Long or Highly Irregular Menstrual Cycles as a Marker for Risk of Type 2 Diabetes Mellitus
Abstract
CONTEXT: Although oligomenorrhea has been associated cross-sectionally with insulin resistance and glucose intolerance, it is not known whether oligomenorrhea is a marker for increased future risk of type 2 diabetes mellitus (DM). OBJECTIVE: To prospectively assess risk of type 2 DM in women with a history of long or highly irregular menstrual cycles. DESIGN AND SETTING: The Nurses' Health Study II, a prospective observational cohort study. PARTICIPANTS: A total of 101 073 women who had no prior history of DM and who reported their usual menstrual cycle pattern at age 18 to 22 years on the baseline (1989) questionnaire. MAIN OUTCOME MEASURE: Incident reports of DM, with follow-up through 1997, compared among women categorized by menstrual cycle length (5 categories). RESULTS: During 564 333 person-years of follow-up, there were 507 cases of type 2 DM. Compared with women with a usual cycle length of 26 to 31 days (referent category) at age 18 to 22 years, the relative risk (RR) of type 2 DM among women with a menstrual cycle length that was 40 days or more or was too irregular to estimate was 2.08 (95% confidence interval [CI], 1.62-2.66), adjusting for body mass index at age 18 years and several other potential confounding variables. The RR of type 2 DM associated with long or highly irregular menstrual cycles was greater in obese women, but was also increased in nonobese women (at body mass indexes at age 18 years of <25, 25-29, and >/=30 kg/m, RRs were 1.67 [95% CI, 1.14-2.45], 1.74 [95% CI, 1.07-2.82], and 3.86 [95% CI, 2.33-6.38], respectively). CONCLUSION: Women with long or highly irregular menstrual cycles have a significantly increased risk for developing type 2 DM that is not completely explained by obesity.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
PCOS is associated with a two times increased risk for type 2 diabetes.
“For this reason, PCOS is associated with a two times increased risk for type 2 diabetes (T2D) [15].”
From From Prediabetes to Type 2 Diabetes Mellitus in Women with Polycystic Ovary Syndrome: Lifestyle and Pharmacological Management (2020) · cites this paper as [15]
Cites
Classification and diagnosis of diabetes mellitus and other categories of glucose intolerance.
National Diabetes Data Group (1979) · Diabetes · doi:10.2337/diab.28.12.1039 · Cited by 4,909 · see citing works
Diet, lifestyle, and the risk of type 2 diabetes mellitus in women.
Hu, F. B., Manson, J. E., Stampfer, M. J., Colditz, G., Liu, S., Solomon, C. G., & Willett, W. C. (2001) · New England Journal of Medicine · doi:10.1056/nejmoa010492 · Cited by 2,901 · see citing works
Self-citationHarris, M. I., Flegal, K. M., Cowie, C. C., Eberhardt, M. S., Goldstein, D. E., Little, R. R., Wiedmeyer, H.-M., & Byrd-Holt, D. D. (1998) · Diabetes Care · doi:10.2337/diacare.21.4.518 · Cited by 2,703 · see citing works
Profound Peripheral Insulin Resistance, Independent of Obesity, in Polycystic Ovary Syndrome
Dunaif, A., Segal, K. R., Futterweit, W., & Dobrjansky, A. (1989) · Diabetes · doi:10.2337/diab.38.9.1165 · Cited by 1,967 · see citing works
Legro, R. S. (1999) · Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.84.1.165 · Cited by 1,743 · see citing works
Lillioja, S., Mott, D. M., Spraul, M., Ferraro, R., Foley, J. E., Ravussin, E., Knowler, W. C., Bennett, P. H., & Bogardus, C. (1993) · New England Journal of Medicine · doi:10.1056/nejm199312303292703 · Cited by 1,508 · see citing works
Prevalence of impaired glucose tolerance and diabetes in women with polycystic ovary syndrome.
Ehrmann, D. A., Barnes, R. B., Rosenfield, R. L., Cavaghan, M. K., & Imperial, J. (1999) · Diabetes Care · doi:10.2337/diacare.22.1.141 · Cited by 1,257 · see citing works
Diamanti‐Kandarakis, E., Kouli, C., Bergiele, A. T., Filandra, F. A., Tsianateli, T. C., Spina, G., Zapanti, E. D., & Bartzis, M. I. (1999) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.84.11.6148 · Cited by 1,107 · see citing works
Screening for type 2 diabetes.
Engelgau, M. M., Narayan, K. M. V., & Herman, W. H. (2000) · Diabetes Care · doi:10.2337/diacare.23.10.1563 · Cited by 1,027 · see citing works
Prevalence of polycystic ovaries in women with anovulation and idiopathic hirsutism.
Adams, J., POLSON, D. W., & Franks, S. (1986) · BMJ · doi:10.1136/bmj.293.6543.355 · Cited by 975 · see citing works
Insulin resistance in nonobese patients with polycystic ovarian disease
CHANG, R. J., NAKAMURA, R. M., JUDD, H. L., & KAPLAN, S. A. (1983) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-57-2-356 · Cited by 704 · see citing works
Manson, J. E. (1991) · Archives of Internal Medicine · doi:10.1001/archinte.1991.00400060077013 · Cited by 675 · see citing works
Dunaif, A. E., GRAF, M., Mandeli, J., Laumas, V., & Dobrjansky, A. (1987) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem-65-3-499 · Cited by 577 · see citing works
Cigarette smoking, relative weight, and menopause.
