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Original Article

Yoga intervention on blood NO in female migraineurs

Mahsa Zamani Boroujeni, Seyed Mohamad Marandi1, Fahimeh Esfarjani1, Mina Sattar1, Vahid Shaygannejad2,
Shaghayegh Haghjooy Javanmard
Department of Physiology, Physiology Research Center, and 2Department of Neurology, Isfahan University of Medical Sciences,
1
Department of Exercise Physiology, University of Isfahan, Isfahan, Iran

Abstract Background: The current survey investigates the effect of 12 weeks yoga training on headache frequency,
severity, duration and blood nitric oxide levels as well as headache impacts on female migraineurs’ lives.
Materials and Methods: Thirty-two female patients with migraine took part and were randomly divided
into two groups. The control group (n = 14) received medication and the yoga group (n = 18) participated
in 12 weeks yoga training in addition to receiving the same medication as that of the control group.
Frequency and duration of headache were assessed by a questionnaire. Visual Analogue Scale was used
to measure the severity of headache, and the metabolite of NO also was measured by Griess reaction.
Headache Impact Test ( HIT-6) was also used to assess the impact of headache on patients’ lives. Data were
analyzed by t-test mean variance.
Results: After 3 months intervention, in the yoga group, there was a significant reduction in the impact of
headache on patients’ lives, headache frequency, and severity and a non-significant reduction in headache
duration in the yoga group. There was no significant difference in the plasma levels of NO between yoga
and control groups before and after the study.
Conclusion: Based on the results, yoga could be recommended as a complementary method to migraine
patients.

Key Words: Asana, headache impact, migraine, NO, pranayama, shavasana

Address for correspondence:

Ms. Shaghayegh Haghjooy Javanmard, Assistant Professor of Physiology, Physiology Research Center, Isfahan University of Medical Sciences, Hezar Jerib
Avenue, Isfahan, Iran. E-mail: [email protected]
Received: 13.03.2014, Accepted: 25.07.2014

INTRODUCTION unilateral, repeated alternatively, and occurs usually

along with vomiting, nausea, photophobia, and
Migraine headaches are often a debilitating condition phonophobia.[1] Although the prevalence of migraine
which affects millions of people throughout the world. may be slightly different in different societies, it is
Migraine is a serious neurological disorder which is strikingly higher in females than in males and its ratio
is changing from 2:1 to 3:1, especially between the ages
Access this article online of 25 and 55 years.[2] Studies show that migraine can
Quick Response Code: not only be a risk factor of cardiovascular diseases
Website: and ischemic stroke, but it also has a relationship
www.advbiores.net with brain structural injuries and lesions like those
of brain circulation which lead to brain stroke.[3,4]
DOI: The majority of the studies show a kind of depression
10.4103/2277-9175.172995 in women migraine sufferers.[5] Food intolerance
and allergies, [6] structural problems, [7] hormonal
Copyright: © 2015 Boroujeni. This is an open‑access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduc‑
tion in any medium, provided the original author and source are credited.

How to cite this article: Boroujeni MZ, Marandi SM, Esfarjani F, Sattar M, Shaygannejad V, Javanmard SH. Yoga intervention on blood NO in female migraineurs.
Adv Biomed Res 2015;4:259.

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Zamani, et al.: Yoga intervention on blood NO

