Racial and Ethnic Differences in the Pathogenesis and Clinical Manifestations of Uterine Leiomyoma

William H. Catherino; Heba M. Eltoukhi; Ayman Al-Hendy

doi:10.1055/s-0033-1348896

Seminars in Reproductive Medicine, Table of Contents

Semin Reprod Med 2013; 31(05): 370-379
DOI: 10.1055/s-0033-1348896

Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Racial and Ethnic Differences in the Pathogenesis and Clinical Manifestations of Uterine Leiomyoma

William H. Catherino

¹Program in Reproductive and Adult Endocrinology, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland

²Department of Obstetrics and Gynecology, Uniformed Services University of the Health Sciences, Bethesda, Maryland

,

Heba M. Eltoukhi

¹Program in Reproductive and Adult Endocrinology, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland

³Department of Obstetrics and Gynecology, Suez Canal University, Ismailia, Egypt

,

Ayman Al-Hendy

⁴Center for Women Health Research, Department of Obstetrics and Gynecology, Meharry Medical College, Nashville, Tennessee

› Author Affiliations

Abstract

Uterine leiomyomas are the most common benign gynecologic condition. The prevalence is three times more common among women of African ethnicity. Disparity in this disease is evidenced by earlier age of onset, greater severity of symptoms, and different response to treatment. Although the pathogenesis of disease development is not completely known, growing evidence focuses on investigating the molecular mechanisms in disease development and the influence of ethnicity. Variation in the expression levels or function of estrogen and progesterone receptors, polymorphism of genes involved in estrogen synthesis and/or metabolism (COMT, CYP17), retinoic acid nuclear receptors (retinoid acid receptor-α, retinoid X receptor-α), and aberrant expression of micro-RNAs (miRNAs) are some of the molecular mechanisms that may be involved. Nutritional factors, such as vitamin D deficiency, might also contribute to the higher incidence in dark skinned populations who are also commonly suffer from hypovitaminosis D. Culture and environmental difference might have a role in disease development. Further analysis and better understanding of these mechanisms will provide insight into the molecular basis of racial disparities in leiomyoma formation and will help to develop new innovations in leiomyoma treatment.

