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Pain tolerance and cardiorespiratory fitness in women with dysmenorrhea

ABSTRACT

BACKGROUND AND OBJECTIVES:

Hormonal changes are known to affect quality of life of women and may interfere in pain tolerance and cardiorespiratory exercise performance. Thus, the aim of this study was to evaluate and compare pressure pain tolerance threshold and cardiorespiratory fitness in women in luteal and follicular phases of the menstrual cycle.

METHODS:

University students aged 18-30 years old with a regular menstrual cycle were evaluated for cardiorespiratory fitness (ergospirometry), pain perception through the visual analog scale and pressure pain tolerance (algometry).

RESULTS:

When evaluated in follicular phase, the 13 participants exhibited a significant increase (p<0.001) in pain perception. Follicular phase also resulted in a significant reduction in pressure pain tolerance in all sites evaluated (p<0.05). At rest, follicular phase resulted in a significant increase (p<0.05) in systolic and diastolic blood pressure, but no effect was observed in heart rate. At peak exercise, follicular phase caused a significant reduction (p<0.05) in heart rate and peak VO2, without significantly affecting speed, test duration and indicators of metabolism efficiency.

CONCLUSION:

Healthy women with dysmenorrhea show higher pain perception in follicular phase, which results in increased pain sensitivity and prejudice in hemodynamic aspects at rest and during exercise, as well as in cardiorespiratory fitness, without significant alterations in metabolism.

Keywords:
Dysmenorrhea; Menstrual cycle; Pain threshold; Physical fitness

INTRODUCTION

During most part of life, women deal with hormonal cycles that generally occur at every 28 days, from menarche to menopause, regulated by the pituitary gland and ovaries through gonadotropic secretions11 Melegario SM, Simão R, Vale RG, Batista LA, Novaes JS. A influência do ciclo menstrual na flexibilidade em praticantes de ginástica de academia. Rev Bras Med Esporte. 2006;12(3):125-8.. These hormones affect psychological aspects, as well as musculoskeletal sensitivity and quality of life of women22 Soares CN, Zitek B. Reproductive hormone sensitivity and risk for depression across the female life cycle: a continuum of vulnerability? Psychiatry Neurosci. 2008;33(4):331-43..

A regular menstrual cycle can be divided into three consecutive phases: follicular (which starts on the first day of menstruation), ovulatory (which can last up to 3 days), and luteal (from the end of ovulation to the beginning of a new menstrual flow. There are reports of clinical conditions related to these phases, such as insulin resistance, supraventricular tachycardia, Raynaud syndrome, sleeping disorders and migraine33 Farage MA, Neill S, MacLean AB. Physiological changes associated with the menstrual cycle: a review. Obstet Gynecol Surv. 2009;64(1):58-72..

Although regular exercise has been reported to reduce dysmenorrhea and physical and psychological symptoms44 Jahromi MK, Gaeini A, Rahimi MZ. Influence of a physical fitness course on menstrual cycle characteristics. Gynecol Endocrinol. 2008;24(11):659-62., changes in cardiorespiratory fitness and function may also occur, most likely in response to changes in body temperature and metabolism, accompanying hormonal curves and influencing aerobic performance and muscle strength33 Farage MA, Neill S, MacLean AB. Physiological changes associated with the menstrual cycle: a review. Obstet Gynecol Surv. 2009;64(1):58-72.,55 Janse de Jonge XA, Boot CR, Thom JM, Ruell PA, Thompson MW. The influence of menstrual cycle phase on skeletal muscle contractile characteristics in humans. J Physiol. 2001;530(Pt 1):161-6.. Regarding cardiorespiratory fitness, due to the growing rate of estrogen and higher secretion of noradrenalin in luteal phase, a significant improvement in exercise performance might be observed. However, in premenstrual stage performance exhibits a noticeable reduction related to the increase in progesterone levels66 Iacovides S, Avidon I, Baker FC. Does pain vary across the menstrual cycle? A review. Eur J Pain. 2015;19(10):1389-405..

Chantler, Mitchell and Fuller77 Chantler I, Mitchell D, Fuller A. Diclofenac potassium attenuates dysmenorrhea and restores exercise performance in women with primary dysmenorrhea. J Pain. 2009;10(2):191-200., found a significant reduction in time of treadmill test and in heart rate of women with dysmenorrhea exercising at follicular phase. Furthermore, there are also studies that could not identify any changes in flexibility, muscle strength, endurance, aerobic performance and reaction time over the menstrual cycle11 Melegario SM, Simão R, Vale RG, Batista LA, Novaes JS. A influência do ciclo menstrual na flexibilidade em praticantes de ginástica de academia. Rev Bras Med Esporte. 2006;12(3):125-8.,88 Fridén C, Hirschberg AL, Saartok T. Muscle strength and endurance do not significantly vary across 3 phases of the menstrual cycle in moderately active premenopausal women. Clin J Sport Med. 2003;13(4):238-41.,99 Wiecek M, Szymura J, Maciejczyk M, Cempla J, Szygula Z. Effect of sex and menstrual cycle in women on starting speed, anaerobic endurance and muscle power. Acta Physiol Hung. 2016;103(1):127-32.. These controversies justify the expansion of information about cardiorespiratory fitness along the menstrual cycle, especially with regard to determinants of cardiorespiratory performance: maximal oxygen uptake (VO2 max), ventilation (VE), ventilatory equivalent of oxygen (VE/VO2) and carbon dioxide (VE/VCO2), anaerobic threshold (AT) and respiratory compensation point (RCP). To the best of our knowledge no study so far has explored this issue.

When it comes to pain, it is more pronounced when estrogen levels fall1010 Colangelo K, Haig S, Bonner A, Zelenietz C, Pope J. Self-reported flaring varies during the menstrual cycle in systemic lupus erythematosus compared with rheumatoid arthritis and fibromyalgia. Rheumatology (Oxford). 2011;50(4):703-8.. However, a recent review66 Iacovides S, Avidon I, Baker FC. Does pain vary across the menstrual cycle? A review. Eur J Pain. 2015;19(10):1389-405. points out that most recent studies show no changes in sensitivity to pain during the phases of the menstrual cycle, yet the authors report that, as there is still no consensus on the influence of the cycle on the sensation of pain in healthy women, more studies on this topic are necessary.

Therefore, the aim of this study was to evaluate and compare pressure pain tolerance threshold and cardiorespiratory fitness in women with dysmenorrhea in luteal and follicular phases of the menstrual cycle.

METHODS

This transversal observational study, female university health students (nursing, physical therapy, nutrition and physical education) were recruited through public announcement in the classrooms of health courses at a private university in the city of São Paulo (Brazil). The ones who agreed to participate (n=21) were invited to attend at the Laboratory of Exercise Physiology, where more instructions about the research protocol were provided. Inclusion criteria were ageing between 18 to 30 years old, having a regular menstrual cycle (between 28 and 32 days)33 Farage MA, Neill S, MacLean AB. Physiological changes associated with the menstrual cycle: a review. Obstet Gynecol Surv. 2009;64(1):58-72. and dysmenorrhea complaint. Students in use of hormonal contraceptives were excluded from the study, as well as current smokers, the ones who were in use of analgesic drugs, pregnant women or the ones who had already had babies, the ones with a history of uterine diseases and the ones who presented motor disabilities or did not perform one or more tests.

After receiving instructions on the research procedures, participants gave informed written participation consent, according to Declaration of Helsinki and Resolution 466/12 from the Brazilian Health Council.

Participants were assessed for anthropometry and body composition at their first visit to the Exercise Physiology Laboratory, where all study evaluations occurred. Height was measured with an appropriate stadiometer, and body weight was assessed in a digital scale with minimum possible clothes. Body composition was assessed by tetrapolar bioelectrical impedance, after 10 minutes of rest. The data collection team was composed by an exercise physiologist and a physical therapist.

All further assessments were conducted in two specific moments of the menstrual cycle11 Melegario SM, Simão R, Vale RG, Batista LA, Novaes JS. A influência do ciclo menstrual na flexibilidade em praticantes de ginástica de academia. Rev Bras Med Esporte. 2006;12(3):125-8.,33 Farage MA, Neill S, MacLean AB. Physiological changes associated with the menstrual cycle: a review. Obstet Gynecol Surv. 2009;64(1):58-72.: premenstrual or luteal phase (10 to 15 days before menstruation) and menstrual or follicular phase (between the first and third day of menstruation).

Pain perception

Data regarding pain intensity were collected by the visual analog scale (VAS). VAS consists of a straight line of 10cm that has “zero” (no pain) in one extremity, and “10” (maximal pain) in the other. Every participant was asked to mark a cross on the line indicating her discomfort level. The closest to zero, the less the level of perceived pain, and the closest to 10, the worse perceived pain was.