imbalances,[8] low blood sugar,[9] hard work,[10] brain subjects were informed that we were conducting a
tumors,[11] cerebrovascular hypoxia caused by reduced study of migraine treatment that was intended to
blood supply to the brain vessels,[12] depression,[13] reduce its negative effects on their personal, family,
high blood pressure,[14] neck trauma,[15] and many and social lives. Evaluations (with diagnosis) were
other unmentioned factors can cause migraine or performed by neurologists, and detailed case histories
make it more severe. Based on genetic evidences, it were taken by trained interviewers. The criteria for
is strongly believed that changes in blood vessels, selection of the subjects among the other migraineurs
disruption in endocrine system, and some micro were according to the definition of the International
metabolism can create a dysfunction in neurovascular Headache Society (IHS).[23] All the patients were in
function and cause cortex depression. [16,17] There menstrual age and have not had any experience of
are important mediators like the neuropeptides yoga training before. They also were under a same
substance P, calcitonin gene-related peptide (CGRP), pharmacological treatment and did not have any other
and vasoactive intestinal polypeptide (VIP), which lead exercise during the treatment period.
to a severe impairment in cerebral cortex function,
vessel expansion, and cause migraine or primary Eighty-five patients agreed to participate in the
headaches. [18] At that time, an electrical current program. Forty-three patients were excluded.
moves to the frontal lobe at a certain speed and causes Seventeen of them were excluded as they were
headache.[19] receiving different medical treatments. Seven
migraineurs were crossed out due to coexisting
Nitric oxide (NO) is an endothelium-derived relaxing diseases and nineteen patients did not meet the
factor (EDRF)-like substance which plays a key role in inclusion criteria. The rest of the migraine patients
regulating brain metabolism and cerebral circulation, were accidently divided into two groups (yoga group
and vascular smooth muscle function.[20] It is one of the and control group). A computer-generated random
responsible factors for cerebral blood flow modulation number list allocated patients to either case or control
in response to changes in oxygen gas and carbon group. In the control group, four patients left the
dioxide; hence, it is not unlikely that impairment in NO intervention because of worsening of their symptoms,
production causes several pathological conditions of two refused to participate in blood test, and one left
brain such as migraine, Alzheimer’s and Huntington’s, the program because our exercise time overlapped
and even inflammation.[21] Repeated exercise helps with her work schedule. In the experimental group,
NO to be kept in higher levels in the blood between one patient refused to continue because of drugs’
exercise sessions. However, in apparent contrast, side effects and two patients left the treatment due
some surveys have suggested that some kinds of to unknown reason. Thirty-two patients were finally
exercise may intensify migraine attacks due to excess analyzed. The steps are shown in Figure 1.
NO production.[22] Yoga, as a Complementary and
Alternative Medicine (CAM), is a popular alternative Procedure
form of mind-body therapy. Due to higher prevalence Patients were informed of the details of the treatment
of migraine in women and the popularity of yoga plan. The initial examination and medication were
among them, in this survey, the effects of this kind of performed by a neurologist who confirmed the
exercise on the frequency, severity, and duration of diagnosis of migraine. Personal information, family
headache, the impact of headache on patient’s life, and headache history, frequency and duration of headache,
the blood NO levels of female patients with migraine and medication were recorded.
have been studied.
Severity of headache
Study design and setting Visual Analogue Scale (VAS) was also used to measure
This study was a randomized, controlled trial the severity of headache pain. The VAS has been
conducted at the Physiology Research Center, shown to be reliable and valid for measuring pain. It
University of Medical Sciences, Isfahan, Iran, from is also applied in different clinical surveys including
April to June 2012. The Ethical Committee of Isfahan migraine, low back pain, colon cancer, etc.[24-27] Each
University of Medical Sciences approved the project subject expresses her headache intensity on a 100-mm
and the protocol. Filled out the consent form before VAS that ranges from no pain (0) to very severe pain.[28]
baseline assessment and randomization.
The headache impact test
MATERIALS AND METHODS The headache impact test (HIT-6) was developed
to measure a wide range of factors contributing to
Patients were selected from a Neurological Institute the burden of headache, and it has shown utility for
under the supervision of a neurologist. All potential producing quantitative and pertinent information on

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Zamani, et al.: Yoga intervention on blood NO