Keywords

uterine leiomyoma - African American - ethnicity - molecular - risk factor

Full Text

References

References
1 Baird DD, Dunson DB, Hill MC, Cousins D, Schectman JM. High cumulative incidence of uterine leiomyoma in black and white women: ultrasound evidence. Am J Obstet Gynecol 2003; 188 (1) 100-107
2 Marshall LM, Spiegelman D, Barbieri RL , et al. Variation in the incidence of uterine leiomyoma among premenopausal women by age and race. Obstet Gynecol 1997; 90 (6) 967-973
3 Kjerulff KH, Langenberg P, Seidman JD, Stolley PD, Guzinski GM. Uterine leiomyomas. Racial differences in severity, symptoms and age at diagnosis. J Reprod Med 1996; 41 (7) 483-490
4 Cardozo ER, Clark AD, Banks NK, Henne MB, Stegmann BJ, Segars JH. The estimated annual cost of uterine leiomyomata in the United States. Am J Obstet Gynecol 2012; 206 (3) e1-e9
5 Shynlova O, Tsui P, Jaffer S, Lye SJ. Integration of endocrine and mechanical signals in the regulation of myometrial functions during pregnancy and labour. Eur J Obstet Gynecol Reprod Biol 2009; 144 (Suppl. 01) S2-S10
6 Walker CL, Stewart EA. Uterine fibroids: the elephant in the room. Science 2005; 308 (5728) 1589-1592
7 Andersen J, Barbieri RL. Abnormal gene expression in uterine leiomyomas. J Soc Gynecol Investig 1995; 2 (5) 663-672
8 Wallach EE, Vlahos NF. Uterine myomas: an overview of development, clinical features, and management. Obstet Gynecol 2004; 104 (2) 393-406
9 Chegini N. Proinflammatory and profibrotic mediators: principal effectors of leiomyoma development as a fibrotic disorder. Semin Reprod Med 2010; 28 (3) 180-203
10 Catherino WH, Leppert PC, Stenmark MH , et al. Reduced dermatopontin expression is a molecular link between uterine leiomyomas and keloids. Genes Chromosomes Cancer 2004; 40 (3) 204-217
11 Leppert PC, Baginski T, Prupas C, Catherino WH, Pletcher S, Segars JH. Comparative ultrastructure of collagen fibrils in uterine leiomyomas and normal myometrium. Fertil Steril 2004; 82 (Suppl. 03) 1182-1187
12 Dimitrova IK, Richer JK, Rudolph MC , et al. Gene expression profiling of multiple leiomyomata uteri and matched normal tissue from a single patient. Fertil Steril 2009; 91 (6) 2650-2663
13 Wei T, Geiser AG, Qian HR , et al. DNA microarray data integration by ortholog gene analysis reveals potential molecular mechanisms of estrogen-dependent growth of human uterine fibroids. BMC Womens Health 2007; 7: 5
14 Wei JJ, Chiriboga L, Arslan AA, Melamed J, Yee H, Mittal K. Ethnic differences in expression of the dysregulated proteins in uterine leiomyomata. Hum Reprod 2006; 21 (1) 57-67
15 Wei JJ, Chiriboga L, Mittal K. Expression profile of the tumorigenic factors associated with tumor size and sex steroid hormone status in uterine leiomyomata. Fertil Steril 2005; 84 (2) 474-484
16 Ahn WS, Kim KW, Bae SM , et al. Targeted cellular process profiling approach for uterine leiomyoma using cDNA microarray, proteomics and gene ontology analysis. Int J Exp Pathol 2003; 84 (6) 267-279
17 Wang H, Mahadevappa M, Yamamoto K , et al. Distinctive proliferative phase differences in gene expression in human myometrium and leiomyomata. Fertil Steril 2003; 80 (2) 266-276
18 Malik M, Norian J, McCarthy-Keith D, Britten J, Catherino WH. Why leiomyomas are called fibroids: the central role of extracellular matrix in symptomatic women. Semin Reprod Med 2010; 28 (3) 169-179
19 Zaitseva M, Vollenhoven BJ, Rogers PA. In vitro culture significantly alters gene expression profiles and reduces differences between myometrial and fibroid smooth muscle cells. Mol Hum Reprod 2006; 12 (3) 187-207
20 Pan Q, Luo X, Chegini N. Genomic and proteomic profiling I: leiomyomas in African Americans and Caucasians. Reprod Biol Endocrinol 2007; 5: 34
