Archives of Gynecology and Obstetrics (2023) 308:163–170

https://doi.org/10.1007/s00404-023-07037-1

GENERAL GYNECOLOGY

Sensory and muscular functions of the pelvic floor in women

with endometriosis – cross‑sectional study
Joyce Pereira da Silva1 · Bianca Maciel de Almeida1 · Renata Santos Ferreira1 ·
Claudia Regina de Paiva Oliveira Lima2 · Leila Maria Álvares Barbosa1 · Caroline Wanderley Souto Ferreira1

Received: 27 December 2022 / Accepted: 1 April 2023 / Published online: 12 April 2023
© The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature 2023

Abstract
Purpose The aim of this study was to analyze the sensory and muscle functions of the pelvic floor in women with endome-
triosis, trying to improve overall knowledge/findings regarding pelvic floor muscle functions in patients with endometriosis.
Methods Sample size calculated as 92 patients with endometriosis, aged between 18 and 45 years, not virgin, without
other causes of pain and could not be pregnant. Patients underwent the Pelvic Floor Sensorial and Muscle Function Exam
(EFSMAP). Descriptive data were recorded with mean and standard deviation, median (range), and absolute and relative
frequency. The Kolmogorov–Smirnov test was used to observe the normality of quantitative variables. The significance
level adopted for this study was 5%.
Results Of 92 women assessed, 93.3% had pain and 75% had increased tone in the levator ani muscle; 50.4% had impaired
pelvic floor relaxation with median strength of 3 by the Oxford scale and endurance of 2 s.
Conclusions The patients had a high prevalence of pain and dysfunction of the pelvic floor muscles, such as low muscle
endurance and difficulty to relax. It shows that these patients should be referred to a pelvic floor physiotherapist, as soon as
they have the diagnosis of endometriosis, to be assessed to prevent and/or treat pelvic floor impairments.

Keyword Levator Ani · Muscle Strength · Muscles · Pelvic floor disorders · Physiotherapy specialty

What does this study add to the clinical work? Introduction

Women with endometriosis have high prevalence of
Endometriosis is a chronic inflammatory disease of ectopic
pelvic floor sensory and muscle dysfunction. There-
nature, characterized by the presence of endometrial glands
fore, they need to be evaluated by a pelvic physi-
and stroma predominantly in the pelvic region, affecting
otherapist early on.
women of reproductive age and being associated with pel-
vic pain [1].
The possible pathophysiology theory of this disease is the
innervation of these endometrial lesions during angiogenesis
in their development, causing the association of bleeding
with pain [2].
This relationship may be due to the clinical symptoms of
endometriosis, since a prevalence of pelvic pain was identi-
fied in about 40% of this population, including dysmenor-
rhea and dyspareunia. The former being the most prevalent,
* Caroline Wanderley Souto Ferreira affecting about 84% of women with endometriosis, and dys-
[email protected] pareunia covering 36% [3].
Pain and visceral inflammation can trigger muscle ten-
1
Department of Physiotherapy, Federal University sion resulting in pelvic floor dysfunction, representing a
of Pernambuco-UFPE, Av Prof. Moraes Rego, 1235. Cidade
Universitária, Recife, Pernambuco CEP: 50670‑901, Brazil mechanism prone to activation of myofascial trigger points.
2 In this sense, the source of continuous nociception generated
Department of Statistic, Federal University
of Pernambuco-UFPE, Recife, Brazil by trigger points, are able to sensitize the nervous system,

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164 Archives of Gynecology and Obstetrics (2023) 308:163–170

