about low sexual desire: a long PGAD where serendipitous administration of varenicline
preliminary fMRI study. Brain Imaging Behav 2013;7: tartrate resulted in symptomatic improvement. J Sex Med
533-542. 2009;6:1479-1486.
163. Klucken T, Wehrum S, Schweckendiek J, et al. The 5-HTTLPR 179. Anzellotti F, Franciotti R, Bonanni L, et al. Persistent genital
polymorphism is associated with altered hemodynamic re- arousal disorder associated with functional hyperconnectivity
sponses during appetitive conditioning. Hum Brain Mapp of an epileptic focus. Neuroscience 2010;167:88-96.
2013;34:2549-2560. 180. Komisaruk BR, Whipple B, Crawford A, et al. Brain activation
164. Georgiadis JR. Functional neuroanatomy of human cortex during vaginocervical self-stimulation and orgasm in women
cerebri in relation to wanting sex and having it. Clin Anat with complete spinal cord injury: fMRI evidence of mediation
2015;28:314-323. by the vagus nerves. Brain Res 2004;1024:77-88.
165. Di Noto PM, Newman L, Wall S, et al. The hermunculus: what 181. Whipple B, Komisaruk BR. Brain (PET) responses to vaginal-
is known about the representation of the female body in the cervical self-stimulation in women with complete spinal cord
brain? Cereb Cortex 2013;23:1005-1013. injury: preliminary findings. J Sex Marital Ther 2002;28:
166. Penfield W, Rasmussen T. The cerebral cortex of man; a 79-86.
clinical study of localization of function. New York: The 182. Borg C, de Jong PJ. Feelings of disgust and disgust-induced
MacMillan Company; 1950. avoidance weaken following induced sexual arousal in
167. Guerit J, Opsomer R-J. Bit-mapped imaging of somatosen- women. PLoS One 2012;7:e44111.
sory evoked potentials after stimulation of the posterior tibial 183. Baird AD, Wilson SJ, Bladin PF, et al. Neurological control of
nerves and dorsal nerve of the penis/clitoris. Electro- human sexual behaviour: insights from lesion studies.
encephalogr Clin Neurophysiol 1991;80:228-237. J Neurol Neurosurg Psychiatry 2007;78:1042-1049.
168. Komisaruk BR, Wise N, Frangos E, et al. Women’s clitoris, 184. van Netten JJ, Georgiadis JR, Nieuwenburg A, et al. 8-13 Hz
vagina, and cervix mapped on the sensory cortex: fMRI evi- fluctuations in rectal pressure are an objective marker of
dence. J Sex Med 2011;8:2822-2830. clitorally-induced orgasm in women. Arch Sex Behav 2008;
37:279-285.
169. Michels L, Mehnert U, Boy S, et al. The somatosensory
representation of the human clitoris: an fMRI study. Neuro- 185. Mah K, Binik YM. The nature of human orgasm: a critical
image 2010;49:177-184. review of major trends. Clin Psychol Rev 2001;21:823-856.
170. Mehnert U, Boy S, Svensson J, et al. Brain activation in 186. Georgiadis JR, Reinders A, Paans AM, et al. Men versus
response to bladder filling and simultaneous stimulation of women on sexual brain function: prominent differences dur-
the dorsal clitoral nerve—an fMRI study in healthy women. ing tactile genital stimulation, but not during orgasm. Hum
Neuroimage 2008;41:682-689. Brain Mapp 2009;30:3089-3101.
171. Georgiadis JR, Kortekaas R, Kuipers R, et al. Regional cerebral 187. Huynh HK, Willemsen AT, Holstege G. Female orgasm but not
blood flow changes associated with clitorally induced orgasm male ejaculation activates the pituitary. A PET-neuro-imaging
in healthy women. Eur J Neurosci 2006;24:3305-3316. study. Neuroimage 2013;76:178-182.