21 Al-Hendy A, Salama SA. Ethnic distribution of estrogen receptor-alpha polymorphism is associated with a higher prevalence of uterine leiomyomas in black Americans. Fertil Steril 2006; 86 (3) 686-693
22 Djuranovic S, Nahvi A, Green R. A parsimonious model for gene regulation by miRNAs. Science 2011; 331 (6017) 550-553
23 Morikawa J, Yoshida S, Kennedy S , et al. Association study between catechol-O-methyltransferase polymorphisms and uterine leiomyomas in a Japanese population. Clin Exp Obstet Gynecol 2008; 35 (1) 35-40
24 Denschlag D, Bentz EK, Hefler L , et al. Genotype distribution of estrogen receptor-alpha, catechol-O-methyltransferase, and cytochrome P450 17 gene polymorphisms in Caucasian women with uterine leiomyomas. Fertil Steril 2006; 85 (2) 462-467
25 Al-Hendy A, Salama SA. Catechol-O-methyltransferase polymorphism is associated with increased uterine leiomyoma risk in different ethnic groups. J Soc Gynecol Investig 2006; 13 (2) 136-144
26 Gooden KM, Schroeder JC, North KE , et al. Val153Met polymorphism of catechol-O-methyltransferase and prevalence of uterine leiomyomata. Reprod Sci 2007; 14 (2) 117-120
27 de Oliveira E, de Aquino Castro R, Gomes MT , et al. The catechol-O-methyltransferase (COMT) gene polymorphism and prevalence of uterine fibroids. Maturitas 2008; 60 (3-4) 235-238
28 Salama SA, Ho SL, Wang HQ, Tenhunen J, Tilgmann C, Al-Hendy A. Hormonal regulation of catechol-O-methyl transferase activity in women with uterine leiomyomas. Fertil Steril 2006; 86 (1) 259-262
29 Ates O, Demirturk F, Toprak M, Sezer S. Polymorphism of catechol-O-methyltransferase and uterine leiomyoma. Mol Cell Biochem 2013; 375 (1-2) 179-183
30 Chuang TD, Panda H, Luo X, Chegini N. miR-200c is aberrantly expressed in leiomyomas in an ethnic-dependent manner and targets ZEBs, VEGFA, TIMP2, and FBLN5. Endocr Relat Cancer 2012; 19 (4) 541-556
31 Wang T, Zhang X, Obijuru L , et al. A micro-RNA signature associated with race, tumor size, and target gene activity in human uterine leiomyomas. Genes Chromosomes Cancer 2007; 46 (4) 336-347
32 Lachman HM, Papolos DF, Saito T, Yu YM, Szumlanski CL, Weinshilboum RM. Human catechol-O-methyltransferase pharmacogenetics: description of a functional polymorphism and its potential application to neuropsychiatric disorders. Pharmacogenetics 1996; 6 (3) 243-250
33 Hassan MH, Fouad H, Bahashwan S, Al-Hendy A. Towards non-surgical therapy for uterine fibroids: catechol-O-methyl transferase inhibitor shrinks uterine fibroid lesions in the Eker rat model. Hum Reprod 2011; 26 (11) 3008-3018
34 Carey AH, Waterworth D, Patel K , et al. Polycystic ovaries and premature male pattern baldness are associated with one allele of the steroid metabolism gene CYP17. Hum Mol Genet 1994; 3 (10) 1873-1876
35 Picado-Leonard J, Miller WL. Cloning and sequence of the human gene for P450c17 (steroid 17 alpha-hydroxylase/17,20 lyase): similarity with the gene for P450c21. DNA 1987; 6 (5) 439-448
36 Amant F, Dorfling CM, de Brabanter J , et al. A possible role of the cytochrome P450c17alpha gene (CYP17) polymorphism in the pathobiology of uterine leiomyomas from black South African women: a pilot study. Acta Obstet Gynecol Scand 2004; 83 (3) 234-239
37 Pakiz M, Potocnik U, But I, Mujezinovic F. A CYP17A1 gene polymorphism in association with multiple uterine leiomyomas: a meta-analysis. Cancer Biomark 2010– 2011; 8 (1) 29-34
38 Taioli E, Trachman J, Chen X, Toniolo P, Garte SJ. A CYP1A1 restriction fragment length polymorphism is associated with breast cancer in African-American women. Cancer Res 1995; 55 (17) 3757-3758
39 El-Shennawy GA, Elbialy AA, Isamil AE, El Behery MM. Is genetic polymorphism of ER-α, CYP1A1, and CYP1B1 a risk factor for uterine leiomyoma?. Arch Gynecol Obstet 2011; 283 (6) 1313-1318
40 Ye Y, Cheng X, Luo HB, Liu L, Li YB, Hou YP. CYP1A1 and CYP1B1 genetic polymorphisms and uterine leiomyoma risk in Chinese women. J Assist Reprod Genet 2008; 25 (8) 389-394
41 Herr D, Bettendorf H, Denschlag D, Keck C, Pietrowski D. Cytochrome P2A13 and P1A1 gene polymorphisms are associated with the occurrence of uterine leiomyoma. Arch Gynecol Obstet 2006; 274 (6) 367-371
42 Willis BC, Borok Z. TGF-beta-induced EMT: mechanisms and implications for fibrotic lung disease. Am J Physiol Lung Cell Mol Physiol 2007; 293 (3) L525-L534
43 Liu Y. Renal fibrosis: new insights into the pathogenesis and therapeutics. Kidney Int 2006; 69 (2) 213-217
44 Yata Y, Gotwals P, Koteliansky V, Rockey DC. Dose-dependent inhibition of hepatic fibrosis in mice by a TGF-beta soluble receptor: implications for antifibrotic therapy. Hepatology 2002; 35 (5) 1022-1030
45 Verrecchia F, Mauviel A, Farge D. Transforming growth factor-beta signaling through the Smad proteins: role in systemic sclerosis. Autoimmun Rev 2006; 5 (8) 563-569
46 Bonniaud P, Margetts PJ, Ask K, Flanders K, Gauldie J, Kolb M. TGF-beta and Smad3 signaling link inflammation to chronic fibrogenesis. J Immunol 2005; 175 (8) 5390-5395
47 Carrino DA, Mesiano S, Barker NM, Hurd WW, Caplan AI. Proteoglycans of uterine fibroids and keloid scars: similarity in their proteoglycan composition. Biochem J 2012; 443 (2) 361-368
48 Sinclair DC, Mastroyannis A, Taylor HS. Leiomyoma simultaneously impair endometrial BMP-2-mediated decidualization and anticoagulant expression through secretion of TGF-β3. J Clin Endocrinol Metab 2011; 96 (2) 412-421
49 Ding L, Xu J, Luo X, Chegini N. Gonadotropin releasing hormone and transforming growth factor beta activate mitogen-activated protein kinase/extracellularly regulated kinase and differentially regulate fibronectin, type I collagen, and plasminogen activator inhibitor-1 expression in leiomyoma and myometrial smooth muscle cells. J Clin Endocrinol Metab 2004; 89 (11) 5549-5557
50 Lee BS, Nowak RA. Human leiomyoma smooth muscle cells show increased expression of transforming growth factor-beta 3 (TGF beta 3) and altered responses to the antiproliferative effects of TGF beta. J Clin Endocrinol Metab 2001; 86 (2) 913-920
51 Eiser AR. Does over-expression of transforming growth factor-beta account for the increased morbidity in African-Americans? Possible clinical study and therapeutic implications. Med Hypotheses 2010; 75 (5) 418-421
52 Arici A, Sozen I. Transforming growth factor-beta3 is expressed at high levels in leiomyoma where it stimulates fibronectin expression and cell proliferation. Fertil Steril 2000; 73 (5) 1006-1011
53 Derynck R, Lindquist PB, Lee A , et al. A new type of transforming growth factor-beta, TGF-beta 3. EMBO J 1988; 7 (12) 3737-3743
54 Norian JM, Malik M, Parker CY , et al. Transforming growth factor beta3 regulates the versican variants in the extracellular matrix-rich uterine leiomyomas. Reprod Sci 2009; 16 (12) 1153-1164
55 Joseph DS, Malik M, Nurudeen S, Catherino WH. Myometrial cells undergo fibrotic transformation under the influence of transforming growth factor beta-3. Fertil Steril 2010; 93 (5) 1500-1508
56 Xu J, Luo X, Chegini N. Differential expression, regulation, and induction of Smads, transforming growth factor-beta signal transduction pathway in leiomyoma, and myometrial smooth muscle cells and alteration by gonadotropin-releasing hormone analog. J Clin Endocrinol Metab 2003; 88 (3) 1350-1361
57 Zhang D, Al-Hendy M, Richard-Davis G, Montgomery-Rice V, Rajaratnam V, Al-Hendy A. Antiproliferative and proapoptotic effects of epigallocatechin gallate on human leiomyoma cells. Fertil Steril 2010; 94 (5) 1887-1893
