[Skip to Navigation]
Sign In
Table 1.  Criteria for Quality of Evidence Classification in Meta-analyses of Cohort Studies
Criteria for Quality of Evidence Classification in Meta-analyses of Cohort Studies
Table 2.  Findings of Significant Associations in Meta-analyses of Randomized Clinical Trials
Findings of Significant Associations in Meta-analyses of Randomized Clinical Trials
Table 3.  Findings of Significant Associations in Meta-analyses of Cohort Studies
Findings of Significant Associations in Meta-analyses of Cohort Studies
1.
United Nations. Contraceptive use by method 2019: data booklet. UN-iLibrary, United Nations; December 2019. Accessed May 15, 2021. https://www.un-ilibrary.org/content/books/9789210046527
2.
Lopez  LM, Grimes  DA, Gallo  MF, Stockton  LL, Schulz  KF.  Skin patch and vaginal ring versus combined oral contraceptives for contraception.   Cochrane Database Syst Rev. 2013;2013(4):CD003552. doi:10.1002/14651858.CD003552.pub4 PubMedGoogle Scholar
3.
Trussell  J.  Understanding contraceptive failure.   Best Pract Res Clin Obstet Gynaecol. 2009;23(2):199-209. doi:10.1016/j.bpobgyn.2008.11.008 PubMedGoogle ScholarCrossref
4.
Roe  A, Bartz  DA, Douglas  PS. Combined estrogen-progestin contraception: side effects and health concerns. UpToDate. Updated October 20, 2021. Accessed August 7, 2020. https://www.uptodate.com/contents/combined-estrogen-progestin-contraception-side-effects-and-health-concerns
5.
Ioannidis  JPA.  Integration of evidence from multiple meta-analyses: a primer on umbrella reviews, treatment networks and multiple treatments meta-analyses.   CMAJ. 2009;181(8):488-493. doi:10.1503/cmaj.081086 PubMedGoogle ScholarCrossref
6.
Moher  D, Liberati  A, Tetzlaff  J, Altman  DG; PRISMA Group.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.   PLoS Med. 2009;6(7):e1000097. doi:10.1371/journal.pmed.1000097 PubMedGoogle Scholar
7.
Stroup  DF, Berlin  JA, Morton  SC,  et al; Meta-analysis of Observational Studies in Epidemiology (MOOSE) Group.  Meta-analysis of observational studies in epidemiology: a proposal for reporting.   JAMA. 2000;283(15):2008-2012. doi:10.1001/jama.283.15.2008 PubMedGoogle ScholarCrossref
8.
Veettil  SK, Wong  TY, Loo  YS,  et al.  Role of diet in colorectal cancer incidence: umbrella review of meta-analyses of prospective observational studies.   JAMA Netw Open. 2021;4(2):e2037341. doi:10.1001/jamanetworkopen.2020.37341 PubMedGoogle Scholar
9.
Dragioti  E, Solmi  M, Favaro  A,  et al.  Association of antidepressant use with adverse health outcomes: a systematic umbrella review.   JAMA Psychiatry. 2019;76(12):1241-1255. doi:10.1001/jamapsychiatry.2019.2859 PubMedGoogle ScholarCrossref
10.
Belbasis  L, Bellou  V, Evangelou  E, Ioannidis  JPA, Tzoulaki  I.  Environmental risk factors and multiple sclerosis: an umbrella review of systematic reviews and meta-analyses.   Lancet Neurol. 2015;14(3):263-273. doi:10.1016/S1474-4422(14)70267-4 PubMedGoogle ScholarCrossref
11.
Shea  BJ, Reeves  BC, Wells  G,  et al.  AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both.   BMJ. 2017;358:j4008. doi:10.1136/bmj.j4008 PubMedGoogle Scholar
12.
Mercuri  M, Gafni  A.  The evolution of GRADE (part 3): a framework built on science or faith?   J Eval Clin Pract. 2018;24(5):1223-1231. doi:10.1111/jep.13016 PubMedGoogle ScholarCrossref
13.
He  Y, Li  X, Gasevic  D,  et al.  Statins and multiple noncardiovascular outcomes: umbrella review of meta-analyses of observational studies and randomized controlled trials.   Ann Intern Med. 2018;169(8):543-553. doi:10.7326/M18-0808 PubMedGoogle ScholarCrossref
14.
Nochaiwong  S, Ruengorn  C, Awiphan  R,  et al.  The association between proton pump inhibitor use and the risk of adverse kidney outcomes: a systematic review and meta-analysis.   Nephrol Dial Transplant. 2018;33(2):331-342. doi:10.1093/ndt/gfw470 PubMedGoogle ScholarCrossref
15.
IntHout  J, Ioannidis  JPA, Borm  GF.  The Hartung-Knapp-Sidik-Jonkman method for random effects meta-analysis is straightforward and considerably outperforms the standard DerSimonian-Laird method.   BMC Med Res Methodol. 2014;14:25. doi:10.1186/1471-2288-14-25 PubMedGoogle ScholarCrossref
16.
DerSimonian  R, Laird  N.  Meta-analysis in clinical trials.   Control Clin Trials. 1986;7(3):177-188. doi:10.1016/0197-2456(86)90046-2 PubMedGoogle ScholarCrossref
17.
Higgins  JPT.  Commentary: heterogeneity in meta-analysis should be expected and appropriately quantified.   Int J Epidemiol. 2008;37(5):1158-1160. doi:10.1093/ije/dyn204 PubMedGoogle ScholarCrossref
18.
Egger  M, Davey Smith  G, Schneider  M, Minder  C.  Bias in meta-analysis detected by a simple, graphical test.   BMJ. 1997;315(7109):629-634. doi:10.1136/bmj.315.7109.629 PubMedGoogle ScholarCrossref
19.
Higgins  JPT, Thompson  SG, Spiegelhalter  DJ.  A re-evaluation of random-effects meta-analysis.   J R Stat Soc Ser A Stat Soc. 2009;172(1):137-159. doi:10.1111/j.1467-985X.2008.00552.x PubMedGoogle ScholarCrossref
20.
Ioannidis  JPA.  Excess significance bias in the literature on brain volume abnormalities.   Arch Gen Psychiatry. 2011;68(8):773-780. doi:10.1001/archgenpsychiatry.2011.28 PubMedGoogle ScholarCrossref
21.
Ioannidis  JPA, Trikalinos  TA.  An exploratory test for an excess of significant findings.   Clin Trials. 2007;4(3):245-253. doi:10.1177/1740774507079441 PubMedGoogle ScholarCrossref
22.
Salanti  G, Ioannidis  JPA.  Synthesis of observational studies should consider credibility ceilings.   J Clin Epidemiol. 2009;62(2):115-122. doi:10.1016/j.jclinepi.2008.05.014 PubMedGoogle ScholarCrossref
23.
Papatheodorou  SI, Tsilidis  KK, Evangelou  E, Ioannidis  JPA.  Application of credibility ceilings probes the robustness of meta-analyses of biomarkers and cancer risk.   J Clin Epidemiol. 2015;68(2):163-174. doi:10.1016/j.jclinepi.2014.09.004 PubMedGoogle ScholarCrossref
24.
Lethaby  A, Hussain  M, Rishworth  JR, Rees  MC.  Progesterone or progestogen-releasing intrauterine systems for heavy menstrual bleeding.   Cochrane Database Syst Rev. 2015;(4):CD002126. doi:10.1002/14651858.CD002126.pub3 PubMedGoogle Scholar
25.
Amiri  M, Ramezani Tehrani  F, Nahidi  F, Kabir  A, Azizi  F, Carmina  E.  Effects of oral contraceptives on metabolic profile in women with polycystic ovary syndrome: a meta-analysis comparing products containing cyproterone acetate with third generation progestins.   Metabolism. 2017;73:22-35. doi:10.1016/j.metabol.2017.05.001Google ScholarCrossref
26.
Ralph  LJ, McCoy  SI, Shiu  K, Padian  NS.  Hormonal contraceptive use and women’s risk of HIV acquisition: a meta-analysis of observational studies.   Lancet Infect Dis. 2015;15(2):181-189. doi:10.1016/S1473-3099(14)71052-7 PubMedGoogle ScholarCrossref
27.
Chin  J, Konje  JC, Hickey  M.  Levonorgestrel intrauterine system for endometrial protection in women with breast cancer on adjuvant tamoxifen.   Cochrane Database Syst Rev. 2009;(4):CD007245. doi:10.1002/14651858.CD007245.pub2 PubMedGoogle Scholar
28.
Liu  H, Yao  J, Wang  W, Zhang  D.  Association between duration of oral contraceptive use and risk of hypertension: a meta-analysis.   J Clin Hypertens (Greenwich). 2017;19(10):1032-1041. doi:10.1111/jch.13042 PubMedGoogle ScholarCrossref
29.
Pladevall-Vila  M, Delclos  GL, Varas  C, Guyer  H, Brugues-Tarradellas  J, Anglada-Arisa  A.  Controversy of oral contraceptives and risk of rheumatoid arthritis: meta-analysis of conflicting studies and review of conflicting meta-analyses with special emphasis on analysis of heterogeneity.   Am J Epidemiol. 1996;144(1):1-14. doi:10.1093/oxfordjournals.aje.a008846 PubMedGoogle ScholarCrossref
30.
Khader  YS, Rice  J, John  L, Abueita  O.  Oral contraceptives use and the risk of myocardial infarction: a meta-analysis.   Contraception. 2003;68(1):11-17. doi:10.1016/S0010-7824(03)00073-8 PubMedGoogle ScholarCrossref
31.
Johnston  SC, Colford  JM  Jr, Gress  DR.  Oral contraceptives and the risk of subarachnoid hemorrhage: a meta-analysis.   Neurology. 1998;51(2):411-418. doi:10.1212/WNL.51.2.411 PubMedGoogle ScholarCrossref
32.
Lobo  RA, Skinner  JB, Lippman  JS, Cirillo  SJ.  Plasma lipids and desogestrel and ethinyl estradiol: a meta-analysis.   Fertil Steril. 1996;65(6):1100-1109. doi:10.1016/S0015-0282(16)58321-6 PubMedGoogle ScholarCrossref
33.
Delgado-Rodriguez  M, Sillero-Arenas  M, Martin-Moreno  JM, Galvez-Vargas  R.  Oral contraceptives and cancer of the cervix uteri. a meta-analysis.   Acta Obstet Gynecol Scand. 1992;71(5):368-376. doi:10.3109/00016349209021075 PubMedGoogle ScholarCrossref
34.
Stampfer  MJ, Willett  WC, Colditz  GA, Speizer  FE, Hennekens  CH.  Past use of oral contraceptives and cardiovascular disease: a meta-analysis in the context of the Nurses’ Health Study.   Am J Obstet Gynecol. 1990;163(1, pt 2):285-291. doi:10.1016/0002-9378(90)90569-S PubMedGoogle ScholarCrossref
35.
Lopez  LM, Grimes  DA, Gallo  MF, Schulz  KF.  Skin patch and vaginal ring versus combined oral contraceptives for contraception.   Cochrane Database Syst Rev. 2008;(1):CD003552. doi:10.1002/14651858.CD003552.pub2 PubMedGoogle Scholar
36.
French  R, Sorhaindo  AM, Van Vliet  HAAM,  et al.  Progestogen-releasing intrauterine systems versus other forms of reversible contraceptives for contraception.   Cochrane Database Syst Rev. 2004;(3):CD001776. doi:10.1002/14651858.CD001776.pub2Google Scholar
37.
Gillum  LA, Mamidipudi  SK, Johnston  SC.  Ischemic stroke risk with oral contraceptives: a meta-analysis.   JAMA. 2000;284(1):72-78. doi:10.1001/jama.284.1.72 PubMedGoogle ScholarCrossref
38.
Ortizo  R, Lee  SY, Nguyen  ET, Jamal  MM, Bechtold  MM, Nguyen  DL.  Exposure to oral contraceptives increases the risk for development of inflammatory bowel disease: a meta-analysis of case-controlled and cohort studies.   Eur J Gastroenterol Hepatol. 2017;29(9):1064-1070. doi:10.1097/MEG.0000000000000915 PubMedGoogle ScholarCrossref
39.
Qi  S, Xin  R, Guo  W, Liu  Y.  Meta-analysis of oral contraceptives and rheumatoid arthritis risk in women.   Ther Clin Risk Manag. 2014;10:915-923. doi:10.2147/TCRM.S70867PubMedGoogle Scholar
40.
Liu  H, Wang  XC, Hu  GH, Huang  TB, Xu  YF.  Oral contraceptive use and kidney cancer risk among women: evidence from a meta-analysis.   Int J Clin Exp Med. 2014;7(11):3954-3963.PubMedGoogle Scholar
41.
Song  J, Jin  Z, Han  H,  et al.  Hormone replacement therapies, oral contraceptives, reproductive factors and colorectal adenoma risk: a systematic review and dose-response meta-analysis of observational studies.   Colorectal Dis. 2019;21(7):748-759. doi:10.1111/codi.14582 PubMedGoogle Scholar
42.
Draper  BH, Morroni  C, Hoffman  M,  et al.  Depot medroxyprogesterone versus norethisterone oenanthate for long-acting progestogenic contraception.   Cochrane Database Syst Rev. 2006;(3):CD005214. doi:10.1002/14651858.CD005214.pub2 PubMedGoogle Scholar
43.
An  N.  Oral contraceptives use and liver cancer risk: a dose-response meta-analysis of observational studies.   Medicine (Baltimore). 2015;94(43):e1619. doi:10.1097/MD.0000000000001619 PubMedGoogle Scholar
44.
Bateson  D, Butcher  BE, Donovan  C,  et al.  Risk of venous thromboembolism in women taking the combined oral contraceptive: a systematic review and meta-analysis.   Aust Fam Physician. 2016;45(1):59-64.PubMedGoogle Scholar
45.
Bosetti  C, Bravi  F, Negri  E, La Vecchia  C.  Oral contraceptives and colorectal cancer risk: a systematic review and meta-analysis.   Hum Reprod Update. 2009;15(5):489-498. doi:10.1093/humupd/dmp017 PubMedGoogle ScholarCrossref
46.
Vercellini  P, Eskenazi  B, Consonni  D,  et al.  Oral contraceptives and risk of endometriosis: a systematic review and meta-analysis.   Hum Reprod Update. 2011;17(2):159-170. doi:10.1093/humupd/dmq042 PubMedGoogle ScholarCrossref
47.
Halperin  IJ, Kumar  SS, Stroup  DF, Laredo  SE.  The association between the combined oral contraceptive pill and insulin resistance, dysglycemia and dyslipidemia in women with polycystic ovary syndrome: a systematic review and meta-analysis of observational studies.   Hum Reprod. 2011;26(1):191-201. doi:10.1093/humrep/deq301 PubMedGoogle ScholarCrossref
48.
Dayan  N, Holcroft  CA, Tagalakis  V.  The risk of venous thrombosis, including cerebral vein thrombosis, among women with thrombophilia and oral contraceptive use: a meta-analysis.   Clin Appl Thromb Hemost. 2011;17(6):E141-E152. doi:10.1177/1076029610391652 PubMedGoogle ScholarCrossref
49.
Martinez  F, Ramirez  I, Perez-Campos  E, Latorre  K, Lete  I.  Venous and pulmonary thromboembolism and combined hormonal contraceptives. systematic review and meta-analysis.   Eur J Contracept Reprod Health Care. 2012;17(1):7-29. doi:10.3109/13625187.2011.643836 PubMedGoogle ScholarCrossref
50.
Mantha  S, Karp  R, Raghavan  V, Terrin  N, Bauer  KA, Zwicker  JI.  Assessing the risk of venous thromboembolic events in women taking progestin-only contraception: a meta-analysis.   BMJ. 2012;345:e4944. doi:10.1136/bmj.e4944Google Scholar
51.
Zhu  H, Lei  X, Feng  J, Wang  Y.  Oral contraceptive use and risk of breast cancer: a meta-analysis of prospective cohort studies.   Eur J Contracept Reprod Health Care. 2012;17(6):402-414. doi:10.3109/13625187.2012.715357 PubMedGoogle ScholarCrossref
52.
Havrilesky  LJ, Moorman  PG, Lowery  WJ,  et al.  Oral contraceptive pills as primary prevention for ovarian cancer: a systematic review and meta-analysis.   Obstet Gynecol. 2013;122(1):139-147. doi:10.1097/AOG.0b013e318291c235 PubMedGoogle ScholarCrossref
