Abstract
Objective
To determine if the ages at pubertal milestones are associated with the prevalence of adolescent migraine.
Background
Migraine headaches are a common disease in adolescent girls. Past studies have evaluated the relationship between age of onset of menarche and migraine headache, but none have studied earlier pubertal milestones such as thelarche and pubarche.
Methods
In this cross-sectional study, a previously validated questionnaire was administered to girls (15–18 years) in Breast Cancer and the Environment Research Program puberty cohort to ascertain if they met criteria for migraine over the past year. Ages of pubertal development were ascertained by serial examinations beginning at 6–8 years of age and ending in late puberty. Logistic regression analyses determined if age of onset of each pubertal milestone (thelarche, pubarche, menarche separately) was associated with adolescent migraine after adjusting for other risk factors.
Results
Of 761girls, 222 (29.2%) met the criteria for migraine. Later thelarche was associated with a lower odds of adolescent migraine (OR 0.83; 95% CI 0.72–0.97, p = 0.019). In models further adjusted for BASC-2 internalizing problems (n = 490), both later thelarche (OR 0.78; 95% CI 0.64–0.96, p = 0.016) and later menarche (OR 0.81; 95%CI 0.67–0.98, p = 0.026) were associated with a lower migraine prevalence. Internalizing problems (OR 1.05; 95% CI 1.03–1.07) externalizing problems (OR 1.05; 95% CI 1.02–1.07) and behavioral symptoms (OR 1.05; 95% CI 1.03–1.08) were associated with increased prevalence of migraine in separate models.
Conclusions
Age of onset of thelarche and menarche, and internalizing, externalizing, and behavioral symptoms were all associated with adolescent migraine.
Similar content being viewed by others
Data availability statement
The data on which this analysis was based are available from the authors in accordance with the Breast Cancer and the Environment Research Program data sharing policies.
Abbreviations
- BASC:
-
Behavioral assessment system for children
- BSI:
-
Behavior symptoms Index
- BCERP:
-
Breast cancer and the environment research program
- BMI:
-
Body mass index
- CIN:
-
Cincinnati
- CI:
-
Confidence interval
- IRB:
-
Institutional review board
- ICHD-3:
-
International classification of headache disorder-III
- NYC:
-
New York City
- OR:
-
Odds ratio
- SFBA:
-
San Francisco Bay Area
References
Victor TW, Hu X, Campbell JC, Buse DC, Lipton RB (2010) Migraine prevalence by age and sex in the United States: a life-span study. Cephalalgia 30(9):1065–1072. https://doi.org/10.1177/0333102409355601
Stewart WF, Lipton RB, Celentano DD, Reed ML (1992) Prevalence of migraine headache in the United States. Relation to age, income, race, and other sociodemographic factors. Jama 267(1):64–9
Hershey AD, Powers SW, Vockell AL, LeCates SL, Segers A, Kabbouche MA (2004) Development of a patient-based grading scale for PedMIDAS. Cephalalgia 24(10):844–849. https://doi.org/10.1111/j.1468-2982.2004.00757.x
Martin VT, Behbehani M (2006) Ovarian hormones and migraine headache: understanding mechanisms and pathogenesis–part 2. Headache 46(3):365–386. https://doi.org/10.1111/j.1526-4610.2006.00370.x
Maleki N, Kurth T, Field AE (2017) Age at menarche and risk of developing migraine or non-migraine headaches by young adulthood: a prospective cohort study. Cephalalgia 37(13):1257–1263. https://doi.org/10.1177/0333102416677999
Aegidius KL, Zwart JA, Hagen K, Dyb G, Holmen TL, Stovner LJ (2011) Increased headache prevalence in female adolescents and adult women with early menarche The Head-HUNT studies. Eur J Neurol 18(2):321–328. https://doi.org/10.1111/j.1468-1331.2010.03143.x
Martin VT, Allen JR, Houle TT et al (2018) Ovarian hormones, age and pubertal development and their association with days of headache onset in girls with migraine: an observational cohort study. Cephalalgia 38(4):707–717. https://doi.org/10.1177/0333102417706980
Operto FF, Craig F, Peschechera A, Mazza R, Lecce PA, Margari L (2017) Parenting stress and emotional/behavioral problems in adolescents with primary headache. Front Neurol 8:749. https://doi.org/10.3389/fneur.2017.00749
Arruda MA, Bigal ME (2012) Behavioral and emotional symptoms and primary headaches in children: a population-based study. Cephalalgia 32(15):1093–100. https://doi.org/10.1177/0333102412454226
Deardorff J, Marceau K, Johnson M et al (2021) Girls’ pubertal timing and tempo and mental health: a longitudinal examination in an ethnically diverse sample. J Adolesc Health 68(6):1197–1203. https://doi.org/10.1016/j.jadohealth.2021.01.020
Hiatt RA, Haslam SZ, Osuch J, Breast C, The Environment Research C (2009) The breast cancer and the environment research centers: transdisciplinary research on the role of the environment in breast cancer etiology. Environ Health Perspect 117(12):1814–22. https://doi.org/10.1289/ehp.0800120
Biro FM, Galvez MP, Greenspan LC et al (2010) Pubertal assessment method and baseline characteristics in a mixed longitudinal study of girls. Pediatrics 126(3):e583–e590. https://doi.org/10.1542/peds.2009-3079
Hillman JB, Huang B, Pinney SM, Biro FM (2013) Early pubertal development and insulin sensitivity among school-aged girls: mediation via adiposity. J Pediatr Adolesc Gynecol 26(1):47–50. https://doi.org/10.1016/j.jpag.2012.09.007
CDC 2000 CDC Growth Charts (2010) In: Prevention CfDCa, ed. Atlanta, GA September 9
Marshall WA, Tanner JM (1969) Variations in pattern of pubertal changes in girls. Arch Dis Child 44(235):291–303. https://doi.org/10.1136/adc.44.235.291
Biro FM, Greenspan LC, Galvez MP et al (2013) Onset of breast development in a longitudinal cohort. Pediatrics 132(6):1019–1027. https://doi.org/10.1542/peds.2012-3773
Biro FM, Pajak A, Wolff MS et al (2018) Age of menarche in a longitudinal US cohort. J Pediatr Adolesc Gynecol 31(4):339–345. https://doi.org/10.1016/j.jpag.2018.05.002
Reynolds CR, Kamphaus RW, Vannest KJ (2011) Behavior assessment system for children (BASC). In: Kreutzer JS, DeLuca J, Caplan B (eds) Encyclopedia of clinical neuropsychology. Springer, New York, pp 366–371
Lipton RB, Stewart WF, Diamond S, Diamond ML, Reed M (2001) Prevalence and burden of migraine in the United States: data from the American migraine study II. Headache 41(7):646–657. https://doi.org/10.1046/j.1526-4610.2001.041007646.x
Dunn OJ (1961) Multiple comparisons among means. J Am Stat Assoc 56(293):52–64. https://doi.org/10.1080/01621459.1961.10482090
Etymologia: Bonferroni correction. Emerg Infect Dis 2015;21(2):289. https://doi.org/10.3201/eid2102.et2102.
