{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,12]],"date-time":"2025-10-12T03:07:35Z","timestamp":1760238455024,"version":"build-2065373602"},"reference-count":55,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2022,8,19]],"date-time":"2022-08-19T00:00:00Z","timestamp":1660867200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJERPH"],"abstract":"<jats:p>To evaluate if experiencing a short-term exposure (18-months) to factors such as menstrual irregularities, dieting, changes in exercise or body weight, and medication usage is associated with bone mineral density (BMD) in college-aged females. A retrospective survey assessing health behaviors during a recent 18-month time period and a DXA scan were completed in 641 females. A total of 45.5% of participants reported amenorrhea during the 18-month time period. Those who experienced amenorrhea had lower femoral neck BMD (p = 0.018), trochanter (p = 0.018) and spine BMD (p = 0.022) compared to eumenorrheic women. Lifetime oral contraceptive usage longer than six months was negatively associated with BMD at femoral neck (p = 0.018) and total hip (p = 0.021). Women who lost weight trended towards having the lowest BMD at all sites compared to women who gained weight. Following a very-low calorie diet during the time period was negatively correlated with spine BMD (p = 0.001). Time spent in vigorous and very vigorous activity was weakly correlated with some hip BMD sites but time spent in extremely vigorous activity was not. In conclusion, females who experienced weight loss, amenorrhea, or a very low-calorie diet within an 18-month period of time in young adulthood had lower BMD. Additionally, oral contraceptive usage for longer than six months during their lifetime was associated with lower BMD.<\/jats:p>","DOI":"10.3390\/ijerph191610363","type":"journal-article","created":{"date-parts":[[2022,8,21]],"date-time":"2022-08-21T22:23:13Z","timestamp":1661120593000},"page":"10363","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Association of Short-Term Changes in Menstrual Frequency, Medication Use, Weight and Exercise on Bone Mineral Density in College-Aged Women"],"prefix":"10.3390","volume":"19","author":[{"given":"Stacie H.","family":"Fleischer","sequence":"first","affiliation":[{"name":"Department of Nutrition, Dietetics and Food Science, College of Life Sciences, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Annalisa K.","family":"Freire","sequence":"additional","affiliation":[{"name":"Department of Nutrition, Dietetics and Food Science, College of Life Sciences, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Katie","family":"Brown","sequence":"additional","affiliation":[{"name":"Department of Nutrition, Dietetics & Food Sciences, College of Agriculture and Applied Sciences, Utah State University, Logan, UT 84322, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Andrew","family":"Creer","sequence":"additional","affiliation":[{"name":"Department of Statistics, College of Physical and Mathematical Sciences, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4109-4827","authenticated-orcid":false,"given":"Dennis L.","family":"Eggett","sequence":"additional","affiliation":[{"name":"Department of Exercise Science & Outdoor Recreation, College of Science, Utah Valley University, Orem, UT 84058, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-5679-7862","authenticated-orcid":false,"given":"Susan","family":"Fullmer","sequence":"additional","affiliation":[{"name":"Department of Nutrition, Dietetics and Food Science, College of Life Sciences, Brigham Young University, Provo, UT 84602, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2022,8,19]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1281","DOI":"10.1007\/s00198-015-3440-3","article-title":"The National Osteoporosis Foundation\u2019s position statement on peak bone mass development and lifestyle factors: A systematic review and implementation recommendations","volume":"27","author":"Weaver","year":"2016","journal-title":"Osteoporos. Int."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"2359","DOI":"10.1007\/s00198-014-2794-2","article-title":"Clinician\u2019s guide to prevention and treatment of osteoporosis","volume":"25","author":"Cosman","year":"2014","journal-title":"Osteoporos. Int."},{"key":"ref_3","doi-asserted-by":"crossref","unstructured":"NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy (2001). Osteoporosis prevention, diagnosis, and therapy. J. Am. Med. Assoc., 285, 785\u2013795.","DOI":"10.1001\/jama.285.6.785"},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Han, C.-S., Kim, H.-K., and Kim, S. (2021). Effects of Adolescents\u2019 Lifestyle Habits and Body Composition on Bone Mineral Density. Int. J. Environ. Res. Public Health, 18.","DOI":"10.3390\/ijerph18116170"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1186\/s40337-020-00365-6","article-title":"Abnormal bone mineral density and content in girls with early-onset anorexia nervosa","volume":"9","author":"Clarke","year":"2021","journal-title":"J. Eat. Disord."