WILLETT, W., STAMPFER, M. J., BAIN, C., LIPNICK, R., SPEIZER, F. E., ROSNER, B., CRAMER, D., & HENNEKENS, C. H. (1983) · American Journal of Epidemiology · doi:10.1093/oxfordjournals.aje.a113598 · Cited by 558 · see citing works
Dunaif, A. E., & Finegood, D. T. (1996) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.81.3.8772555 · Cited by 454 · see citing works
Epidemiology of infertility and polycystic ovarian disease: endocrinological and demographic studies
Hull, M. G. R. (1987) · Gynecological Endocrinology · doi:10.3109/09513598709023610 · Cited by 423 · see citing works
Induction of insulin resistance by androgens and estrogens
Polderman, K. H., Gooren, L. J., Asscheman, H., Bakker, A., & Heine, R. J. (1994) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.79.1.8027240 · Cited by 382 · see citing works
The validity of recalled weight among younger women.
Troy, L. M., Hunter, D. J., Manson, J. E., Colditz, G. A., Stampfer, M. J., & Willett, W. C. (1995) · PubMed · Cited by 330 · see citing works
Insulin resistance, secretion, and metabolism in users of oral contraceptives
Godsland, I. F., Walton, C., Felton, C. V., Proudler, A. J., Patel, A., & Wynn, V. (1992) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.74.1.1530790 · Cited by 252 · see citing works
Haffner, S. M., Valdez, R. A., Morales, P. A., Hazuda, H. P., & D, M. P. S. M. (1993) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.77.1.8325960 · Cited by 178 · see citing works
The relationship of sex hormones to hyperinsulinemia and hyperglycemia
Haffner, S. M., Katz, M. S., Stern, M. P., & Dunn, J. F. (1988) · Metabolism · doi:10.1016/0026-0495(88)90091-1 · Cited by 140 · see citing works
Menstrual disorders in college students
Singh, K. B. (1981) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(81)90277-5 · Cited by 93 · see citing works
American Diabetes Association (1998) · Diabetes Care · doi:10.2337/diacare.21.1.s20 · Cited by 77 · see citing works
DIAGNOSIS OF POLYCYSTIC OVARY SYNDROME
Chang, R. J., & Katz, S. E. (1999) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(05)70076-1 · Cited by 71 · see citing works
The Relationship of Menstrual Irregularity to Type 2 Diabetes in Pima Indian Women
Roumain, J., Charles, M.-A. A., de Courten, M., Hanson, R. L., Brodie, T. D., Pettitt, D. J., & Knowler, W. C. (1998) · Diabetes Care · doi:10.2337/diacare.21.3.346 · Cited by 55 · see citing works
Weiss, D. J., Charles, M.-A. A., Dunaif, A. E., Prior, D. E., Lillioja, S., Knowler, W. C., & Herman, W. H. (1994) · Metabolism · doi:10.1016/0026-0495(94)90257-7 · Cited by 48 · see citing works
Polycystic ovary syndrome: Current and future treatment paradigms
Legro, R. S. (1998) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(98)70240-6 · Cited by 47 · see citing works
Streets, P. (2001) · BMJ · doi:10.1136/bmj.323.7310.453a · Cited by 40 · see citing works
Chasan‐Taber, L., Willett, W. C., Stampfer, M. J., Hunter, D. J., Colditz, G. A., Spiegelman, D. L., & Manson, J. E. (1997) · ScholarWorks@UMassAmherst (University of Massachusetts Amherst) · Cited by 2 · see citing works
Hosmer (1997) · doi:10.1002/(sici)1097-0258(19970515)16:9
Flagged first, then by citations
1 of the 31 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
The Prevalence and Features of the Polycystic Ovary Syndrome in an Unselected Population
Azziz, R., Woods, K. S., Reyna, R., Key, T. J., Knochenhauer, E. S., & Yıldız, B. O. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-032046 · Cited by 2,715 · see citing works
“4% rate of physician-diagnosed hirsutism reported by the participants of the Nurses’ Health Study II (19).”
Azziz, R., Carmina, E., Dewailly, D., Diamanti-Kandarakis, E., Escobar-Morreale, H. F., Futterweit, W., Janssen, O. E., Legro, R. S., Norman, R. J., Taylor, A. E., et al. (2009) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.06.035 · Cited by 2,132 · see citing works
“9% reported by 101,073 women participating in the Nurses’ Health Study II for cycles R32 days in length (57).”
BackgroundFauser, B. C. J. M., Tarlatzis, B. C., Rebar, R. W., Legro, R. S., Balen, A. H., Lobo, R., Carmina, E., Chang, J., Yildiz, B. O., Laven, J. S. E., et al. (2012) · Fertility and Sterility · doi:10.1016/j.fertnstert.2011.09.024 · Cited by 1,976 · see citing works
Diamanti-Kandarakis, E., & Dunaif, A. (2012) · Endocrine Reviews · doi:10.1210/er.2011-1034 · Cited by 1,947 · see citing works
Azziz, R., Carmina, E., Chen, Z., Dunaif, A., Laven, J. S. E., Legro, R. S., Lizneva, D., Natterson-Horowtiz, B., Teede, H. J., & Yildiz, B. O. (2016) · Nature Reviews Disease Primers · doi:10.1038/nrdp.2016.57 · Cited by 2,005 · see citing works
Norman, R. J., Dewailly, D., Legro, R. S., & Hickey, T. E. (2007) · The Lancet · doi:10.1016/s0140-6736(07)61345-2 · Cited by 1,360 · see citing works
Franks, S. (1997) · Archives of Disease in Childhood · doi:10.1136/adc.77.1.89 · Cited by 802 · see citing works
Day, F., Karaderi, T., Jones, M. R., Meun, C., He, C., Drong, A., Kraft, P., Lin, N., Huang, H., Broer, L., et al. (2018) · PLOS Genetics · doi:10.1371/journal.pgen.1007813 · Cited by 619 · see citing works
Azziz, R., Marin, C., Hoq, L., Badamgarav, E., & Song, P. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-0628 · Cited by 537 · see citing works
Menstrual cycle irregularity and risk for future cardiovascular disease
Solomon, C. G., Hu, F. B., Dunaif, A., Rich-Edwards, J. E., Stampfer, M. J., Willett, W. C., Speizer, F. E., & Manson, J. E. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.5.8471 · Cited by 528 · see citing works
“In populationbased studies, oligomenorrhea has been associated with hyperinsulinemia (1) and with increased prevalence (4) and future risk of type 2 diabetes mellitus (5).”
BackgroundResultInfluentialSelf-citationPolycystic ovary syndrome and cardiovascular disease: a premature association?
Legro, R. S. (2003) · Endocrine Reviews · doi:10.1210/er.2003-0004 · Cited by 466 · see citing works
“The Nurse’s Health Study has also identified oligomenorrhea and highly irregular menstrual cycles as risk factors for developing type 2 diabetes, a major risk factor in itself for CVD, especially in women (67).”
BackgroundInsulin resistance, polycystic ovary syndrome, and type 2 diabetes mellitus
Ovalle, F., & Azziz, R. (2002) · Fertility and Sterility · doi:10.1016/s0015-0282(02)03111-4 · Cited by 428 · see citing works
Shaw, L. J., Bairey Merz, C. N., Azziz, R., Stanczyk, F. Z., Sopko, G., Braunstein, G. D., Kelsey, S. F., Kip, K. E., Cooper-DeHoff, R. M., Johnson, B. D., et al. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2007-0425 · Cited by 427 · see citing works
“Consistent with prior data, we did find a significantly higher prevalence of diabetes mellitus among our postmenopausal women with clinical features of PCOS (32, 41), but notably our results also demonstrate a strong association between PCOS status and CV events that is independent of diabetes.”
ResultRetractedEpidemiology and Adverse Cardiovascular Risk Profile of Diagnosed Polycystic Ovary Syndrome
Lo, J. C.-M., Feigenbaum, S. L., Yang, J., Pressman, A. R., Selby, J. V., & Go, A. S. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2430 · Cited by 414 · see citing works
“Women with PCOS are more likely to be insulin resistant, overweight, and obese, and several studies have demonstrated that PCOS is associated with an increased risk of glucose intolerance and type 2 diabetes mellitus, independent of body mass index (BMI) (7–10).”
BackgroundImproving reproductive performance in overweight/obese women with effective weight management
Norman, R. J. (2004) · Human Reproduction Update · doi:10.1093/humupd/dmh018 · Cited by 378 · see citing works
“86 for BMI at age 18 of <25, 25± 29 and >30 respectively) (Solomon et al., 2001).”
BackgroundInfluentialVariability in the phases of the menstrual cycle
Fehring, R. J., Schneider, M., & Raviele, K. (2006) · Journal of Obstetric, Gynecologic & Neonatal Nursing · doi:10.1111/j.1552-6909.2006.00051.x · Cited by 376 · see citing works
“Clinicians should be alert for women who have greater than normal variability in their menstrual cycle parameters, this can be a sign of future risk of type 2 diabetes mellitus, heart disease, infertility, poly cystic ovarian disease, and other health problems (Solomon et al., 2001, 2002).”
Consensus on women's health aspects of polycystic ovary syndrome (PCOS)
The Amsterdam ESHRE/ASRM-Sponsored 3rd PCOS Consensus Workshop Group, Fauser, B. C. J. M., Tarlatzis, B. C., Rebar, R. W., Legro, R. S., Balen, A. H., Lobo, R. A., Carmina, H., Chang, R. J., Yıldız, B. O., et al. (2011) · Human Reproduction · doi:10.1093/humrep/der396 · Cited by 368 · see citing works
“There is now compelling evidence from epidemiological data (Solomon et al., 2001) that PCOS is associated with increased risk of impaired glucose tolerance (IGT), GDM and T2D (Dunaif, 1997; Boomsma et al., 2006; Moran et al., 2010).”
BackgroundRegensteiner, J. G., Golden, S., Huebschmann, A. G., Barrett-Connor, E., Chang, A. Y., Chyun, D., Fox, C. S., Kim, C., Mehta, N., Reckelhoff, J. F., et al. (2015) · Circulation · doi:10.1161/cir.0000000000000343 · Cited by 334 · see citing works
Cardiometabolic Aspects of the Polycystic Ovary Syndrome
Randeva, H. S., Tan, B. K., Weickert, M. O., Lois, K. B., Nestler, J. E., Sattar, N. A., & Lehnert, H. (2012) · Endocrine Reviews · doi:10.1210/er.2012-1003 · Cited by 329 · see citing works
Merz, C. N. B., Johnson, B. D., Sharaf, B. L., Bittner, V., Berga, S. L., Braunstein, G. D., Hodgson, T. K., Matthews, K. A., Pepine, C. J., Reís, S. E., et al. (2003) · Journal of the American College of Cardiology · doi:10.1016/s0735-1097(02)02763-8 · Cited by 287 · see citing works
“Menstrual irregularity is also predictive of future diabetes (39) and may be a marker for polycystic ovary syndrome (40), although the low levels of LH observed in women in our study suggest that polycystic ovary disease was not a contributor in this population.”
BackgroundIliodromiti, S., Kelsey, T., Anderson, R. A., & Nelson, S. M. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-1393 · Cited by 281 · see citing works
Obesity and PCOS: Implications for Diagnosis and Treatment
Legro, R. S. (2012) · Seminars in Reproductive Medicine · doi:10.1055/s-0032-1328878 · Cited by 280 · see citing works
Elkind-Hirsch, K., Marrioneaux, O., Bhushan, M., Vernor, D., & Bhushan, R. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-0115 · Cited by 276 · see citing works
“Obesity, particularly abdominal obesity, exacerbates the reproductive and metabolic dysfunction (6, 7). Moreover, the incidence of glucose (Glu) intolerance, gestational diabetes, and type 2 diabetesmellitus(DM2)isincreasedinwomenwithPCOS(2, 8 ,9).”
BackgroundMuscle GLUT4 regulation by estrogen receptors ERβ and ERα
Barros, R. P. A., Machado, U. F., Warner, M., & Gustafsson, J.-Å. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0510391103 · Cited by 263 · see citing works
Descriptive review of the evidence for the use of metformin in polycystic ovary syndrome
Harborne, L., Fleming, R., Lyall, H., Norman, J. E., & Sattar, N. A. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13493-9 · Cited by 256 · see citing works
Influence of Medical Conditions and Lifestyle Factors on the Menstrual Cycle
Rowland, A. S., Baird, D. D., Long, S., Wegienka, G., Harlow, S. D., Alavanja, M., & Sandler, D. P. (2002) · Epidemiology · doi:10.1097/00001648-200211000-00011 · Cited by 239 · see citing works
ACOG Practice Bulletin No. 194: polycystic ovary syndrome
(2018) · Obstetrics & Gynecology · doi:10.1097/aog.0000000000002656 · Cited by 231 · see citing works
“However, a number of cohort studies, including the Nurse’s Health Study, have suggested an increased dose–response risk of cardiovascular disease or events in the presence of increasing oligomenorrhea (40) or with more symptoms of PCOS in a menopausal population (41, 42).”
Is polycystic ovary syndrome associated with high sympathetic nerve activity and size at birth?
Sverrisdóttir, Y. B., Mogren, T., Kataoka, J., Janson, P. O., & Stener-Victorin, E. (2008) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00725.2007 · Cited by 216 · see citing works
“The augmented sympathetic outflow may contribute to the increased prevalence of vascular disease reported in these individuals (4, 30, 40), as well as being involved in the etiology of the condition (15).”
BackgroundOrtega-González, C., Luna, S. L., Hernández, L., Crespo, G., Aguayo, P., Arteaga‐Troncoso, G., & Parra, A. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1965 · Cited by 211 · see citing works
“Women with PCOS and IR have a greater risk for carbohydrate intolerance and type 2 diabetes mellitus (DM) (9, 10), dyslipidemia (11), arterial hypertension (12), coagulation disorders induced by endothelial dysfunction (13), and probably cardiovascular disease (14).”
BackgroundThe management of patients with polycystic ovary syndrome
Jayasena, C. N., & Franks, S. (2014) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2014.102 · Cited by 196 · see citing works
The metabolic syndrome in polycystic ovary syndrome
Essah, P. A., & Nestler, J. E. (2006) · Journal of Endocrinological Investigation · doi:10.1007/bf03345554 · Cited by 194 · see citing works
An epidemiological survey of symptoms of menstrual loss in the community.
Shapley, M., Jordan, K. P., & Croft, P. R. (2004) · Europe PMC (PubMed Central) · Cited by 193 · see citing works
Polycystic ovary syndrome: a “risk-enhancing” factor for cardiovascular disease
Guan, C. S., Zahid, S., Minhas, A., Ouyang, P., Vaught, A. “. J., Baker, V. L., & Michos, E. D. (2022) · Fertility and Sterility · doi:10.1016/j.fertnstert.2022.03.009 · Cited by 207 · see citing works
Female reproduction and type 1 diabetes: From mechanisms to clinical findings
Codner, E., Merino, P. M., & Tena-Sempere, M. (2012) · Human Reproduction Update · doi:10.1093/humupd/dms024 · Cited by 182 · see citing works
“women are linked to increased cardiovascular and metabolic dysfunction (Weiss et al., 1994; Solomon et al., 2001; Solomon et al., 2002), which are also common in women with T1D (Snell-Bergeon et al.”
BackgroundEstrogen receptors: new players in diabetes mellitus
Barros, R. P. A., Machado, U. F., & Gustafsson, J.-Α. (2006) · Trends in Molecular Medicine · doi:10.1016/j.molmed.2006.07.004 · Cited by 183 · see citing works
Insulin resistance: A significant risk factor of endometrial cancer
Mu, N., Zhu, Y., Wang, Y., Zhang, H., & Xue, F. (2012) · Gynecologic Oncology · doi:10.1016/j.ygyno.2012.03.032 · Cited by 186 · see citing works
“found that long or highly irregular menstrual cycles, which suggest functional deficiencies of the ovaries, placed women at increased risk for type II diabetes, and obesity could not completely explain this increased risk [58].”