Alashqar ASS, Ahmed SF, AlThufairi H, Owayed S, AlHamdan F, Alroughani R, Al-Hashel JY (2020) Impact of puberty in girls on prevalence of primary headache disorder among female schoolchildren in Kuwait. Front Neurol 11:594. https://doi.org/10.3389/fneur.2020.00594
Biro FM, Huang B, Crawford PB et al (2006) Pubertal correlates in black and white girls. J Pediatr 148(2):234–240. https://doi.org/10.1016/j.jpeds.2005.10.020
Li N, Papandonato GD, Calafat AM et al (2020) Gestational and childhood exposure to phthalates and child behavior. Environ Health 144:106036. https://doi.org/10.1016/2Fj.envint.2020.106036
Orr SL, Potter BK, Ma J, Colman I (2017) Migraine and mental health in a population-based sample of adolescents. Can J Neurol Sci 44(1):44–50. https://doi.org/10.1017/cjn.2016.402
Anttila P, Sourander A, Metsahonkala L, Aromaa M, Helenius H, Sillanpaa M (2004) Psychiatric symptoms in children with primary headache. J Am Acad Child Adolesc Psychiatry 43(4):412–419. https://doi.org/10.1097/00004583-200404000-00007
Anda R, Tietjen G, Schulman E, Felitti V, Croft J (2010) Adverse childhood experiences and frequent headaches in adults. Headache 50(9):1473–1481. https://doi.org/10.1111/j.1526-4610.2010.01756.x
Hammond NG, Orr SL, Colman I (2019) Early life stress in adolescent migraine and the mediational influence of symptoms of depression and anxiety in a Canadian cohort. Headache 59(10):1687–1699. https://doi.org/10.1111/head.13644
Tietjen GE, Buse DC, Collins SA (2016) Childhood maltreatment in the migraine patient. Curr Treat Options Neurol 18(7):31. https://doi.org/10.1007/s11940-016-0415-4
Aegidius KL, Zwart JA, Hagen K, Dyb G, Holmen TL, Stovner LJ (2011) Increased headache prevalence in female adolescents and adult women with early menarche. The head-hunt studies. Eur J Neurol 18(2):321–328. https://doi.org/10.1111/j.1468-1331.2010.03143.x
Biro FM, Pinney SM, Huang B, Baker ER, Walt Chandler D, Dorn LD (2014) Hormone changes in peripubertal girls. J Clin Endocrinol Metab 99(10):3829–35. https://doi.org/10.1210/jc.2013-4528
Abu-Arefeh I, Russell G (1994) Prevalence of headache and migraine in school children. Bmj 309(6957):765–9. https://doi.org/10.1136/bmj.309.6957.765
Francis MV (2013) Brief migraine episodes in children and adolescents-a modification to international headache society pediatric migraine (without aura) diagnostic criteria. Springerplus 2(1):77. https://doi.org/10.1186/2193-1801-2-77
Mortimer M, Kay J, Jaron A (1992) Childhood migraine in general practice: clinical features and characteristics. Cephalalgia 12(4):238–243. https://doi.org/10.1046/j.1468-2982.1992.1204238.x
Martin VT, Behbehani M (2006) Ovarian hormones and migraine headache: understanding mechanisms and pathogenesis—part 1. Headache 46:3–23. https://doi.org/10.1111/j.1526-4610.2006.00309.x
Funding
R03HD094236, U01ES012770, U01ES012801, U01ES019435, U01ES019453, U01ES019457, U01ES012771, U01ES019454, P30ES006096, T32ES010957. Sponsors had no role in the design the study design, collection, analysis and interpretation of data, the writing of the report and the decision to submit the manuscript for publication.
Author information
Authors and Affiliations
Contributions
Conception and design-Martin, Fassler, Brunst, Ying, Teitelbaum, Windham, Deardorff, Wolff, Kushi, Biro, Pinney; Acquisition of data-Teitelbaum, Windham, Deardorff, Wolff, Kushi, Biro, Pinney; Analysis and interpretation of data—Martin, Fassler, Brunst, Ying, Biro, Pinney; Drafting the manuscript—Martin, Fassler, Brunst, Ying, Teitelbaum, Windham, Deardorff, Wolff, Kushi, Biro, Pinney; Revision for intellectual content- Martin, Fassler, Brunst, Biro, Pinney; Final approval—Martin, Fassler, Brunst, Ying, Teitelbaum, Windham, Deardorff, Wolff, Kushi, Biro, Pinney.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no conflicts of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Martin, V.T., Fassler, C.S., Brunst, K.J. et al. Migraine and its association with pubertal maturation and behavioral traits among adolescent girls. Acta Neurol Belg 123, 1279–1289 (2023). https://doi.org/10.1007/s13760-022-02161-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13760-022-02161-2