Pressure pain tolerance threshold (PPT) corresponds to the amount of pressure an individual can tolerate in a given site, measured in pounds by algometry (JTech Medical, Salt Lake City, UT, USA). Reliability of this test has already been demonstrated1111 Ylinen J, Nykänen M, Kautiainen H, Häkkinen A. Evaluation of repeatability of pressure algometry on the neck muscles for clinical use. Man Ther. 2007;12(2):192-7.. Pressure was applied at a 90° angle (between the stimulation surface and the stimulated point) with a constant speed of 1kg/s. Volunteers were evaluated by the same examiner and equipment. The test was interrupted once the volunteer indicated the onset of pain, and the final amount of force applied was recorded. PPT was assessed bilaterally at the muscles vastus medialis, vastus lateralis, gluteus maximus, gluteus medius, iliopsoas, tibialis anterior, lumbar paraspinals, lumbar quadrate, pectoralis major and trapezius, as well as at the supraspinous ligaments between L4-S11212 Imamura M, Chen J, Matsubayashi SR, Targino RA, Alfieri FM, Bueno DK, Hsing WT. Changes in pressure pain threshold in patients with chronic nonspecific low back pain. Spine. 2013;38(24):2098-107.,1313 Imamura M, Alfieri FM, Filippo TR, Battistella LR. Pressure pain thresholds in patients with chronic nonspecific low back pain. J Back Musculoskelet Rehabil. 2016;29(2):327-36..

Cardiorespiratory fitness was assessed by a ramp protocol in a breath-by-breath gas analysis system (Cortex Biophysik Metalyzer 3B, Stationary CPX System, Leipzig, Germany). The test was conducted in a treadmill with adjustable incline and speed (Albatroz VT2500, Vitally, São Paulo, Brazil). Data were collected and analyzed by a specific software (Cortex Biophysik Meta Soft CPX testing software, Leipzig, Germany).

Before testing, volunteers had their resting heart rate and blood pressure assessed, after 15 minutes of rest, with a heart rate monitor and a calibrated sphygmomanometer, respectively.

All participants were familiarized with the exercise of walking/running on a treadmill to determine the maximum comfortable cadence before testing. The actual test started with a speed of 3km/h and was increased by 0.5km/h at every 30 seconds, so that after 3 minutes test speed was reached. After that, the progressive ramp protocol began, with increasing incline of 1% at every 60s until the voluntary requested interruption (between 8 and 12 minutes).

The effort was considered maximal when three of the five following criteria were reached1414 Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF, et al. Clinician's Guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation. 2010;122(2):191-225.: 1) heart rate (HR) equal to or higher than 95% of maximum predicted heart rate, 2) ventilation exceeding 60% of maximum predicted voluntary ventilation (MVV), 3) respiratory quotient (RQ) equal to or higher than 1.10, 4) evidence of respiratory compensation point, and 5) presence of plateau of oxygen consumption (VO2), i.e., increased effort without subsequent increase in VO2.

After testing, the participant walked at a speed that allowed her HR to reach 120 bpm or less. Maximal predicted heart rate for age was calculated as follows: 208 - 0.7 x age1515 American College of Sports Medicine (ACSM). Guidelines for Exercise Testing and Prescription. 9th ed. Philadelphia, USA: Wolters Kluwer-Lippincott Williams & Wilkins; 2014.. Forced expiratory volume in the first second (FEV1) was calculated by the following equation1616 Pereira CC, Jansen JM, Barreto SSM. Espirometria. Diretrizes para testes de função pulmonar. J Bras Pneumol. 2002;28(3):S1-82.: FEV1 (liters) = 0.0309 x height (cm) - 0.0201 x age (years) - 1,405. The expected MVV was calculated as follows1616 Pereira CC, Jansen JM, Barreto SSM. Espirometria. Diretrizes para testes de função pulmonar. J Bras Pneumol. 2002;28(3):S1-82.: 37.5 x FEV1 +15.8.

Ventilatory and metabolic parameters (VO2, HR and RQ)1414 Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF, et al. Clinician's Guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation. 2010;122(2):191-225.,1717 Higa MN, Silva E, Neves VF, Catai AM, Gallo L Jr, Silva de Sá MF. Comparison of anaerobic threshold determined by visual and mathematical methods in healthy women. Braz J Med Biol Res 2007;40(4):501-8.,1818 Mezzani A, Agostoni P, Cohen-Solal A, Corrà U, Jegier A, Kouidi E, et al. Standards for the use of cardiopulmonary exercise testing for the functional evaluation of cardiac patients: a report from the Exercise Physiology Section of the European Association for Cardiovascular Prevention and Rehabilitation. Eur J Cardiovasc Prev Rehabil. 2009;16(3):249-67. were determined at AT, RCP and at the highest VO2 observed in the last 30 seconds of exercise (peak VO2). Ventilatory equivalent of oxygen (VE/VO2) and carbon dioxide (VE/VCO2), as well as oxygen pulse were determined only at peak VO2. The respiratory exchange ratio (RER) represents the relationship between VCO2 and VO21414 Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF, et al. Clinician's Guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation. 2010;122(2):191-225., and oxygen pulse (O2 pulse) is the relationship between VO2 and HR1919 Wasserman K, Hansen JE, Sue DY, Stringer WW, Whipp BJ. Principles of exercise testing and interpretation: including pathophysiology and clinical applications. Philadelphia: Lippincott Williams & Wilkins; 1999. 206p.. VE/VO2 and VE/VCO2 are ventilatory efficiency indicators and O2 pulse is an indicative of left ventricular ejection.

This study was approved by the local Ethics Committee (CAAE 43429215.9.0000.5377)

Data analysis

Data were analyzed using the statistical package GraphPad Prism version 6.0 for Windows (www.graphpad.com). Results were expressed as means±standard deviations. Comparisons between luteal and follicular phases were performed by Student’s t test. The established significance level was 5% (p<0.05).

RESULTS

Out of the 21 women initially enrolled in the study, 8 were excluded from the sample for not attending the assessments or for taking analgesic drugs. Thus, the final sample of this study was composed by 13 women with dysmenorrhea complaint. Most of them (77%) presented adequate BMI, but less than half (46%) exhibited adequate adiposity. Body water content and angle of phase were adequate in 92% of them (between 41% and 60% and between 5.3º and 10º, respectively), as shown in table 1.

Table 1
General characteristics of the sample (n=13)

Results of pain perception and pressure pain tolerance (algometry) are described in table 2. When evaluated in follicular phase, participants exhibited a significant increase (p<0.001) in pain perception (assessed by VAS), and correlation between VAS in luteal and follicular phases showed moderate association (r=0.58, p<0.001). Also, follicular phase resulted in a significant reduction in pressure pain tolerance in all sites evaluated, indicating increase in pain sensitivity (p<0.05).

Table 2
Pressure pain tolerance threshold in muscles and ligaments evaluated (n=13)

The impact of follicular phase on several metabolic and cardiorespiratory parameters is shown in table 3. At rest, follicular phase resulted in a significant increase (p<0.05) of 8mmHg in systolic and diastolic blood pressure (BP), but no effect was observed in HR.

Table 3
Hemodynamic, ergospirometry and metabolic parameters of women in luteal and follicular phases of the menstrual cycle

No effects in ergospirometry parameters evaluated at AT (first ventilatory threshold) were observed in follicular phase when compared to luteal phase. Nonetheless, at RCP (second ventilatory threshold), parameters occurred sooner at follicular phase, but statistical significance was observed only in VO2 and VO2 relative to predicted values (p<0.05).

Finally, at peak exercise, follicular phase caused a significant reduction (p<0.05) in HR (4%), in HR relative to predicted (3 percentage points), peak VO2 (13%) and VO2 relative to predicted (8 percentage points), without significantly affecting speed, test duration, RQ and the indicators of ventilatory efficiency (VE/VO2 e VE/VCO2).

DISCUSSION

It is known that pain tolerance threshold differs in luteal and follicular phases, and that women bear less pressure pain at different points of the body during follicular phase2020 de Tommaso M. Pain perception during menstrual cycle. Curr Pain Headache Rep. 2011;15(5):400-6.. This phenomenon was identified in this study. Women from our sample bore on average, 31% less pressure at the 16 points assessed by algometry. Moreover, although several studies have indicated losses in functional capacity due to physical pain in follicular phase, the present study provides unprecedented data of cardiorespiratory and metabolic parameters obtained by ergospirometry.