53.
Nindrea  RD, Aryandono  T, Anwar  SL, Lazuardi  L, Harahap  WA, Dwiprahasto  I.  Oral contraceptive used more than 5 years is associated with increased risk of breast cancer: a meta-analysis of 28,776 South East Asian women.   Research Square. Preprint posted online November 19, 2019. doi:10.5530/srp.2019.2.22Google Scholar
54.
Moorman  PG, Havrilesky  LJ, Gierisch  JM,  et al.  Oral contraceptives and risk of ovarian cancer and breast cancer among high-risk women: a systematic review and meta-analysis.   J Clin Oncol. 2013;31(33):4188-4198. doi:10.1200/JCO.2013.48.9021 PubMedGoogle ScholarCrossref
55.
Peragallo Urrutia  R, Coeytaux  RR, McBroom  AJ,  et al.  Risk of acute thromboembolic events with oral contraceptive use: a systematic review and meta-analysis.   Obstet Gynecol. 2013;122(2, pt 1):380-389. doi:10.1097/AOG.0b013e3182994c43 PubMedGoogle ScholarCrossref
56.
Chen  Q, Jin  Z, Xiang  C, Cai  Q, Shi  W, He  J.  Absence of protective effect of oral contraceptive use on the development of rheumatoid arthritis: a meta-analysis of observational studies.   Int J Rheum Dis. 2014;17(7):725-737. doi:10.1111/1756-185X.12413 PubMedGoogle ScholarCrossref
57.
de Bastos  M, Stegeman  BH, Rosendaal  FR,  et al.  Combined oral contraceptives: venous thrombosis.   Cochrane Database Syst Rev. 2014;(3):CD010813. doi:10.1002/14651858.CD010813.pub2PubMedGoogle Scholar
58.
Lagergren  K, Lagergren  J, Brusselaers  N.  Hormone replacement therapy and oral contraceptives and risk of oesophageal adenocarcinoma: a systematic review and meta-analysis.   Int J Cancer. 2014;135(9):2183-2190. doi:10.1002/ijc.28869 PubMedGoogle ScholarCrossref
59.
Shere  M, Bapat  P, Nickel  C, Kapur  B, Koren  G.  Association between use of oral contraceptives and folate status: a systematic review and meta-analysis.   J Obstet Gynaecol Can. 2015;37(5):430-438. doi:10.1016/S1701-2163(15)30258-9 PubMedGoogle ScholarCrossref
60.
Li  F, Zhu  L, Zhang  J,  et al.  Oral contraceptive use and increased risk of stroke: a dose-response meta-analysis of observational studies.   Front Neurol. 2019;10:993. doi:10.3389/fneur.2019.00993 PubMedGoogle ScholarCrossref
61.
Xu  Z, Li  Y, Tang  S, Huang  X, Chen  T.  Current use of oral contraceptives and the risk of first-ever ischemic stroke: a meta-analysis of observational studies.   Thromb Res. 2015;136(1):52-60. doi:10.1016/j.thromres.2015.04.021 PubMedGoogle ScholarCrossref
62.
Xu  JL, Sun  L, Liu  C, Sun  ZH, Min  X, Xia  R.  Effect of oral contraceptive use on the incidence of dry socket in females following impacted mandibular third molar extraction: a meta-analysis.   Int J Oral Maxillofac Surg. 2015;44(9):1160-1165. doi:10.1016/j.ijom.2015.05.017 PubMedGoogle ScholarCrossref
63.
Wu  L, Zhu  J.  Linear reduction in thyroid cancer risk by oral contraceptive use: a dose-response meta-analysis of prospective cohort studies.   Hum Reprod. 2015;30(9):2234-2240. doi:10.1093/humrep/dev160 PubMedGoogle ScholarCrossref
64.
Luan  NN, Wu  L, Gong  TT, Wang  YL, Lin  B, Wu  QJ.  Nonlinear reduction in risk for colorectal cancer by oral contraceptive use: a meta-analysis of epidemiological studies.   Cancer Causes Control. 2015;26(1):65-78. doi:10.1007/s10552-014-0483-2 PubMedGoogle ScholarCrossref
65.
Baratloo  A, Safari  S, Rouhipour  A,  et al.  The risk of venous thromboembolism with different generation of oral contraceptives; a systematic review and meta-analysis.   Emerg (Tehran). 2014;2(1):1-11.PubMedGoogle Scholar
66.
Dragoman  MV, Tepper  NK, Fu  R, Curtis  KM, Chou  R, Gaffield  ME.  A systematic review and meta-analysis of venous thrombosis risk among users of combined oral contraception.   Int J Gynaecol Obstet. 2018;141(3):287-294. doi:10.1002/ijgo.12455 PubMedGoogle ScholarCrossref
67.
Xu  Z, Yue  Y, Bai  J,  et al.  Association between oral contraceptives and risk of hemorrhagic stroke: a meta-analysis of observational studies.   Arch Gynecol Obstet. 2018;297(5):1181-1191. doi:10.1007/s00404-018-4723-7 PubMedGoogle ScholarCrossref
68.
Glisic  M, Shahzad  S, Tsoli  S,  et al.  Association between progestin-only contraceptive use and cardiometabolic outcomes: a systematic review and meta-analysis.   Eur J Prev Cardiol. 2018;25(10):1042-1052. doi:10.1177/2047487318774847 PubMedGoogle ScholarCrossref
69.
Oedingen  C, Scholz  S, Razum  O.  Systematic review and meta-analysis of the association of combined oral contraceptives on the risk of venous thromboembolism: the role of the progestogen type and estrogen dose.   Thromb Res. 2018;165:68-78. doi:10.1016/j.thromres.2018.03.005Google ScholarCrossref
70.
Lan  YL, Wang  X, Lou  JC,  et al.  Update on the effect of exogenous hormone use on glioma risk in women: a meta-analysis of case-control and cohort studies.   J Neurooncol. 2018;137(2):357-365. doi:10.1007/s11060-017-2725-0 PubMedGoogle ScholarCrossref
71.
Wang  X, Fan  X, Deng  H,  et al.  Use of oral contraceptives and risk of ulcerative colitis—a systematic review and meta-analysis.   Pharmacol Res. 2019;139:367-374. doi:10.1016/j.phrs.2018.11.036Google ScholarCrossref
72.
Morrison  CS, Chen  PL, Kwok  C,  et al.  Hormonal contraception and the risk of HIV acquisition: an individual participant data meta-analysis.   PLoS Med. 2015;12(1):e1001778. doi:10.1371/journal.pmed.1001778 PubMedGoogle Scholar
73.
Gallo  MF, Nanda  K, Grimes  DA, Lopez  LM, Schulz  KF.  20 microg versus >20 microg estrogen combined oral contraceptives for contraception.   Cochrane Database Syst Rev. 2008;(4):CD003989. doi:10.1002/14651858.CD003989.pub3PubMedGoogle Scholar
74.
Lopez  LM, Grimes  DA, Schulz  KF.  Steroidal contraceptives: effect on carbohydrate metabolism in women without diabetes mellitus.   Cochrane Database Syst Rev. 2014;(4):CD006133. doi:10.1002/14651858.CD006133.pub5 PubMedGoogle Scholar
75.
Goshtasebi  A, Subotic Brajic  T, Scholes  D, Lederer Goldberg  TB, Berenson  A, Prior  JC.  Adolescent use of combined hormonal contraception and peak bone mineral density accrual: a meta-analysis of international prospective controlled studies.   Clin Endocrinol (Oxf). 2019;90(4):517-524. doi:10.1111/cen.13932 PubMedGoogle ScholarCrossref
76.
Perez-Lopez  FR, Perez-Roncero  GR, Lopez-Baena  MT, Santabarbara  J, Chedraui  P.  Hormonal contraceptives and the risk of suicide: a systematic review and meta-analysis.   Eur J Obstet Gynecol Reprod Biol. 2020;251:28-35. doi:10.1016/j.ejogrb.2020.04.053Google ScholarCrossref
77.
Conz  L, Mota  BS, Bahamondes  L,  et al.  Levonorgestrel-releasing intrauterine system and breast cancer risk: a systematic review and meta-analysis.   Acta Obstet Gynecol Scand. 2020;99(8):970-982. doi:10.1111/aogs.13817 PubMedGoogle ScholarCrossref
78.
Asthana  S, Busa  V, Labani  S.  Oral contraceptives use and risk of cervical cancer—a systematic review & meta-analysis.   Eur J Obstet Gynecol Reprod Biol. 2020;247:163-175. doi:10.1016/j.ejogrb.2020.02.014Google ScholarCrossref
79.
Teede  H, Tassone  EC, Piltonen  T,  et al.  Effect of the combined oral contraceptive pill and/or metformin in the management of polycystic ovary syndrome: a systematic review with meta-analyses.   Clin Endocrinol (Oxf). 2019;91(4):479-489. doi:10.1111/cen.14013 PubMedGoogle ScholarCrossref
80.
Costello  M, Shrestha  B, Eden  J, Sjoblom  P, Johnson  N.  Insulin-sensitising drugs versus the combined oral contraceptive pill for hirsutism, acne and risk of diabetes, cardiovascular disease, and endometrial cancer in polycystic ovary syndrome.   Cochrane Database Syst Rev. 2007;(1):CD005552. doi:10.1002/14651858.CD005552.pub2 PubMedGoogle Scholar
81.
Costello  MF, Shrestha  B, Eden  J, Johnson  NP, Sjoblom  P.  Metformin versus oral contraceptive pill in polycystic ovary syndrome: a Cochrane review.   Hum Reprod. 2007;22(5):1200-1209. doi:10.1093/humrep/dem005 PubMedGoogle ScholarCrossref
82.
Meade  TW.  Risks and mechanisms of cardiovascular events in users of oral contraceptives.   Am J Obstet Gynecol. 1988;158(6, pt 2):1646-1652. doi:10.1016/0002-9378(88)90203-7 PubMedGoogle ScholarCrossref
83.
Burkman  RT, Robinson  JC, Kruszon-Moran  D, Kimball  AW, Kwiterovich  P, Burford  RG.  Lipid and lipoprotein changes associated with oral contraceptive use: a randomized clinical trial.   Obstet Gynecol. 1988;71(1):33-38.PubMedGoogle Scholar
84.
Tuppurainen  M, Klimscheffskij  R, Venhola  M, Dieben  TOM.  The combined contraceptive vaginal ring (NuvaRing) and lipid metabolism: a comparative study.   Contraception. 2004;69(5):389-394. doi:10.1016/j.contraception.2004.01.004 PubMedGoogle ScholarCrossref
85.
Walsh  BW, Sacks  FM.  Effects of low dose oral contraceptives on very low density and low density lipoprotein metabolism.   J Clin Invest. 1993;91(5):2126-2132. doi:10.1172/JCI116437 PubMedGoogle ScholarCrossref
86.
Armstrong  C.  ACOG releases guidelines on hormonal contraceptives in women with coexisting medical conditions.   Am Fam Physician. 2007;75(8):1252-1258. Accessed December 7, 2021. https://www.aafp.org/afp/2007/0415/p1252.htmlGoogle Scholar
87.
Diamanti-Kandarakis  E, Dunaif  A.  Insulin resistance and the polycystic ovary syndrome revisited: an update on mechanisms and implications.   Endocr Rev. 2012;33(6):981-1030. doi:10.1210/er.2011-1034 PubMedGoogle ScholarCrossref
88.
Korytkowski  MT, Mokan  M, Horwitz  MJ, Berga  SL.  Metabolic effects of oral contraceptives in women with polycystic ovary syndrome.   J Clin Endocrinol Metab. 1995;80(11):3327-3334. doi:10.1210/jcem.80.11.7593446PubMedGoogle Scholar
89.
Antoniou  A, Pharoah  PDP, Narod  S,  et al.  Average risks of breast and ovarian cancer associated with BRCA1 or BRCA2 mutations detected in case series unselected for family history: a combined analysis of 22 studies.   Am J Hum Genet. 2003;72(5):1117-1130. doi:10.1086/375033 PubMedGoogle ScholarCrossref
90.
Chen  S, Iversen  ES, Friebel  T,  et al.  Characterization of BRCA1 and BRCA2 mutations in a large United States sample.   J Clin Oncol. 2006;24(6):863-871. doi:10.1200/JCO.2005.03.6772 PubMedGoogle ScholarCrossref
91.
Veljkovic  M, Veljkovic  S.  The risk of breast cervical, endometrial and ovarian cancer in oral contraceptive users.  Article in Serbian.  Med Pregl. 2010;63(9-10):657-661. doi:10.2298/MPNS1010657VPubMedGoogle ScholarCrossref
92.
Kubba  AA.  Breast cancer and the pill.   J R Soc Med. 2003;96(6):280-283. doi:10.1177/014107680309600606 PubMedGoogle ScholarCrossref
93.
Collaborative Group on Hormonal Factors in Breast Cancer.  Breast cancer and hormonal contraceptives: further results.   Contraception. 1996;54(3)(suppl):1S-106S. doi:10.1016/s0010-7824(15)30002-0PubMedGoogle ScholarCrossref
94.
Hannaford  P.  Health consequences of combined oral contraceptives.   Br Med Bull. 2000;56(3):749-760. doi:10.1258/0007142001903337 PubMedGoogle ScholarCrossref
95.
Appleby  P, Beral  V, Berrington de Gonzalez  A,  et al; International Collaboration of Epidemiological Studies of Cervical Cancer.  Cervical cancer and hormonal contraceptives: collaborative reanalysis of individual data for 16,573 women with cervical cancer and 35,509 women without cervical cancer from 24 epidemiological studies.   Lancet. 2007;370(9599):1609-1621. doi:10.1016/S0140-6736(07)61684-5 PubMedGoogle Scholar
96.
Nasu  K, Takai  N, Nishida  M, Narahara  H.  Tumorigenic effects of tamoxifen on the female genital tract.   Clin Med Pathol. 2008;1:17-34. doi:10.4137/CPath.S487 PubMedGoogle ScholarCrossref
97.
Arnes  M, Hvingel  B, Orbo  A.  Levonorgestrel-impregnated intrauterine device reduces occurrence of hyperplastic polyps: a population-based follow-up cohort study.   Anticancer Res. 2014;34(5):2319-2324.PubMedGoogle Scholar
98.
Trinh  XB, Tjalma  WAA, Makar  AP, Buytaert  G, Weyler  J, van Dam  PA.  Use of the levonorgestrel-releasing intrauterine system in breast cancer patients.   Fertil Steril. 2008;90(1):17-22. doi:10.1016/j.fertnstert.2007.05.033 PubMedGoogle ScholarCrossref
99.
Rennert  G, Rennert  HS, Pinchev  M, Gruber  SB, Lavie  O.  Hormonal and reproductive factors and reduction in the risk of colorectal cancer.   Eur J Cancer Prev. 2020;29(3):229-237. doi:10.1097/CEJ.0000000000000538 PubMedGoogle ScholarCrossref
100.
Michels  KA, Pfeiffer  RM, Brinton  LA, Trabert  B.  Modification of the associations between duration of oral contraceptive use and ovarian, endometrial, breast, and colorectal cancers.   JAMA Oncol. 2018;4(4):516-521. doi:10.1001/jamaoncol.2017.4942 PubMedGoogle ScholarCrossref
101.
Tsilidis  KK, Allen  NE, Key  TJ,  et al.  Oral contraceptives, reproductive history and risk of colorectal cancer in the European Prospective Investigation Into Cancer and Nutrition.   Br J Cancer. 2010;103(11):1755-1759. doi:10.1038/sj.bjc.6605965 PubMedGoogle ScholarCrossref
102.
World Health Organization.  Medical Eligibility Criteria for Contraceptive Use. 5th ed. World Health Organization; 2015.
103.
Curtis  KM, Tepper  NK, Jatlaoui  TC,  et al.  U.S. medical eligibility criteria for contraceptive use, 2016.   MMWR Recomm Rep. 2016;65(3):1-103. doi:10.15585/mmwr.rr6503a1PubMedGoogle ScholarCrossref
104.
Tepper  NK, Curtis  KM, Cox  S, Whiteman  MK.  Update to U.S. medical eligibility criteria for contraceptive use, 2016: updated recommendations for the use of contraception among women at high risk for HIV infection.   MMWR Morb Mortal Wkly Rep. 2020;69(14):405-410. doi:10.15585/mmwr.mm6914a3PubMedGoogle ScholarCrossref
Original Investigation
Obstetrics and Gynecology
January 14, 2022