BackgroundThe impact of bariatric surgery on menstrual patterns
Teitelman, M., Grotegut, C., Williams, N., & Lewis, J. (2006) · Obesity Surgery · doi:10.1381/096089206778870148 · Cited by 179 · see citing works
Wang, Y., Arvizu, M., Rich-Edwards, J. W., Stuart, J. J., Manson, J. E., Missmer, S. A., Pan, A., & Chavarro, J. E. (2020) · BMJ · doi:10.1136/bmj.m3464 · Cited by 179 · see citing works
Diamanti‐Kandarakis, E., Baillargeon, J., Iuorno, M. J., Jakubowicz, D. J., & Nestler, J. E. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021528 · Cited by 168 · see citing works
Yamamoto, K., Okazaki, A., Sakamoto, Y., & Funatsu, M. (2009) · Journal of PHYSIOLOGICAL ANTHROPOLOGY · doi:10.2114/jpa2.28.129 · Cited by 163 · see citing works
Factors associated with menstrual cycle irregularity and menopause
Bae, J., Park, S., & Kwon, J. (2018) · BMC Women s Health · doi:10.1186/s12905-018-0528-x · Cited by 161 · see citing works
Participation of ERα and ERβ in glucose homeostasis in skeletal muscle and white adipose tissue
Barros, R. P. A., Gabbi, C., Morani, A., Warner, M., & Gustafsson, J.-Å. (2009) · American Journal of Physiology-Endocrinology and Metabolism · doi:10.1152/ajpendo.00189.2009 · Cited by 155 · see citing works
Validity of Self-Reported Menstrual Cycle Length
Small, C. M., Manatunga, A. K., & Marcus, M. (2006) · Annals of Epidemiology · doi:10.1016/j.annepidem.2006.05.005 · Cited by 154 · see citing works
Ethnic differences in the phenotypic expression of polycystic ovary syndrome
Zhao, Y., & Qiao, J. (2013) · Steroids · doi:10.1016/j.steroids.2013.04.006 · Cited by 152 · see citing works
Clinical characteristics of polycystic ovary syndrome in Indian women
Ramanand, S., Ghongane, B. B., Ramanand, J. B., Patwardhan, M., Ghanghas, R. R., & Jain, S. (2013) · Indian Journal of Endocrinology and Metabolism · doi:10.4103/2230-8210.107858 · Cited by 142 · see citing works
“Nurses’ Health study II reported that over an 8‐year period, the conversion rate to type 2 diabetes among oligomenorrheic women was approximately two‐fold greater than that for eumenorrheic women, regardless of whether the oligomenorrheic women were obese or lean, indicating that oligomenorrhea was an independent pred…”
Bloomgarden, Z. T. (2003) · Diabetes Care · doi:10.2337/diacare.26.3.933 · Cited by 144 · see citing works
Insulin Sensitizers for Polycystic Ovary Syndrome
Baillargeon, J., Iuorno, M. J., & Nestler, J. E. (2003) · Clinical Obstetrics & Gynecology · doi:10.1097/00003081-200306000-00011 · Cited by 132 · see citing works
“An analysis of 101,073 women in the Nurses’ Health Study II reported that over an 8-year period, the conversion rate to type 2 diabetes among oligomenorrheic women was approximately twice than that for eumenorrheic women, regardless of whether the oligomenorrheic women were obese or lean, indicating that oligomenorrhe…”
BackgroundEisenhardt, S., Schwarzmann, N., Henschel, V., Germeyer, A., von Wolff, M., Hamann, A., & Strowitzki, T. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-1994 · Cited by 130 · see citing works
Menstrual Cycle Characteristics
Small, C. M., Manatunga, A. K., Klein, M., Feigelson, H. S., Dominguez, C. E., McChesney, R. E., & Marcus, M. (2005) · Epidemiology · doi:10.1097/01.ede.0000190540.95748.e6 · Cited by 128 · see citing works
Menstrual cycle related mood changes in women with bipolar disorder
Rasgon, N., Bauer, M., Glenn, T., Elman, S., & Whybrow, P. C. (2003) · Bipolar Disorders · doi:10.1034/j.1399-5618.2003.00010.x · Cited by 119 · see citing works
Reproductive function and risk for PCOS in women treated for bipolar disorder
Rasgon, N., Altshuler, L. L., Fairbanks, L. A., Elman, S., Bitran, J. A., Labarca, R., Saad, M. F., Kupka, R., Nolen, W. A., Frye, M. A., et al. (2005) · Bipolar Disorders · doi:10.1111/j.1399-5618.2005.00201.x · Cited by 118 · see citing works
The importance of insulin resistance in polycystic ovary syndrome
Goodarzi, M. O., & Korenman, S. G. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)00734-9 · Cited by 118 · see citing works
“In the Nurses’ Health Study, the risk of development of diabetes was increased two-fold among women with long or irregular menstrual cycles, including the nonobese women (39).”
BackgroundPolycystic Ovary Syndrome and Risk for Long-Term Diabetes and Dyslipidemia
Wang, E. T., Calderon-Margalit, R., Cedars, M. I., Daviglus, M. L., Merkin, S. S., Schreiner, P. J., Sternfeld, B., Wellons, M., Schwartz, S. M., Lewis, C. E., et al. (2011) · Obstetrics & Gynecology · doi:10.1097/aog.0b013e31820209bb · Cited by 146 · see citing works
Lo, J. C., Feigenbaum, S. L., Escobar, G. J., Yang, J., Crites, Y. M., & Ferrara, A. (2006) · Diabetes Care · doi:10.2337/dc06-0877 · Cited by 112 · see citing works
Taponen, S., Martikainen, H. K., Järvelin, M., Sovio, U., Laitinen, J. H., Pouta, A. M., Hartikainen, A., McCarthy, M. I., Franks, S., Paldanius, M., et al. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-031720 · Cited by 111 · see citing works
The Utility of Menstrual Cycle Length as an Indicator of Cumulative Hormonal Exposure
Mumford, S. L., Steiner, A. Z., Pollack, A. Z., Perkins, N. J., Filiberto, A. C., Albert, P. S., Mattison, D. R., Wactawski‐Wende, J., & Schisterman, E. F. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-1350 · Cited by 109 · see citing works
Searching for polycystic ovary syndrome in postmenopausal women
Krentz, A. J., von Mühlen, D. G., & Barrett-Connor, E. L. (2007) · Menopause The Journal of The North American Menopause Society · doi:10.1097/gme.0b013e31802cc7ab · Cited by 108 · see citing works
“irregular menses predicts the development of both CVD(62) and diabetes.(63) A recent cross-sectional study from Finland reported that premenopausal women”
BackgroundMenstrual Bleeding Patterns Among Regularly Menstruating Women
Dasharathy, S. S., Mumford, S. L., Pollack, A. Z., Perkins, N. J., Mattison, D. R., Wactawski‐Wende, J., & Schisterman, E. F. (2012) · American Journal of Epidemiology · doi:10.1093/aje/kwr356 · Cited by 107 · see citing works
“Our findings provide a baseline for women and medical professionals when considering abnormalities in bleeding patterns in regularly menstruating women and suggest that detailed characterizations of bleeding patterns may provide noninvasive markers for endocrine status in a given cycle, which could be associated with…”
BackgroundCobin, R. H., Futterweit, W., Nestler, J. E., Reaven, G. M., Jellinger, P. S., Handelsman, Y., Redmond, G. P., & Thatcher, S. S. (2005) · Endocrine Practice · doi:10.4158/ep.11.2.125 · Cited by 104 · see citing works
Li, K., Urteaga, I., Wiggins, C. H., Druet, A., Shea, A. A., Vitzthum, V. J., & Elhadad, N. (2020) · npj Digital Medicine · doi:10.1038/s41746-020-0269-8 · Cited by 100 · see citing works
Sam, S., Legro, R. S., Essah, P. A., Apridonidze, T., & Dunaif, A. E. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0602025103 · Cited by 96 · see citing works
LeBlanc, E. S., Kapphahn, K., Hedlin, H., Desai, M., Parikh, N. I., Liu, S., Parker, D. R., Anderson, M. L., Aroda, V. R., Sullivan, S. D., et al. (2016) · Menopause The Journal of The North American Menopause Society · doi:10.1097/gme.0000000000000714 · Cited by 95 · see citing works
Gender-related hormonal risk factors for oral cancer
Suba, Z. (2007) · Pathology & Oncology Research · doi:10.1007/bf02893499 · Cited by 94 · see citing works
Menstrual Cycle Irregularity and Metabolic Disorders: A Population-Based Prospective Study
Dovom, M. R., Tehrani, F. R., Djalalinia, S., Cheraghi, L., Behboudi‐Gandevani, S., & Azizi, F. (2016) · PLoS ONE · doi:10.1371/journal.pone.0168402 · Cited by 90 · see citing works
Menstrual irregularity and asthma and lung function
Real, F. G., Svanes, C., Omenaas, E. R., Antó, J. M., Plana, E., Janson, C., Jarvis, D., Zemp, E., Wjst, M., Leynaert, B., et al. (2007) · Journal of Allergy and Clinical Immunology · doi:10.1016/j.jaci.2007.04.041 · Cited by 90 · see citing works
Merz, C. N. B., Shaw, L. J., Azziz, R., Stanczyk, F. Z., Sopko, G., Braunstein, G. D., Kelsey, S. F., Kip, K. E., Cooper-DeHoff, R. M., Johnson, B. D., et al. (2016) · Journal of Women's Health · doi:10.1089/jwh.2015.5441 · Cited by 87 · see citing works
“%) were postmenopausal, nonhormone therapy and nonoral contraceptive users, who could be classified for clinical features of PCOS.”
BackgroundInfluentialLongterm management of Polycystic Ovarian Syndrome (PCOS)
Bates, G. W., & Legro, R. S. (2013) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2012.10.029 · Cited by 106 · see citing works
“The second iteration of the Nurses Health Study demonstrated that women who reported long or irregular cycles between 18 and 22 years of age were twice as likely to subsequently develop diabetes even when controlling for obesity (Solomon et al., 2001).”
Insulin resistance of pregnancy involves estrogen-induced repression of muscle GLUT4
Barros, R. P. A., Morani, A., Moriscot, A. S., & Machado, U. F. (2008) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2008.07.008 · Cited by 84 · see citing works
“…be involved in the gestational-induced insulin resistance, since other41 conditions characterized by elevated levels of estrogen are also accompanied by insulin 42 resistance (Solomon et al., 2001, Okuno et al., 1995, Livingstone and Collison, 2002, Kaaja 43 and Greer, 2005, Dunaif et al., 1989).”
BackgroundWang, Y., Shan, Z., Arvizu, M., Pan, A., Manson, J. E., Missmer, S. A., Sun, Q., & Chavarro, J. E. (2020) · JAMA Network Open · doi:10.1001/jamanetworkopen.2020.27928 · Cited by 83 · see citing works
Bloomgarden, Z. T. (2003) · Diabetes Care · doi:10.2337/diacare.26.4.1297 · Cited by 81 · see citing works
Association between sleep duration and menstrual cycle irregularity in Korean female adolescents
Nam, G. E., Han, K., & Lee, G. (2017) · Sleep Medicine · doi:10.1016/j.sleep.2017.04.009 · Cited by 80 · see citing works
The Severity of Menstrual Dysfunction as a Predictor of Insulin Resistance in PCOS
Brower, M. A., Brennan, K., Pall, M., & Azziz, R. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-2815 · Cited by 79 · see citing works
The hypothalamus–pituitary–ovary axis and type 1 diabetes mellitus: a mini review
Arrais, R. F., & Dib, S. A. (2005) · Human Reproduction · doi:10.1093/humrep/dei353 · Cited by 79 · see citing works
“…as a possible indicator for predicting the risk of glucose intolerance or of the development of T2DM (Pulido and Salazar, 1999; Cooper et al., 2000; Solomon et al., 2001) within the general population and especially in high-risk groups such as the Pima Indian women of Arizona (Roumain et al.,…”
InfluentialDefinitions of the Insulin Resistance Syndrome
Bloomgarden, Z. T. (2004) · Diabetes Care · doi:10.2337/diacare.27.3.824 · Cited by 78 · see citing works
“Women with PCOS have 30 and 10% prevalence of impaired glucose tolerance and diabetes, respectively (22), and in the Nurses’ Health Study (NHS) of 101,073 women followed for 8 years, oligomenorrheic women had a twofold higher rate of conversion to type 2 diabetes (23).”
