Advertisement

Prevalence and Risk Factors Associated with Primary Dysmenorrhea among Chinese Female University Students: A Cross-sectional Study

Open AccessPublished:September 17, 2019DOI:https://doi.org/10.1016/j.jpag.2019.09.004

      Abstract

      Study Objective

      To examine prevalence and risk factors associated with primary dysmenorrhea among Chinese female university students in Hunan province, China.

      Design

      A cross-sectional study.

      Setting

      Female university students in Changsha city, Hunan province, China.

      Participants

      Four thousand six hundred six female individuals selected using a multistage cluster random sampling method.

      Interventions

      A self-administered questionnaire, which included sociodemographic information, lifestyle habits, emotional characteristics, and menstruation pattern, was used to collect data.

      Main Outcome Measures

      Information about menarche, body mass index, cycle length and regularity, primary dysmenorrhea, physical exercise, depression, and anxiety.

      Results

      The prevalence of primary dysmenorrhea was 41.7% (1921/4606) among Chinese female university students. Multivariate binary logistic regression indicated that being a minority (odds ratio [OR], 1.335; 95% confidence interval [CI], 1.083-1.646), underweight (OR, 1.249; 95% CI, 1.08-1.42), annual household income less than 80,000 CNY (OR, 1.169; 95% CI, 1.018-1.342), maternal history of dysmenorrhea (OR, 2.553; 95% CI, 2.236-2.915), age at menarche younger than 12 years (OR, 1.161; 95% CI, 1.013-1.329), irregular menstrual cycle (OR, 1.216; 95% CI, 1.063-1.391), and skipping breakfast (OR, 1.294; 95% CI, 1.124-1.490) were associated risk factors of primary dysmenorrhea.

      Conclusion

      The prevalence of primary dysmenorrhea among Chinese university students is relatively high. Various risk factors were identified that associated with primary dysmenorrhea. More effort and attention should therefore be directed toward this health problem in China.

      Key Words

      Introduction

      Dysmenorrhea, which is the most common gynecological problem among adolescent girls and women of reproductive age,
      • Abd El-Mawgod M.M.
      • Alshaibany A.S.
      • Al-Anazi A.M.
      Epidemiology of dysmenorrhea among secondary-school students in Northern Saudi Arabia.
      can be classified as either primary or secondary dysmenorrhea. Primary dysmenorrhea (PD) refers to painful menses or cramps in the lower abdomen before and/or during menstruation without an identifiable organic pathology.
      • Iacovides S.
      • Avidon I.
      • Baker F.C.
      What we know about primary dysmenorrhea today: a critical review.
      In contrast, secondary dysmenorrhea refers to menstrual pain resulting from anatomic and/or evident pelvic pathology, such as endometriosis.
      • Osayande A.S.
      • Mehulic S.
      Diagnosis and initial management of dysmenorrhea.
      The onset of PD usually occurs in adolescence, at approximately 6-24 months after menarche.
      • Dawood M.Y.
      Primary dysmenorrhea: advances in pathogenesis and management.
      PD is characterized by painful cramping that lasts for 8-72 hours that is most severe during the first or second day of menstruation.
      • Ruoff G.
      • Lema M.
      Strategies in pain management: new and potential indications for COX-2 specific inhibitors.
      Typically, pain is frequently accompanied by symptoms such as dizziness, vomiting, fatigue, and insomnia.
      Because of the different definitions and the methods of assessment, studies conducted in menstruating women have shown that the prevalence of PD varies from 45% to 95%.
      • Iacovides S.
      • Avidon I.
      • Baker F.C.
      What we know about primary dysmenorrhea today: a critical review.
      Among the female university student population, the reported prevalence of PD was 85.7% in Saudi Arabia,
      • Rafique N.
      • Al-Sheikh M.H.
      Prevalence of primary dysmenorrhea and its relationship with body mass index.
      85.4% in Ethiopia,
      • Hailemeskel S.
      • Demissie A.
      • Assefa N.
      Primary dysmenorrhea magnitude, associated risk factors, and its effect on academic performance: evidence from female university students in Ethiopia.
      64.0% in Mexico,
      • Ortiz M.I.
      Primary dysmenorrhea among Mexican university students: prevalence, impact and treatment.
      and 89.10% in Iran.
      • Habibi N.
      • Huang M.S.
      • Gan W.Y.
      • et al.
      Prevalence of primary dysmenorrhea and factors associated with its intensity among undergraduate students: a cross-sectional study.
      As a debilitating condition for many women, dysmenorrhea is one of the leading causes of absenteeism from school or work, which has a negative effect on quality of life, daily living, work productivity, and academic activities.
      • Sharma A.
      • Taneja D.K.
      • Sharma P.
      • et al.
      Problems related to menstruation and their effect on daily routine of students of a medical college in Delhi, India.
      ,
      • Titilayo A.
      • Agunbiade O.M.
      • Banjo O.
      • et al.
      Menstrual discomfort and its influence on daily academic activities and psychosocial relationship among undergraduate female students in Nigeria.
      Therefore, this condition poses a huge public health and academic challenge because of its high prevalence, the broad population it affects, the costs of medications, and decreased productivity.
      Many studies in the current literature have shown that a range of risk factors might be associated with PD, including biological, psychological, social, and lifestyle factors. Biological factors might include earlier age at menarche, heavier menstrual flow, and family history of dysmenorrhea
      • Ortiz M.I.
      • Rangel-Flores E.
      • Carrillo-Alarcon L.C.
      • et al.
      Prevalence and impact of primary dysmenorrhea among Mexican high school students.
      ,
      • Zegeye D.T.
      • Megabiaw B.
      • Mulu A.
      Age at menarche and the menstrual pattern of secondary school adolescents in northwest Ethiopia.
      ; psychological factors include stress, anxiety, and depression
      • Dorn L.D.
      • Negriff S.
      • Huang B.
      • et al.
      Menstrual symptoms in adolescent girls: association with smoking, depressive symptoms, and anxiety.
      ; social factors include a lower level of social support
      • Faramarzi M.
      • Salmalian H.
      Association of psychologic and nonpsychologic factors with primary dysmenorrhea.
      ; and lifestyle factors include cigarette smoking and irregular diet.
      • Ju H.
      • Jones M.
      • Mishra G.
      The prevalence and risk factors of dysmenorrhea.
      However, until now, few studies have explored the prevalence and characteristics of PD among female university students in China. Furthermore, published studies that included a large sample size and that have identified a wide range of factors associated with PD in this population are also scarce.
      Therefore, the purpose of our current study was to investigate the prevalence of PD among Chinese female university students in Changsha City and to identify the risk factors associated with PD.