Figure 1: Flow diagram of patient participation through the study

the impact of headache. The HIT-6 consists of six items: Serum NOx and nitrate measurement
Pain, social functioning, role functioning, vitality, For measuring the total nitrite (NOx) concentration
cognitive functioning, and psychological distress. in serum samples, total NO/nitrite/nitrate assay kit
The patient answers each of the six related questions (R & D Systems) was used which is based on the
with one of the following five responses: “Never”, enzymatic conversion of nitrate to nitrite by nitrate
“rarely”, “sometimes”, “very often”, and “always”. reductase. The reaction is followed by colorimetric
These responses are summed to produce a total HIT- detection of nitrite as an azo dye product of the Griess
6 score that ranges from 36 to 78, where a higher reaction. Briefly, serum samples were added into wells
score indicates a greater impact of headache on the (96-well enzymatic assay plate). Then equal volume of
daily life of the respondent. Scores can be interpreted NADH and dilute nitrate reductase were added to all
using four groupings that demonstrate the severity wells. The samples were incubated for 30 min at 37°C.
of impact of headache on the patient’s life. Extensive At the end of this step, nitrate in the samples gets
testing has shown the HIT-6 to be highly reliable and reduced to nitrite. Then the concentration of nitrite in
the samples was measured as mentioned above. For
internally consistent, and it has been translated into
determining the nitrate concentration in the sample,
various languages. The HIT-6 also exhibits excellent
the endogenous nitrite concentration was subtracted
accessibility and ease of use. Although HIT-6 is a very
from the NOx concentration.[30]
promising instrument, little data exists for comparing
HIT-6 scores with the real amount of disability, which Patients were randomly divided into two groups (yoga
would help in interpreting the results when creating and control groups). The control group received only
a management plan.[29] medication for 12 weeks and the yoga group was placed
in a yoga training program that consisted of three
Serum nitrite measurement
sessions per week (each session 75 min) in addition
The level of serum nitrite (stable NO metabolite) to the same medical treatment. During 3 months,
was measured using a colorimetric assay kit (R&D the control group was under the supervision of a
Systems, Minneapolis, MN, USA) that involves neurologist, medically and mentally. Yoga program was
the Griess reaction. Briefly, serum was added into chosen from Hatha yoga Pradipika. It included asanas
wells (96-well enzymatic assay plate). Sulfanilamide (yoga movements), pranayama (breathing exercises),
solution was added to all experimental samples, and shavasanas (relaxation). Asanas largely dealt
and after incubation, N-1-naphtylethylenediamine with the positions related to head and neck, although
dihydrochloride solution was added. Then, the lower extremity, arms, and shoulder exercises were
absorbance was measured using a microreader at also involved. Eye-related exercises, pavanmoktasana,
540 nm wavelength. The sample’s nitrite concentration pre-pranayama and pranayama, positions in lying,
was determined on comparing it to a nitrite standard sitting, and standing status, palming, Neti exercises,
reference curve. The detection limit was 0.25 µM and Shavasana were the kinds of exercises which
nitrite. were done under the supervision of a trainer. Surya

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Zamani, et al.: Yoga intervention on blood NO

namaskar was another part of the program, which mass index (BMI) in the yoga group was 66.8 ± 4.47 and
includes 12 positions itself, and it is mainly used for in the control group was 63.8 ± 6.19. When comparing
warm up, stretch, strength, and increasing flexibility. yoga and control groups after 12 weeks, the results
The protocol details are given in Table 1. showed a reduction in headache severity, frequency,
and headache impact on patients’ lives after the
Blood test was performed for all patients in the intervention in the yoga group [Figures 2-4]; however,
physiology research center at Isfahan Faculty of the changes in the control group were not significant.
Medicine between 8 a.m. and 10 a.m. in a fasting Duration of headache also reduced after 12 weeks in
condition. In the first session of exercises, patients the yoga group, but the results were not significant
were asked to mark their headache frequency during [Figure 5]. A non-significant increase was seen in blood
these 3 months in a table to which they were given. NO level in both groups after treatment [Figure 6].
The mean, standard deviation, and independent t-test
Statistical analysis and other results which are related to this study are
All statistical analyses were performed using SPSS shown in Table 2.
for Windows version 16.0. All data were normally
distributed and presented as mean ± SD. Independent DISCUSSION
t-test was used to compare the mean differences
between groups before and after training. Differences The aim of this research was to investigate
of P ≤ 0.01 were considered significant for all the effectiveness of yoga-based intervention on
statistical analyses. migraine headache and endothelial dysfunction.
Although the reduction in duration of headache
RESULTS was not significant in this study, yoga was found
to have a beneficial effect on various migraine
The mean age was 35.4 ± 7.9 years in the exercise group parameters (frequency, intensity, duration of attack,
and 34.9 ± 8.37 years in the control group. The body medication score, and the nature of the pain).[31,32]

Table 1: Details of selected yoga exercises during 3 months

Exercises Effects on body
Eye-related exercises Stimulates the nerves of the eye, produces alpha waves in the brain, and calms the mind and body down
Backward bending exercises Give calmness to the related muscles with a direct effect on the neck and lumbar parasympathetic nervous system
First pavanmoktasana Rheumatism anti-locker and is the most important method for mind confliction, especially in the area of wrist
and ankle. This is the most important method to release blocked energies in the body
Second pavanmoktasana Carminative. Non-normative nutrition, lack of proper function in digestive system, and other causes related to
these disorders, blocks energy in this area, because the concentration of this energy creates a discomfort in head
and neck that can lead to headache. Yoga can affect beneficially by removing negative energy.
Third pavanmoktasana Anti-locker includes 12 main asanas. Regulates hormones and body energy
Pre-pranayama yoga Increases respiratory volume along with serratus muscle stretching, stimulates the nerves in the region, the alpha
wave production in the brain, and causes tranquility
Standing–sitting and lying Stretches vertebras, releases blocked energy of the region, and prevents muscle spasm and pain
out screw position
Palming Causes facial muscles and eyes getting relaxed, makes relaxation deeper, defeats nervous tension, gives vitality
to the skin and eyes, cools the brain down, and helps in depression, stress, and anxiety
Neti exercises Helps to prevent infection, asthma, bronchitis, chronic pain caused by sinusitis, and chronic diseases,
in addition to clearing the facial area. This is one of the most effective methods in treating migraine
Shavasana or relaxation Done at the end of one session. Different senses are reinforced in different sessions. Auditory sense is reinforced
by listening to different sounds in the environment. Touching sense is reinforced by palming, feeling the skin, face
and body limbs. The sense of smell is reinforced by movement of air through the nose and diagnoses the odors.
Tasting sense also is reinforced by imaging basal tastes.