BackgroundRacial and Ethnic Differences in Physiology and Clinical Symptoms of Polycystic Ovary Syndrome
Wang, S.-P., & Alvero, R. J. (2013) · Seminars in Reproductive Medicine · doi:10.1055/s-0033-1348895 · Cited by 74 · see citing works
Menses resumption after cancer treatment–induced amenorrhea occurs early or not at all
Jacobson, M. H., Mertens, A. C., Spencer, J. B., Manatunga, A. K., & Howards, P. P. (2015) · Fertility and Sterility · doi:10.1016/j.fertnstert.2015.11.020 · Cited by 75 · see citing works
“Further, it may serve as a marker for more than just reproductive health (3); recent literature suggests that menstrual function patterns are linked to bone fracture and osteoporosis (8, 9), cardiovascular disease (10, 11) and mortality (12), breast (13) and ovarian cancer (14), diabetes mellitus (15, 16), and decreas…”
BackgroundAssociation of asthma and hay fever with irregular menstruation
Svanes, C. (2005) · Thorax · doi:10.1136/thx.2004.032615 · Cited by 74 · see citing works
Retarding the progression of renal disease
Brenner, B. M. (2003) · Kidney International · doi:10.1046/j.1523-1755.2003.t01-2-00052.x · Cited by 74 · see citing works
Yu, M., Han, K., & Nam, G. E. (2016) · Journal of Affective Disorders · doi:10.1016/j.jad.2016.11.036 · Cited by 73 · see citing works
“…health; women with this condition could experience serious health outcomes, such as breast cancer (Harlow and Ephross, 1995), type 2 diabetes (Solomon et al., 2001), cardiovascular disease (Solomon et al., 2002), osteoporosis (Kaplan and Manuck, 2004), and infertility (Klemetti et al.,…”
Timing of Menopause and Patterns of Menstrual Bleeding
Weinstein, M. (2003) · American Journal of Epidemiology · doi:10.1093/aje/kwg223 · Cited by 67 · see citing works
Tomlinson, J., Millward, A., Stenhouse, E., & Pinkney, J. (2010) · Diabetic Medicine · doi:10.1111/j.1464-5491.2010.02994.x · Cited by 66 · see citing works
Key Developments in Endocrine Disrupter Research and Human Health
Phillips, K. P., & Foster, W. G. (2008) · Journal of Toxicology and Environmental Health Part B · doi:10.1080/10937400701876194 · Cited by 67 · see citing works
“A role for sex steroids, including estrogens, in glucose homeostasis was suggested by both normal physiology (menstrual cycle [Case & Reid, 2001; Solomon et al., 2001], pregnancy [Okuno et al., 1995; Kaaja and Greer, 2005]) and pathological conditions, including gestational diabetes mellitus…”
BackgroundCardiometabolic Risk in PCOS: More than a Reproductive Disorder
Torchen, L. C. (2017) · Current Diabetes Reports · doi:10.1007/s11892-017-0956-2 · Cited by 65 · see citing works
Palm-Fischbacher, S., & Ehlert, U. (2014) · Journal of Psychosomatic Obstetrics & Gynecology · doi:10.3109/0167482x.2014.912209 · Cited by 67 · see citing works
Sharma, S. T., & Nestler, J. E. (2006) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2006.02.003 · Cited by 64 · see citing works
Flannery, C. A., Rackow, B., Cong, X., Duran, E., Selen, D. J., & Burgert, T. S. (2013) · Pediatric Diabetes · doi:10.1111/j.1399-5448.2012.00902.x · Cited by 62 · see citing works
Glueck, C. J., Morrison, J. A., Daniels, S., Wang, P., & Stroop, D. (2011) · The Journal of Pediatrics · doi:10.1016/j.jpeds.2011.01.018 · Cited by 63 · see citing works
Glucose intolerance states in women with the polycystic ovary syndrome
Pasquali, R., & Gambineri, A. (2013) · Journal of Endocrinological Investigation · doi:10.1007/bf03346757 · Cited by 63 · see citing works
“In the Nurses Health Study II (14), the risk for T2D was significantly increased in women with menstrual irregularities, even after adjusting for multiple confounders [relative risk 1.”
Whitworth, K. W., Baird, D. D., Stene, L. C., Skjærven, R., & Longnecker, M. P. (2010) · Diabetologia · doi:10.1007/s00125-010-2003-6 · Cited by 63 · see citing works
“However, the Nurses’ Health Study reported an increased risk of developing type 2 diabetes among women with long cycles (RR 2.0 [95% CI 1.6–2.7]) or very irregular cycles (RR 1.5 [95% CI 1.3–1.8]) [ 4 ].”