      Materials and Methods

      This was a cross-sectional study that was conducted in Changsha City of Hunan province in China from September 2017 to June 2018. This study was approved by the Ethics Committee of Xiangya School of Public Health of Central South University (XYGW-2017-16). Written informed consent was obtained from all participants.

       Sample Size

      Sample size was calculated using the following formula for cross-sectional studies:
      N=z1α/22p(1p)d2


      where Z1-α/2 = 1.96 when α = 0.05, p is the prevalence of PD among Chinese female university students (which was 60.5% according to a previous study
      • Na Z.
      • Yang L.
      • Bao-huan Z.
      • et al.
      Current status of primary dysmenorrhea and its relationship with lifestyle among female students in a college in Guangzhou City.
      ) and d is admissible error (which was 2% here). According to the formula, the theoretical sample size was 2525 students, which included an extra 10% to allow for subjects’ no response during the study.

       Study Population and Procedure

      To select a representative sample of female university students, a multistage cluster randomized sampling method was used. This was done in consideration that the Chinese university system has been classified into 3 categories: key university, general university, and vocational college. In addition, within each university or college there are many schools. Thus, in this sampling method, “cluster” was defined as school of a university or vocational college. Therefore, in the first stage, 1 key university (Central South University), 2 general universities (Changsha University and Hunan Women's University), and 2 vocational colleges (Changsha Health Vocational College and Changsha Social Work College) were randomly selected according to the scale of the 3-level universities. In the second stage, 4 schools of Central South University, 2 schools of Changsha University, 2 schools of Hunan Women's University, 1 school of Changsha Health Vocational College, and 1 school of Changsha Social Work College were randomly selected according to the students scale. In the third stage, all female students who were freshman to junior from each of the chosen schools were invited to participate in this study. All international students were excluded. The theoretical sample from the selected 10 schools was 4874 students. Of these, 135 were not in school during the investigation period and 133 refused to participate in this study. Finally, a total of 4606 female students participated in this study. Among them, 152 were excluded for indicating that they were diagnosed with gynecological diseases or secondary dysmenorrhea, and 26 were excluded for having incomplete data, leaving a total of 4428 female students for analysis.

       Data Collection

      All data were collected by trained research assistants from each class in approximately 30 minutes using a self-administered questionnaire designed in Chinese. It has 3 parts, the first part containing sociodemographic information of study participants. The second part was the lifestyle behaviour and emotional characteristics. The third part was about menstrual pattern and information. The questionnaire was distributed to every participant and collected on the same day to ensure confidentiality and prevent information contamination. The research assistants presented the completed questionnaires to the supervisors for verification. Finally, the principal investigator of each school checked the completion of data collection using a quality control from.
      Sociodemographic information, including age, ethnicity, education level of the father and mother, family size, and annual household income, was first collected. Moreover, ethnicity was classified into Han and minority. The minority groups included Tujia, Miao, Tibetan, Uyghur, Zhuang, Hui, Dong, Manchu, Mongolian, Yao, and others. Education level of each participant's father and mother were indicated on the basis of the following choices: primary school and below, middle school, and high school and above. Family size was determined according to the number of current residents in the family. Anthropometric data including height and weight were self-reported and recorded accurately by the interviewer. Body mass index (BMI) was calculated as weight in kilograms divided by the height in meters squared; according to their BMI, participants were subsequently classified into 3 groups
      • Chen C.
      • Lu F.C.
      The guidelines for prevention and control of overweight and obesity in Chinese adults.
      : underweight (<18.5), normal (18.5-24.0), and overweight or obese (≥24.0).
      Menstrual information including age at menarche, cycle regularity, maternal history of dysmenorrhea, and menstruation pain was also collected. Cycle regularity refers to a difference less than or equal to 8 days between 2 menstrual cycles. PD was identified on the basis of the questions, “Have you experienced one or more of menstrual cramps or abdominal pain during your menstruation for the last one year?” and, “Do you have the following diseases or symptoms?” Listed diseases in this regard included pelvic inflammation, endometriosis, adenomyosis, hysteromyoma, secondary dysmenorrhea, and other diseases. Students who reported having any of these listed diseases were excluded from this study. Participants who experienced 1 or more of menstrual cramps or abdominal pain had to answer additional questions, which included the intensity of pain, the moment at which pain is perceived, duration of dysmenorrhea, and the pain symptoms they experienced. The painful intensity of dysmenorrhea was assessed using the visual analogue scale (VAS). Scores from the VAS were categorized on a scale of 1-10 (1-3, mild; 4-7, moderate; 8-10, severe). Pain symptoms were assessed using the Cox menstrual symptom scale, which has high validity and reliability in the Chinese female population (Cronbach α = 0.833).
      • Ma Y.
      • Ma H.
      • Chen S.
      • et al.
      The validity and reliability of the Cox menstrual symptom scale of Chinese version.
      Pain symptoms included lower abdominal pain, dizziness, headache, nausea, vomiting, fatigue, diarrhea, insomnia, and irritability in this study.
      Lifestyle habits included smoking, alcohol drinking, caffeine consumption, physical exercise, daily sitting time, sleep duration, bedtime, and skipping breakfast. A smoker was defined as a woman who smoked at least 1 cigarette per day in the past 6 months. Alcohol drinking refers to drinking at least 1 glass of wine (approximately 250 mL) per month during the past 6 months. Caffeine consumption was determined as infrequent if intake of caffeine-containing foods (eg, coffee, tea, and chocolate) less than 3 times per week in the past month in the daily diet. Regular physical excise was defined as exercise 3 or more times each week for at least 30 minutes. Daily sitting time was self-reported and subsequently separated into 2 categories: (<8 hours and ≥8 hours). Sleep duration was used to classify the participants into 3 groups (<7 hours per night, 7-9 hours per night, and >9 hours per night) on the basis of the recommendations for the optimal amount of sleep for adolescents.
      • Hirshkowitz M.
      • Whiton K.
      • Albert S.M.
      • et al.
      National Sleep Foundation’s updated sleep duration recommendations: final report.
      In this study, participants who did not eat breakfast 1 or more times in the past week were considered breakfast skippers.
      • Mushtaq M.U.
      • Gull S.
      • Mushtaq K.
      • et al.
      Dietary behaviors, physical activity and sedentary lifestyle associated with overweight and obesity, and their socio-demographic correlates, among Pakistani primary school children.
      Emotional problems included depression symptoms and anxiety symptoms. Depression symptoms during the previous 2 weeks were assessed using the Chinese version of the Patient Health Questionnaire-9 (PHQ-9) scale. This scale has been shown to have high reliability and validity among Chinese populations.
      • Sun X.Y.
      • Li Y.X.
      • Yu C.Q.
      • et al.
      Reliability and validity of depression scales of Chinese version: a systematic review.
      According to a previous study, a cutoff score of 7 and above for the PHQ-9 had a sensitivity of 0.86 and a specificity of 0.86 for the determination of depression in the general Chinese population.
      • Wang W.
      • Bian Q.
      • Zhao Y.
      • et al.
      Reliability and validity of the Chinese version of the Patient Health Questionnaire (PHQ-9) in the general population.
      Thus, in this study, individuals with PHQ-9 scores of 7 or higher were considered to have depression. Anxiety was assessed using the Chinese version of the Generalized Anxiety Disorder-7 scale (GAD-7). The GAD-7 is a 7-item self-report instrument, and each item is used to assess 1 of the typical symptoms of generalized anxiety disorder over the past 2 weeks, with a total score that ranges from 0 to 21. Participants who scored 10 and above were considered to be anxious in this study.
      • Spitzer R.L.
      • Kroenke K.
      • Williams J.B.
      • et al.
      A brief measure for assessing generalized anxiety disorder: the GAD-7.

       Data Analyses

      All data were input into Epidata 3.1 software by 2 independent administrators according to the questionnaire records. Statistical analysis of the data was performed using SPSS version 20.0 software (IBM Corp). Descriptive data were described as n (%) for categorical variables and as the mean ± SD for numerical variables. The χ2 test was used to compare the differences between groups with and without PD as well as the distribution difference of PD characteristics between the groups with different pain intensities. A binary logistic regression model was computed to test the association between independent and dependent variables. All predictors variables in the χ2 test with P less than .1 were included in the multivariate backward stepwise Wald logistic regression model. The strength of association was estimated as the odds ratio (OR) and 95% confidence interval (CI). All statistical tests were 2-tailed and P less than .05 was considered statistically significant.

      Results

       Characteristics of the Study Subjects

      A total of 4606 female university students participated in this study; of these, 1921 female students were reported to have experienced PD in the past year. The prevalence of PD was 41.7% (95% CI, 40.4%-43.1%) in this investigation. However, 152 students were diagnosed with gynecological diseases or secondary dysmenorrhea, and 21 subjects with PD and 5 without PD were excluded in this study because of incomplete data, leaving data of 4428 female students for analysis. The average age of the participants was 19.0 ± 1.2 years, and approximately 30% of the patients were at least 20 years of age. Most patients were Han Chinese with a normal BMI. In all, 61.8% of the families of the subjects had an annual household income below 80,000 CNY, and 50% of fathers and 38.4% of mothers had completed high school and above. In terms of menstruation, the mean age at menarche was 13.0 ± 1.4 years, and approximately 30% of female students with an irregular cycle and their mothers had a history of dysmenorrhea. The χ2 test indicated statistically significant differences in the distribution of age, ethnicity, BMI, annual household income, maternal history of dysmenorrhea, age at menarche, and cycle regularity between those with and without PD (all P < .05). The results are shown in Table 1.
      Table 1Characteristics of the Study Sample in This Study
      CharacteristicOverall (N = 4428)Primary DysmenorrheaP
      Yes (n = 1900)No (n = 2528)
      Age
       Younger than 20 years3079 (69.5)1284 (67.6)1795 (71.0).014
       20 Years or older1349 (30.5)616 (32.4)733 (29.0)
      Ethnicity
       Han4006 (90.5)1691 (89.0)2315 (91.6).004
       Minority422 (9.5)209 (11.0)213 (8.4)
      Body mass index
       Underweight1359 (30.7)630 (33.2)729 (28.8).008
       Normal2826 (63.8)1168 (61.5)1658 (65.6)
       Overweight/obese243 (5.5)102 (5.3)141 (5.6)
      Family size
       3 or fewer1711 (38.6)741 (39.0)970 (38.4).670
       4 or more2717 (61.4)1159 (61.0)1558 (61.6)
      Annual household income
       Less than 80,000 CNY2738 (61.8)1210 (63.7)1528 (60.4).028
       80,000 CNY or more1690 (38.2)690 (36.3)1000 (39.6)
      Education level of father
       Primary school and below632 (14.3)291 (15.3)341 (13.5).178
       Middle school1582 (35.7)660 (34.7)922 (36.5)
       High school and above2214 (50.0)949 (50.0)1265 (50.0)
      Education level of mother
       Primary school and below1012 (22.9)438 (23.1)574 (22.7).412
       Middle school1717 (38.8)716 (37.7)1001 (39.6)
       High school and above1699 (38.4)746 (39.2)953 (37.7)
      Maternal history of dysmenorrhea
       Yes1366 (30.8)805 (42.4)561 (22.2)<.001
       No3062 (69.2)1095 (57.6)1967 (77.8)
      Age at menarche
       Younger than 12 years1354 (30.6)615 (32.4)739 (29.2).025
       12 years or older3074 (69.4)1285 (67.6)1789 (70.8)
      Cycle regularity
       Regular3070 (69.3)1258 (66.2)1812 (71.7)<.001
       Irregular1358 (30.7)642 (33.8)716 (28.3)
      Data are presented as n (%) except where otherwise noted.