Association of Hormonal Contraceptive Use With Adverse Health Outcomes: An Umbrella Review of Meta-analyses of Randomized Clinical Trials and Cohort Studies

Author Affiliations
  • 1School of Postgraduate Studies, International Medical University, Kuala Lumpur, Malaysia
  • 2Department of Pharmacotherapy, College of Pharmacy, University of Utah, Salt Lake City
  • 3Department of Obstetrics and Gynecology, University of Utah, Salt Lake City
  • 4Department of Pharmacy, Sarikei Public Health Clinic, Sarawak, Malaysia
  • 5Department of Obstetrics and Gynecology, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
  • 6Department of Pharmacy Practice, School of Pharmacy, International Medical University, Kuala Lumpur, Malaysia
  • 7Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Rajavithi Hospital, Bangkok, Thailand
  • 8Department of Obstetrics and Gynecology, Faculty of Medicine, Siriraj Hospital, Mahidol University, Bangkok, Thailand
  • 9Department of Family Medicine, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
  • 10Department of Clinical Epidemiology and Biostatistics, Faculty of Medicine, Ramathibodi Hospital, Mahidol University, Bangkok, Thailand
  • 11School of Pharmacy, University of Wisconsin–Madison, Madison
JAMA Netw Open. 2022;5(1):e2143730. doi:10.1001/jamanetworkopen.2021.43730
Key Points

Question  What are the quality and certainty of evidence for an association between hormonal contraceptive use and the risk of adverse health outcomes in meta-analyses of randomized clinical trials and cohort studies?

Findings  In this umbrella review of 58 meta-analyses of randomized clinical trials and cohort studies describing 156 associations between hormonal contraceptive use and adverse health outcomes among women, no associations with adverse outcomes, including cardiovascular and cancer risk, were supported by high-quality evidence. However, the association between the use of a levonorgestrel-releasing intrauterine system and reductions in endometrial polyps associated with tamoxifen use was graded as having high-quality evidence.

Meaning  The results of this umbrella review supported preexisting understandings of the risks and benefits associated with hormonal contraceptive use, suggesting that the associations between hormonal contraceptive use and adverse health outcomes are not supported by high-quality evidence.

Abstract

Importance  Meta-analyses have reported conflicting data on the safety of hormonal contraception, but the quality of evidence for the associations between hormonal contraceptive use and adverse health outcomes has not been quantified in aggregate.

Objective  To grade the evidence from meta-analyses of randomized clinical trials (RCTs) and cohort studies that assessed the associations between hormonal contraceptive use and adverse health outcomes among women.

Data Sources  MEDLINE, Embase, and the Cochrane Database of Systematic Reviews were searched from database inception to August 2020. Search terms included hormonal contraception, contraceptive agents, progesterone, desogestrel, norethindrone, megestrol, algestone, norprogesterones, and levonorgestrel combined with terms such as systematic review or meta-analysis.

Evidence Review  The methodological quality of each meta-analysis was graded using the Assessment of Multiple Systematic Reviews, version 2, which rated quality as critically low, low, moderate, or high. The Grading of Recommendation, Assessment, Development and Evaluations approach was used to assess the certainty of evidence in meta-analyses of RCTs, with evidence graded as very low, low, moderate, or high. Evidence of associations from meta-analyses of cohort studies was ranked according to established criteria as nonsignificant, weak, suggestive, highly suggestive, or convincing.