Although the exact mechanisms are still unclear, female gonadal hormones interact with nociceptive processes at multiple levels of the peripheral and central nervous system, and variations in hormonal levels are associated with variations in pain experience66 Iacovides S, Avidon I, Baker FC. Does pain vary across the menstrual cycle? A review. Eur J Pain. 2015;19(10):1389-405.. Some hemodynamic determinants may also vary across the menstrual cycle, but they seem to be more influenced by epinephrine reactivity to stress than by sex hormones themselves2121 Gordon JL, Girdler SS. Mechanisms underlying hemodynamic and neuroendocrine stress reactivity at different phases of the menstrual cycle. Psychophysiology. 2014;51(4):309-18..

There are indications of a strong inverse correlation between level of pain (measured by VAS) and performance in a physical exercise on treadmill (r=0.69, p=0.01)77 Chantler I, Mitchell D, Fuller A. Diclofenac potassium attenuates dysmenorrhea and restores exercise performance in women with primary dysmenorrhea. J Pain. 2009;10(2):191-200.. Chantler, Mitchell and Fuller77 Chantler I, Mitchell D, Fuller A. Diclofenac potassium attenuates dysmenorrhea and restores exercise performance in women with primary dysmenorrhea. J Pain. 2009;10(2):191-200. et al.,77 Chantler I, Mitchell D, Fuller A. Diclofenac potassium attenuates dysmenorrhea and restores exercise performance in women with primary dysmenorrhea. J Pain. 2009;10(2):191-200.showed that women with dysmenorrhea pain exhibited significantly less time of test (Bruce protocol), decreased muscle strength (1 repetition maximal in leg press exercise at 45º) and more time to perform an exercise (bending down and getting up carrying a load) in comparison to controls (in use of anti-inflammatory drug). Oral administration of diclofenac potassium (50mg), a nonsteroidal anti-inflammatory drug (inhibitor of prostaglandins) suppressed these declines. Similar results were found in this study. Although there was no significant reduction in test duration, follicular phase resulted in losses ranging from 3.7 to 17.6% in the peak HR (3.9%), peak VO2 (12.8%), and VO2 at RCP (17.6%), without significant changes in AT, ventilatory efficiency (VE/VO2 and VE/VCO2) and rate of gas exchange (RQ). Together, these results indicate that the prejudice in cardiorespiratory fitness in follicular phase was related to oxygen consumption and ventilatory efficiency or changes in the use of energy substrates (RQ). Additionally, at rest, there was a significant increase in systolic and diastolic BP (7.4 and 11.8%, respectively), indicating a greater hemodynamic stress in follicular phase.

Pain is a very complex phenomenon and depends on cognition, emotion, environment and biological status of nerve structures2222 Tracey I, Mantyh PW. The cerebral signature for pain perception and its modulation. Neuron. 2007;55(3):377-91.. Although a limitation of this study might be the sample size, we sought to standardize the sample so it was as homogeneous as possible, as women from our study had little variation in age, were students of health courses (with similar cognition), inserted in the same university context and had no other possible bias such as contraceptive use and previous uterine diseases. However, dysmenorrhea was assessed by self-report, which does not allow full discrimination between primary or secondary dysmenorrhea.

If the menstrual cycle is relevant to the determination of painful symptoms, it must be considered as a factor influenced by women’s pain experience2020 de Tommaso M. Pain perception during menstrual cycle. Curr Pain Headache Rep. 2011;15(5):400-6.. In the present study, we sought to evaluate this experience through dolorimetry. This type of evaluation, using a digital algometer, is considered a gold standard for the measurement of pressure pain sensitivity2323 Egloff N, Klingler N, von Känel R, Cámara RJ, Curatolo M, Wegmann B, et al. Algometry with a clothes peg compared to an electronic pressure algometer: a randomized cross-sectional study in pain patients. BMC Musculoskelet Disord. 2011;12:174.. With respect to the sites assessed by algometry in this study, it was found that different areas of the pelvic region and muscles of the upper limbs and trunk were also negatively influenced in the follicular phase, revealing that hormonal changes affect pain tolerance in general. In a way, our results counteract a recent review pointing out that currently, most studies show that menstrual cycle has no effect on pain perception in healthy women66 Iacovides S, Avidon I, Baker FC. Does pain vary across the menstrual cycle? A review. Eur J Pain. 2015;19(10):1389-405.. However, unravelling the present findings, the authors of the review study66 Iacovides S, Avidon I, Baker FC. Does pain vary across the menstrual cycle? A review. Eur J Pain. 2015;19(10):1389-405. acknowledge that hormonal interaction and pain perception are complex and not fully understood.