58 Halder SK, Goodwin JS, Al-Hendy A. 1,25-Dihydroxyvitamin D3 reduces TGF-beta3-induced fibrosis-related gene expression in human uterine leiomyoma cells. J Clin Endocrinol Metab 2011; 96 (4) E754-E762
59 Di X, Andrews DM, Tucker CJ , et al. A high concentration of genistein down-regulates activin A, Smad3 and other TGF-β pathway genes in human uterine leiomyoma cells. Exp Mol Med 2012; 44 (4) 281-292
60 Grudzien MM, Low PS, Manning PC, Arredondo M, Belton Jr RJ, Nowak RA. The antifibrotic drug halofuginone inhibits proliferation and collagen production by human leiomyoma and myometrial smooth muscle cells. Fertil Steril 2010; 93 (4) 1290-1298
61 Zhang CH, Wen ZQ, Li JF , et al. Inhibition of proliferation and transforming growth factor beta3 protein expression by peroxisome proliferators-activated receptor gamma ligands in human uterine leiomyoma cells. Chin Med J (Engl) 2008; 121 (2) 166-171
62 Wang J, Ohara N, Wang Z , et al. A novel selective progesterone receptor modulator asoprisnil (J867) down-regulates the expression of EGF, IGF-I, TGFbeta3 and their receptors in cultured uterine leiomyoma cells. Hum Reprod 2006; 21 (7) 1869-1877
63 Bajracharya P, Lee EJ, Lee DM , et al. Effect of different ingredients in traditional Korean medicine for human uterine leiomyoma on normal myometrial and leiomyomal smooth muscle cell proliferation. Arch Pharm Res 2009; 32 (11) 1555-1563
64 Malik M, Catherino WH. Development and validation of a three-dimensional in vitro model for uterine leiomyoma and patient-matched myometrium. Fertil Steril 2012; 97 (6) 1287-1293
65 Catherino WH, Malik M. Uterine leiomyomas express a molecular pattern that lowers retinoic acid exposure. Fertil Steril 2007; 87 (6) 1388-1398
66 Boettger-Tong H, Shipley G, Hsu CJ, Stancel GM. Cultured human uterine smooth muscle cells are retinoid responsive. Proc Soc Exp Biol Med 1997; 215 (1) 59-65
67 Tsibris JC, Porter KB, Jazayeri A , et al. Human uterine leiomyomata express higher levels of peroxisome proliferator-activated receptor gamma, retinoid X receptor alpha, and all-trans retinoic acid than myometrium. Cancer Res 1999; 59 (22) 5737-5744
68 Malik M, Webb J, Catherino WH. Retinoic acid treatment of human leiomyoma cells transformed the cell phenotype to one strongly resembling myometrial cells. Clin Endocrinol (Oxf) 2008; 69 (3) 462-470
69 Huang ME, Ye YC, Chen SR , et al. Use of all-trans retinoic acid in the treatment of acute promyelocytic leukemia. Blood 1988; 72 (2) 567-572
70 Lippman SM, Parkinson DR, Itri LM , et al. 13-cis-retinoic acid and interferon alpha-2a: effective combination therapy for advanced squamous cell carcinoma of the skin. J Natl Cancer Inst 1992; 84 (4) 235-241
71 Kessler JF, Meyskens Jr FL, Levine N, Lynch PJ, Jones SE. Treatment of cutaneous T-cell lymphoma (mycosis fungoides) with 13-cis-retinoic acid. Lancet 1983; 1 (8338) 1345-1347
72 Toma S, Bonelli L, Sartoris A , et al. 13-cis retinoic acid in head and neck cancer chemoprevention: results of a randomized trial from the Italian Head and Neck Chemoprevention Study Group. Oncol Rep 2004; 11 (6) 1297-1305
73 Gamage SD, Bischoff ED, Burroughs KD , et al. Efficacy of LGD1069 (Targretin), a retinoid X receptor-selective ligand, for treatment of uterine leiomyoma. J Pharmacol Exp Ther 2000; 295 (2) 677-681
74 De Coster R, Wouters W, Van Ginckel R , et al. Experimental studies with liarozole (R 75,251): an antitumoral agent which inhibits retinoic acid breakdown. J Steroid Biochem Mol Biol 1992; 43 (1-3) 197-201
75 Bhushan M, Burden AD, McElhone K, James R, Vanhoutte FP, Griffiths CE. Oral liarozole in the treatment of palmoplantar pustular psoriasis: a randomized, double-blind, placebo-controlled study. Br J Dermatol 2001; 145 (4) 546-553
76 Gilden M, Malik M, Britten J, Delgado T, