Women who deliver twins are more likely to smoke and have high frequencies of specific SNPs: Results from a sample of African-American women who delivered preterm, low birth weight babies
2015; Wiley; Volume: 27; Issue: 5 Linguagem: Inglês
10.1002/ajhb.22723
ISSN1520-6300
AutoresHong Huang, Kathryn B. H. Clancy, Crystal Burhance, Yilliang Zhu, Lorena Madrigal,
Tópico(s)Demographic Trends and Gender Preferences
ResumoAmerican Journal of Human BiologyVolume 27, Issue 5 p. 605-612 Original Research Article Women who deliver twins are more likely to smoke and have high frequencies of specific SNPs: Results from a sample of African–American women who delivered preterm, low birth weight babies Hong Huang, Hong Huang School of Information, University of South Florida, 4202 E. Fowler Av, Tampa, Florida, 33620Search for more papers by this authorKathryn B.H. Clancy, Kathryn B.H. Clancy Department of Anthropology, University of Illinois at Urbana-Champaign, 109 Davenport Hall, 607 S. Mathews Ave., Urbana, Illinois, 61801Search for more papers by this authorCrystal Burhance, Crystal Burhance Department of Anthropology, University of South Florida, 4202 E. Fowler Av, Tampa, Florida, 33620Search for more papers by this authorYilliang Zhu, Yilliang Zhu Department of Epidemiology and Biostatistics, College of Public Health, University of South FloridaSearch for more papers by this authorLorena Madrigal, Corresponding Author Lorena Madrigal Department of Anthropology, University of South Florida, 4202 E. Fowler Av, Tampa, Florida, 33620Correspondence to: L. Madrigal, Department of Anthropology, University of South Florida, 4202 E. Fowler Av, Tampa, FL 33620. E-mail: [email protected]Search for more papers by this author Hong Huang, Hong Huang School of Information, University of South Florida, 4202 E. Fowler Av, Tampa, Florida, 33620Search for more papers by this authorKathryn B.H. Clancy, Kathryn B.H. Clancy Department of Anthropology, University of Illinois at Urbana-Champaign, 109 Davenport Hall, 607 S. Mathews Ave., Urbana, Illinois, 61801Search for more papers by this authorCrystal Burhance, Crystal Burhance Department of Anthropology, University of South Florida, 4202 E. Fowler Av, Tampa, Florida, 33620Search for more papers by this authorYilliang Zhu, Yilliang Zhu Department of Epidemiology and Biostatistics, College of Public Health, University of South FloridaSearch for more papers by this authorLorena Madrigal, Corresponding Author Lorena Madrigal Department of Anthropology, University of South Florida, 4202 E. Fowler Av, Tampa, Florida, 33620Correspondence to: L. Madrigal, Department of Anthropology, University of South Florida, 4202 E. Fowler Av, Tampa, FL 33620. E-mail: [email protected]Search for more papers by this author First published: 16 April 2015 https://doi.org/10.1002/ajhb.22723Citations: 9Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract Objectives We examine if there are genetic and environmental differences between mothers of singleton and multiple pregnancies in a sample of African–American mothers. Methods We focus on genomic areas suggested to increase or decrease the odds of multiple pregnancies. We computed the odds ratio (OR) and the 95% confidence interval (CI) for each SNP unadjusted or adjusted with smoking. SNPs' allelic differences between mothers of multiple pregnancies and singletons were also tested using Fisher's exact test. We considered additive terms for the SNPs' genotypes, smoking, and a multiplicative interaction term of two selected SNPs' genotypes. Results We found significant interactions between smoking and SNPs of the CYP19A, MDM4, MTHFR and TP53 genes which correlated with higher odds of twinning. We also found a significant interaction between SNPs at the TP53 (rs8079544) and MTHFR gene (rs4846049), where the interaction between the homozygotes (TT for rs8079544, GG for rs4846049) correlated with lowered odds of multiple pregnancy. Conclusions We provide a mechanistic explanation and preliminary evidence for previous reports that mothers of twins are more likely to have smoked, despite seemingly conflicting evidence for the fertility-reducing effects of nicotine. Nicotine, as an aromatase inhibitor, inhibits estrogen synthesis and may allow for greater production of gonadotropins. While smoking may have deleterious effects on fertility across many genotypes, in women of specific genotypes it may raise their odds of producing twins. TP53 involvement suggests the necessity of future work examining relationships between women who bear multiples and cancer risk. Am. J. Hum. Biol. 27:605–612, 2015. © 2015 Wiley Periodicals, Inc. LITERATURE CITED Akinboro A, Azeez MA, Bakare AA. 2008. Incidence of twinning in Southwest Nigeria. Ind J Hum Genet 14: 41–47. 10.4103/0971-6866.44104 CASPubMedGoogle Scholar Al-Fozan H, Al-Khadouri M, Tan SL, Tulandi T. 2004. A randomized trial of letrozole versus clomiphene citrate in women undergoing superovulation. Fertil Steril 82: 1561–1563. 10.1016/j.fertnstert.2004.04.070 CASPubMedWeb of Science®Google Scholar Al-Hendy A, Moshynska O, Saxena A, Feyles V. 2000. Association between mutations of the follicle-stimulating-hormone receptor and repeated twinning. Lancet 356: 914–914. 10.1016/S0140-6736(00)02687-8 CASPubMedWeb of Science®Google Scholar Alexander BM, Van Kirk EA, Naughton LMA, Murdoch WJ. 2007. Ovarian morphometrics in TP53-deficient mice. Anat Rec 290: 59–64. 10.1002/ar.20409 CASPubMedWeb of Science®Google Scholar Anunciação O, Gomes B, Vinga S, Gaspar J, Oliveira A, Rueff J. 2010. A data mining approach for the detection of high-risk breast cancer groups. In: Rocha M, Fernandez-Riverola F, Shatkay H, Corchado J, editors. Advances in bioinformatics. Heidelberg: Springer Berlin Heidelberg. p 43–51. Google Scholar Anunciação O, Gomes BC, Vinga S, Gaspar J, Oliveira AL, Rueff J. 2010. A data mining approach for the detection of high-risk breast cancer groups. Conference: Advances in Bioinformatics - 4th International Workshop on Practical Applications of Computational Biology and Bioinformatics 2010 (IWPACBB 2010), Guimarñes, Portugal, 16–18. Google Scholar Arcand SL, Maugard CM, Ghadirian P, Robidoux A, Perret C, Zhang P, Fafard E, Mes-Masson A-M, Foulkes WD, Provencher D, et al. 2008. Germline TP53 mutations in BRCA1 and BRCA2 mutation-negative french canadian breast cancer families. Breast Cancer Res Treat 108: 399–408. 10.1007/s10549-007-9608-6 CASPubMedWeb of Science®Google Scholar Asai T, Loza E, Roig GVG, Ajioka Y, Tsuchiya Y, Yamamoto M, Nakamura K. 2014. High Frequency of TP53 but not K-ras Gene Mutations in Bolivian Patients with Gallbladder Cancer. Asian Pac J Cancer Prev 15: 5449–5454. 10.7314/APJCP.2014.15.13.5449 PubMedWeb of Science®Google Scholar Atay V, Cam C, Muhcu M, Cam M, Karateke A. 2006. Comparison of letrozole and clomiphene citrate in women with polycystic ovaries undergoing ovarian stimulation. J Int Med Res 34: 73–76. 10.1177/147323000603400109 CASPubMedWeb of Science®Google Scholar Badawy A, Mosbah A, Tharwat A, Eid M. 2009. Extended letrozole therapy for ovulation induction in clomiphene-resistant women with polycystic ovary syndrome: a novel protocol. Fertil Steril 92: 236–239. 10.1016/j.fertnstert.2008.04.065 CASPubMedWeb of Science®Google Scholar Barbieri RL, Gochberg J, Ryan KJ. 1986. Nicotine, cotinine, and anabasine inhibit aromatase in human trophoblast in vitro. J Clin Invest 77: 1727–1733. 10.1172/JCI112494 CASPubMedWeb of Science®Google Scholar Barbujani G, Colonna V. 2010. Human genome diversity: frequently asked questions. Trend Genet 26: 285–295. 10.1016/j.tig.2010.04.002 CASPubMedWeb of Science®Google Scholar Barbujani G, Ghirotto S, Tassi F. 2013. Nine things to remember about human genome diversity. Tissue Antigens 82: 155–164. 10.1111/tan.12165 CASPubMedWeb of Science®Google Scholar Birgander R, Sjalander A, Beckman G, Beckman L. 1996. Effect of p53 alleles on placental weight. Human Heredity 46: 290–297. 10.1159/000154365 CASPubMedWeb of Science®Google Scholar Bribiescas R, Muehlenbein M. 2010. Evolutionary endocrinology. In: M Muehlenbein, editor. Human evolutionary biology, 1st ed. Cambridge: Cambridge University Press. p 127–143. 10.1017/CBO9780511781193.010 Google Scholar Bryois J, Buil A, Evans DM, Kemp JP, Montgomery SB, Conrad DF, Ho KM, Ring S, Hurles M, Deloukas P, et al. 2014. Cis and trans effects of human genomic variants on gene expression. Plos Genet 10. 10.1371/journal.pgen.1004461 PubMedWeb of Science®Google Scholar Bulmer M. 1970. The biology of twinning in man. Oxford: Oxford University Press. Web of Science®Google Scholar Busjahn A, Knoblauch H, Faulhaber HD, Aydin A, Uhlmann R, Tuomilehto J, Kaprio J, Jedrusik P, Januszewicz A, Strelau J, et al. 2000. A region on chromosome 3 is linked to dizygotic twinning. Nat Genet 26: 398–399. 10.1038/82515 CASPubMedWeb of Science®Google Scholar Canzian F, Cox DG, Setiawan VW, Stram DO, Ziegler RG, Dossus L, Beckmann L, Blanche H, Barricarte A, Berg CD, et al. 2010. Comprehensive analysis of common genetic variation in 61 genes related to steroid hormone and insulin-like growth factor-I metabolism and breast cancer risk in the NCI breast and prostate cancer cohort consortium. Hum Mol Genet 19: 3873–3884. 10.1093/hmg/ddq291 CASPubMedWeb of Science®Google Scholar Chen Z-J, Zhao H, He L, Shi Y, Qin Y, Shi Y, Li Z, You L, Zhao J, Liu J, et al. 2011. Genome-wide association study identifies susceptibility loci for polycystic ovary syndrome on chromosome 2p16.3, 2p21 and 9q33.3. Nat Genet 43: 55–U75. 10.1038/ng.732 CASPubMedWeb of Science®Google Scholar Christensen B, Arbour L, Tran P, Leclerc D, Sabbaghian N, Platt R, Gilfix BM, Rosenblatt DS, Gravel RA, Forbes P, et al. 1999. Genetic polymorphisms in methylenetetrahydrofolate reductase and methionine synthase, folate levels in red blood cells, and risk of neural tube defects. Am J Med Genet 84: 151–157. 10.1002/(SICI)1096-8628(19990521)84:2 3.0.CO;2-T CASPubMedWeb of Science®Google Scholar Colonna V, Pagani L, Xue YL, Tyler-Smith C. 2011. A world in a grain of sand: human history from genetic data. Genome Biol 12: 9. 10.1186/gb-2011-12-11-234 Web of Science®Google Scholar Coulam CB, Kay C, Jeyendran RS. 2006. Role of p53 codon 72 polymorphism in recurrent pregnancy loss. Reprod Biomed Online 12: 378–382. 10.1016/S1472-6483(10)61013-9 CASPubMedWeb of Science®Google Scholar Crawford D, Nord A, Badzioch M, Ranchalis J, MCKinstry L, Hhearn M, VBertucci C, Shephard C, Wong M, Rieder M, et al. 2007. A common VLDLR polymorphism interacts with APOE genotype in the prediction of carotid artery disease risk. J Lipid Res 49: 588–596. 10.1194/jlr.M700409-JLR200 CASPubMedWeb of Science®Google Scholar Cyranoski D. 2009. Reproduction: two by two. Nature 458: 826–829. 10.1038/458826a CASPubMedWeb of Science®Google Scholar Czeizel AE, Vargha P. 2004. Periconceptional folic acid/multivitamin supplementation and twin pregnancy. Am J Obstet Gynecol 191: 790–794. 10.1016/j.ajog.2004.02.018 CASPubMedWeb of Science®Google Scholar De Oliveira MZ, Schueler-Faccini L, Demarchi DA, Alfaro EL, Dipierri JE, Veronez MR, Cassel MC, Tagliani-Ribeiro A, Matte US, Ramallo V. 2013. So Close, So Far Away: analysis of Surnames in a Town of Twins (Candido Godoi, Brazil). Ann Hum Genet 77: 125–136. 10.1111/ahg.12001 PubMedWeb of Science®Google Scholar Detmar J, Rabaglino T, Taniuchi Y, Oh J, Acton BM, Benito A, Nunez G, Jurisicova A. 2006. Embryonic loss due to exposure to polycyclic aromatic hydrocarbons is mediated by Bax. Apoptosis 11: 1413–1425. 10.1007/s10495-006-8442-3 CASPubMedWeb of Science®Google Scholar Echternkamp SE, Aad PY, Eborn DR, Spicer LJ. 2012. Increased abundance of aromatase and follicle stimulating hormone receptor mRNA and decreased insulin-like growth factor-2 receptor mRNA in small ovarian follicles of cattle selected for twin births. J Anim Sci 90: 2193–2200. 10.2527/jas.2011-4735 CASPubMedWeb of Science®Google Scholar Eriksson AL, Lorentzon M, Vandenput L, Labrie F, Lindersson M, Syvanen A-C, Orwoll ES, Cummings SR, Zmuda JM, Ljunggren O, et al. 2009. Genetic Variations in sex steroid-related genes as predictors of serum estrogen levels in men. J Clin Endocrinol Metab 94: 1033–1041. 10.1210/jc.2008-1283 CASPubMedWeb of Science®Google Scholar Feng ZH, Zhang C, Kang HJ, Sun Y, Wang HJ, Naqvi A, Frank AK, Rosenwaks Z, Murphy ME, Levine AJ, et al. 2011. Regulation of female reproduction by p53 and its family members. Faseb J 25: 2245–2255. 10.1096/fj.10-180166 CASPubMedWeb of Science®Google Scholar Fernandez-Cuesta L, Anaganti S, Hainaut P, Olivier M. 2011. p53 status influences response to tamoxifen but not to fulvestrant in breast cancer cell lines. Int J Cancer 128: 1813–1821. 10.1002/ijc.25512 CASPubMedWeb of Science®Google Scholar Firouzabadi RD, Ghasemi N, Rozbahani MA, Tabibnejad N. 2009. Association of p53 polymorphism with ICSI/IVF failure and recurrent pregnancy loss. Aust N Z J Obstet Gynaecol 49: 216–219. 10.1111/j.1479-828X.2009.00972.x PubMedWeb of Science®Google Scholar Fraga L, Dutra C, Boquett J, Vianna F, Goncalalves R, Paskulin DD, Costa O, Ashton-Prolla P, Sanseverino M, Schuler-Faccini L. 2014. p53 signaling pathway polymorphisms associated to recurrent pregnancy loss. Mol Biol Rep 41: 1871–1877. 10.1007/s11033-014-3036-6 CASPubMedWeb of Science®Google Scholar Ganesh SK, Tragante V, Guo W, Guo Y, Lanktree MB, Smith EN, Johnson T, Castillo BA, Barnard J, Baumert J, et al. 2013. Loci influencing blood pressure identified using a cardiovascular gene-centric array. Hum Mol Genet 22: 1663–1678. 10.1093/hmg/dds555 CASPubMedWeb of Science®Google Scholar Garritano S, Gemignani F, Voegele C, Nguyen-Dumont T, Le Calvez-Kelm F, De Silva D, Lesueur F, Landi S, Tavtigian SV. 2009. Determining the effectiveness of High Resolution Melting analysis for SNP genotyping and mutation scanning at the TP53 locus. BMC Genet 10. 10.1186/1471-2156-10-5 PubMedWeb of Science®Google Scholar Gocze PM, Szabo I, Freeman DA. 1999. Influence of nicotine, cotinine, anabasine and cigarette smoke extract on human granulosa cell progesterone and estradiol synthesis. Gynecol Endocrinol 13: 266–272. 10.3109/09513599909167565 CASPubMedWeb of Science®Google Scholar Hartwig F. 2013. SNP-SNP Interactions: focusing on variable coding for complex models of epistasis. Genet Syndrome Gene Ther 4: 1–6. Google Scholar Hatzirodos N, Hummitzsch K, Irving-Rodgers HF, Harland ML, Morris SE, Rodgers RJ. 2014. Transcriptome profiling of granulosa cells from bovine ovarian follicles during atresia. BMC Genomics 15. Google Scholar Healey S, Tan SL, Tulandi T, Biljan MM. 2003. Effects of letrozole on superovulation with gonadotropins in women undergoing intrauterine insemination. Fertil Steril 80: 1325–1329. 10.1016/j.fertnstert.2003.03.001 PubMedWeb of Science®Google Scholar Healey SC, Duffy DL, Martin NG, Turner G. 1997. Is fragile X syndrome a risk factor for dizygotic twinning? Am J Med Genet 72: 245–246. 10.1002/(SICI)1096-8628(19971017)72:2 3.0.CO;2-M CASPubMedWeb of Science®Google Scholar Hoekstra C, Willemsen G, van Beijsterveldt T, Lambalk CB, Montgomery GW, Boomsma DI. 2010. Body composition, smoking, and spontaneous dizygotic twinning. Fertil Steril 93: 885–893. 10.1016/j.fertnstert.2008.10.012 PubMedWeb of Science®Google Scholar Hoekstra C, Zhao ZZ, Lambalk CB, Willemsen G, Martin NG, Boomsma DI, Montgomery GW. 2008. Dizygotic twinning. Hum Reprod Update 14: 37–47. 10.1093/humupd/dmm036 CASPubMedWeb of Science®Google Scholar Infante-Rivard C, Weinberg CR, Guiguet M. 2006. Xenobiotic-metabolizing genes and small-for-gestational-age births—interaction with maternal smoking. Epidemiology 17: 38–46. 10.1097/01.ede.0000187669.34003.b1 PubMedWeb of Science®Google Scholar James WH. 1997. An hypothesis on the association between maternal smoking and dizygotic twinning. Hum Reprod 12: 1391–1392. 10.1093/humrep/12.7.1391 CASPubMedWeb of Science®Google Scholar Jasienska G. 2010. Why women vary in ovarian function. In: M Muehlenbein, editor. Human evolutionary biology. Cambridge: Cambridge University Press. p 322–337. 10.1017/CBO9780511781193.024 Google Scholar Kallen K. 1998. Maternal smoking and twinning. Twin Res 1: 206–211. 10.1375/136905298320566177 CASPubMedGoogle Scholar Kallen B. 2004. Use of folic acid supplementation and risk for dizygotic twinning. Early Hum Dev 80: 143–151. 10.1016/j.earlhumdev.2004.06.002 CASPubMedWeb of Science®Google Scholar Kiefer AK, Tung JY, Do CB, Hinds DA, Mountain JL, Francke U, Eriksson N. 2013. Genome-wide analysis points to roles for extracellular matrix remodeling, the visual cycle, and neuronal development in myopia. PLOS Genet 9. 10.1371/journal.pgen.1003299 PubMedWeb of Science®Google Scholar Levine AJ, Tomasini R, McKeon FD, Mak TW, Melino G. 2011. The p53 family: guardians of maternal reproduction. Nat Rev Mol Cell Biol 12: 259–+. 10.1038/nrm3086 CASPubMedWeb of Science®Google Scholar Li Z, Gindler J, Wang H, Berry RJ, Li S, Correa A, Zheng JC, Erickson JD, Wang Y. 2003. Folic acid supplements during early pregnancy and likelihood of multiple births: a population-based cohort study. Lancet 361: 380–384. 10.1016/S0140-6736(03)12390-2 CASPubMedWeb of Science®Google Scholar Liao WX, Roy AC, Ng SC. 2001. Follicle-stimulating-hormone receptor and twinning. Lancet 357: 230–230. 10.1016/S0140-6736(05)71329-5 CASPubMedWeb of Science®Google Scholar Lin M, Stewart DJ, Spitz MR, Hildebrandt MAT, Lu C, Lin J, Gu J, Huang M, Lippman SM, Wu X. 2011. Genetic variations in the transforming growth factor-beta pathway as predictors of survival in advanced non-small cell lung cancer. Carcinogenesis 32: 1050–1056. 10.1093/carcin/bgr067 CASPubMedWeb of Science®Google Scholar Lumley J, Watson L, Watson M, Bower C. 2001. Modelling the potential impact of population-wide periconceptional folate/multivitamin supplementation on multiple births. Brit J Obstet Gynaecol 108: 937–942. 10.1111/j.1471-0528.2001.00228.x CASPubMedWeb of Science®Google Scholar Madrigal L. 1994. Twinning rates in admixed Costa Rican populations. Am J Hum Biol 6: 215–218. 10.1002/ajhb.1310060209 Web of Science®Google Scholar Madrigal L. 1995. Differential fertility of mothers of twins and mothers of singletons. A study in Limon, Costa Rica. Hum Biol 67: 779–787. PubMedWeb of Science®Google Scholar Madrigal L, Barbujani G. 2007. Partitioning of genetic variation in human populations and the concept of race. In: M Crawford, editor. Anthropological genetics: theory, methdos, and applications. Cambridge: Cambridge University Press. p 19–37. Google Scholar Mathews F, Murphy M, Wald NJ, Hackshaw A. 1999. Twinning and folic acid use. Lancet 353: 291–292. 10.1016/S0140-6736(05)74937-0 CASPubMedWeb of Science®Google Scholar Minarik M, Benesova L, Fantova L, Horacek J, Heracek J, Loukola A. 2006. Parallel optimization and genotyping of multiple single-nucleotide polymorphism markers by sample pooling approach using cycling-gradient CE with multiple injections. Electrophoresis 27: 3856–3863. 10.1002/elps.200600289 CASPubMedWeb of Science®Google Scholar Moen EL, Zhang X, Mu W, Delaney SM, Wing C, McQuade J, Myers J, Godley LA, Dolan ME, Zhang W. 2013. Genome-wide variation of cytosine modifications between European and African populations and the implications for complex traits. Genetics 194: 987–+. 10.1534/genetics.113.151381 CASPubMedWeb of Science®Google Scholar Molinari AM, Bontempo P, Schiavone EM, Tortora V, Verdicchio MA, Napolitano M, Nola E, Moncharmont B, Medici N, Nigro V, et al. 2000. Estradiol induces functional inactivation of p53 by intracellular redistribution. Cancer Res 60: 2594–2597. Google Scholar Murdoch WJ. 2003. Metaplastic potential of p53 down-regulation in ovarian surface epithelial cells affected by ovulation. Cancer Lett 191: 75–81. 10.1016/S0304-3835(02)00623-7 CASPubMedWeb of Science®Google Scholar Nahid L, Sirous K. 2012. Comparison of the effects of letrozole and clomiphene citrate for ovulation induction in infertile women with polycystic ovary syndrome. Miner Ginecol 64: 253–258. Google Scholar Oikonen M, Tikkanen E, Juhola J, Tuovinen T, Seppala I, Juonala M, Taittonen L, Mikkila V, Kahonen M, Ripatti S, et al. 2011. Genetic variants and blood pressure in a population-based cohort the cardiovascular risk in young finns study. Hypertension 58: 1079–U1228. 10.1161/HYPERTENSIONAHA.111.179291 CASPubMedWeb of Science®Google Scholar Painter JN, Willemsen G, Nyholt D, Hoekstra C, Duffy DL, Henders AK, Wallace L, Healey S, Cannon-Albright LA, Skolnick M, et al. 2010. A genome wide linkage scan for dizygotic twinning in 525 families of mothers of dizygotic twins. Hum Reprod 25: 1569–1580. 10.1093/humrep/deq084 CASPubMedWeb of Science®Google Scholar Palmer JS, Zhao ZZ, Hoekstra C, Hayward NK, Webb PM, Whiteman DC, Martin NG, Boomsma DI, Duffy DL, Montgomery GW. 2006. Novel variants in growth differentiation factor 9 in mothers of dizygotic twins. J Clin Endocrinol Metab 91: 4713–4716. 10.1210/jc.2006-0970 CASPubMedWeb of Science®Google Scholar Palmieri RT, Wilson MA, Iversen ES, Clyde MA, Calingaert B, Moorman PG, Poole C, Anderson AR, Anderson S, Anton-Culver H, et al. 2008. Polymorphism in the IL18 gene and epithelial ovarian cancer in non-hispanic white women. Cancer Epidemiol Biomarker Prev 17: 3567–3572. 10.1158/1055-9965.EPI-08-0548 CASPubMedWeb of Science®Google Scholar Parazzini F, Chatenoud L, Benzi G, DiCintio E, DalPino D, Tozzi L, Fedele L. 1996. Coffee and alcohol intake, smoking and risk of multiple pregnancy. Hum Reprod 11: 2306–2309. 10.1093/oxfordjournals.humrep.a019094 CASPubMedWeb of Science®Google Scholar Perni SC, Kalish RB, Hutson JM, Karasahin E, Bongiovanni AM, Ratushny V, Chasen ST, Witkin SS. 2005. Differential expression of immune system-related components in midtrimester amniotic fluid from singleton-and twin pregnancies. Am J Obstet Gynecol 193: 942–946. 10.1016/j.ajog.2005.05.081 CASPubMedWeb of Science®Google Scholar Prelog M. 2011. Smoking and reproduction. In: D Bernhard, editor. Cigarette smoke toxicity: linking individual chemicals to human diseases. Weinheim: Wiley-VCH Verlag GmbH & Co. KGaZ. Google Scholar Reilly R, McNulty H, Pentieva K, Strain JJ, Ward M. 2014. MTHFR 677TT genotype and disease risk: is there a modulating role for B-vitamins? Proc Nutr Soc 73: 47–56. 10.1017/S0029665113003613 CASPubMedWeb of Science®Google Scholar Rosenthal L, Lobel M. 2011. Explaining racial disparities in adverse birth outcomes: unique sources of stress for Black American women. Soc Sci Med 72: 977–983. 10.1016/j.socscimed.2011.01.013 PubMedWeb of Science®Google Scholar Saleemuddin A, Folkins AK, Garrett L, Garber J, Muto MG, Crum CP, Tworoger S. 2008. Risk factors for a serous cancer precursor ("p53 signature") in women with inherited BRCA mutations. Gynecol Oncol 111: 226–232. 10.1016/j.ygyno.2008.07.018 PubMedWeb of Science®Google Scholar Satija M, Sharma S, Soni RK, Sachar RK, Singh GPI. 2008. Twinning and its correlates: community-based study in a rural area of India. Hum Biol 80: 611–621. 10.3378/1534-6617-80.6.611 PubMedWeb of Science®Google Scholar Schelonka RL, Maheshwari A, Carlo WA, Taylor S, Hansen NI, Schendel DE, Thorsen P, Skogstrand K, Hougaard DM, Higgins RD, et al. 2011. T cell cytokines and the risk of blood stream infection in extremely low birth weight infants. Cytokine 53: 249–255. 10.1016/j.cyto.2010.11.003 CASPubMedWeb of Science®Google Scholar Schildkraut JM, Bastos E, Berchuck A. 1997. Relationship between lifetime ovulatory cycles and overexpression of mutant p53 in epithelial ovarian cancer. J Natl Cancer Inst 89: 932–938. 10.1093/jnci/89.13.932 CASPubMedWeb of Science®Google Scholar Schildkraut JM, Goode EL, Clyde MA, Iversen ES, Moorman PG, Berchuck A, Marks JR, Lissowska J, Brinton L, Peplonska B, et al. 2009. Single nucleotide polymorphisms in the TP53 region and susceptibility to invasive epithelial ovarian cancer. Cancer Res 69: 2349–2357. 10.1158/0008-5472.CAN-08-2902 CASPubMedWeb of Science®Google Scholar Schlebusch CM, Skoglund P, Sjodin P, Gattepaille LM, Hernandez D, Jay F, Li S, De Jongh M, Singleton A, Blum MGB, et al. 2012. Genomic variation in seven Khoe-San groups reveals adaptation and complex African history. Science 338: 374–379. 10.1126/science.1227721 CASPubMedWeb of Science®Google Scholar Schmidt HD, Rosing FW, Schmidt DE. 1983. Causes of an extremely high local twinning rate. Ann Hum Biol 10: 371−380. 10.1080/03014468300006541 CASPubMedWeb of Science®Google Scholar Sear R, Shanley D, McGregor IA, Mace R. 2001. The fitness of twin mothers: evidence from rural Gambia. J Evol Biol 14: 433–443. 10.1046/j.1420-9101.2001.00287.x Web of Science®Google Scholar Shaw GM, Carmichael SL, Nelson V, Selvin S, Schaffer DM. 2003. Food fortification with folic acid and twinning among California infants. Am J Med Genet Part A 119A: 137–140. 10.1002/ajmg.a.20145 PubMedWeb of Science®Google Scholar Smits J, Monden C. 2011. Twinning across the Developing World. Plos One 6. 10.1371/journal.pone.0025239 Web of Science®Google Scholar Tagliani-Ribeiro A, Paskulin DD, Oliveira M, Zagonel-Oliveira M, Longo D, Ramallo V, Ashton-Prolla P, Saraiva-Pereira ML, Fagundes NJR, Schuler-Faccini L, et al. 2012. High twinning rate in Cndido Godi: a new role for p53 in human fertility. Hum Reprod 27: 2866–2871. 10.1093/humrep/des217 CASPubMedWeb of Science®Google Scholar Toledo F, Wahl GM. 2006. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 6: 909–923. 10.1038/nrc2012 CASPubMedWeb of Science®Google Scholar Velez DR, Fortunato S, Thorsen P, Lombardi SJ, Williams SM, Menon R. 2009. Spontaneous preterm birth in African Americans is associated with infection and inflammatory response gene variants. Am J Obstet Gynecol 200: 209.e1. 10.1016/j.ajog.2008.08.051 CASPubMedWeb of Science®Google Scholar Vijai J, Gaudet MM, Dutra-Clarke A, Hansen N, Devlin V, Kauff N, Hudis CA, Bond GL, Offit K, Kirchhoff T. 2010. Genetic variation of human MDM4 confers increased risk to breast cancer in Ashkenazi Jewish (AJ) population. Proc Am Assoc Cancer Res 51: 691–691. Google Scholar Vinet A, Drouilhet L, Bodin L, Mulsant P, Fabre S, Phocas F. 2012. Genetic control of multiple births in low ovulating mammalian species. Mammal Genome 23: 727–740. 10.1007/s00335-012-9412-4 PubMedWeb of Science®Google Scholar Vollset SE, Gjessing HK, Tandberg A, Ronning T, Irgens LM, Baste V, Nilsen RM, Daltveit AK. 2005. Folate supplementation and twin pregnancies. Epidemiology 16: 201–205. 10.1097/01.ede.0000152914.84962.13 PubMedWeb of Science®Google Scholar Wakeel F, Wisk LE, Gee R, Chao SM, Witt WP. 2013. The balance between stress and personal capital during pregnancy and the relationship with adverse obstetric outcomes: findings from the 2007 Los Angeles Mommy and Baby (LAMB) study. Arch Womens Mental Health 16: 435–451. 10.1007/s00737-013-0367-6 PubMedWeb of Science®Google Scholar Werler MM, Cragan JD, Wasserman CR, Shaw GM, Erickson JD, Mitchell AA. 1997. Multivitamin supplementation and multiple births. Am J Med Genet 71: 93–96. 10.1002/(SICI)1096-8628(19970711)71:1 3.0.CO;2-Q CASPubMedWeb of Science®Google Scholar Westra H-J, Peters MJ, Esko T, Yaghootkar H, Schurmann C, Kettunen J, Christiansen MW, Fairfax BP, Schramm K, Powell JE, et al. 2013. Systematic identification of trans eQTLs as putative drivers of known disease associations. Nat Genet 45: 1238–U1195. 10.1038/ng.2756 CASPubMedWeb of Science®Google Scholar Woods SM, Melville JL, Guo Y, Fan M-Y, Gavin A. 2010. Psychosocial stress during pregnancy. Am J Obstet Gynecol 202: e1–e7. PubMedWeb of Science®Google Scholar Wu X, Zhao L, Zhu H, He D, Tang W, Luo Y. 2012. Association between the MTHFR C677T polymorphism and recurrent pregnancy loss: a meta-analysis. Genet Test Mol Biomarkers 16: 806–811. 10.1089/gtmb.2011.0318 CASPubMedWeb of Science®Google Scholar Yapura J, Mapletoft RJ, Pierson R, Singh J, Naile J, Giesy JP, Adams GP. 2011. A bovine model for examining the effects of an aromatase inhibitor on ovarian function in women. Fertil Steril 96: 434–U507. 10.1016/j.fertnstert.2011.05.038 CASPubMedWeb of Science®Google Scholar Zhang T, Lou J, Zhong R, Wu J, Zou L, Sun Y, Lu X, Liu L, Miao X, Xiong G. 2013. Genetic variants in the folate pathway and the risk of neural tube defects: a meta-analysis of the published literature. Plos One 8. 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