InfluentialGaete, X., Vivanco, M., Eyzaguirre, F. C., López, P., Rhumie, H. K., Unanue, N., & Codner, E. (2010) · Fertility and Sterility · doi:10.1016/j.fertnstert.2009.08.039 · Cited by 73 · see citing works
History of infertility and risk of type 2 diabetes mellitus: a prospective cohort study
Tobias, D. K., Gaskins, A. J., Missmer, S. A., Hu, F. B., Manson, J. E., Louis, G. M. B., Zhang, C., & Chavarro, J. E. (2015) · Diabetologia · doi:10.1007/s00125-015-3493-z · Cited by 62 · see citing works
“However, in support of a role for PCOS in the observed association, long and irregular menstrual cycles (a manifestation of PCOS) were previously linked to a higher risk of type 2 diabetes in this cohort [36].”
BackgroundAssociations Between Psychiatric Disorders and Menstrual Cycle Characteristics
Barron, M. L., Flick, L. H., Cook, C. A. L., Homan, S. M., & Campbell, C. R. (2008) · Archives of Psychiatric Nursing · doi:10.1016/j.apnu.2007.11.001 · Cited by 60 · see citing works
“…cycle patterns can have a direct influence on physical well-being, including ovarian function, pregnancy maintenance, cardiovascular disease, migraine headaches, diabetes mellitus, and breast cancer (Solomon et al., 2002; Solomon et al, 2001; Terry, Willett, RichEdwards, Hunter & Michels, 2005).”
BackgroundTreatment of polycystic ovary syndrome with insulin-lowering agents
Wang, P., Streicher, P., & Glueck, C. J. (2002) · Expert Opinion on Pharmacotherapy · doi:10.1517/14656566.3.8.1177 · Cited by 62 · see citing works
“In Type 2 diabetes, 82% of women have polycystic ovaries on ultrasound [84] and 27% of women with Type 2 diabetes have been shown to have PCOS [85].”
BackgroundMental health, psychotropic medication use, and menstrual cycle characteristics
Nillni, Y. I., Wesselink, A. K., Hatch, E. E., Mikkelsen, E. M., Gradus, J. L., Rothman, K. J., & Wise, L. A. (2018) · Clinical Epidemiology · doi:10.2147/clep.s152131 · Cited by 61 · see citing works
Insulin-sensitizing agents: use in pregnancy and as therapy in polycystic ovary syndrome
Checa, M. Á., Requena, A., Salvador, C., Tur, R., Callejo, J., Espinós, J. J., Fábregues, F., Herrero, J. C., & (Reproductive Endocrinology Interest Group of the Spanish Society of Fertility) (2005) · Human Reproduction Update · doi:10.1093/humupd/dmi015 · Cited by 60 · see citing works
“mellitus in women with PCOS may be independent of obesity (Solomon et al., 2001).”
BackgroundPolycystic ovary syndrome and reproductive health of women: a curious association
Zehravi, M., Maqbool, M., & Ara, I. (2021) · International Journal of Adolescent Medicine and Health · doi:10.1515/ijamh-2021-0031 · Cited by 61 · see citing works
Reproductive risk factors across the female lifecourse and later metabolic health
Nichols, A. R., Chavarro, J. E., & Oken, E. (2024) · Cell Metabolism · doi:10.1016/j.cmet.2024.01.002 · Cited by 59 · see citing works
Insulin resistance in patients with polycystic ovary syndrome
Schröder, A. K., Tauchert, S., Ortmann, O., Diedrich, K., & Weiss, J. M. (2004) · Annals of Medicine · doi:10.1080/07853890410035296 · Cited by 59 · see citing works
Effect of Air Pollution on Menstrual Cycle Length—A Prognostic Factor of Women’s Reproductive Health
Merklinger-Gruchała, A., Grazyna Jasienska, A., & Kapiszewska, M. (2017) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph14070816 · Cited by 58 · see citing works
“Identifying environmental factors affecting menstrual cycle and phase-length is vital from the perspective of public health, because it may have important implications for population health, namely infertility, reproductive cancers [26,27], osteoporosis [28], and metabolic disorders [29,30].”
BackgroundApoptotic Markers Indicate Nonalcoholic Steatohepatitis in Polycystic Ovary Syndrome
Tan, S., Bechmann, L. P., Benson, S., Dietz, T., Eichner, S., Hahn, S., Janssen, O. E., Lahner, H., Gerken, G., Mann, K., et al. (2009) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-1834 · Cited by 58 · see citing works
- Authors
- Solomon, C. G.
- Affiliations
- Brigham and Women's Hospital (US)
- Corresponding author
- Solomon, Caren G.
- ORCID
- Solomon, Caren G.
- Venue
- JAMA
- Publisher
- American Medical Association (AMA)
- Published
- 2001-11-21
- Volume
- 286
- Issue
- 19
- Pages
- 2421
- ISSN
- 0002-9955 (ISSN-L)
- 0098-7484
- OpenAlex
- W2043815784
- Cited by
- 362
- References
- 31
- Citations by year
- 2026: 5 · 2025: 4 · 2024: 11 · 2023: 15 · 2022: 25 · 2021: 23 · 2020: 12 · 2019: 6 · 2018: 15 · 2017: 15 · 2016: 13 · 2015: 14 · 2014: 9 · 2013: 15 · 2012: 23
- FWCI
- 17.24
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- JAMA (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Cancer Institute (CA50385, R01CA050385)
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Ovarian function and disorders
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes, Cardiovascular Risks, and Lipoproteins
- Health Sciences › Medicine › Reproductive Medicine › Hypothalamic control of reproductive hormones
- Keywords
- type 2 diabetes, menstrual cycle length, oligomenorrhea, menstrual irregularity, diabetes risk, obesity, insulin resistance, impaired glucose tolerance, women's health, Nurses' Health Study II
- MeSH terms
- Adult, Diabetes Mellitus, Type 2, Female, Humans, Menstrual Cycle, Obesity, Oligomenorrhea, Prospective Studies, Regression Analysis, Risk Factors, Body Mass Index
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review