causing motor and autonomic disorders that can affect even The eligible volunteers who agreed to participate voluntarily
the function of pelvic organs [2]. signed the Free and Informed Consent Form—FICF, and
It is important to remember that the function of the pelvic then the anamnesis was performed by the researcher, which
floor muscles (PFM) goes beyond supporting the pelvic and investigated the variables: sociodemographic (age, marital
abdominal viscera. These muscles ensure urinary and fecal status, education level), anthropometric (weight, height,
continence and help in lumbopelvic control, modulating body mass index (BMI), gynecological and obstetric (history
postural activity and contributing to breath. Therefore, it is of dysmenorrhea, age of menarche, length of the menstrual
feasible to associate pelvic floor dysfunction with systemic cycle, number of pregnancies, deliveries and abortions, type
changes. [4]. of previous delivery).
Due to the above, the aim of this study was to identify the Then, the patients were placed in the gynecological
sensory and muscular changes of the pelvic floor in women position for assessment. The Examination of Pelvic Floor
with endometriosis, trying to improve overall knowledge/ Sensory and Muscle Functions (EFSMAP) was performed
findings regarding pelvic floor muscle functions in patients through inspection, digital palpation and vaginal manometry,
with endometriosis. to observe proprioceptive function, pain, muscle tone, invol-
untary contraction reflex during coughing, control of con-
traction and relaxation, coordination (isolated contraction
Materials and methods of the PMF) and muscle strength, that was graded through
intravaginal palpation with the Oxford scale and the contrac-
Study recruitment, sample size and inclusion/ tion pressure with the perineometer PelvAirUnit-Miotec [6].
exclusion criteria The patients who could not perform the contraction of the
perineal muscles when requested during palpation, could not
This is a cross-sectional study, carried out from August proceed with the rest of the examination, thus, relaxation,
2021 to August 2022, in the Laboratory of Physiotherapy of coordination, resistance and perineometry were not evalu-
Women's Health and Pelvic Floor (LAFISMA), located in ated, as per the criteria of EFSMAP.
the Department of Physiotherapy of the Federal University The strength of the PFM was evaluated using the Oxford
of Pernambuco (UFPE), Recife-PE. The study was approved scale, which varies from 0 to 5, where zero is no perceptible
by the Ethics and Human Research Committee of the UFPE, muscle contraction and five is a strong and firm contraction
approval number 4.627.309. The patients were referred by that raises the examiner's fingers towards the pubic sym-
specialist doctors from the Hospital das Clínicas of Pernam- physis [7]. The perineometer was inserted into the vaginal
buco (the University Hospital), and on a volunteer basis, canal with an un-lubricated Blowtex condom and water-
through advertising on social networks and other services. based lubricating gel (Lubrigel), then the patient was asked
The sample size was estimated based on a 51% prevalence to perform three perineal contractions, of three seconds, with
of musculoskeletal dysfunction in women with endometrio- a 1-min interval, and the highest pressure (cm/H2O) was
sis [5] and a relative error of 20%, resulting in 92 partici- recorded, as specified in EFSMAP.
pants. The inclusion criteria were women aged 18–45 years All data collection procedures, per participant, were car-
with a clinical diagnosis of endometriosis as determined ried out in a single assessment by the same physiotherapist
by a medical specialist. The exclusion criteria were virgin and lasted approximately 40 min.
women, pelvic pain due to another cause (such as fibromy-
algia, acute pelvic inflammatory disease, interstitial cystitis,
retocolitis, etc.), pregnant women, postpartum period of six
months or less, neurological diseases, history of surgery and/ Statistical analysis
or fracture of the spine and pelvis, history of neoplasia in
the abdominal or pelvic region, and cognitive or comprehen- Statistical analysis was performed using IBM Statistical
sion issues that would make it impossible to carry out the Package for the Social Sciences (SPSS) software version
research. 20.0. A confidence level of 95% and a significance level
of 5% (p < 0.05) were assigned. A descriptive analysis was
performed using mean, standard deviation, for quantitative
Data collection variables with normal distribution and in median and inter-
quartile range (Q25-Q75) for non-normal variables. Qualita-
Before starting the evaluation, each volunteer received an tive variables were described as frequency and percentage.
explanation about the objectives of the study. The women The Kolmogorov–Smirnov test was used to observe the nor-
who showed interest in taking part in the research answered a mality of quantitative variables.
questionnaire, containing questions about eligibility criteria.

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Archives of Gynecology and Obstetrics (2023) 308:163–170 165

Fig. 1  Flowchart of uptake

women with endometriosis. Women with endometriosis(n=137)
Recife/PE, 2021–2022

Total excluded (n = 45)

1. Ineligible (n = 23)
• Neurological disease (n = 1)
• Surgery for endometriosis without pelvic pain (n
= 8)
• History of spine and pelvis surgery and/or
fracture (n = 5)
• Had other causes of pain (n = 8)
• Time of delivery less than or equal to six months
(n = 1)

2. Eligible but not recruited (n = 22)

• Unavailability for participation (n = 14)
• Refusal to participate (n = 7)

Included in the anamnesis phase (n = 92)

Total Excluded (n = 2)
• Pain from the unidigital vaginal touch (n = 1)
• Uncomfortable with the procedure (n = 1)

Included in the physical examination

(n = 90)

Total Excluded (n = 6)
• Unable to perform the contraction of the Pelvic
Floor Muscle(n = 3)
• Could not stand the placement of the
perineometer probe(n = 3)

Included in the Pelvic Floor Sensorial and

Muscle Function Exam and perineometry
(n = 84)

Results had more than 12 years of study. The median BMI was
26.45 kg/m2 with an interquartile range of (24.4–31.5) of
To reach the required sample size of 92 women with which 31 (33.7%) were pre-obese and 23 (25%) had grade
endometriosis, 137 patients were evaluated and 45 were 1 obesity. A total of 89 (96.7%) patients reported having
excluded (Fig. 1). a history of dysmenorrhea. As for the number of pregnan-
Ninety-two women with endometriosis were evalu- cies, 54 (58.7%) of the patients were nulliparous, and of
ated with a mean age of 33.7 years, with the majority the patients who had delivered babies, 13 (14.1%) were
aged ≤ 35 years, 41 (44.6%) were married, and 49(53.3%) primiparous, 17 (18.5%) were multiparous, and 18 (19.6%)

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166 Archives of Gynecology and Obstetrics (2023) 308:163–170

had abortions. As for delivery, 14 (46.7%) had cesarean Table 1  Characterization of women with endometriosis. Recife/PE,
deliveries (Table 1). 2021–2022
Of the 92 patients evaluated, two refused to participate Variables N = 92 N (%) Mean ± SD or
in the physical examination, through EFSMAP, one for median (Q25–Q75)a

reporting pain from the unidigital vaginal touch, felt during Sociodemographic variables
the examination, and the other was uncomfortable with the Age (years) – 33.7 ± (6.95)
procedure. ≤ 35 years 55 (59.8) –
Of the 90 women who underwent the EFSMAP, 3 were 36–39 years 16 (17.45) –
unable to perform the contraction of the PFM, therefore, ≥ 40 years 21 (22.8) –
they did not continue the test. Another 3 women could not Marital status
stand the placement of the perineometer probe, due to pain, Single 31 (33.7) –
so they could not be assessed by the perineometer. Married 41 (44.6) –
The majority (93.3%) of the patients evaluated by EFS- Divorced 7 (7.6) –
Widow 1 (1.1) –
MAP had pain in the levator ani muscle, 75% had increased
De facto 12 (13) –
muscle tone, 50.4% had difficulty relaxing the muscle and
Years of study
63% was not able to contract the levator ani muscle without
≤ 9 years 10 (10.9) –
synergists, indicating poor coordination (Table 2).
≤ 12 years 33 (35.9) –
Regarding the levator ani muscle strength, the patients > 12 years 49 (53.3) –
presented a median score of three, according to the Oxford Anthropometric variables
scale. The median endurance of two seconds, according to Weight (Kg) – 71.1 ± (14.9)
the maximum voluntary contraction, with 3 times repetition, Height (meter) – 1.60 ± (0.06)
with the same contraction time and force. For the number BMI (Kg/m2)b – 26.45 (24.4–31.5)a
of fast contractions, the patients were able to perform five Underweight 3 (3.3) –
repetitions, in median, with the same strength, and time less Healthy weight 26 (28.3) –
than 3 s (Table 2). Overweight 31 (33.7) –
Obesity Class 1 23 (25) –
Obesity Class 2 8 (8.7) –
Discussion Obesity Class 3 1 (1.1) –
Gyneco-obsteric variables
History of dysmenorrhea 89 (96.7) –
The majority of subjects in the present study were of repro-
Age at menarche (years) – 12 (11–13)a
ductive age, had completed more than 12 years of education,
Menstrual cycle length (days) – 28 (25–30)a
were overweight, and were married. The history of dysmen-
Number of pregnancies 38 (41.3) 2 (1–2)a
orrhea was the most common gynecological variable, fol- Nulligravida 54 (58.7) –
lowed by nulliparity. Women with endometriosis presented Primigravida 13 (14.1) –
changes in sensory and muscular functions of the pelvic Secundigravida 17 (18.5)
floor, such as pain in the levator ani muscle, increased tone, Multigravida 8 (8.7) –
moderate muscle strength (according to the Oxford scale), Number of deliveries 30 (32.6) 2 (1–2.25)a
low endurance and inability to perform isolated contraction Nulliparous 62 (67.4) –
of the PFM. Primiparous 13 (14.1) –
The mean age of our patients was 33.7 years. This result Multiparous 17 (18.5) –
corroborates the findings of a study with 237 women with Number of abortions 18 (19.6) 1 (1–2)a
endometriosis, where most (65.4%) were of reproductive Previous delivery type
age (29–39 years). Another similarity found in both studies Cesarean 14 (46.7) –
Vaginal 10 (33.3) –
was in relation to BMI, where they showed a prevalence of
Instrumental 1 (3.3) –
overweight patients [8].
Cesarean and vaginal 5 (16.7) –
Being overweight may be associated with the high rates
of inflammation already found in women with endometriosis a
Median and interquartile range for non-normal variables
since obesity is an important factor related to the secretion b
BMI—Body Mass Index: > 18.5 kg/m2—Underweight; 18.5–
of cytokines and proteins that influence inflammatory fac- 24.9 kg/m2—healthy weight; 25–29.9 kg/m2—overweight; 30.0–
tors. This may occur due to the state of increased proteinic 34.9 kg/m2—Obesity Class 1; 35.0–39.9 kg/m2 Obesity Class 2; ˃
40.0 kg/m2—Obesity Class 3; Kg-kilogram; Kg/m2- kilogram/square
oxidative stress in the peritoneal fluid of women with endo- meter
metriosis, as well as, by the deregulation of the prostaglan-
din pathway in the endometrium of women suffering from

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Archives of Gynecology and Obstetrics (2023) 308:163–170 167

Table 2  Description of the Pelvic Floor Sensorial and Muscle Function Exam (EFS- N = ­90a n (%) Median (Q25-Q75)
pelvic floor sensory and muscle MAP)
function exam (EFSMAP) in
women with endometriosis Proprioceptive function
Present 53 (58.9) –
Absent 37 (41.1) –
Pain located in the levator ani muscle
Present 84 (93.3) –
Absent 6 (6.7) –
Muscle tone
Low 8 (8.9) –
Normal 7 (7.8) –
Increased 75 (83.3) –
Reaction (involuntary contraction during cough)
Present 87 (96.7) –
Absent 3 (3.3) –
Control (contraction)–inspectionb
Present 87 (94.6) –
Absent 3 (3.3) –
Control (contraction) – ­palpationb
Present 87 (96.7) –
Absent 3 (3.3) –
Control (relaxation)b
Absent 3 (3.3) –
Partial/slow 41 (47.1) –
Present 43 (49.4) –
Coordination (isolated PFM contraction)b
Present 32 (36.8) –
Absent 55 (63.2) –
Muscle strength
Oxford scale – 3 (2–3)
Perineometer (Cm/H2O)c
Resting tone – 20 (20–20)
Contraction (MVC) – 40 (30–60)
Muscle ­enduranceb
Endurance (s) – 2 (2–3)
Amount of endurance contraction – 3 (0–4)
Amount of fast contraction – 5 (3–6)

Recife/PE, 2021–2022
MVC maximum voluntary contraction; cmH20 centimeter of water; PFM pelvic floor muscles
a
Loss of 2 patients because EFSMAP was not performed
b
Loss of 3 women who were unable to perform the PFM contraction and therefore did not perform the rest
of the exam
c
Loss of 6 women, 3 who were unable to perform the PFM contraction and 3 who could not bear the place-
ment of the perineometer in the vaginal canal, (s)- second

endometriosis by the benefit of an increased expression of impact on the quality of life of women with endometriosis,
prostaglandin-endoperoxide synthase 2 (PTGS2) [9, 10]. affecting 57.2% of the study population [11]. Furthermore,
Along with these findings, there is the report of dysmen- in a study that analyzed the quality of life, stress, depres-
orrhea, which is a striking variable among the population sion, and pain in women with endometriosis, a correlation
of the present study, with a frequency of 96.7% of patients. between impairments in quality of life and pelvic pain was
This corroborates with the study by Chapron, et al. which found [12].
showed dysmenorrhea as a persistent variant in the real