Results  A total of 2996 records were screened; of those, 310 full-text articles were assessed for eligibility, and 58 articles (13 meta-analyses of RCTs and 45 meta-analyses of cohort studies) were selected for evidence synthesis. Sixty associations were described in meta-analyses of RCTs, and 96 associations were described in meta-analyses of cohort studies. Among meta-analyses of RCTs, 14 of the 60 associations were nominally statistically significant (P ≤ .05); no associations between hormonal contraceptive use and adverse outcomes were supported by high-quality evidence. The association between the use of a levonorgestrel-releasing intrauterine system and reductions in endometrial polyps associated with tamoxifen use (odds ratio [OR], 0.22; 95% CI, 0.13-0.38) was graded as having high-quality evidence, and this evidence ranking was retained in the subgroup analysis. Among meta-analyses of cohort studies, 40 of the 96 associations were nominally statistically significant; however, no associations between hormonal contraceptive use and adverse outcomes were supported by convincing evidence in the primary and subgroup analyses. The risk of venous thromboembolism among those using vs not using oral contraception (OR, 2.42; 95% CI, 1.76-3.32) was initially supported by highly suggestive evidence, but this evidence was downgraded to weak in the sensitivity analysis.

Conclusions And Relevance  The results of this umbrella review supported preexisting understandings of the risks and benefits associated with hormonal contraceptive use. Overall, the associations between hormonal contraceptive use and cardiovascular risk, cancer risk, and other major adverse health outcomes were not supported by high-quality evidence.

Introduction

Hormonal contraceptive use has been increasing worldwide. In 2019, approximately 1.1 billion women of reproductive age were in need of family planning services worldwide, with almost 50% of those women using various hormonal contraceptive methods,1 including either estrogen and progesterone or progesterone only. These drugs are available in different dosages and forms, such as tablets, implants, intrauterine systems, intramuscular injections, intravaginal rings, and skin patches.2 Overall, when used correctly and consistently, all hormonal contraceptive agents (alone or in combination) have been found to be effective, safe, and reversible forms of contraception.3

However, contradictory results have been reported from several meta-analyses2,4 on the associations between hormonal contraceptive use and adverse health outcomes. The use of hormonal contraception has been associated with either reduced or increased risk of many adverse health outcomes, including cancer, cardiovascular, fracture, gastrointestinal, and metabolic outcomes.4 These risks vary depending on the dose, route, duration of use, and generations and formulations of hormonal contraceptive agents. Because this heterogeneity is present in previous meta-analyses, robust grading of the evidence is needed. To our knowledge, there has been little synthesis of the certainty and quality of the evidence in aggregate across meta-analyses. Umbrella reviews summarize the evidence from multiple meta-analyses on the same topic by assessing the certainty and precision of the associations and the presence of bias, thereby enabling the grading of evidence using well-defined criteria.5

This umbrella review aimed to systematically identify relevant meta-analyses of randomized clinical trials (RCTs) and cohort studies of hormonal contraceptive agents, summarize their findings, and assess the certainty of their evidence to provide a comprehensive understanding of the associations between hormonal contraception and adverse health outcomes.

Methods

The protocol for this study was registered at the International Prospective Register of Systematic Reviews (PROSPERO; registration number: CRD42021231959). The study followed the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) reporting guideline6 and the Meta-analysis of Observational Studies in Epidemiology (MOOSE) reporting guideline.7

Literature Search and Selection Criteria

A systematic literature search was conducted in MEDLINE, Embase, and the Cochrane Database of Systematic Reviews from database inception until August 2020. Our search strategy combined terms associated with hormonal contraceptive exposure, adverse health outcomes, and meta-analysis. Sample search terms included hormonal contraception, contraceptive agents, progesterone, desogestrel, norethindrone, megestrol, algestone, norprogesterones, and levonorgestrel combined with terms such as systematic review or meta-analysis (a full list of search terms is available in eTable 1 in the Supplement). No language restriction was applied.

We included meta-analyses of RCTs and cohort studies investigating any association between hormonal contraceptive use and adverse health outcomes, with no restrictions on comparators or populations. We included meta-analyses that reported a higher or lower risk of adverse health outcomes when using hormones for contraception or treatment (eg, polycystic ovarian syndrome [PCOS]). We did not include meta-analyses of nonspecific adverse events, such as abdominal pain and similar gastrointestinal discomforts, acne, leucorrhea, or breast changes. Adverse health outcomes reported in meta-analyses were extracted as defined by the original authors of each meta-analysis. When more than 1 meta-analysis was available for the same research question, we selected the meta-analysis with the largest data set, as previously described elsewhere.8-10 Detailed inclusion and exclusion criteria and explanations of the selection between overlapping meta-analyses are provided in eTable 2 in the Supplement.

Titles and abstracts of articles were screened by 2 reviewers (S.B. and M.K.) independently. The same 2 reviewers independently assessed the full text of potentially eligible articles. Any discrepancies were resolved by a third reviewer (S.V.) via consensus.

Data Extraction

Data extraction was independently performed by 2 reviewers (S.B. and V.R.), with any disagreement referred to a third reviewer (S.V.) for resolution. We extracted data at both the meta-analysis and individual study levels (eTable 2 in the Supplement). To grade the methodological quality of each meta-analysis, we used the Assessment of Multiple Systematic Reviews, version 2 (AMSTAR-2) tool, which rated quality as critically low, low, moderate, or high.11

Assessment of Evidence Credibility

For meta-analyses of RCTs, we evaluated the certainty of the evidence for each association using the Grading of Recommendation, Assessment, Development and Evaluations (GRADE) framework, which classified evidence as very low, low, moderate, or high.12 For meta-analyses of cohort studies, we applied several criteria in accordance with previous umbrella reviews to grade the quality of evidence.8,9,13 Associations from meta-analyses of cohort studies that were nominally significant (ie, P ≤ .05) were graded as having convincing (class 1), highly suggestive (class 2), suggestive (class 3), or weak (class 4) evidence based on the amount of evidence, statistical significance, heterogeneity, small-study effect, excess significance bias, prediction interval, and credibility ceiling test (details of classification criteria are provided in Table 1).

Sensitivity Analysis

We performed a series of sensitivity analyses to determine the robustness of the findings for each association that was initially graded as having high or moderate evidence (for RCTs) or convincing or highly suggestive evidence (for cohort studies). These sensitivity analyses were performed by excluding small studies (<25th percentile) and primary studies with high risk of bias or low-quality evidence.14 Another sensitivity analysis was conducted based on the approach used for random-effects meta-analyses. We used the Hartung-Knapp-Sidik-Jonkman approach rather than the DerSimonian and Laird method for associations reported in fewer than 5 studies.15

Statistical Analysis

For each association between hormonal contraceptive exposure and outcome, we extracted effect sizes of individual studies included in each meta-analysis based on study design, and we repeated the meta-analyses separately for RCTs and cohort studies to calculate the pooled effect sizes and 95% CIs using random-effects models.16 We assessed heterogeneity using the I2 statistic.17 The evidence for small-study effects was evaluated using the Egger test.18

For meta-analyses of cohort studies, we also estimated the 95% prediction interval, which evaluated the uncertainty of effect that would be expected in a new population addressing a similar association.19 We also applied excess significance assessment using an χ2 test, which evaluated whether the observed number of studies with statistically significant results differed from the expected number of studies with statistically significant results.20,21 We also performed a credibility ceiling test using a ceiling of 10% to reflect our level of confidence in the cohort studies.22,23 All statistical analyses were conducted using Stata software, version 16.0 (StataCorp LLC). The level of significance was set at 2-sided P = .05 for all tests, with the exception of the Egger and excess significance tests, which had significance levels of 2-sided P = .10.

Results
Study Selection

In total, we screened 2996 records and assessed 310 full-text articles for eligibility. Of those, 102 articles (32.8%) were eligible for preliminary data extraction (eFigure 1 in the Supplement). After the selection criteria for the overlapping meta-analyses were applied (Table 2), 58 articles24-81 were selected for evidence synthesis; of those, 13 articles24-27,35,36,42,72-74,79-81 were meta-analyses of RCTs, and 45 articles25,28-31,33,34,38,40,41,43-72,75-79 were meta-analyses of cohort studies. The list of articles excluded after the selection criteria for the overlapping meta-analyses were applied is provided in eTable 3 in the Supplement.

Meta-analyses of RCTs
Characteristics

Thirteen eligible meta-analyses24-27,35,36,42,72-74,79-81 described 60 potential associations, including 60 individual study estimates of adverse health outcomes associated with hormonal contraceptive exposure. The median number of RCTs per meta-analysis was 2 (IQR, 2-3), with a median sample of 91 participants (IQR, 75-154 participants) and a follow-up duration ranging from 3 months to 10 years. Additional descriptive characteristics are provided in eTable 4 in the Supplement.

Evaluation of the methodological quality of 13 meta-analyses24-27,35,36,42,72-74,79-81 using the AMSTAR-2 tool revealed that 8 meta-analyses24,27,35,36,42,73,74 (61.5%) were of high quality, 3 meta-analyses25,26,72 (23.1%) were of low quality, and 2 meta-analyses80,81 (15.4%) were of critically low quality (Table 2; eTable 5 in the Supplement).

Findings

Fourteen24-27 of the 60 associations24-27,35,36,42,72-74,79-81 (23.3%) were nominally statistically significant (P ≤ .05) based on random-effects models. A total of 21 associations25,35 (35.0%) had high heterogeneity (I2 > 50%). Small-study effects were found for 3 associations25,26 (5.0%). Summaries of all significant and nonsignificant associations are provided in Table 2 and eTable 5 in the Supplement, respectively

Among the 14 statistically significant associations,24-27 7 associations24-26 reported an increased risk of adverse health outcomes but no major adverse health outcomes (eg, cardiovascular or cancer-associated outcomes) (Table 2). For treatment purposes, one of the associations24 with moderate-quality evidence reported an increased risk of weight gain among women with regular heavy menstrual bleeding who were using a levonorgestrel-releasing intrauterine system (risk ratio [RR], 2.60; 95% CI, 1.16-5.84) compared with women who were not using this system. Another association25 with moderate-quality evidence reported an increased fasting insulin level with combined oral contraceptive use (desogestrel and low-dose ethinyl estradiol, 30 µg) for the treatment of PCOS (mean difference, 2.32; 95% CI, 1.15-3.49). No sensitivity analyses were conducted for these 2 associations24,25 because of the limited number of studies.

We identified 7 associations25,27 between hormonal contraceptive use and reductions in the risk of adverse health outcomes (Table 2). One association27 between the use of a levonorgestrel-releasing intrauterine system and a 78% reduction in the risk of endometrial polyps among pre- and postmenopausal women receiving tamoxifen and endometrial surveillance was graded as having high-quality evidence (odds ratio [OR], 0.22; 95% CI, 0.13-0.38). A subgroup analysis of this association including only postmenopausal women retained the same evidence ranking (eTable 6 and eFigure 2 in the Supplement). Another association25 between combined oral contraceptive use (cyproterone acetate and ethinyl estradiol, 30 µg) and reductions in fasting blood glucose (FBG) levels among women with PCOS was graded as having moderate-quality evidence (mean difference, −2.05; 95% CI −2.82 to −1.28). This association was upgraded to high-quality evidence after a sensitivity analysis excluding studies with high risk of bias (eTable 6 and eFigure 3 in the Supplement). Among women with PCOS using combined oral contraception, the findings suggested increased high-density lipoprotein levels (mean difference ranging from 6.50 [95% CI, 1.91-11.09] to 10.00 [95% CI, 8.41-11.59]25). In addition, women with PCOS experienced increases in low-density lipoprotein levels (mean difference ranging from 11.53 [95% CI, 4.73-18.34] to 15.08 [95% CI, 12.74-17.43]25) and total cholesterol levels (mean difference, 42.20; 95% CI, 17.01-67.3825). Associations that were initially graded as having evidence of very low to high quality in the primary analysis are provided in eFigure 6 and eFigure 7 in the Supplement, and more details on sensitivity analyses are reported in eTable 6 in the Supplement.