Adding to the findings of the influence of menstrual cycle on pain, cardiorespiratory capacity also presented worse results in follicular phase. Although a previous study has not found differences in other physical capacities such as flexibility11 Melegario SM, Simão R, Vale RG, Batista LA, Novaes JS. A influência do ciclo menstrual na flexibilidade em praticantes de ginástica de academia. Rev Bras Med Esporte. 2006;12(3):125-8., muscle strength and endurance88 Fridén C, Hirschberg AL, Saartok T. Muscle strength and endurance do not significantly vary across 3 phases of the menstrual cycle in moderately active premenopausal women. Clin J Sport Med. 2003;13(4):238-41., anaerobic performance, and walking speed99 Wiecek M, Szymura J, Maciejczyk M, Cempla J, Szygula Z. Effect of sex and menstrual cycle in women on starting speed, anaerobic endurance and muscle power. Acta Physiol Hung. 2016;103(1):127-32., this study revealed that, with respect to cardiorespiratory fitness, evaluated by a progressive maximal cardiopulmonary exercise test, several parameters are negatively affected by pain.

Reduction in exercise performance associated to increased pain sensitivity may have important repercussions in daily living activities, social life and quality of life of women, as previously observed by authors who studied pain in follicular phase2424 Iacovides S, Avidon I, Bentley A, Baker FC. Reduced quality of life when experiencing menstrual pain in women with primary dysmenorrhea.Acta Obstet Gynecol Scand. 2014;93(2):213-7.,2525 Potur DC, Bilgin NC, Komurcu N. Prevalence of dysmenorrhea in university students in Turkey: effect on daily activities and evaluation of different pain management methods. Pain Manag Nurs. 2014;15(4):768-77.. Despite this finding, women should not avoid exercising in follicular phase, as exercise contributes to the reduction of dysmenorrhea symptoms44 Jahromi MK, Gaeini A, Rahimi MZ. Influence of a physical fitness course on menstrual cycle characteristics. Gynecol Endocrinol. 2008;24(11):659-62.. Health professionals must provide orientations to women with dysmenorrhea about these physiological transitory changes that accompany menstrual cycles, as well as when and how to use pharmacological and non-pharmacological methods of pain management, in order to minimize the negative impacts in their quality of life.

CONCLUSION

Healthy women with dysmenorrhea show higher pain perception in follicular phase, which results in increased pain sensitivity and prejudice in hemodynamic aspects at rest and during exercise, as well as in cardiorespiratory fitness, without significant alterations in metabolism.

  • Sponsoring sources: Taxa Capes/ppgeh/UPF.