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168 Archives of Gynecology and Obstetrics (2023) 308:163–170

The present study further found that a majority of the that analyzed the perineometry in women with urinary
population was nulligravida (58.7%) and nulliparous incontinence. In the contrasting study, the results showed
(67.4%). This corroborates with the study of Cardoso, et al., a median pressure of the maximum voluntary contraction
who identified that 41.3% of women diagnosed with endo- of 22.85(18.8–26.6) Cm/H2O [19], revealing that women
metriosis through surgery, were nulliparous [8]. This data with urinary incontinence have a lower pelvic floor muscle
can be further clarified by Prescott, et al., who explain the strength than women with endometriosis.
association of endometriosis with a two times higher risk of In another study that analyzed perineometry in healthy
infertility in these women [13]. women, it was observed that the mean pressure of the max-
As the risk of infertility compromises the quality of life imum voluntary contraction was higher (77.70 ± 31.97Cm/
of women with endometriosis, it was observed in a study H2O) [22] than in the women in the present study. Thus,
that analyzed the quality of life, using the Endometriosis it is clear that women with endometriosis need to improve
Health Profile-5 (EHP-5) questionnaire, that infertile women pelvic floor muscle strength. This contrast in muscle
had higher scores on the EHP-5 compared to fertile women, strength between healthy women and women with endo-
proving impairment in quality of life due to infertility [14]. metriosis can be explained by the muscle tone because
In the present study’s samples, a change in the sensitivity 75(83.3%) of our patients had a levator ani with its tone
of the muscle was found as a decrease in muscle proprio- increased. In addition, Fraga, et al. showed a predomi-
ception in 41.1% of the patients. This was also found by nance of weak contractions (2.63 ± 0.56) and hypertonia
Efstathiou et al., that observed a connection between pain in about 30% of women with endometriosis, where mus-
and proprioceptive deficit, within alterations of the central cle strength and tone were compared among 160 women
nervous system. It is believed that muscles that are perma- (80 with endometriosis and 80 without), aged from 18 to
nently tense, cause pain and may affect neurophysiological 45 years [7, 23].
mechanisms related to the integration of the central process- In addition to the increased tone, it was found that 50.4%
ing of sensory stimuli, altering the sensory perception of of our patients had problems to relax the muscle. Fraga et al.
these muscles [15]. had a similar result with 45% of their patients, that were
A large majority of our patients (93.3%) suffered from unable to relax completely the PFM [23]. To explain this
pain in the levator ani muscle, and this finding may be relationship, there is evidence in the literature of the pres-
related to altered sensitivity. This is discussed in the study ence of trigger points in about 50%-90% of women with
by Bonder, et al., who evaluated the sensitivity to the pain endometriosis, even when treated pharmacologically or after
of the levator ani muscle in women, with pelvic pain related undergoing surgery [24]. These trigger points may be related
to endometriosis, and found that 89% of patients presented to the inability to adequate contraction and relaxation of the
changes in sensitivity and pain [16]. As seen in Lamvu, et al. PMF, leading to muscle weakness [25].
the visceral structures of the pelvis receive and send signals It was found that 63.2% of our patients were unable to
to the central nervous system, generating stimuli that can contract only the PMF when asked, they always contracted
affect pelvic floor muscle contraction and function, leading some synergist muscle together. The same was observed by
to generalized pelvic muscle dysfunction [17]. Fraga, et al., in 41% of their sample (women with endo-
In the present study, the levator ani muscle strength had metriosis) [23]. It shows that these patients have a lack of
a median score of 3 (Oxford scale), and the maximum vol- coordination in their PFM contraction [23].
untary contraction pressure, measured by a perineometer, Our study had several strengths which are: the sample
showed a median of 40(30–60) Cm/H2O. Despite the pain, size; the material and the methods adopted where the evalu-
we found that our patients demonstrated good contraction ation was performed by a same trained physiotherapist using
of the levator ani muscle, with reference to a study that ana- the same equipment on all patients. Additionally, it is the
lyzed pelvic floor muscle strength in women of childbearing first research to evaluate the sensory functions of the pelvic
age [18]. floor and assess the levator ani muscle by a perineometer in
The perineometer is a tool used to accurately assess mus- women with endometriosis, that we are aware of.
cle strength. In addition, as it is an intravaginal device, it Our study also had some limitations. It was not possible
provides sensory biofeedback and assists in the perception to observe the temporal and causal linearity between the
of pelvic floor contraction [19, 20]. It was shown that women findings and the underlying disease. In addition, the use of
who performed a home workout for the pelvic floor mus- pressure biofeedback may have interference from the pres-
cle, with an intravaginal device, had better results than ones sure that emanates from the abdomen.
without the intravaginal device [21]. In conclusion, the data show that women with endome-
Regarding the median pressure of the maximum vol- triosis present changes in sensory and muscular functions
untary contraction found in the present study (40 cm/ of the pelvic floor, such as pain in the levator ani muscle,
H 2O), it is possible to observe a contrast with a study hypertonia, moderate muscle strength, according to the