Meta-analyses of Cohort Studies
Characteristics

Forty-five eligible meta-analyses25,28-31,33,34,38,40,41,43-72,75-79 described 96 potential associations, including 171 individual study estimates of adverse health outcomes associated with hormonal contraceptive exposure. The median number of studies per meta-analysis was 3 (IQR, 2-5), and the follow-up duration ranged from 3 months to 42 years. The median sample based on 47 associations was 199 participants (IQR, 107-2470 participants). For 29 of 96 associations (30.2%), the number of participants was greater than 1000. Additional descriptive characteristics are provided in Table 3 and eTable 7 in the Supplement, and details of adjustments made for potential confounding variables in the included meta-analyses are available in eTable 7 in the Supplement.

Analysis of the methodological quality of 45 meta-analyses25,28-31,33,34,38,40,41,43-72,75-79 using the AMSTAR-2 tool revealed that 6 meta-analyses41,57,62,66,68,77 (13.3%) were of high quality, 14 meta-analyses40,44,46,49,50,52-54,63,65,70,75,76,78 (31.1%) were of moderate quality, 7 meta-analyses25,48,59-61,72,79 (15.6%) were of low quality, and the remaining 18 meta-analyses28-31,33,34,38,43,45,47,51,55,56,58,64,67,69,71 (40.0%) were of critically low quality (Table 3; eTable 8 in the Supplement).

Findings

Forty25,28,31,33,38,40,43-47,49,50,52,54,59,61,62,64-66,69-71,76,78 of the 96 examined associations (41.7%) were nominally statistically significant (P ≤ .05), and only 4 associations44,46,65,78 (4.2%) reached high significance with a P value of 1.00 × 10−6 or less (Table 3). Thirty-eight associations25,28,29,31,33,38,40,41,44,47-49,51-53,57,59,60,62,64,65,67,69,72,75,77,78 (39.6%) had high heterogeneity (I2 > 50%). The 95% prediction interval excluded the null value for only 5 associations46,64,70,78 (5.2%). Small-study effects were found for 10 associations33,44,49,69 (10.4%), and no excess significance bias was observed for any association. Among 40 statistically significant associations,25,28,31,33,38,40,43-47,49,50,52,54,59,61,62,64-66,69-71,76,78 only 18 associations25,31,38,44,46,47,49,59,62,64,65,69,70,78 (45.0%) passed the credibility ceiling test using a ceiling value of 10%. Summaries of all significant and nonsignificant associations are provided in Table 3 and eTable 8 in the Supplement, respectively.

Thirty associations25,28,31,33,38,44,46,47,49,54,59,61,62,65,66,69,71,76,78 with an increased risk of adverse health outcomes, including cardiovascular risk, cancer risk, or other major adverse outcomes (such as Crohn disease, ulcerative colitis, and risk of suicide), were statistically significant (Table 3). One of those associations46(past oral contraceptive use and increased risk of endometriosis among women undergoing surgery for endometriosis) was supported by class 1 evidence (RR, 1.60; 95% CI, 1.40-1.82). Two associations44,65 revealing increased risk of venous thromboembolism (VTE) were graded as having class 2 evidence. One of those associations65 was among women using oral contraception compared with women not using oral contraception (OR, 2.42; 95% CI, 1.76-3.32), whereas the other association44 was among women using low-dose combined oral contraception (desogestrel and ethinyl estradiol, <50 µg) compared with women using a levonorgestrel-releasing intrauterine system (OR, 2.05; 95% CI, 1.59-2.64). Among women with PCOS receiving combined oral contraception, findings suggested increased triglyceride levels (mean difference ranging from 0.73 [95% CI, 0.05-1.41] to 39.82 [95% CI, 23.43-56.22]25). In addition, women with PCOS experienced an increase in total cholesterol levels (mean difference, 13.70; 95% CI, 3.74-23.6625).

The association between past oral contraceptive use and the risk of endometriosis46 was downgraded from class 1 to class 4 after a subgroup analysis excluding the population with surgically diagnosed endometriosis (eFigure 4 in the Supplement). Of 2 associations44,65 initially graded as class 2, neither retained the same evidence ranking after sensitivity analyses (eTable 9 and eFigure 5 in the Supplement). Additional results from the sensitivity and subgroup analyses are provided in eTable 9 in the Supplement.

We also identified 10 significant associations25,40,41,45,46,50,64,70 between hormonal contraceptive use and reductions in the risk of adverse health outcomes. However, none of those associations had class 1 or class 2 evidence (Table 3). Associations that were initially graded as having suggestive, highly suggestive, or convincing evidence in the primary analysis are provided in eFigure 8 in the Supplement.

Discussion

This umbrella review examined 60 associations reported in 13 meta-analyses of RCTs24-27,35,36,42,72-74,79-81 and found that none of the 14 statistically significant associations24-27 between hormonal contraceptive use and increases in the risk of adverse outcomes were supported by high-quality evidence in the primary or sensitivity analyses. The association between the use of a levonorgestrel-releasing intrauterine system and reductions in the risk of endometrial polyps among postmenopausal women receiving tamoxifen27 was supported by high-quality evidence, and the association with reductions in FBG levels among women with PCOS25 was also graded as having high-quality evidence after sensitivity analysis. Another association between the use of cyproterone acetate and ethinyl estradiol, 30 µg, and reductions in FBG levels among women with PCOS14 was also graded as having high-quality evidence after sensitivity analysis.

We also assessed 96 associations from 45 meta-analyses of cohort studies.25,28-31,33,34,38,40,41,43-72,75-79 We found that none of the 40 statistically significant associations25,28,31,33,38,40,43-47,49,50,52,54,59,61,62,64-66,69-71,76,78 between hormonal contraceptive use and adverse health outcomes were supported by convincing evidence in the primary and subgroup analyses. The risk of VTE among those who used oral contraception compared with those who did not was initially supported by highly suggestive evidence, but the evidence was downgraded to weak in the sensitivity analysis. Overall, the findings of this umbrella review suggested that the associations between hormonal contraceptive use and cardiovascular risk, cancer risk, and other major adverse health outcomes were not supported by high-quality evidence.

Hormonal Contraception and VTE

All meta-analyses of cohort studies evaluating estrogen-containing hormonal contraceptive agents44,49,65,66,69 found that these agents were associated with an approximate 1.5- to 2.5-fold increase in the risk of VTE. None of the meta-analyses had class 1 evidence, but 2 meta-analyses44,65 did meet the criteria for class 2 evidence. The remaining meta-analyses49,66,69 had class 3 or class 4 evidence; however, the associations between the use of combined oral contraceptive use and VTE risk reported in these meta-analyses were significant, suggesting that concern about VTE risk is warranted. Estrogen increases hepatic production of prothrombotic clotting factors and decreases production of factors that promote clot breakdown, resulting in an increased risk of thrombotic events.82 The consequences of the generation of progestin and its ability to promulgate estrogen’s VTE risk have been extensively studied and remain controversial. As observed in 3 of the included meta-analyses,44,49,69 the effect size of progestin type was modest and potentially confounded by inconsistent controlling for body mass index (calculated as weight in kilograms divided by height in meters squared) and age, 2 factors known to be associated with VTE risk. Overall, this small variance was unlikely to be clinically meaningful when selecting a type of combined oral contraception.

Hormonal Contraception and Metabolic Changes

In our umbrella review, metabolic changes were only assessed among women with PCOS.25 Therefore, it was difficult to extrapolate these associations to the general population because women with PCOS are typically obese and at risk of metabolic syndrome, insulin resistance, and hyperlipidemia. Estrogen modifies lipid metabolism in the liver and regulates serum lipoprotein levels, resulting in increased high-density lipoprotein and triglyceride levels and decreased low-density lipoprotein and total cholesterol levels.83 Progestin type can also have consequences for the extent of lipid profile change induced by exogenous estrogen.84 Notably, the types of triglyceride particles increased by ethinyl estradiol have not been associated with increases in the risk of atherosclerotic disease.85 Among women with PCOS using combined oral contraception, the findings from our review of meta-analyses of RCTs suggested increases in high-density lipoprotein levels (mean difference ranging from 6.50 to10.0025), and the findings from our review of meta-analyses of cohort studies suggested increases in triglyceride levels (mean difference ranging from 0.7351 to 39.8225). Contrary to previous evidence,86 our review found an increase in low-density lipoprotein levels (mean difference ranging from 11.53 to 15.08 in a meta-analysis of RCTs25) and total cholesterol levels (mean difference of 42.20 in a meta-analysis of RCTs25 and 13.70 in a meta-analysis of cohort studies25) among women with PCOS. This difference potentially represents the consequences of different progestin formulations, follow-up durations, and compounding of factors underlying the metabolic changes of PCOS. The quality of evidence was rated class 4 in the cohort studies25,47 and ranged from low to very low in the RCTs25 for associations between women using combined oral contraception and lipid changes, such as increased total cholesterol and triglyceride levels. In addition, the absolute increase in laboratory values was unlikely to be clinically meaningful.

One meta-analysis of RCTs25 had moderate- to high-quality evidence for an association between hormonal contraceptive use and increases in fasting insulin levels as well as decreases in FBG levels among women with PCOS. Although these findings appear to be contradictory, the progestin formulations in the tablets were different; desogestrel was used in the RCT reporting increased fasting insulin levels, and cyproterone acetate was used in the RCT reporting decreased FBG levels. The consequences of combined oral contraception for insulin sensitivity were mainly associated with the progestin component; therefore, the antiandrogenic properties of cyproterone acetate may be associated with decreases in insulin resistance and reductions in circulating androgen levels among women with PCOS, thereby producing the FBG levels observed.87 However, the clinical importance of the impact of different progestins was likely to be minimal, and the use of any combined oral contraceptive agent was unlikely to be associated with diabetes among women with PCOS.88

Hormonal Contraception and Breast and Cervical Cancer Risk

In 2 meta-analyses of cohort studies,54,78 we found evidence of an approximately 1.5-fold increase in the risk of breast cancer54 and an approximately 1.5- to 2.5-fold increase in the risk of cervical cancer78 with the use of combined oral contraception, although the evidence was of class 3 and class 4 quality. Notably, the breast cancer associations reported54 were among women with BRCA1 (OMIM 113705) and BRCA2 (OMIM 600185) variants rather than women in the general population. Individuals with BRCA1 or BRCA2 variants have an increased baseline risk of breast cancer, and the additive impact of combined oral contraceptive risks would be magnified.89,90 Current and recent use of estrogen-containing hormonal contraception is thought to increase breast cancer risk through a tumor promoter effect rather than an initiator effect on preexisting cancer cells.91,92 In addition, any increased risk of breast cancer returns to baseline 10 years after cessation of combined oral contraception.93

This umbrella review also found class 4 evidence to suggest an association between combined oral contraceptive use and an increased risk of cervical cancer in a meta-analysis by Asthana et al.78 Few studies included in that meta-analysis controlled for human papilloma virus infection status, which is an important factor associated with cervical cancer risk. In the meta-analysis by Asthana et al,78 the subgroup analysis of studies including participants with known human papilloma virus infection suggested a modest increase in risk associated with combined oral contraceptive use. However, women using combined oral contraception have been reported to have more sexual partners and higher rates of human papilloma virus infection and to receive a greater number of Papanicolaou tests.94 A combination of these factors likely explains the increased risk of cervical cancer among women currently using combined oral contraception. Similar to breast cancer risk, the risk of cervical cancer appears to be time sensitive, with little to no increased risk when combined oral contraception has been used for less than 5 years or has not been used for more than 10 years.95

Benefits Associated With Hormonal Contraception

Our umbrella review suggested several benefits associated with hormonal contraception, including reductions in endometrial polyps in the setting of tamoxifen use27 and decreases in the incidence of ovarian and colorectal cancers.41,45,52,64 The most significant association that was supported by high-quality evidence was found in a meta-analysis of RCTs27 in which the use vs nonuse of a levonorgestrel-releasing intrauterine system was associated with a 78% reduction in the risk of endometrial polyps among those receiving tamoxifen. Tamoxifen, a nonsteroidal selective estrogen receptor modulator, is known to induce the formation of endometrial polyps through its estrogen agonist effects on the endometrial lining.96 The use of a levonorgestrel-releasing intrauterine system mitigates this risk through its suppressive action on endometrial proliferation.27,97 Of note, controversy exists regarding the use of a levonorgestrel-releasing intrauterine system among patients with progesterone receptor–positive breast cancer because of the potential risk of disease recurrence.98 Additional noncontraceptive benefits associated with combined oral contraception include reductions in the risk of ovarian52 and colorectal cancers,41,45,64 and the results of our review supported these findings. Although these associations27,49,56,67 were graded as class 4 in quality, they have also been observed in multiple epidemiological studies.99-101