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"2594","DOI":"10.1210\/jc.2007-2644","article-title":"Influence of age at menarche on forearm bone microstructure in healthy young women","volume":"93","author":"Chevalley","year":"2008","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_7","first-page":"1867","article-title":"American College of Sports Medicine position stand. The female athlete triad","volume":"39","author":"Nattiv","year":"2007","journal-title":"Med. Sci. Sports Exerc."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"371","DOI":"10.1016\/j.bone.2007.05.003","article-title":"Bone mineral density in female high school athletes: Interactions of menstrual function and type of mechanical loading","volume":"41","author":"Nichols","year":"2007","journal-title":"Bone"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"433","DOI":"10.1093\/humupd\/dmh033","article-title":"Physiological aspects and clinical sequelae of energy deficiency and hypoestrogenism in exercising women","volume":"10","author":"Williams","year":"2004","journal-title":"Hum. Reprod. Update"},{"key":"ref_10","first-page":"116","article-title":"The Female Athlete Triad: Energy Deficiency, Physiologic Consequences, and Treatment","volume":"26","author":"Hergenroeder","year":"2015","journal-title":"Adolesc. Med. State Art Rev."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1123\/ijsnem.2015-0072","article-title":"Body Mass-Related Predictors of the Female Athlete Triad among Adolescent Athletes","volume":"26","author":"Thralls","year":"2016","journal-title":"Int. J. Sport Nutr. Exerc. Metab."},{"key":"ref_12","doi-asserted-by":"crossref","unstructured":"Deng, K.-L., Yang, W.-Y., Hou, J.-L., Li, H., Feng, H., and Xiao, S.-M. (2021). Association between Body Composition and Bone Mineral Density in Children and Adolescents: A Systematic Review and Meta-Analysis. Int. J. Environ. Res. Public Health, 18.","DOI":"10.3390\/ijerph182212126"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"373","DOI":"10.1007\/s001980050077","article-title":"Weight variability, weight change and the incidence of hip fracture: A prospective study of 39000 middle-aged norwegians","volume":"8","author":"Meyer","year":"1998","journal-title":"Osteoporos. Int."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1740","DOI":"10.1046\/j.1532-5415.2003.51558.x","article-title":"Intentional and unintentional weight loss increase bone loss and hip fracture risk in older women","volume":"51","author":"Ensrud","year":"2003","journal-title":"J. Am. Geriatr. Soc."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1359\/JBMR.040410","article-title":"Dose-response relationships between energy availability and bone turnover in young exercising women","volume":"19","author":"Ihle","year":"2004","journal-title":"J. Bone Miner. Res."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1850","DOI":"10.1002\/jbmr.63","article-title":"Cross-sectional evidence of suppressed bone mineral accrual among female adolescent runners","volume":"25","author":"Barrack","year":"2010","journal-title":"J. Bone Miner. Res."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"544","DOI":"10.1007\/s00774-019-01081-1","article-title":"Oral contraceptive use, bone mineral density, and bone turnover markers over 12 months in college-aged females","volume":"38","author":"Almstedt","year":"2020","journal-title":"J. Bone Miner. Metab."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"517","DOI":"10.1111\/cen.13932","article-title":"Adolescent use of combined hormonal contraception and peak bone mineral density accrual: A meta-analysis of international prospective controlled studies","volume":"90","author":"Goshtasebi","year":"2019","journal-title":"Clin. Endocrinol."},{"key":"ref_19","first-page":"227","article-title":"Combined hormonal contraceptives use and bone mineral density changes in adolescent and young women in a prospective population-based Canada-wide observational study","volume":"18","author":"Brajic","year":"2018","journal-title":"J. Musculoskelet Neuronal Interact."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1123\/ijsnem.16.1.1","article-title":"The prevalence of disordered eating, menstrual dysfunction, and low bone mineral density among US collegiate athletes","volume":"16","author":"Beals","year":"2006","journal-title":"Int. J. Sport Nutr. Exerc. Metab."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"711","DOI":"10.1249\/01.MSS.0000064935.68277.E7","article-title":"Disordered eating, menstrual irregularity, and bone mineral density in female runners","volume":"35","author":"Cobb","year":"2003","journal-title":"Med. Sci. Sports Exerc."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1001\/archpedi.160.2.137","article-title":"Prevalence of the female athlete triad syndrome among high school athletes","volume":"160","author":"Nichols","year":"2006","journal-title":"Arch. Pediatr. Adolesc. Med."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"393","DOI":"10.1016\/j.bone.2019.06.030","article-title":"Bone mineral density and bone mineral content among female elite athletes","volume":"127","author":"Bellver","year":"2019","journal-title":"Bone"},{"key":"ref_24","first-page":"403","article-title":"Bone mineral density in collegiate female athletes: Comparisons among sports","volume":"42","author":"Mudd","year":"2007","journal-title":"J. Athl. Train."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1684\/epd.2014.0673","article-title":"Osteoporosis is associated with antiepileptic drugs: A population-based study","volume":"16","author":"Wu","year":"2014","journal-title":"Epileptic Disord."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"263","DOI":"10.2310\/7060.2003.2690","article-title":"Health-related challenges in United States Peace Corps volunteers serving for two years in Madagascar","volume":"10","author":"Leutscher","year":"2003","journal-title":"J. Travel Med."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Freire, A.N., Brown, K.N., Fleischer, S.H., Eggett, D.L., Creer, A.R., Graf, M.I., Dyckman, J., Turley, J.M., and Fullmer, S. (2022). Prevalence of Female Athlete Triad Risk Factors among Female International Volunteers and College Age-Matched Controls. Int. J. Environ. Res. Public Health, 19.","DOI":"10.3390\/ijerph19031223"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"324","DOI":"10.2174\/1874325001105010324","article-title":"Bone mineral density in healthy female adolescents according to age, bone age and pubertal breast stage","volume":"5","author":"Moretto","year":"2011","journal-title":"Open Orthop. J."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"363","DOI":"10.1016\/S8756-3282(97)00148-8","article-title":"Physical activity in adolescence and bone density in periand postmenopausal women: A population-based study","volume":"21","author":"Puntila","year":"1997","journal-title":"Bone"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1023\/A:1007496126098","article-title":"Physical activity and bone mineral density in Italian middle-aged women","volume":"14","author":"Bidoli","year":"1998","journal-title":"Eur. J. Epidemiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1249\/00005768-199301000-00011","article-title":"Compendium of physical activities: Classification of energy costs of human physical activities","volume":"25","author":"Ainsworth","year":"1993","journal-title":"Med. Sci. Sports Exerc."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1196\/annals.1429.040","article-title":"The Menstrual Cycle","volume":"1135","author":"Popat","year":"2008","journal-title":"Ann. N. Y. Acad. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"652","DOI":"10.3109\/09513590.2010.486452","article-title":"Hypoestrogenism in young women and its influence on bone mass density","volume":"26","author":"Meczekalski","year":"2010","journal-title":"Gynecol. Endocrinol."},{"key":"ref_34","doi-asserted-by":"crossref","unstructured":"Ravi, S., Kujala, U.M., Tammelin, T.H., Hirvensalo, M., Kovanen, V., Valtonen, M., Waller, B., Aukee, P., Sipil\u00e4, S., and Laakkonen, E.K. (2020). Adolescent sport participation and age at menarche in relation to midlife body composition, bone mineral density, fitness, and physical activity. J. Clin. Med., 9.","DOI":"10.3390\/jcm9123797"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"394","DOI":"10.1080\/03014460802154777","article-title":"Age at menarche of three-generation families in Taiwan","volume":"35","author":"Chang","year":"2008","journal-title":"Ann. Hum. Biol."},{"key":"ref_36","first-page":"361","article-title":"A study to evaluate the relation between the age at menarche and bone mineral density in pre-and post-menopausal women","volume":"9","author":"Gavit","year":"2019","journal-title":"Natl. J. Physiol. Pharm. Pharmacol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"2392","DOI":"10.1210\/jc.2018-00338","article-title":"Bone parameters in anorexia nervosa and athletic amenorrhea: Comparison of two hypothalamic amenorrhea states","volume":"103","author":"Kandemir","year":"2018","journal-title":"J. Clin. Endocrinol. Metab."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1111\/acps.12556","article-title":"Bone mineral density, osteoporosis, and fractures among people with eating disorders: A systematic review and meta-analysis","volume":"133","author":"Solmi","year":"2016","journal-title":"Acta Psychiatr. Scand."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1379","DOI":"10.1111\/sms.13679","article-title":"Effect of transdermal estradiol therapy on bone mineral density of amenorrheic female athletes","volume":"30","author":"Yoshino","year":"2020","journal-title":"Scand. J. Med. Sci. Sports"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1577","DOI":"10.1249\/MSS.0000000000000574","article-title":"Fractures in relation to menstrual status and bone parameters in young athletes","volume":"47","author":"Ackerman","year":"2015","journal-title":"Med. Sci. Sports Exerc."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1020","DOI":"10.1016\/j.fertnstert.2019.01.008","article-title":"Oral contraceptives partially protect from bone loss in young women with anorexia nervosa","volume":"111","author":"Renard","year":"2019","journal-title":"Fertil. Steril."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"213","DOI":"10.1080\/13625187.2020.1743826","article-title":"Contraception in adolescents with anorexia nervosa. Is there evidence for a negative impact of combined hormonal contraceptives on bone mineral density and the course of the disease?","volume":"25","author":"Bitzer","year":"2020","journal-title":"Eur. J. Contracept. Reprod. Health Care"},{"key":"ref_43","first-page":"100223","article-title":"Oral ethinyl estradiol treatment in women with cystic fibrosis is associated with lower bone mineral density","volume":"20","author":"Wu","year":"2020","journal-title":"J. Clin. Transl. Endocrinol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"98","DOI":"10.1016\/j.afos.2017.02.001","article-title":"The correlation between bone mineral density\/trabecular bone score and body mass index, height, and weight","volume":"3","author":"Kim","year":"2017","journal-title":"Osteoporos. Sarcopen."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"323061","DOI":"10.1155\/2012\/323061","article-title":"Are selective serotonin reuptake inhibitors a secondary cause of low bone density?","volume":"2012","author":"Chau","year":"2012","journal-title":"J. Osteoporos."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"2655","DOI":"10.1007\/s00198-016-3617-4","article-title":"The effects of weight loss approaches on bone mineral density in adults: A systematic review and meta-analysis of randomized controlled trials","volume":"27","author":"Soltani","year":"2016","journal-title":"Osteoporos. Int."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1002\/jbmr.5650050614","article-title":"Influence of age and body weight on spine and femur bone mineral density in US white men","volume":"5","author":"Mazess","year":"1990","journal-title":"J. Bone Miner. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1007\/s40519-018-0521-2","article-title":"Associations between exercise, bone mineral density, and body composition in adolescents with anorexia nervosa","volume":"24","author":"Nagata","year":"2019","journal-title":"Eat. Weight Disord."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"100","DOI":"10.1055\/s-0030-1268503","article-title":"Effect of high-impact aerobics and strength training on BMD in young women aged 20\u201335 years","volume":"32","author":"Liang","year":"2011","journal-title":"Int. J. Sports Med."},{"key":"ref_50","unstructured":"Fullmer, S. (2004). Lumbar Spine and Total Hip Bone Mineral Density Are Not Related to Current Aerobic Activity in Healthy College-Age Women. [Doctoral Disseratation, Brigham Young University]."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"67","DOI":"10.1136\/bjsm.37.1.67","article-title":"Physiological factors associated with low bone mineral density in female endurance runners","volume":"37","author":"Burrows","year":"2003","journal-title":"Br. J. Sports Med."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"74","DOI":"10.4082\/kjfm.2018.39.2.74","article-title":"The association between fat mass, lean mass and bone mineral density in premenopausal women in Korea: A cross-sectional study","volume":"39","author":"Kim","year":"2018","journal-title":"Korean J. Fam. Med."},{"key":"ref_53","doi-asserted-by":"crossref","unstructured":"Bierhals, I.O., dos Santos Vaz, J., Bielemann, R.M., de Mola, C.L., Barros, F.C., Gon\u00e7alves, H., Wehrmeister, F.C., and Assun\u00e7\u00e3o, M.C.F. (2019). Associations between body mass index, body composition and bone density in young adults: Findings from a southern Brazilian cohort. BMC Musculoskelet. Disord., 20.","DOI":"10.1186\/s12891-019-2656-3"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1002\/ajpa.23398","article-title":"Relationship between body mass, lean mass, fat mass, and limb bone cross-sectional geometry: Implications for estimating body mass and physique from the skeleton","volume":"166","author":"Pomeroy","year":"2018","journal-title":"Am. J. Phys. Anthropol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"E448","DOI":"10.1152\/ajpendo.00293.2017","article-title":"Increased body fat mass explains the positive association between circulating estradiol and insulin resistance in postmenopausal women","volume":"314","author":"Marchand","year":"2018","journal-title":"Am. J. Physiol.-Endocrinol. Metab."}],"container-title":["International Journal of Environmental Research and Public Health"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/16\/10363\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T00:12:38Z","timestamp":1760141558000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1660-4601\/19\/16\/10363"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,19]]},"references-count":55,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2022,8]]}},"alternative-id":["ijerph191610363"],"URL":"https:\/\/doi.org\/10.3390\/ijerph191610363","relation":{},"ISSN":["1660-4601"],"issn-type":[{"type":"electronic","value":"1660-4601"}],"subject":[],"published":{"date-parts":[[2022,8,19]]}}}