       Lifestyle Habits and Emotional Factors of the Study Subjects

      A small proportion of female university students smoked, consumed alcohol, sat for less than 8 hours each day, slept less than 7 hours, and never skipped breakfast. Among those participants with PD, 8.0% had consumed alcohol compared with 7.4% without dysmenorrhea. Moreover, 7.0% of the group with dysmenorrhea smoked, whereas 6.6% in the group without dysmenorrhea smoked. In terms of daily sitting time, 60.7% of subjects with PD sat for more than 8 hours compared with 56.5% of subjects without PD. For depression, the average PHQ-9 score was 6.8 ± 4.1 points, and 51.1% of participants reported some degree of depression. For anxiety, the average GAD-7 score was 4.6 ± 3.9 points, and 9.9% of participants reported having anxiety symptoms. The χ2 test showed that the differences in the distribution of daily sitting time, bedtime, skipping breakfast, depression, and anxiety were significantly statistically different between those with and without PD (all P < .05). The results are shown in Table 2.
      Table 2Lifestyle Habits and Emotional Factors Among Female University Students
      Lifestyle HabitOverall (N = 4428)Primary DysmenorrheaP
      Yes (n = 1900)No (n = 2528)
      Smoking
       Yes311 (7.0)143 (7.5)168 (6.6).256
       No4117 (93.0)1757 (92.5)2360 (93.4)
      Alcohol drinking
       Yes354 (8.0)166 (8.7)188 (7.4).114
       No4074 (92.0)1734 (91.3)2340 (92.6)
      Caffeine consumption
       Frequently1205 (27.2)542 (28.5)663 (26.2).089
       Infrequently3223 (72.8)1358 (71.5)1865 (73.8)
      Daily sitting time
       Less than 8 hours1846 (41.7)747 (39.3)1099 (43.5).005
       8 hours or more2582 (58.3)1153 (60.7)1429 (56.5)
      Regular physical exercise
       Yes1881 (42.5)779 (41.0)1102 (43.6).084
       No2547 (57.5)1121 (59.0)1426 (56.4)
      Sleep duration
       Less than 7 hours1019 (23.0)471 (24.8)548 (21.7).051
       7-9 hours3218 (72.7)1350 (71.1)1868 (73.9)
       9 hours or more191 (4.3)79 (4.1)112 (4.4)
      Bedtime
       23:00 and before1768 (39.9)697 (36.7)1071 (42.4)<.001
       After 23:002660 (60.1)1203 (63.3)1457 (57.6)
      Skipping breakfast
       Yes3057 (69.0)1393 (73.3)1664 (65.8)<.001
       No1371 (31.0)507 (26.7)864 (34.2)
      Depression
       Yes2264 (51.1)1028 (54.1)1236 (48.9).001
       No2164 (48.9)872 (45.9)1292 (51.1)
      Anxiety
       Yes438 (9.9)218 (11.5)220 (8.7).002
       No3990 (90.1)1682 (88.5)2308 (91.3)
      Data are presented as n(%).

       Characteristics of PD

      Among 1900 subjects with PD, 35.1% described their menstrual pain as mild, 51.5% described their pain as moderate, and 13.8% described their pain as severe on the basis of the VAS score. The mean severity of pain was 4.81 ± 2.31 on the VAS. Approximately 60% of subjects perceived pain on the first day of menstruation and less than 5% of subjects experienced a pain duration of more than 3 days. Lower abdominal pain (85.9%), fatigue (60.9%), and irritability (50.8%) were the most commonly reported symptoms. The distribution of symptoms between the 3 groups were significant statistically (all P < .001). The results are shown in Table 3.
      Table 3Primary Dysmenorrhea Characteristics and Symptoms During Menstruation
      CharacteristicOverall (N = 1900)VAS for painP
      Mild (n = 667)Moderate (n = 970)Severe (n = 263)
      Start time of dysmenorrhea
       1-3 days before menstruation466 (24.5)145 (21.7)258 (26.6)63 (24.0).020
       First day of menstruation1155 (60.8)426 (63.9)557 (57.4)172 (65.4)
       Second or third day279 (14.7)96 (14.4)155 (16.0)28 (10.6)
      Duration of dysmenorrhea
       3 days or fewer1811 (95.3)649 (97.3)921 (94.9)241 (91.6).001
       More than 3 days89 (4.7)18 (2.7)49 (5.1)22 (8.4)
      Lower abdominal pain
       Yes1632 (85.9)541 (81.1)851 (87.7)240 (91.3)<.001
       No268 (14.1)126 (18.9)119 (12.3)23 (8.7)
      Headache
       Yes443 (23.3)103 (15.4)233 (24.0)107 (40.7)<.001
       No1457 (76.7)564 (84.6)737 (76.0)156 (59.3)
      Dizziness
       Yes416 (21.9)91 (13.6)232 (23.9)93 (35.4)<.001
       No1484 (78.1)576 (76.4)738 (76.1)170 (64.6)
      Nausea and vomiting
       Yes234 (12.3)44 (6.6)110 (11.3)80 (30.4)<.001
       No1666 (87.7)623 (93.4)860 (88.7)183 (69.6)
      Diarrhea
       Yes603 (31.7)151 (22.6)323 (33.3)129 (49.0)<.001
       No1297 (68.3)516 (77.4)647 (66.7)134 (51.0)
      Insomnia
       Yes462 (24.3)103 (15.4)256 (26.4)103 (39.2)<.001
       No1438 (75.7)564 (84.6)714 (73.6)160 (60.8)
      Fatigue
       Yes1158 (60.9)328 (49.2)629 (64.8)201 (76.4)<.001
       No742 (39.1)339 (50.8)341 (35.2)62 (23.6)
      Irritability
       Yes965 (50.8)277 (41.5)523 (53.9)165 (62.7)<.001
       No935 (49.2)390 (58.5)447 (46.1)98 (37.3)
      VAS, visual analogue scale.
      Data are presented as n(%).

       Factors Associated with PD

      PD was selected as the dependent variable and classified into 2 groups (1, yes; 2, no). Age (1, age <20 years; 2, age ≥20 years), ethnicity (1, Han; 2, minority), BMI (1, underweight; 2, normal; 3, overweight/obese), annual household income (1, >80,000 CNY; 2, ≤80,000 CNY), maternal history of dysmenorrhea (1, yes; 2, no), age at menarche (1, ≥12 years; 2, <12 years), cycle regularity (1, regular; 2, irregular), daily sitting time (1, <8 hours; 2, ≥8 hours), bedtime (1, 23:00 and before; 2, after 23:00), depression (1, yes; 2, no), and anxiety (1, yes; 2, no) were entered as independent variables. Multivariate binary logistic regression results showed that the risk factors associated with PD among Chinese female university students were minority status (OR, 1.335; 95% CI, 1.083-1.646), underweight (OR, 1.249; 95% CI, 1.08-1.42), annual household income less than 80,000 CNY (OR, 1.169; 95% CI, 1.018-1.342), maternal history of dysmenorrhea (OR, 2.553; 95% CI, 2.236-2.915), age at menarche younger than 12 years (OR, 1.161; 95% CI, 1.013-1.329), irregular menstrual cycle (OR, 1.216; 95% CI, 1.063-1.391), and skipping breakfast (OR, 1.294; 95% CI, 1.124-1.490). The results are shown in Table 4.
      Table 4Risk Factors Associated With Primary Dysmenorrhea Among Female Students
      Risk FactorBSEWaldOR (95% CI)P
      Ethnicity
       Han1.00
       Minority0.2890.1077.3321.335 (1.083-1.646).007
      Body mass index
       Normal1.00
       Underweight0.2220.07010.2381.249 (1.090-1.431).001
       Overweight/obese−0.0350.1410.0620.965 (0.733-1.272).803
      Annual household income
       80,000 CNY or more1.00
       Less than 80,000 CNY0.1560.0714.8851.169 (1.018-1.342).027
      Maternal history of dysmenorrhea
       No1.00
       Yes0.9370.068191.7972.553 (2.236-2.915)<.001
      Age at menarche
       12 years or older1.00
       Younger than 12 years0.1490.0694.6231.161 (1.013-1.329).032
      Cycle regularity
       Regular1.00
       Irregular0.1960.0698.1601.216 (1.063-1.391).004
      Skipping breakfast
       No1.00
       Yes0.2580.07212.8681.294 (1.124-1.490)<.001
      CI, confidence interval; OR, odds ratio; SE, standard error.