Robust grading of previous meta-analyses offers clinicians a tool to better evaluate hormonal contraceptive recommendations for at-risk patients. This grading may assist health care practitioners in the selection of hormonal contraceptive agents for their patients and encourage the consideration of existing individual risk factors, such as VTE, cancer, and cardiovascular risk. The medical eligibility criteria guidelines published by the World Health Organization102 and the Centers for Disease Control and Prevention103,104 can be used to select appropriate hormonal contraception for specific groups of patients based on these risk factors. Future research would ideally include well-designed RCTs comparing adverse health outcomes among those using vs not using hormonal contraception. However, the feasibility of conducting RCTs large enough to detect many of these adverse outcomes is limited. Rigorous cohort studies may aid in better delineating these risks.13,84,85,87

Limitations

This study has several limitations. The umbrella review focused on existing meta-analyses. We found that some adverse outcomes were not included in these meta-analyses, precluding us from performing a comprehensive evaluation of safety aspects of hormonal contraceptive agents. The quality of all primary studies included in each meta-analysis relied on the assessment reported by the respective meta-analysis. Most systematic reviews and meta-analyses included in our review were focused on estrogen-containing combined oral contraceptive agents. When drawing conclusions about clinical practice from the findings of this umbrella review, it is necessary to be mindful that progestin-only methods (ie, progesterone-only tablets, depot medroxyprogesterone acetate injections, progesterone implants, and levonorgestrel-releasing intrauterine systems) are not represented in a clinically meaningful way. However, the conclusions drawn from the combined oral contraceptive data do have implications for clinical practice.

Conclusions

In this umbrella review, the associations between hormonal contraceptive use and cardiovascular risk, cancer risk, and other major adverse health outcomes were not supported by high-quality evidence. The findings reinforced preexisting understandings of the risks and benefits associated with hormonal contraceptive agents.

Back to top
Article Information

Accepted for Publication: November 22, 2021.

Published: January 14, 2022. doi:10.1001/jamanetworkopen.2021.43730

Open Access: This is an open access article distributed under the terms of the CC-BY License. © 2022 Brabaharan S et al. JAMA Network Open.

Corresponding Author: Nathorn Chaiyakunapruk, PharmD, PhD, Department of Pharmacotherapy, College of Pharmacy, University of Utah, 30 2000 E, Salt Lake City, UT 84112 (nathorn.chaiyakunapruk@utah.edu).

Author Contributions: Mr Brabaharan and Dr Chaiyakunapruk had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Brabaharan, Veettil, Kaiser, Maharajan, Talungchit, Thakkinstian, Chaiyakunapruk.

Acquisition, analysis, or interpretation of data: Brabaharan, Veettil, Kaiser, Raja Rao, Wattanayingcharoenchai, Insin, Talungchit, Anothaisintawee, Thakkinstian, Chaiyakunapruk.

Drafting of the manuscript: Brabaharan, Veettil, Kaiser, Raja Rao, Maharajan, Insin, Talungchit.

Critical revision of the manuscript for important intellectual content: Brabaharan, Veettil, Wattanayingcharoenchai, Anothaisintawee, Thakkinstian, Chaiyakunapruk.

Statistical analysis: Brabaharan, Veettil, Raja Rao, Thakkinstian, Chaiyakunapruk.

Obtained funding: Maharajan.

Administrative, technical, or material support: Brabaharan, Veettil, Maharajan, Talungchit, Chaiyakunapruk.

Supervision: Brabaharan, Veettil, Kaiser, Maharajan, Talungchit, Anothaisintawee, Chaiyakunapruk.

Conflict of Interest Disclosures: None reported.

References
1.
United Nations. Contraceptive use by method 2019: data booklet. UN-iLibrary, United Nations; December 2019. Accessed May 15, 2021. https://www.un-ilibrary.org/content/books/9789210046527
2.
Lopez  LM, Grimes  DA, Gallo  MF, Stockton  LL, Schulz  KF.  Skin patch and vaginal ring versus combined oral contraceptives for contraception.   Cochrane Database Syst Rev. 2013;2013(4):CD003552. doi:10.1002/14651858.CD003552.pub4 PubMedGoogle Scholar
3.
Trussell  J.  Understanding contraceptive failure.   Best Pract Res Clin Obstet Gynaecol. 2009;23(2):199-209. doi:10.1016/j.bpobgyn.2008.11.008 PubMedGoogle ScholarCrossref
4.
Roe  A, Bartz  DA, Douglas  PS. Combined estrogen-progestin contraception: side effects and health concerns. UpToDate. Updated October 20, 2021. Accessed August 7, 2020. https://www.uptodate.com/contents/combined-estrogen-progestin-contraception-side-effects-and-health-concerns
5.
Ioannidis  JPA.  Integration of evidence from multiple meta-analyses: a primer on umbrella reviews, treatment networks and multiple treatments meta-analyses.   CMAJ. 2009;181(8):488-493. doi:10.1503/cmaj.081086 PubMedGoogle ScholarCrossref
6.
Moher  D, Liberati  A, Tetzlaff  J, Altman  DG; PRISMA Group.  Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.   PLoS Med. 2009;6(7):e1000097. doi:10.1371/journal.pmed.1000097 PubMedGoogle Scholar
7.
Stroup  DF, Berlin  JA, Morton  SC,  et al; Meta-analysis of Observational Studies in Epidemiology (MOOSE) Group.  Meta-analysis of observational studies in epidemiology: a proposal for reporting.   JAMA. 2000;283(15):2008-2012. doi:10.1001/jama.283.15.2008 PubMedGoogle ScholarCrossref
8.
Veettil  SK, Wong  TY, Loo  YS,  et al.  Role of diet in colorectal cancer incidence: umbrella review of meta-analyses of prospective observational studies.   JAMA Netw Open. 2021;4(2):e2037341. doi:10.1001/jamanetworkopen.2020.37341 PubMedGoogle Scholar
9.
Dragioti  E, Solmi  M, Favaro  A,  et al.  Association of antidepressant use with adverse health outcomes: a systematic umbrella review.   JAMA Psychiatry. 2019;76(12):1241-1255. doi:10.1001/jamapsychiatry.2019.2859 PubMedGoogle ScholarCrossref
10.
Belbasis  L, Bellou  V, Evangelou  E, Ioannidis  JPA, Tzoulaki  I.  Environmental risk factors and multiple sclerosis: an umbrella review of systematic reviews and meta-analyses.   Lancet Neurol. 2015;14(3):263-273. doi:10.1016/S1474-4422(14)70267-4 PubMedGoogle ScholarCrossref
11.
Shea  BJ, Reeves  BC, Wells  G,  et al.  AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both.   BMJ. 2017;358:j4008. doi:10.1136/bmj.j4008 PubMedGoogle Scholar
12.
Mercuri  M, Gafni  A.  The evolution of GRADE (part 3): a framework built on science or faith?   J Eval Clin Pract. 2018;24(5):1223-1231. doi:10.1111/jep.13016 PubMedGoogle ScholarCrossref
13.
He  Y, Li  X, Gasevic  D,  et al.  Statins and multiple noncardiovascular outcomes: umbrella review of meta-analyses of observational studies and randomized controlled trials.   Ann Intern Med. 2018;169(8):543-553. doi:10.7326/M18-0808 PubMedGoogle ScholarCrossref
14.
Nochaiwong  S, Ruengorn  C, Awiphan  R,  et al.  The association between proton pump inhibitor use and the risk of adverse kidney outcomes: a systematic review and meta-analysis.   Nephrol Dial Transplant. 2018;33(2):331-342. doi:10.1093/ndt/gfw470 PubMedGoogle ScholarCrossref
15.
IntHout  J, Ioannidis  JPA, Borm  GF.  The Hartung-Knapp-Sidik-Jonkman method for random effects meta-analysis is straightforward and considerably outperforms the standard DerSimonian-Laird method.   BMC Med Res Methodol. 2014;14:25. doi:10.1186/1471-2288-14-25 PubMedGoogle ScholarCrossref
16.
DerSimonian  R, Laird  N.  Meta-analysis in clinical trials.   Control Clin Trials. 1986;7(3):177-188. doi:10.1016/0197-2456(86)90046-2 PubMedGoogle ScholarCrossref
17.
Higgins  JPT.  Commentary: heterogeneity in meta-analysis should be expected and appropriately quantified.   Int J Epidemiol. 2008;37(5):1158-1160. doi:10.1093/ije/dyn204 PubMedGoogle ScholarCrossref
18.
Egger  M, Davey Smith  G, Schneider  M, Minder  C.  Bias in meta-analysis detected by a simple, graphical test.   BMJ. 1997;315(7109):629-634. doi:10.1136/bmj.315.7109.629 PubMedGoogle ScholarCrossref
19.
Higgins  JPT, Thompson  SG, Spiegelhalter  DJ.  A re-evaluation of random-effects meta-analysis.   J R Stat Soc Ser A Stat Soc. 2009;172(1):137-159. doi:10.1111/j.1467-985X.2008.00552.x PubMedGoogle ScholarCrossref
20.
Ioannidis  JPA.  Excess significance bias in the literature on brain volume abnormalities.   Arch Gen Psychiatry. 2011;68(8):773-780. doi:10.1001/archgenpsychiatry.2011.28 PubMedGoogle ScholarCrossref
21.
Ioannidis  JPA, Trikalinos  TA.  An exploratory test for an excess of significant findings.   Clin Trials. 2007;4(3):245-253. doi:10.1177/1740774507079441 PubMedGoogle ScholarCrossref
22.
Salanti  G, Ioannidis  JPA.  Synthesis of observational studies should consider credibility ceilings.   J Clin Epidemiol. 2009;62(2):115-122. doi:10.1016/j.jclinepi.2008.05.014 PubMedGoogle ScholarCrossref
23.
Papatheodorou  SI, Tsilidis  KK, Evangelou  E, Ioannidis  JPA.  Application of credibility ceilings probes the robustness of meta-analyses of biomarkers and cancer risk.   J Clin Epidemiol. 2015;68(2):163-174. doi:10.1016/j.jclinepi.2014.09.004 PubMedGoogle ScholarCrossref
24.
Lethaby  A, Hussain  M, Rishworth  JR, Rees  MC.  Progesterone or progestogen-releasing intrauterine systems for heavy menstrual bleeding.   Cochrane Database Syst Rev. 2015;(4):CD002126. doi:10.1002/14651858.CD002126.pub3 PubMedGoogle Scholar
25.
Amiri  M, Ramezani Tehrani  F, Nahidi  F, Kabir  A, Azizi  F, Carmina  E.  Effects of oral contraceptives on metabolic profile in women with polycystic ovary syndrome: a meta-analysis comparing products containing cyproterone acetate with third generation progestins.   Metabolism. 2017;73:22-35. doi:10.1016/j.metabol.2017.05.001Google ScholarCrossref
26.
Ralph  LJ, McCoy  SI, Shiu  K, Padian  NS.  Hormonal contraceptive use and women’s risk of HIV acquisition: a meta-analysis of observational studies.   Lancet Infect Dis. 2015;15(2):181-189. doi:10.1016/S1473-3099(14)71052-7 PubMedGoogle ScholarCrossref
27.
Chin  J, Konje  JC, Hickey  M.  Levonorgestrel intrauterine system for endometrial protection in women with breast cancer on adjuvant tamoxifen.   Cochrane Database Syst Rev. 2009;(4):CD007245. doi:10.1002/14651858.CD007245.pub2 PubMedGoogle Scholar
28.
Liu  H, Yao  J, Wang  W, Zhang  D.  Association between duration of oral contraceptive use and risk of hypertension: a meta-analysis.   J Clin Hypertens (Greenwich). 2017;19(10):1032-1041. doi:10.1111/jch.13042 PubMedGoogle ScholarCrossref
29.
Pladevall-Vila  M, Delclos  GL, Varas  C, Guyer  H, Brugues-Tarradellas  J, Anglada-Arisa  A.  Controversy of oral contraceptives and risk of rheumatoid arthritis: meta-analysis of conflicting studies and review of conflicting meta-analyses with special emphasis on analysis of heterogeneity.   Am J Epidemiol. 1996;144(1):1-14. doi:10.1093/oxfordjournals.aje.a008846 PubMedGoogle ScholarCrossref
30.
Khader  YS, Rice  J, John  L, Abueita  O.  Oral contraceptives use and the risk of myocardial infarction: a meta-analysis.   Contraception. 2003;68(1):11-17. doi:10.1016/S0010-7824(03)00073-8 PubMedGoogle ScholarCrossref
31.
Johnston  SC, Colford  JM  Jr, Gress  DR.  Oral contraceptives and the risk of subarachnoid hemorrhage: a meta-analysis.   Neurology. 1998;51(2):411-418. doi:10.1212/WNL.51.2.411 PubMedGoogle ScholarCrossref
32.
Lobo  RA, Skinner  JB, Lippman  JS, Cirillo  SJ.  Plasma lipids and desogestrel and ethinyl estradiol: a meta-analysis.   Fertil Steril. 1996;65(6):1100-1109. doi:10.1016/S0015-0282(16)58321-6 PubMedGoogle ScholarCrossref
33.
Delgado-Rodriguez  M, Sillero-Arenas  M, Martin-Moreno  JM, Galvez-Vargas  R.  Oral contraceptives and cancer of the cervix uteri. a meta-analysis.   Acta Obstet Gynecol Scand. 1992;71(5):368-376. doi:10.3109/00016349209021075 PubMedGoogle ScholarCrossref
34.
Stampfer  MJ, Willett  WC, Colditz  GA, Speizer  FE, Hennekens  CH.  Past use of oral contraceptives and cardiovascular disease: a meta-analysis in the context of the Nurses’ Health Study.   Am J Obstet Gynecol. 1990;163(1, pt 2):285-291. doi:10.1016/0002-9378(90)90569-S PubMedGoogle ScholarCrossref
35.
Lopez  LM, Grimes  DA, Gallo  MF, Schulz  KF.  Skin patch and vaginal ring versus combined oral contraceptives for contraception.   Cochrane Database Syst Rev. 2008;(1):CD003552. doi:10.1002/14651858.CD003552.pub2 PubMedGoogle Scholar
36.
French  R, Sorhaindo  AM, Van Vliet  HAAM,  et al.  Progestogen-releasing intrauterine systems versus other forms of reversible contraceptives for contraception.   Cochrane Database Syst Rev. 2004;(3):CD001776. doi:10.1002/14651858.CD001776.pub2Google Scholar
37.
Gillum  LA, Mamidipudi  SK, Johnston  SC.  Ischemic stroke risk with oral contraceptives: a meta-analysis.   JAMA. 2000;284(1):72-78. doi:10.1001/jama.284.1.72 PubMedGoogle ScholarCrossref
38.
Ortizo  R, Lee  SY, Nguyen  ET, Jamal  MM, Bechtold  MM, Nguyen  DL.  Exposure to oral contraceptives increases the risk for development of inflammatory bowel disease: a meta-analysis of case-controlled and cohort studies.   Eur J Gastroenterol Hepatol. 2017;29(9):1064-1070. doi:10.1097/MEG.0000000000000915 PubMedGoogle ScholarCrossref
39.
Qi  S, Xin  R, Guo  W, Liu  Y.  Meta-analysis of oral contraceptives and rheumatoid arthritis risk in women.   Ther Clin Risk Manag. 2014;10:915-923. doi:10.2147/TCRM.S70867PubMedGoogle Scholar
40.
Liu  H, Wang  XC, Hu  GH, Huang  TB, Xu  YF.  Oral contraceptive use and kidney cancer risk among women: evidence from a meta-analysis.   Int J Clin Exp Med. 2014;7(11):3954-3963.PubMedGoogle Scholar
41.
Song  J, Jin  Z, Han  H,  et al.  Hormone replacement therapies, oral contraceptives, reproductive factors and colorectal adenoma risk: a systematic review and dose-response meta-analysis of observational studies.   Colorectal Dis. 2019;21(7):748-759. doi:10.1111/codi.14582 PubMedGoogle Scholar
42.
Draper  BH, Morroni  C, Hoffman  M,  et al.  Depot medroxyprogesterone versus norethisterone oenanthate for long-acting progestogenic contraception.   Cochrane Database Syst Rev. 2006;(3):CD005214. doi:10.1002/14651858.CD005214.pub2 PubMedGoogle Scholar
43.
An  N.  Oral contraceptives use and liver cancer risk: a dose-response meta-analysis of observational studies.   Medicine (Baltimore). 2015;94(43):e1619. doi:10.1097/MD.0000000000001619 PubMedGoogle Scholar
44.
Bateson  D, Butcher  BE, Donovan  C,  et al.  Risk of venous thromboembolism in women taking the combined oral contraceptive: a systematic review and meta-analysis.   Aust Fam Physician. 2016;45(1):59-64.PubMedGoogle Scholar
45.
Bosetti  C, Bravi  F, Negri  E, La Vecchia  C.  Oral contraceptives and colorectal cancer risk: a systematic review and meta-analysis.   Hum Reprod Update. 2009;15(5):489-498. doi:10.1093/humupd/dmp017 PubMedGoogle ScholarCrossref
46.
Vercellini  P, Eskenazi  B, Consonni  D,  et al.  Oral contraceptives and risk of endometriosis: a systematic review and meta-analysis.   Hum Reprod Update. 2011;17(2):159-170. doi:10.1093/humupd/dmq042 PubMedGoogle ScholarCrossref
47.
Halperin  IJ, Kumar  SS, Stroup  DF, Laredo  SE.  The association between the combined oral contraceptive pill and insulin resistance, dysglycemia and dyslipidemia in women with polycystic ovary syndrome: a systematic review and meta-analysis of observational studies.   Hum Reprod. 2011;26(1):191-201. doi:10.1093/humrep/deq301 PubMedGoogle ScholarCrossref
48.
Dayan  N, Holcroft  CA, Tagalakis  V.  The risk of venous thrombosis, including cerebral vein thrombosis, among women with thrombophilia and oral contraceptive use: a meta-analysis.   Clin Appl Thromb Hemost. 2011;17(6):E141-E152. doi:10.1177/1076029610391652 PubMedGoogle ScholarCrossref
49.
Martinez  F, Ramirez  I, Perez-Campos  E, Latorre  K, Lete  I.  Venous and pulmonary thromboembolism and combined hormonal contraceptives. systematic review and meta-analysis.   Eur J Contracept Reprod Health Care. 2012;17(1):7-29. doi:10.3109/13625187.2011.643836 PubMedGoogle ScholarCrossref
50.
Mantha  S, Karp  R, Raghavan  V, Terrin  N, Bauer  KA, Zwicker  JI.  Assessing the risk of venous thromboembolic events in women taking progestin-only contraception: a meta-analysis.   BMJ. 2012;345:e4944. doi:10.1136/bmj.e4944Google Scholar
51.
Zhu  H, Lei  X, Feng  J, Wang  Y.  Oral contraceptive use and risk of breast cancer: a meta-analysis of prospective cohort studies.   Eur J Contracept Reprod Health Care. 2012;17(6):402-414. doi:10.3109/13625187.2012.715357 PubMedGoogle ScholarCrossref
52.
Havrilesky  LJ, Moorman  PG, Lowery  WJ,  et al.  Oral contraceptive pills as primary prevention for ovarian cancer: a systematic review and meta-analysis.   Obstet Gynecol. 2013;122(1):139-147. doi:10.1097/AOG.0b013e318291c235 PubMedGoogle ScholarCrossref
53.
Nindrea  RD, Aryandono  T, Anwar  SL, Lazuardi  L, Harahap  WA, Dwiprahasto  I.  Oral contraceptive used more than 5 years is associated with increased risk of breast cancer: a meta-analysis of 28,776 South East Asian women.   Research Square. Preprint posted online November 19, 2019. doi:10.5530/srp.2019.2.22Google Scholar