REFERENCES

  • 1
    Melegario SM, Simão R, Vale RG, Batista LA, Novaes JS. A influência do ciclo menstrual na flexibilidade em praticantes de ginástica de academia. Rev Bras Med Esporte. 2006;12(3):125-8.
  • 2
    Soares CN, Zitek B. Reproductive hormone sensitivity and risk for depression across the female life cycle: a continuum of vulnerability? Psychiatry Neurosci. 2008;33(4):331-43.
  • 3
    Farage MA, Neill S, MacLean AB. Physiological changes associated with the menstrual cycle: a review. Obstet Gynecol Surv. 2009;64(1):58-72.
  • 4
    Jahromi MK, Gaeini A, Rahimi MZ. Influence of a physical fitness course on menstrual cycle characteristics. Gynecol Endocrinol. 2008;24(11):659-62.
  • 5
    Janse de Jonge XA, Boot CR, Thom JM, Ruell PA, Thompson MW. The influence of menstrual cycle phase on skeletal muscle contractile characteristics in humans. J Physiol. 2001;530(Pt 1):161-6.
  • 6
    Iacovides S, Avidon I, Baker FC. Does pain vary across the menstrual cycle? A review. Eur J Pain. 2015;19(10):1389-405.
  • 7
    Chantler I, Mitchell D, Fuller A. Diclofenac potassium attenuates dysmenorrhea and restores exercise performance in women with primary dysmenorrhea. J Pain. 2009;10(2):191-200.
  • 8
    Fridén C, Hirschberg AL, Saartok T. Muscle strength and endurance do not significantly vary across 3 phases of the menstrual cycle in moderately active premenopausal women. Clin J Sport Med. 2003;13(4):238-41.
  • 9
    Wiecek M, Szymura J, Maciejczyk M, Cempla J, Szygula Z. Effect of sex and menstrual cycle in women on starting speed, anaerobic endurance and muscle power. Acta Physiol Hung. 2016;103(1):127-32.
  • 10
    Colangelo K, Haig S, Bonner A, Zelenietz C, Pope J. Self-reported flaring varies during the menstrual cycle in systemic lupus erythematosus compared with rheumatoid arthritis and fibromyalgia. Rheumatology (Oxford). 2011;50(4):703-8.
  • 11
    Ylinen J, Nykänen M, Kautiainen H, Häkkinen A. Evaluation of repeatability of pressure algometry on the neck muscles for clinical use. Man Ther. 2007;12(2):192-7.
  • 12
    Imamura M, Chen J, Matsubayashi SR, Targino RA, Alfieri FM, Bueno DK, Hsing WT. Changes in pressure pain threshold in patients with chronic nonspecific low back pain. Spine. 2013;38(24):2098-107.
  • 13
    Imamura M, Alfieri FM, Filippo TR, Battistella LR. Pressure pain thresholds in patients with chronic nonspecific low back pain. J Back Musculoskelet Rehabil. 2016;29(2):327-36.
  • 14
    Balady GJ, Arena R, Sietsema K, Myers J, Coke L, Fletcher GF, et al. Clinician's Guide to cardiopulmonary exercise testing in adults: a scientific statement from the American Heart Association. Circulation. 2010;122(2):191-225.
  • 15
    American College of Sports Medicine (ACSM). Guidelines for Exercise Testing and Prescription. 9th ed. Philadelphia, USA: Wolters Kluwer-Lippincott Williams & Wilkins; 2014.
  • 16
    Pereira CC, Jansen JM, Barreto SSM. Espirometria. Diretrizes para testes de função pulmonar. J Bras Pneumol. 2002;28(3):S1-82.
  • 17
    Higa MN, Silva E, Neves VF, Catai AM, Gallo L Jr, Silva de Sá MF. Comparison of anaerobic threshold determined by visual and mathematical methods in healthy women. Braz J Med Biol Res 2007;40(4):501-8.
  • 18
    Mezzani A, Agostoni P, Cohen-Solal A, Corrà U, Jegier A, Kouidi E, et al. Standards for the use of cardiopulmonary exercise testing for the functional evaluation of cardiac patients: a report from the Exercise Physiology Section of the European Association for Cardiovascular Prevention and Rehabilitation. Eur J Cardiovasc Prev Rehabil. 2009;16(3):249-67.
  • 19
    Wasserman K, Hansen JE, Sue DY, Stringer WW, Whipp BJ. Principles of exercise testing and interpretation: including pathophysiology and clinical applications. Philadelphia: Lippincott Williams & Wilkins; 1999. 206p.
  • 20
    de Tommaso M. Pain perception during menstrual cycle. Curr Pain Headache Rep. 2011;15(5):400-6.
  • 21
    Gordon JL, Girdler SS. Mechanisms underlying hemodynamic and neuroendocrine stress reactivity at different phases of the menstrual cycle. Psychophysiology. 2014;51(4):309-18.
  • 22
    Tracey I, Mantyh PW. The cerebral signature for pain perception and its modulation. Neuron. 2007;55(3):377-91.
  • 23
    Egloff N, Klingler N, von Känel R, Cámara RJ, Curatolo M, Wegmann B, et al. Algometry with a clothes peg compared to an electronic pressure algometer: a randomized cross-sectional study in pain patients. BMC Musculoskelet Disord. 2011;12:174.
  • 24
    Iacovides S, Avidon I, Bentley A, Baker FC. Reduced quality of life when experiencing menstrual pain in women with primary dysmenorrhea.Acta Obstet Gynecol Scand. 2014;93(2):213-7.
  • 25
    Potur DC, Bilgin NC, Komurcu N. Prevalence of dysmenorrhea in university students in Turkey: effect on daily activities and evaluation of different pain management methods. Pain Manag Nurs. 2014;15(4):768-77.

Publication Dates

  • Publication in this collection
    Oct-Dec 2017

History

  • Received
    31 May 2017
  • Accepted
    01 Nov 2017
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