      Discussion

      To our knowledge, this study currently represents the largest population-based study of PD among female university students in China. Our study showed a relatively high prevalence of PD (41.7%) among Chinese female university students in Changsha City. This result was in agreement with the 45% among young college nursing students in India.
      • Shah M.
      • Monga A.
      • Patel S.
      • et al.
      A study of prevalence of primary dysmenorrhea in young students-a cross-sectional study.
      However, in this population, the prevalence was lower than 80.0% in Hong Kong,
      • Chia C.F.
      • Lai J.H.
      • Cheung P.K.
      • et al.
      Dysmenorrhoea among Hong Kong university students: prevalence, impact, and management.
      85.4% in Ethiopia,
      • Hailemeskel S.
      • Demissie A.
      • Assefa N.
      Primary dysmenorrhea magnitude, associated risk factors, and its effect on academic performance: evidence from female university students in Ethiopia.
      and 89.1% in Iran.
      • Habibi N.
      • Huang M.S.
      • Gan W.Y.
      • et al.
      Prevalence of primary dysmenorrhea and factors associated with its intensity among undergraduate students: a cross-sectional study.
      A reason for the differences in these estimates might be explained by the ethnic and sociocultural factors of the study groups. Moreover, this difference might result from the absence of a standardized definition of PD and objective assessment methods used to determine this condition. The common symptoms associated with PD identified in this study were lower abdominal pain (85.9%), fatigue (60.9%), and irritability (50.8%), which are similar to those in a study among Spanish female university students. That study indicated edema (92.7%), irritability (81.9%), and fatigue (79.3%) as common symptoms,
      • Fernandez-Martinez E.
      • Onieva-Zafra M.D.
      • Parra-Fernandez M.L.
      Lifestyle and prevalence of dysmenorrhea among Spanish female university students.
      although irritability and fatigue were more common than observed in this study. Similarly, the symptoms observed in this study are comparable with those in a study performed among Mexican university students in which the major symptoms associated with dysmenorrhea were lower abdominal pain (93%), irritability (50%), and depression (48%).
      • Ortiz M.I.
      Primary dysmenorrhea among Mexican university students: prevalence, impact and treatment.
      Lower abdominal pain, however, was substantially more common in that Mexican sample than observed in this study. Also, among female university students in Ethiopia,
      • Hailemeskel S.
      • Demissie A.
      • Assefa N.
      Primary dysmenorrhea magnitude, associated risk factors, and its effect on academic performance: evidence from female university students in Ethiopia.
      headache (29.3%) was a common symptom associated with dysmenorrhea. Besides, abdominal pain (88.3%) and irritability (57.8%) were slightly more frequent than in this study. Furthermore, among female university students in Turkey, the most common symptoms associated with PD were nervousness (54.5%), breast tenderness (52.7%), and fatigue (47.5%),
      • Ozerdogan N.
      • Sayiner D.
      • Ayranci U.
      • et al.
      Prevalence and predictors of dysmenorrhea among students at a university in Turkey.
      which was remarkably less common than in this study. Additionally, the proportion of fatigue (61.4%) was almost the same as in this study among the Palestinian female university students for whom nervousness (40.0%) and arthralgia (28.6%) were other common symptoms associated with dysmenorrhea. The foregoing between samples differences in the symptoms associated with dysmenorrhea could be attributed to social and cultural differences about dysmenorrhea, and differences in the tools used for measuring symptoms associated with dysmenorrhea between the study samples. Despite these differences, it is evident that the symptoms associated with dysmenorrhea among university or college students are severe, suggesting that dysmenorrhea is an emerging serious gynecological and public health problem among university students, which highlights the need for better intervention and prevention of this condition.
      Our study showed that the prevalence of PD was higher in minorities compared with Han Chinese. One conceivable explanation is that university students of different nationalities find difficulty in adapting to a new environment in terms of climate and dietary habits within a short time. Another explanation is the differences in culture and religious beliefs. For example, Tibetan peoples are ashamed to have gynecological diseases and believe these diseases allow for further discipline and training of their bodies. Our study results revealed an association between family income and risk of PD. This was consistent with other studies that have shown that socioeconomic status influences the severity of menstruation pain.
      • Abdul-Razzak K.K.
      • Ayoub N.M.
      • Abu-Taleb A.A.
      • et al.
      Influence of dietary intake of dairy products on dysmenorrhea.
      ,
      • Zurawiecka M.
      • Wronka I.
      Association of primary dysmenorrhea with anthropometrical and socio-economic factors in Polish university students.
      For instance, a study performed in 581 women aged 18-45 years in central North Carolina indicated that low income increased the development of dysmenorrhea and dyspareunia.
      • Jamieson D.J.
      • Steege J.F.
      The prevalence of dysmenorrhea, dyspareunia, pelvic pain, and irritable bowel syndrome in primary care practices.
      Another study conducted in Ethiopia among 440 female university students showed that the risk of PD was nearly 5 times higher among students whose monthly income was less than 9 USD than those whose monthly income was greater than 18 USD.
      • Hailemeskel S.
      • Demissie A.
      • Assefa N.
      Primary dysmenorrhea magnitude, associated risk factors, and its effect on academic performance: evidence from female university students in Ethiopia.
      In contrast, a prospective study conducted in 823 enrolled Japanese women reported no distinct relationship between dysmenorrhea and household income.
      • Ohde S.
      • Tokuda Y.
      • Takahashi O.
      • et al.
      Dysmenorrhea among Japanese women.
      Similar results were presented in other 2 studies, which showed no obvious association between monthly income and dysmenorrhea.
      • Habibi N.
      • Huang M.S.
      • Gan W.Y.
      • et al.
      Prevalence of primary dysmenorrhea and factors associated with its intensity among undergraduate students: a cross-sectional study.
      ,
      • Jang I.A.
      • Kim M.Y.
      • Lee S.R.
      • et al.
      Factors related to dysmenorrhea among Vietnamese and Vietnamese marriage immigrant women in South Korea.
      The mixed results could be explained by the differences in the study population and different definitions of various economic situations (eg, stipend or allowance) and require further understanding.
      Our study showed that a maternal history of dysmenorrhea was a major risk factor for the development of PD. Most previous studies also supported the finding that women with a family history of dysmenorrhea had an increased risk of dysmenorrhea.
      • Ozerdogan N.
      • Sayiner D.
      • Ayranci U.
      • et al.
      Prevalence and predictors of dysmenorrhea among students at a university in Turkey.
      ,
      • Tavallaee M.
      • Joffres M.R.
      • Corber S.J.
      • et al.
      The prevalence of menstrual pain and associated risk factors among Iranian women.
      ,
      • Muluneh A.A.
      • Nigussie T.S.
      • Gebreslasie K.Z.
      • et al.