Table 2: Mean ± SD of the results before and after intervention in the study groups
Groups variable Yoga group (n = 15) Control group (n =15) Significance t
Pre-test Mean ± SD Post-test Mean ± SD Pre-test Mean ± SD Post-test Mean ± SD value
Severity of headache 7.67±1.8 5.27±2.09 6.64±2.01 6.73±2.41 0.002* −3.561
Headache frequency 5.07±4.77 2.27±1.49 3.72±2.61 5.09±2.98 0.007* −2.962
Duration of headache (days) 1.67 ±.48 1.4±0.51 2.09±0.07 1.82±0.87 0.98 0.025
Headache impact (HIT-6) 64±10.5 55.67±8.15 64.18±6.4 64.36±5.85 0.001* −3.741
Blood NO level (µM) 2.34±0.65 2.55±1.63 1.91±0.13 2.02±0.44 0.84 0.2
*Significant difference between two groups, P < 0.001

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Zamani, et al.: Yoga intervention on blood NO

Figure 2: Severity of headache before and after yoga training between Figure 3: Frequency of headache before and after yoga training
yoga and control groups between yoga and control groups

Figure 4: Impact of headache before and after yoga training between Figure 5: During of Headache before and after yoga training between
yoga and control groups yoga and control groups

For a migraine sufferer, there is a sudden shift in the

blood vessels and they abruptly dilate, increasing
the blood flow to the head. This occurrence results in
the severe pain of the migraine episode. If patients
can somehow keep their body’s nervous system more
relaxed daily, the initial narrowing of the blood
vessels that predisposes someone to a migraine
might be eliminated and the chance of the migraine
is minimized.[33-35]

Many surveys and experiments have shown that

aerobic exercise significantly leads to cardiovascular
fitness improvement, regulates vessel tone regulation,
and decreases migraine attacks.[36]
Figure 6: Nitric Oxide before and after yoga training between yoga
and control groups Yoga also affect psychological parameters like
anxiety and depression which are the causes of the
One contemporary theory of how migraines occur headache impact on the life of migraine sufferers.[37]
states that the arteries that feed the brain narrow Yogic breathing is useful for balancing the autonomic
temporarily due to a variety of factors, with stress nervous system and has a special influence on
and muscular tension being the two common ones. psychological and stress-related disorders.[34] Certain

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Zamani, et al.: Yoga intervention on blood NO

mechanisms which describe a state of calm alertness pertaining to grasping something about the nature of
include increased parasympathetic drive, calming of the self at rest.
stress response systems, neuroendocrine release of
hormones, and thalamic generators.[32] CONCLUSION

If done correctly, yoga can significantly release It is too early to recommend yoga for treatment or
tensions accumulated around the areas of pain prevention of migraines. However, there is some
(forehead, temples, neck, and shoulders) and also evidence showing that taking up yoga could enhance
loosen the tight muscles, especially in the back and overall health. It controls the negative impacts of
neck. Since tight muscles can trigger headaches, yoga migraine and helps patients lead a healthy lifestyle,
could potentially assist.[38] be more effective and live happier. It also eliminates
the modifiable risk factors for the other diseases.[25]
Nasal water cleansing (Kriya-Jalaneti) which is
followed by forced exhalation (Kapalbhanti) goes ACKNOWLEDGMENT
beyond stimulating and regulating the nerve tone,
This study was sponsored by Isfahan University of Medical
glands, and organs of the entire nasal and cranial
Sciences and Department of Exercise Physiology, University
area, including the eyes, sinuses, ears, and cranium.[39] of Isfahan.

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