J Sex Med 2016;13:733e759


Female Sexual Function and Dysfunction 757

188. Basson R, Leiblum S, Brotto L, et al. Revised definitions of 205. Serati M, Salvatore S, Uccella S, et al. Female urinary incon-
women’s sexual dysfunction. J Sex Med 2004;1:40-48. tinence during intercourse: a review on an understudied
problem for women’s sexuality. J Sex Med 2009;6:40-48.
189. Basson R, Berman J, Burnett A, et al. Report of the inter-
national consensus development conference on female sexual 206. Haylen BT, de Ridder D, Freeman RM, et al. An International
dysfunction: definitions and classifications. J Urol 2000; Urogynecological Association (IUGA)/International Conti-
163:888-893. nence Society (ICS) joint report on the terminology for female
pelvic floor dysfunction. Int Urogynecol J 2010;21:5-26.
190. Traish AM, Botchevar E, Kim NN. Biochemical factors
modulating female genital sexual arousal physiology. J Sex 207. Mouritsen L. Pathophysiology of sexual dysfunction as related
Med 2010;7:2925-2946. to pelvic floor disorders. Int Urogynecol J Pelvic Floor Dys-
funct 2009;20(Suppl. 1):S19-S25.
191. Miner M, Esposito K, Guay A, et al. Cardiometabolic risk and
female sexual health: the Princeton III summary. J Sex Med 208. Hilton P. Urinary incontinence during sexual intercourse: a
2012;9:641-652. common, but rarely volunteered, symptom. Br J Obstet
Gynaecol 1988;95:377-381.
192. Doumas M, Tsiodras S, Tsakiris A, et al. Female sexual
dysfunction in essential hypertension: a common problem 209. El-Azab AS, Yousef HA, Seifeldein GS. Coital incontinence:
being uncovered. J Hypertens 2006;24:2387-2392. relation to detrusor overactivity and stress incontinence.
Neurourol Urodyn 2011;30:520-524.
193. Latif RA, Muhamad R, Ann AY, et al. Duration of hypertension
and antihypertensive agents in correlation with the phases of 210. Jha S, Ammenbal M, Metwally M. Impact of incontinence
female sexual response cycle. Compr Psychiatry 2014;55- surgery on sexual function: a systematic review and meta-
(Suppl. 1):S7-S12. analysis. J Sex Med 2012;9:34-43.

194. Spatz ES, Canavan ME, Desai MM, et al. Sexual activity and 211. Hansen BL. Lower urinary tract symptoms (LUTS) and sex-
function among middle-aged and older men and women with ual function in both sexes. Eur Urol 2004;46:229-234.
hypertension. J Hypertens 2013;31:1096-1105. 212. Salonia A, Zanni G, Nappi RE, et al. Sexual dysfunction is
195. Esposito K, Ciotola M, Maiorino MI, et al. Hyperlipidemia and common in women with lower urinary tract symptoms and
sexual function in premenopausal women. J Sex Med 2009; urinary incontinence: results of a cross-sectional study. Eur
6:1696-1703. Urol 2004;45:642-648.

196. Veronelli A, Mauri C, Zecchini B, et al. Sexual dysfunction is frequent 213. Maas CP, Weijenborg PT, ter Kuile MM. The effect of hys-
in premenopausal women with diabetes, obesity, and hypothy- terectomy on sexual functioning. Annu Rev Sex Res 2003;
roidism, and correlates with markers of increased cardiovascular 14:83-113.
risk. A preliminary report. J Sex Med 2009;6:1561-1568. 214. Castiglione F, Bergamini A, Albersen M, et al. Pelvic nerve
injury negatively impacts female genital blood flow and in-
197. Harte CB, Meston CM. The inhibitory effects of nicotine on
duces vaginal fibrosis-implications for human nerve-sparing
physiological sexual arousal in nonsmoking women: results
radical hysterectomy. BJOG 2015;122:1457-1465.
from a randomized, double-blind, placebo-controlled, cross-
over trial. J Sex Med 2008;5:1184-1197. 215. Long Y, Yao DS, Pan XW, et al. Clinical efficacy and safety of
nerve-sparing radical hysterectomy for cervical cancer: a
198. Battaglia C, Battaglia B, Mancini F, et al. Cigarette smoking
systematic review and meta-analysis. PLoS One 2014;
decreases the genital vascularization in young healthy,
9:e94116.
eumenorrheic women. J Sex Med 2011;8:1717-1725.
216. Bogani G, Serati M, Nappi R, et al. Nerve-sparing approach
199. Choi J, Shin DW, Lee S, et al. Dose-response relationship
reduces sexual dysfunction in patients undergoing laparo-
between cigarette smoking and female sexual dysfunction.
scopic radical hysterectomy. J Sex Med 2014;11:3012-3020.
Obstet Gynecol Sci 2015;58:302-308.
217. Rodriguez MC, Chedraui P, Schwager G, et al. Assessment of
200. Enzlin P, Rosen R, Wiegel M, et al. Sexual dysfunction in
sexuality after hysterectomy using the Female Sexual Func-
women with type 1 diabetes: long-term findings from the
tion Index. J Obstet Gynaecol 2012;32:180-184.
DCCT/ EDIC study cohort. Diabetes Care 2009;32:780-785.
218. El-Bahnasawy MS, Osman Y, El-Hefnawy A, et al. Radical
201. Esposito K, Maiorino MI, Bellastella G, et al. Determinants of
cystectomy and urinary diversion in women: impact on sexual
female sexual dysfunction in type 2 diabetes. Int J Impot Res
function. Scand J Urol Nephrol 2011;45:332-338.
2010;22:179-184.
219. Attaallah W, Ertekin C, Tinay I, et al. High rate of sexual
202. Pontiroli AE, Cortelazzi D, Morabito A. Female sexual
dysfunction following surgery for rectal cancer. Ann Colo-
dysfunction and diabetes: a systematic review and meta-
proctol 2014;30:210-215.
analysis. J Sex Med 2013;10:1044-1051.
220. Hendren SK, O’Connor BI, Liu M, et al. Prevalence of male
203. Bjerggaard M, Charles M, Kristensen E, et al. Prevalence of
and female sexual dysfunction is high following surgery for
sexual concerns and sexual dysfunction among sexually
rectal cancer. Ann Surg 2005;242:212-223.
active and inactive men and women with screen-detected
type 2 diabetes. Sex Med 2015;3:302-310. 221. Incrocci L, Jensen PT. Pelvic radiotherapy and sexual function
in men and women. J Sex Med 2013;10(Suppl. 1):53-64.
204. Fatton B, de Tayrac R, Costa P. Stress urinary incontinence
and LUTS in women—effects on sexual function. Nat Rev 222. Jensen PT, Groenvold M, Klee MC, et al. Longitudinal study of
Urol 2014;11:565-578. sexual function and vaginal changes after radiotherapy for