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Archives of Gynecology and Obstetrics (2023) 308:163–170 169

Oxford scale, low endurance and inability to have an isolated functions? A cross-sectional study. Physiotherapy 109:85–93.
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nard Donnelly for proofreading the manuscript regarding English, as a org/​10.​1016/​S0031-​9406(05)​61108-X
native English Speaker, the Federal University of Pernambuco (UFPE) 8. Cardoso JV, Machado DE, Silva MC, Berardo PT, Ferrari R,
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data analysis, interpretation of data, manuscript writing, approval of 9. Santulli P, Chouzenoux S, Fiorese M, Marcellin L, Lemarechal H,
the final version. BMA: data collection, data analysis, interpretation Millischer AE, Batteux F, Borderie D, Chapron C (2015) Protein
of data, manuscript writing, approval of the final version. RSF: data oxidative stress markers in peritoneal fluids of women with deep
collection, data analysis, approval of the final version. CRPOL: data infiltrating endometriosis are increased. Hum Reprod 30(1):49–
analysis, interpretation of data, revision of the manuscript, approval of 60. https://​doi.​org/​10.​1093/​humrep/​deu290
the final version. LMAB: project development, data analysis, interpre- 10. Santulli P, Borghese B, Noël JC, Fayt I, Ziegler VAD, Batteux
tation of data, revision of the manuscript, approval of the final version. F, Vaiman D, Chapron C (2014) Hormonal therapy deregulates
CWSF: project development, data analysis, interpretation of data, revi- prostaglandin-endoperoxidase synthase 2 (PTGS2) expression in
sion of the manuscript, approval of the final version. endometriotic tissues. J Clin Endocrinol Metab 99(3):881–890.
https://​doi.​org/​10.​1210/​jc.​2013-​2950
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rior, Universidade Federal de Pernambuco. A, Romanov V, Maisonobe P, Cabri P (2016) Factors and regional
differences associated with endometriosis: a multi-country case–
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available from the corresponding author, [CWSF], upon reasonable 1007/​s12325-​016-​0366-x
request. 12. Škegro B, Bjedov S, Mikuš M, Mustač F, Lešin J, Matijević
V, Ćorić M, Elveđi Gašparović V, Medić F, Sokol Karadjole V
(2021) Endometriosis, pain and mental health. Psychiatr Danub
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Conflict of interest The authors declare that they have no conflict of Chavarro JE, Rich-Edwards JW, Barbieri RL, Missmer SA (2016)
interest. A prospective cohort study of endometriosis and subsequent risk
of infertility. Hum Reprod 31(7):1475–1482. https://​doi.​org/​10.​
Ethical approval and consent to participate This study was conducted 1093/​humrep/​dew085
in accordance with the terms of the National Health Council (Resolu- 14. Mikuš M, Matak L, Vujić G, Škegro B, Škegro I, Augustin G,
tion 466/12) and was approved by the Ethics and Human Research Lagana AS, Ćorić M (2023) The short form endometriosis health
Committee of the Federal University of Pernambuco, approval number profile questionnaire (EHP-5): psychometric validity assessment
4,627,309. of a croatian version. Arch Gynecol Obstet 307(1):87–92. https://​
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da pressão perineal em nulíparas. Scientia Medica 29(1):e32614. jurisdictional claims in published maps and institutional affiliations.
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