      Prevalence and associated factors of dysmenorrhea among secondary and preparatory school students in Debremarkos town, North-West Ethiopia.
      One reason for this could be related to behaviors that girls learn from their mothers for the possibility of societal reward or that control pain.
      • Ozerdogan N.
      • Sayiner D.
      • Ayranci U.
      • et al.
      Prevalence and predictors of dysmenorrhea among students at a university in Turkey.
      Another reason for this could be related to genetic factors.
      • Silberg J.L.
      • Martin N.G.
      • Heath A.C.
      Genetic and environmental factors in primary dysmenorrhea and its relationship to anxiety, depression, and neuroticism.
      Our study showed that female students who were underweight were associated with increased risk of dysmenorrhea compared with those who had a normal BMI. These results are compatible with other research findings.
      • Rafique N.
      • Al-Sheikh M.H.
      Prevalence of primary dysmenorrhea and its relationship with body mass index.
      ,
      • Chauhan M.
      • Kala J.
      Relation between dysmenorrhea and body mass index in adolescents with rural versus urban variation.
      A meta-analysis that included 5 trials showed that a BMI of less than 20 increased the risk for dysmenorrhea by 42%.
      • Latthe P.
      • Mignini L.
      • Gray R.
      • et al.
      Factors predisposing women to chronic pelvic pain: systematic review.
      However, the association between BMI and PD is still controversial. Many studies have revealed no relationship between BMI and dysmenorrhea,
      • Ohde S.
      • Tokuda Y.
      • Takahashi O.
      • et al.
      Dysmenorrhea among Japanese women.
      ,
      • Tavallaee M.
      • Joffres M.R.
      • Corber S.J.
      • et al.
      The prevalence of menstrual pain and associated risk factors among Iranian women.
      whereas other studies have shown an increased prevalence of PD in overweight or obese subjects.
      • Sharma A.
      • Taneja D.K.
      • Sharma P.
      • et al.
      Problems related to menstruation and their effect on daily routine of students of a medical college in Delhi, India.
      ,
      • Nohara M.
      • Momoeda M.
      • Kubota T.
      • et al.
      Menstrual cycle and menstrual pain problems and related risk factors among Japanese female workers.
      Still, some other data have confirmed a U-shaped relationship between BMI and dysmenorrhea.
      • Ju H.
      • Jones M.
      • Mishra G.D.
      A U-shaped relationship between body mass index and dysmenorrhea: a longitudinal study.
      ,
      • Jiang W.
      • Hua X.G.
      • Hu C.Y.
      • et al.
      The prevalence and risk factors of menstrual pain of married women in Anhui Province, China.
      Despite that the pathophysiological mechanisms are still unclear, a possible hypothesis is that a lower amount of body fat affects normal ovulation and menstrual cycles and thus leads to excessive release of prostaglandin (PGs); higher circulating levels of PGs have been reported in women with dysmenorrhea compared with asymptomatic women during menstruation.
      • Frisch R.E.
      The right weight: body fat, menarche and ovulation.
      According to our study results, women with earlier menarche and an irregular menstrual cycle are more likely to experience menstrual pain. This finding was in accord with previous studies.
      • Zegeye D.T.
      • Megabiaw B.
      • Mulu A.
      Age at menarche and the menstrual pattern of secondary school adolescents in northwest Ethiopia.
      ,
      • Harel Z.
      Dysmenorrhea in adolescents and young adults: etiology and management.
      A systematic review that included 63 studies and 64,286 women showed that earlier menarche and an irregular cycle increased the risk of dysmenorrhea by 54% and 102%, respectively.
      • Latthe P.
      • Mignini L.
      • Gray R.
      • et al.
      Factors predisposing women to chronic pelvic pain: systematic review.
      However, some studies have shown that the prevalence of dysmenorrhea was higher in women with older age at menarche.
      • Ozerdogan N.
      • Sayiner D.
      • Ayranci U.
      • et al.
      Prevalence and predictors of dysmenorrhea among students at a university in Turkey.
      ,
      • Svanberg L.
      • Ulmsten U.
      The incidence of primary dysmenorrhea in teenagers.
      Although the underlying etiologic mechanisms of these associations are not well understood, the mechanism is probably related to ovulatory efficiency, higher levels of uterine activity during menstruation, and the increased production of uterine PGs.
      • Dawood M.Y.
      Primary dysmenorrhea: advances in pathogenesis and management.
      ,
      • Calesnick B.
      • Dinan A.M.
      Prostaglandins and NSAIDs in primary dysmenorrhea.
      Our study showed that skipping breakfast was associated with increased risk for dysmenorrhea by 25% in female students, which is in accord with other studies.
      • Fujiwara T.
      • Sato N.
      • Awaji H.
      • et al.
      Skipping breakfast adversely affects menstrual disorders in young college students.
      ,
      • Abu Helwa H.A.
      • Mitaeb A.A.
      • Al-Hamshri S.
      • et al.
      Prevalence of dysmenorrhea and predictors of its pain intensity among Palestinian female university students.
      A study performed in young Japanese women showed that students who skip breakfast tend to experience a higher intensity of dysmenorrhea-associated pain than those who eat breakfast regularly.
      • Fujiwara T.
      Skipping breakfast is associated with dysmenorrhea in young women in Japan.
      According to a systematic review, the prevalence of skipping breakfast ranged from 10% to 30%, with an increasing trend in adolescents, mainly in girls, which was associated with a worse lipid profile, worse blood pressure, and metabolic syndrome.
      • Monzani A.
      • Ricotti R.
      • Caputo M.
      • et al.
      A systematic review of the association of skipping breakfast with weight and cardiometabolic risk factors in children and adolescents. What should we better investigate in the future?.
      Although the mechanisms underlying the adverse effect of skipping breakfast are unclear, they might be related to inadequate intake of certain foods and might induce some degree of nutritional defect in the morning. For instance, low dietary intake of some fiber-containing foods and dairy products was found to be inversely correlated with menstrual pain.
      • Abdul-Razzak K.K.
      • Ayoub N.M.
      • Abu-Taleb A.A.
      • et al.
      Influence of dietary intake of dairy products on dysmenorrhea.
      ,
      • Nagata C.
      • Hirokawa K.
      • Shimizu N.
      • et al.
      Associations of menstrual pain with intakes of soy, fat and dietary fiber in Japanese women.
      To our best knowledge, this study currently represents the largest population-based study of PD among female university students in China. However, our present study has some limitations that we would like to address. First, temporal and causal relationships could not be assessed because of the cross-sectional study design. Second, the present study only involved female Chinese students who were freshmen to juniors because many seniors were involved in external internships. Further comparative studies with foreign students and senior students are needed to generalize the results. Third, the occurrence of menstrual pain and the characteristics of PD were measured only on the basis of self-reports, which might not be accurate. Finally, there could be recall bias because the students were asked about some events that occurred before the study. Further cohort and longitudinal studies should be conducted to verify our findings and to garner a deeper understanding.

       Conclusions

      A high proportion of female students had PD in Changsha City, China. Minority status, being underweight, lower family income, irregular menstrual cycle, earlier age at menarche, maternal history of dysmenorrhea, and skipping breakfast were risk factors for PD among female Chinese university students.

      Acknowledgment

      We thank all universities and female university students in this study for their cooperation.
      This study was funded by the independent exploration innovation subject for the graduate students of Central South University , Changsha, China (No. 1053320171229 ). This study was approved by the Ethics Committee of Xiangya School of Public Health in Central South University (XYGW-2017-16).

      References

        • Abd El-Mawgod M.M.
        • Alshaibany A.S.
        • Al-Anazi A.M.
        Epidemiology of dysmenorrhea among secondary-school students in Northern Saudi Arabia.
        J Egypt Public Health Assoc. 2016; 91: 115
        • Iacovides S.
        • Avidon I.
        • Baker F.C.
        What we know about primary dysmenorrhea today: a critical review.
        Hum Reprod Update. 2015; 21: 762
        • Osayande A.S.
        • Mehulic S.
        Diagnosis and initial management of dysmenorrhea.
        Am Fam Physician. 2014; 89: 341
        • Dawood M.Y.
        Primary dysmenorrhea: advances in pathogenesis and management.
        Obstet Gynecol. 2006; 108: 428
        • Ruoff G.
        • Lema M.
        Strategies in pain management: new and potential indications for COX-2 specific inhibitors.
        J Pain Symptom Manage. 2003; 25: S21
        • Rafique N.
        • Al-Sheikh M.H.
        Prevalence of primary dysmenorrhea and its relationship with body mass index.
        J Obstet Gynaecol Res. 2018; 44: 1773
        • Hailemeskel S.
        • Demissie A.
        • Assefa N.
        Primary dysmenorrhea magnitude, associated risk factors, and its effect on academic performance: evidence from female university students in Ethiopia.
        Int J Womens Health. 2016; 8: 489
        • Ortiz M.I.
        Primary dysmenorrhea among Mexican university students: prevalence, impact and treatment.
        Eur J Obstet Gynecol Reprod Biol. 2010; 152: 73
        • Habibi N.
        • Huang M.S.
        • Gan W.Y.
        • et al.
        Prevalence of primary dysmenorrhea and factors associated with its intensity among undergraduate students: a cross-sectional study.
        Pain Manag Nurs. 2015; 16: 855
        • Sharma A.
        • Taneja D.K.
        • Sharma P.
        • et al.
        Problems related to menstruation and their effect on daily routine of students of a medical college in Delhi, India.
        Asia Pac J Public Health. 2008; 20: 234
        • Titilayo A.
        • Agunbiade O.M.
        • Banjo O.
        • et al.
        Menstrual discomfort and its influence on daily academic activities and psychosocial relationship among undergraduate female students in Nigeria.
        Tanzan J Health Res. 2009; 11: 181
        • Ortiz M.I.
        • Rangel-Flores E.
        • Carrillo-Alarcon L.C.
        • et al.
        Prevalence and impact of primary dysmenorrhea among Mexican high school students.
        Int J Gynaecol Obstet. 2009; 107: 240
        • Zegeye D.T.
        • Megabiaw B.
        • Mulu A.
        Age at menarche and the menstrual pattern of secondary school adolescents in northwest Ethiopia.
        BMC Womens Health. 2009; 9: 29
        • Dorn L.D.
        • Negriff S.
        • Huang B.
        • et al.
        Menstrual symptoms in adolescent girls: association with smoking, depressive symptoms, and anxiety.
        J Adolesc Health. 2009; 44: 237
        • Faramarzi M.
        • Salmalian H.
        Association of psychologic and nonpsychologic factors with primary dysmenorrhea.
        Iran Red Crescent Med J. 2014; 16: e16307
        • Ju H.
        • Jones M.
        • Mishra G.
        The prevalence and risk factors of dysmenorrhea.
        Epidemiol Rev. 2014; 36: 104
        • Na Z.
        • Yang L.
        • Bao-huan Z.
        • et al.
        Current status of primary dysmenorrhea and its relationship with lifestyle among female students in a college in Guangzhou City.
        Practical Preventive Medicine. 2014; 23 ([in Chinese]): 1537
        • Chen C.
        • Lu F.C.
        The guidelines for prevention and control of overweight and obesity in Chinese adults.
        Biomed Environ Sci. 2004; 17: 1
        • Ma Y.
        • Ma H.
        • Chen S.
        • et al.
        The validity and reliability of the Cox menstrual symptom scale of Chinese version.
        J Shandong Univ TCM. 2015; 39 ([in Chinese]): 5
        • Hirshkowitz M.
        • Whiton K.
        • Albert S.M.
        • et al.
        National Sleep Foundation’s updated sleep duration recommendations: final report.
        Sleep Health. 2015; 1: 233
        • Mushtaq M.U.
        • Gull S.
        • Mushtaq K.
        • et al.
        Dietary behaviors, physical activity and sedentary lifestyle associated with overweight and obesity, and their socio-demographic correlates, among Pakistani primary school children.
        Int J Behav Nutr Phys Act. 2011; 8: 130
        • Sun X.Y.
        • Li Y.X.
        • Yu C.Q.
        • et al.
        Reliability and validity of depression scales of Chinese version: a systematic review.
        Zhonghua Liu Xing Bing Xue Za Zhi. 2017; 38 ([in Chinese]): 110
        • Wang W.
        • Bian Q.
        • Zhao Y.
        • et al.
        Reliability and validity of the Chinese version of the Patient Health Questionnaire (PHQ-9) in the general population.
        Gen Hosp Psychiatry. 2014; 36: 539
        • Spitzer R.L.
        • Kroenke K.
        • Williams J.B.
        • et al.
        A brief measure for assessing generalized anxiety disorder: the GAD-7.
        Arch Intern Med. 2006; 166: 1092
        • Shah M.
        • Monga A.
        • Patel S.
        • et al.
        A study of prevalence of primary dysmenorrhea in young students-a cross-sectional study.
        Indian J Community Med. 2013; 4: 30
        • Chia C.F.
        • Lai J.H.
        • Cheung P.K.
        • et al.
        Dysmenorrhoea among Hong Kong university students: prevalence, impact, and management.
        Hong Kong Med J. 2013; 19: 222
        • Fernandez-Martinez E.
        • Onieva-Zafra M.D.
        • Parra-Fernandez M.L.
        Lifestyle and prevalence of dysmenorrhea among Spanish female university students.
        PLoS One. 2018; 13: e0201894
        • Ozerdogan N.
        • Sayiner D.
        • Ayranci U.
        • et al.
        Prevalence and predictors of dysmenorrhea among students at a university in Turkey.
        Int J Gynaecol Obstet. 2009; 107: 39
        • Abdul-Razzak K.K.
        • Ayoub N.M.
        • Abu-Taleb A.A.
        • et al.
        Influence of dietary intake of dairy products on dysmenorrhea.
        J Obstet Gynaecol Res. 2010; 36: 377
        • Zurawiecka M.
        • Wronka I.
        Association of primary dysmenorrhea with anthropometrical and socio-economic factors in Polish university students.
        J Obstet Gynaecol Res. 2018; 44: 1259
        • Jamieson D.J.
        • Steege J.F.
        The prevalence of dysmenorrhea, dyspareunia, pelvic pain, and irritable bowel syndrome in primary care practices.
        Obstet Gynecol. 1996; 87: 55
        • Ohde S.
        • Tokuda Y.
        • Takahashi O.
        • et al.
        Dysmenorrhea among Japanese women.
        Int J Gynecol Obstet. 2008; 100: 13
        • Jang I.A.
        • Kim M.Y.
        • Lee S.R.
        • et al.
        Factors related to dysmenorrhea among Vietnamese and Vietnamese marriage immigrant women in South Korea.
        Obstet Gynecol Sci. 2013; 56: 242
        • Tavallaee M.
        • Joffres M.R.
        • Corber S.J.
        • et al.
        The prevalence of menstrual pain and associated risk factors among Iranian women.
        J Obstet Gynaecol Res. 2011; 37: 442
        • Muluneh A.A.
        • Nigussie T.S.
        • Gebreslasie K.Z.
        • et al.
        Prevalence and associated factors of dysmenorrhea among secondary and preparatory school students in Debremarkos town, North-West Ethiopia.
        BMC Womens Health. 2018; 18: 57
        • Silberg J.L.
        • Martin N.G.
        • Heath A.C.
        Genetic and environmental factors in primary dysmenorrhea and its relationship to anxiety, depression, and neuroticism.
        Behav Genet. 1987; 17: 363
        • Chauhan M.
        • Kala J.
        Relation between dysmenorrhea and body mass index in adolescents with rural versus urban variation.
        J Obstet Gynaecol India. 2012; 62: 442
        • Latthe P.
        • Mignini L.
        • Gray R.
        • et al.
        Factors predisposing women to chronic pelvic pain: systematic review.
        BMJ. 2006; 332: 749
        • Nohara M.
        • Momoeda M.
        • Kubota T.
        • et al.
        Menstrual cycle and menstrual pain problems and related risk factors among Japanese female workers.
        Ind Health. 2011; 49: 228
        • Ju H.
        • Jones M.
        • Mishra G.D.
        A U-shaped relationship between body mass index and dysmenorrhea: a longitudinal study.
        PLoS One. 2015; 10: e0134187
        • Jiang W.
        • Hua X.G.
        • Hu C.Y.
        • et al.
        The prevalence and risk factors of menstrual pain of married women in Anhui Province, China.
        Eur J Obstet Gynecol Reprod Biol. 2018; 229: 190
        • Frisch R.E.
        The right weight: body fat, menarche and ovulation.
        Baillieres Clin Obstet Gynaecol. 1990; 4: 419
        • Harel Z.
        Dysmenorrhea in adolescents and young adults: etiology and management.
        J Pediatr Adolesc Gynecol. 2006; 19: 363
        • Svanberg L.
        • Ulmsten U.
        The incidence of primary dysmenorrhea in teenagers.
        Arch Gynecol. 1981; 230: 173
        • Calesnick B.
        • Dinan A.M.
        Prostaglandins and NSAIDs in primary dysmenorrhea.
        Am Fam Physician. 1987; 35: 223
        • Fujiwara T.
        • Sato N.
        • Awaji H.
        • et al.
        Skipping breakfast adversely affects menstrual disorders in young college students.
        Int J Food Sci Nutr. 2009; 60: 23
        • Abu Helwa H.A.
        • Mitaeb A.A.
        • Al-Hamshri S.
        • et al.
        Prevalence of dysmenorrhea and predictors of its pain intensity among Palestinian female university students.
        BMC Womens Health. 2018; 18: 18
        • Fujiwara T.
        Skipping breakfast is associated with dysmenorrhea in young women in Japan.
        Int J Food Sci Nutr. 2003; 54: 505
        • Monzani A.
        • Ricotti R.
        • Caputo M.
        • et al.
        A systematic review of the association of skipping breakfast with weight and cardiometabolic risk factors in children and adolescents. What should we better investigate in the future?.
        Nutrients. 2019; 11: E387
        • Nagata C.
        • Hirokawa K.
        • Shimizu N.
        • et al.
        Associations of menstrual pain with intakes of soy, fat and dietary fiber in Japanese women.
        Eur J Clin Nutr. 2005; 59: 88