J Sex Med 2016;13:733e759


758 Levin et al

cervical cancer. Int J Radiat Oncol Biol Phys 2003;56: 238. Hamilton LD, Julian AM. The relationship between daily
937-949. hassles and sexual function in men and women. J Sex
Marital Ther 2014;40:379-395.
223. Vomvas D, Iconomou G, Soubasi E, et al. Assessment of
sexual function in patients with cancer undergoing radio- 239. Lutfey KE, Link CL, Rosen RC, et al. Prevalence and correlates
therapy—a single centre prospective study. Anticancer Res of sexual activity and function in women: results from the
2012;32:657-664. Boston Area Community Health (BACH) Survey. Arch Sex
Behav 2009;38:514-527.
224. Brotto LA, Klein C. Psychological factors involved in women’s
sexual dysfunctions. Expert Rev Obstet Gynecol 2010; 240. Kalmbach DA, Ciesla JA, Janata JW, et al. Specificity of
5:93-104. anhedonic depression and anxious arousal with sexual prob-
lems among sexually healthy young adults. J Sex Med 2012;
225. Laurent SM, Simons AD. Sexual dysfunction in depression
9:505-513.
and anxiety: conceptualizing sexual dysfunction as part of an
internalizing dimension. Clin Psychol Rev 2009;29:573-585. 241. Kalmbach DA, Pillai V, Kingsberg SA, et al. The transaction
between depression and anxiety symptoms and sexual
226. McCabe M, Althof SE, Assalian P, et al. Psychological and functioning: a prospective study of premenopausal, healthy
interpersonal dimensions of sexual function and dysfunction. women. Arch Sex Behav 2015;44:1635-1649.
J Sex Med 2010;7:327-336.
242. Lykins AD, Janssen E, Graham CA. The relationship between
227. Thompson WK, Charo L, Vahia IV, et al. Association between negative mood and sexuality in heterosexual college woman
higher levels of sexual function, activity, and satisfaction and and men. J Sex Res 2006;43:136-143.
self-rated successful aging in older postmenopausal women.
J Am Geriatr Soc 2011;59:1503-1508. 243. Chang SR, Ho HN, Chen KH, et al. Depressive symptoms as a
predictor of sexual function during pregnancy. J Sex Med
228. Burleson MH, Trevathan WR, Todd M. In the mood for love or 2012;9:2582-2589.
vice versa? Exploring the relations among sexual activity,
physical affection, affect, and stress in the daily lives of mid- 244. Chivers ML, Pittini R, Grigoriadis S, et al. The relationship be-
aged women. Arch Sex Behav 2007;36:357-368. tween sexual functioning and depressive symptomatology in
postpartum women: a pilot study. J Sex Med 2011;8:792-799.
229. Hodgson B, Kukkonen TM, Binik YM, et al. Using the dual
control model to investigate the relationship between mood, 245. Laumann EO, Nicolosi A, Glasser DB, et al. Sexual problems
genital, and self-reported sexual arousal in men and women. among women and men aged 40e80 y: prevalence and
J Sex Res. E-pub ahead of print. correlates identified in the Global Study of Sexual Attitudes
and Behaviors. Int J Impot Res 2005;17:39-57.
230. ter Kuile MM, Both S, van Uden J. The effects of
experimentally-induced sad and happy mood on sexual 246. Shifren JL, Monz BU, Russo PA, et al. Sexual problems and
arousal in sexually healthy women. J Sex Med 2010;7: distress in United States women: prevalence and correlates.
1177-1184. Obstet Gynecol 2008;112:970-978.

231. Mccabe MP, Giles K. Differences between sexually functional 247. Dettore D, Pucciarelli M, Santarnecchi E. Anxiety and female
and dysfunctional women in childhood experiences and indi- sexual functioning: an empirical study. J Sex Marital Ther
vidual and relationship domains. Int J Sex Health 2012; 2013;39:216-240.
24:181-194. 248. Bradford A, Meston CM. The impact of anxiety on sexual
232. Peterson ZD, Janssen E. Ambivalent affect and sexual arousal in women. Behav Res Ther 2006;44:1067-1077.
response: the impact of co-occurring positive and negative 249. Rellini AH, Meston CM. Psychophysiological sexual arousal in
emotions on subjective and physiological sexual responses to women with a history of child sexual abuse. J Sex Marital
erotic stimuli. Arch Sex Behav 2007;36:793-807. Ther 2006;32:5-22.
233. Brotto LA, Bitzer J, Laan E, et al. Women’s sexual desire and 250. Lorenz TA, Harte CB, Hamilton LD, et al. Evidence for a
arousal disorders. J Sex Med 2010;7:586-614. curvilinear relationship between sympathetic nervous system
234. Rellini AH, Elinson S, Janssen E, et al. The effect of pre- activation and women’s physiological sexual arousal. Psy-
existing affect on the sexual responses of women with and chophysiology 2012;49:111-117.
without a history of childhood sexual abuse. Arch Sex Behav 251. Bodenmann G, Ledermann T, Blattner D, et al. Associations
2012;41:329-339. among everyday stress, critical life events, and sexual prob-
235. Johannes CB, Clayton AH, Odom DM, et al. Distressing lems. J Nerv Ment Dis 2006;194:494-501.
sexual problems in United States women revisited: prevalence 252. Bodenmann G, Atkins DC, Schar M, et al. The association
after accounting for depression. J Clin Psychiatry 2009; between daily stress and sexual activity. J Fam Psychol 2010;
70:1698-1706. 24:271-279.
236. Clayton AH, Montejo AL. Major depressive disorder, antide- 253. Bodenmann G, Ledermann T, Bradbury TN. Stress, sex, and
pressants, and sexual dysfunction. J Clin Psychiatry 2006; satisfaction in marriage. Pers Relatsh 2007;14:551-569.
67(Suppl. 6):33-37. 254. ter Kuile MM, Vigeveno D, Laan E. Preliminary evidence that
237. Montgomery SA, Baldwin DS, Riley A. Antidepressant med- acute and chronic daily psychological stress affect sexual
ications: a review of the evidence for drug-induced sexual arousal in sexually functional women. Behav Res Ther 2007;
dysfunction. J Affect Disord 2002;69:119-140. 45:2078-2089.

J Sex Med 2016;13:733e759


Female Sexual Function and Dysfunction 759

255. Hamilton LD, Meston CM. Chronic stress and sexual function history of childhood sexual abuse. J Trauma Stress 2009;
in women. J Sex Med 2013;10:2443-2454. 22:557-565.
256. Meston CM, Lorenz TA. Physiological stress responses pre- 271. Rellini A, Meston C. Sexual function and satisfaction in adults
dict sexual functioning and satisfaction differently in women based on the definition of child sexual abuse. J Sex Med
who have and have not been sexually abused in childhood. 2007;4:1312-1321.
Psychol Trauma 2013;5:350-358.
272. Rellini AH, Meston CM. Sexual self-schemas, sexual dysfunc-
257. Hamilton LD, Rellini AH, Meston CM. Cortisol, sexual arousal, tion, and the sexual responses of women with a history of
and affect in response to sexual stimuli. J Sex Med 2008; childhood sexual abuse. Arch Sex Behav 2011;40:351-362.
5:2111-2118.
273. Staples J, Rellini AH, Roberts SP. Avoiding experiences: sexual
258. Hamilton LD, Meston CM. The role of salivary cortisol and dysfunction in women with a history of sexual abuse in childhood
DHEA-S in response to sexual, humorous, and anxiety- and adolescence. Arch Sex Behav 2012;41:341-350.
inducing stimuli. Horm Behav 2011;59:765-771.
274. Graham CA, Sanders SA, Milhausen RR, et al. Turning on and
259. Van Anders SM, Brotto L, Farrell J, et al. Associations among turning off: a focus group study of the factors that affect
physiological and subjective sexual response, sexual desire, women’s sexual arousal. Arch Sex Behav 2004;33:527-538.
and salivary steroid hormones in healthy premenopausal
275. Pujols Y, Seal BN, Meston CM. The association between
women. J Sex Med 2009;6:739-751.
sexual satisfaction and body image in women. J Sex Med
260. van Lankveld J, Bergh S. The interaction of state and trait 2010;7:905-916.
aspects of self-focused attention affects genital, but not
276. Woertman L, van den Brink F. Body image and female sexual
subjective, sexual arousal in sexually functional women.
functioning and behavior: a review. J Sex Res 2012;49:
Behav Res Ther 2008;46:514-528.
184-211.
261. Seal BN, Meston CM. The impact of body awareness on
277. Satinsky S, Reece M, Dennis B, et al. An assessment of body
sexual arousal in women with sexual dysfunction. J Sex Med
appreciation and its relationship to sexual function in women.
2007;4:990-1000.
Body Image 2012;9:137-144.
262. Salemink E, van Lankveld JJ. The effects of increasing neutral
278. Middleton LS, Kuffel SW, Heiman JR. Effects of experimen-
distraction on sexual responding of women with and without
tally adopted sexual schemas on vaginal response and sub-
sexual problems. Arch Sex Behav 2006;35:179-190.
jective sexual arousal: a comparison between women with
263. Prause N, Heiman J. Reduced labial temperature in response sexual arousal disorder and sexually healthy women. Arch
to sexual films with distractors among women with lower Sex Behav 2008;37:950-961.
sexual desire. J Sex Med 2010;7:951-963.
279. Burri A, Schweitzer R, O’Brien J. Correlates of female sexual
264. Prause N, Janssen E, Hetrick WP. Attention and emotional functioning: adult attachment and differentiation of self.
responses to sexual stimuli and their relationship to sexual J Sex Med 2014;11:2188-2195.
desire. Arch Sex Behav 2008;37:934-949.
280. Witting K, Santtila P, Varjonen M, et al. Female sexual
265. Roberts VM, Prause N. Effects of individual differences on the dysfunction, sexual distress, and compatibility with partner.
efficacy of different distracters during visual sexual stimula- J Sex Med 2008;5:2587-2599.
tion in women. Arch Sex Behav 2012;41:297-310.
281. Fisher WA, Rosen RC, Eardley I, et al. Sexual experience of
266. Anderson AB, Hamilton LD. Assessment of distraction from female partners of men with erectile dysfunction: the Female
erotic stimuli by nonerotic interference. J Sex Res 2015; Experience of Men’s Attitudes to Life Events and Sexuality
52:317-326. (FEMALES) study. J Sex Med 2005;2:675-684.
267. Rellini A. Review of the empirical evidence for a theoretical 282. Both S, Brauer M, Laan E. Classical conditioning of sexual
model to understand the sexual problems of women with a response in women: a replication study. J Sex Med 2011;
history of CSA. J Sex Med 2008;5:31-46. 8:3116-3131.
268. Leonard LM, Iverson KM, Follette VM. Sexual functioning and 283. Brom M, Laan E, Everaerd W, et al. Extinction of aversive
sexual satisfaction among women who report a history of classically conditioned human sexual response. J Sex Med
childhood and/or adolescent sexual abuse. J Sex Marital Ther 2015;12:916-935.
2008;34:375-384. 284. Both S, Laan E, Everaerd W. Focusing “hot” or focusing
269. Meston CM, Rellini AH, Heiman JR. Women’s history of sexual “cool”: attentional mechanisms in sexual arousal in men and
abuse, their sexuality, and sexual self-schemas. J Consult Clin women. J Sex Med 2011;8:167-179.
Psychol 2006;74:229-236. 285. Both S, Laan E, Spiering M, et al. Appetitive and aversive
270. Rellini AH, Hamilton LD, Delville Y, et al. The cortisol response classical conditioning of female sexual response. J Sex Med
during physiological sexual arousal in adult women with a 2008;5:1386-1401.

J Sex Med 2016;13:733e759

View publication stats

You might also like