54.
Moorman  PG, Havrilesky  LJ, Gierisch  JM,  et al.  Oral contraceptives and risk of ovarian cancer and breast cancer among high-risk women: a systematic review and meta-analysis.   J Clin Oncol. 2013;31(33):4188-4198. doi:10.1200/JCO.2013.48.9021 PubMedGoogle ScholarCrossref
55.
Peragallo Urrutia  R, Coeytaux  RR, McBroom  AJ,  et al.  Risk of acute thromboembolic events with oral contraceptive use: a systematic review and meta-analysis.   Obstet Gynecol. 2013;122(2, pt 1):380-389. doi:10.1097/AOG.0b013e3182994c43 PubMedGoogle ScholarCrossref
56.
Chen  Q, Jin  Z, Xiang  C, Cai  Q, Shi  W, He  J.  Absence of protective effect of oral contraceptive use on the development of rheumatoid arthritis: a meta-analysis of observational studies.   Int J Rheum Dis. 2014;17(7):725-737. doi:10.1111/1756-185X.12413 PubMedGoogle ScholarCrossref
57.
de Bastos  M, Stegeman  BH, Rosendaal  FR,  et al.  Combined oral contraceptives: venous thrombosis.   Cochrane Database Syst Rev. 2014;(3):CD010813. doi:10.1002/14651858.CD010813.pub2PubMedGoogle Scholar
58.
Lagergren  K, Lagergren  J, Brusselaers  N.  Hormone replacement therapy and oral contraceptives and risk of oesophageal adenocarcinoma: a systematic review and meta-analysis.   Int J Cancer. 2014;135(9):2183-2190. doi:10.1002/ijc.28869 PubMedGoogle ScholarCrossref
59.
Shere  M, Bapat  P, Nickel  C, Kapur  B, Koren  G.  Association between use of oral contraceptives and folate status: a systematic review and meta-analysis.   J Obstet Gynaecol Can. 2015;37(5):430-438. doi:10.1016/S1701-2163(15)30258-9 PubMedGoogle ScholarCrossref
60.
Li  F, Zhu  L, Zhang  J,  et al.  Oral contraceptive use and increased risk of stroke: a dose-response meta-analysis of observational studies.   Front Neurol. 2019;10:993. doi:10.3389/fneur.2019.00993 PubMedGoogle ScholarCrossref
61.
Xu  Z, Li  Y, Tang  S, Huang  X, Chen  T.  Current use of oral contraceptives and the risk of first-ever ischemic stroke: a meta-analysis of observational studies.   Thromb Res. 2015;136(1):52-60. doi:10.1016/j.thromres.2015.04.021 PubMedGoogle ScholarCrossref
62.
Xu  JL, Sun  L, Liu  C, Sun  ZH, Min  X, Xia  R.  Effect of oral contraceptive use on the incidence of dry socket in females following impacted mandibular third molar extraction: a meta-analysis.   Int J Oral Maxillofac Surg. 2015;44(9):1160-1165. doi:10.1016/j.ijom.2015.05.017 PubMedGoogle ScholarCrossref
63.
Wu  L, Zhu  J.  Linear reduction in thyroid cancer risk by oral contraceptive use: a dose-response meta-analysis of prospective cohort studies.   Hum Reprod. 2015;30(9):2234-2240. doi:10.1093/humrep/dev160 PubMedGoogle ScholarCrossref
64.
Luan  NN, Wu  L, Gong  TT, Wang  YL, Lin  B, Wu  QJ.  Nonlinear reduction in risk for colorectal cancer by oral contraceptive use: a meta-analysis of epidemiological studies.   Cancer Causes Control. 2015;26(1):65-78. doi:10.1007/s10552-014-0483-2 PubMedGoogle ScholarCrossref
65.
Baratloo  A, Safari  S, Rouhipour  A,  et al.  The risk of venous thromboembolism with different generation of oral contraceptives; a systematic review and meta-analysis.   Emerg (Tehran). 2014;2(1):1-11.PubMedGoogle Scholar
66.
Dragoman  MV, Tepper  NK, Fu  R, Curtis  KM, Chou  R, Gaffield  ME.  A systematic review and meta-analysis of venous thrombosis risk among users of combined oral contraception.   Int J Gynaecol Obstet. 2018;141(3):287-294. doi:10.1002/ijgo.12455 PubMedGoogle ScholarCrossref
67.
Xu  Z, Yue  Y, Bai  J,  et al.  Association between oral contraceptives and risk of hemorrhagic stroke: a meta-analysis of observational studies.   Arch Gynecol Obstet. 2018;297(5):1181-1191. doi:10.1007/s00404-018-4723-7 PubMedGoogle ScholarCrossref
68.
Glisic  M, Shahzad  S, Tsoli  S,  et al.  Association between progestin-only contraceptive use and cardiometabolic outcomes: a systematic review and meta-analysis.   Eur J Prev Cardiol. 2018;25(10):1042-1052. doi:10.1177/2047487318774847 PubMedGoogle ScholarCrossref
69.
Oedingen  C, Scholz  S, Razum  O.  Systematic review and meta-analysis of the association of combined oral contraceptives on the risk of venous thromboembolism: the role of the progestogen type and estrogen dose.   Thromb Res. 2018;165:68-78. doi:10.1016/j.thromres.2018.03.005Google ScholarCrossref
70.
Lan  YL, Wang  X, Lou  JC,  et al.  Update on the effect of exogenous hormone use on glioma risk in women: a meta-analysis of case-control and cohort studies.   J Neurooncol. 2018;137(2):357-365. doi:10.1007/s11060-017-2725-0 PubMedGoogle ScholarCrossref
71.
Wang  X, Fan  X, Deng  H,  et al.  Use of oral contraceptives and risk of ulcerative colitis—a systematic review and meta-analysis.   Pharmacol Res. 2019;139:367-374. doi:10.1016/j.phrs.2018.11.036Google ScholarCrossref
72.
Morrison  CS, Chen  PL, Kwok  C,  et al.  Hormonal contraception and the risk of HIV acquisition: an individual participant data meta-analysis.   PLoS Med. 2015;12(1):e1001778. doi:10.1371/journal.pmed.1001778 PubMedGoogle Scholar
73.
Gallo  MF, Nanda  K, Grimes  DA, Lopez  LM, Schulz  KF.  20 microg versus >20 microg estrogen combined oral contraceptives for contraception.   Cochrane Database Syst Rev. 2008;(4):CD003989. doi:10.1002/14651858.CD003989.pub3PubMedGoogle Scholar
74.
Lopez  LM, Grimes  DA, Schulz  KF.  Steroidal contraceptives: effect on carbohydrate metabolism in women without diabetes mellitus.   Cochrane Database Syst Rev. 2014;(4):CD006133. doi:10.1002/14651858.CD006133.pub5 PubMedGoogle Scholar
75.
Goshtasebi  A, Subotic Brajic  T, Scholes  D, Lederer Goldberg  TB, Berenson  A, Prior  JC.  Adolescent use of combined hormonal contraception and peak bone mineral density accrual: a meta-analysis of international prospective controlled studies.   Clin Endocrinol (Oxf). 2019;90(4):517-524. doi:10.1111/cen.13932 PubMedGoogle ScholarCrossref
76.
Perez-Lopez  FR, Perez-Roncero  GR, Lopez-Baena  MT, Santabarbara  J, Chedraui  P.  Hormonal contraceptives and the risk of suicide: a systematic review and meta-analysis.   Eur J Obstet Gynecol Reprod Biol. 2020;251:28-35. doi:10.1016/j.ejogrb.2020.04.053Google ScholarCrossref
77.
Conz  L, Mota  BS, Bahamondes  L,  et al.  Levonorgestrel-releasing intrauterine system and breast cancer risk: a systematic review and meta-analysis.   Acta Obstet Gynecol Scand. 2020;99(8):970-982. doi:10.1111/aogs.13817 PubMedGoogle ScholarCrossref
78.
Asthana  S, Busa  V, Labani  S.  Oral contraceptives use and risk of cervical cancer—a systematic review & meta-analysis.   Eur J Obstet Gynecol Reprod Biol. 2020;247:163-175. doi:10.1016/j.ejogrb.2020.02.014Google ScholarCrossref
79.
Teede  H, Tassone  EC, Piltonen  T,  et al.  Effect of the combined oral contraceptive pill and/or metformin in the management of polycystic ovary syndrome: a systematic review with meta-analyses.   Clin Endocrinol (Oxf). 2019;91(4):479-489. doi:10.1111/cen.14013 PubMedGoogle ScholarCrossref
80.
Costello  M, Shrestha  B, Eden  J, Sjoblom  P, Johnson  N.  Insulin-sensitising drugs versus the combined oral contraceptive pill for hirsutism, acne and risk of diabetes, cardiovascular disease, and endometrial cancer in polycystic ovary syndrome.   Cochrane Database Syst Rev. 2007;(1):CD005552. doi:10.1002/14651858.CD005552.pub2 PubMedGoogle Scholar
81.
Costello  MF, Shrestha  B, Eden  J, Johnson  NP, Sjoblom  P.  Metformin versus oral contraceptive pill in polycystic ovary syndrome: a Cochrane review.   Hum Reprod. 2007;22(5):1200-1209. doi:10.1093/humrep/dem005 PubMedGoogle ScholarCrossref
82.
Meade  TW.  Risks and mechanisms of cardiovascular events in users of oral contraceptives.   Am J Obstet Gynecol. 1988;158(6, pt 2):1646-1652. doi:10.1016/0002-9378(88)90203-7 PubMedGoogle ScholarCrossref
83.
Burkman  RT, Robinson  JC, Kruszon-Moran  D, Kimball  AW, Kwiterovich  P, Burford  RG.  Lipid and lipoprotein changes associated with oral contraceptive use: a randomized clinical trial.   Obstet Gynecol. 1988;71(1):33-38.PubMedGoogle Scholar
84.
Tuppurainen  M, Klimscheffskij  R, Venhola  M, Dieben  TOM.  The combined contraceptive vaginal ring (NuvaRing) and lipid metabolism: a comparative study.   Contraception. 2004;69(5):389-394. doi:10.1016/j.contraception.2004.01.004 PubMedGoogle ScholarCrossref
85.
Walsh  BW, Sacks  FM.  Effects of low dose oral contraceptives on very low density and low density lipoprotein metabolism.   J Clin Invest. 1993;91(5):2126-2132. doi:10.1172/JCI116437 PubMedGoogle ScholarCrossref
86.
Armstrong  C.  ACOG releases guidelines on hormonal contraceptives in women with coexisting medical conditions.   Am Fam Physician. 2007;75(8):1252-1258. Accessed December 7, 2021. https://www.aafp.org/afp/2007/0415/p1252.htmlGoogle Scholar
87.
Diamanti-Kandarakis  E, Dunaif  A.  Insulin resistance and the polycystic ovary syndrome revisited: an update on mechanisms and implications.   Endocr Rev. 2012;33(6):981-1030. doi:10.1210/er.2011-1034 PubMedGoogle ScholarCrossref
88.
Korytkowski  MT, Mokan  M, Horwitz  MJ, Berga  SL.  Metabolic effects of oral contraceptives in women with polycystic ovary syndrome.   J Clin Endocrinol Metab. 1995;80(11):3327-3334. doi:10.1210/jcem.80.11.7593446PubMedGoogle Scholar
89.
Antoniou  A, Pharoah  PDP, Narod  S,  et al.  Average risks of breast and ovarian cancer associated with BRCA1 or BRCA2 mutations detected in case series unselected for family history: a combined analysis of 22 studies.   Am J Hum Genet. 2003;72(5):1117-1130. doi:10.1086/375033 PubMedGoogle ScholarCrossref
90.
Chen  S, Iversen  ES, Friebel  T,  et al.  Characterization of BRCA1 and BRCA2 mutations in a large United States sample.   J Clin Oncol. 2006;24(6):863-871. doi:10.1200/JCO.2005.03.6772 PubMedGoogle ScholarCrossref
91.
Veljkovic  M, Veljkovic  S.  The risk of breast cervical, endometrial and ovarian cancer in oral contraceptive users.  Article in Serbian.  Med Pregl. 2010;63(9-10):657-661. doi:10.2298/MPNS1010657VPubMedGoogle ScholarCrossref
92.
Kubba  AA.  Breast cancer and the pill.   J R Soc Med. 2003;96(6):280-283. doi:10.1177/014107680309600606 PubMedGoogle ScholarCrossref
93.
Collaborative Group on Hormonal Factors in Breast Cancer.  Breast cancer and hormonal contraceptives: further results.   Contraception. 1996;54(3)(suppl):1S-106S. doi:10.1016/s0010-7824(15)30002-0PubMedGoogle ScholarCrossref
94.
Hannaford  P.  Health consequences of combined oral contraceptives.   Br Med Bull. 2000;56(3):749-760. doi:10.1258/0007142001903337 PubMedGoogle ScholarCrossref
95.
Appleby  P, Beral  V, Berrington de Gonzalez  A,  et al; International Collaboration of Epidemiological Studies of Cervical Cancer.  Cervical cancer and hormonal contraceptives: collaborative reanalysis of individual data for 16,573 women with cervical cancer and 35,509 women without cervical cancer from 24 epidemiological studies.   Lancet. 2007;370(9599):1609-1621. doi:10.1016/S0140-6736(07)61684-5 PubMedGoogle Scholar
96.
Nasu  K, Takai  N, Nishida  M, Narahara  H.  Tumorigenic effects of tamoxifen on the female genital tract.   Clin Med Pathol. 2008;1:17-34. doi:10.4137/CPath.S487 PubMedGoogle ScholarCrossref
97.
Arnes  M, Hvingel  B, Orbo  A.  Levonorgestrel-impregnated intrauterine device reduces occurrence of hyperplastic polyps: a population-based follow-up cohort study.   Anticancer Res. 2014;34(5):2319-2324.PubMedGoogle Scholar
98.
Trinh  XB, Tjalma  WAA, Makar  AP, Buytaert  G, Weyler  J, van Dam  PA.  Use of the levonorgestrel-releasing intrauterine system in breast cancer patients.   Fertil Steril. 2008;90(1):17-22. doi:10.1016/j.fertnstert.2007.05.033 PubMedGoogle ScholarCrossref
99.
Rennert  G, Rennert  HS, Pinchev  M, Gruber  SB, Lavie  O.  Hormonal and reproductive factors and reduction in the risk of colorectal cancer.   Eur J Cancer Prev. 2020;29(3):229-237. doi:10.1097/CEJ.0000000000000538 PubMedGoogle ScholarCrossref
100.
Michels  KA, Pfeiffer  RM, Brinton  LA, Trabert  B.  Modification of the associations between duration of oral contraceptive use and ovarian, endometrial, breast, and colorectal cancers.   JAMA Oncol. 2018;4(4):516-521. doi:10.1001/jamaoncol.2017.4942 PubMedGoogle ScholarCrossref
101.
Tsilidis  KK, Allen  NE, Key  TJ,  et al.  Oral contraceptives, reproductive history and risk of colorectal cancer in the European Prospective Investigation Into Cancer and Nutrition.   Br J Cancer. 2010;103(11):1755-1759. doi:10.1038/sj.bjc.6605965 PubMedGoogle ScholarCrossref
102.
World Health Organization.  Medical Eligibility Criteria for Contraceptive Use. 5th ed. World Health Organization; 2015.
103.
Curtis  KM, Tepper  NK, Jatlaoui  TC,  et al.  U.S. medical eligibility criteria for contraceptive use, 2016.   MMWR Recomm Rep. 2016;65(3):1-103. doi:10.15585/mmwr.rr6503a1PubMedGoogle ScholarCrossref
104.
Tepper  NK, Curtis  KM, Cox  S, Whiteman  MK.  Update to U.S. medical eligibility criteria for contraceptive use, 2016: updated recommendations for the use of contraception among women at high risk for HIV infection.   MMWR Morb Mortal Wkly Rep. 2020;69(14):405-410. doi:10.15585/mmwr.mm6914a3PubMedGoogle ScholarCrossref
×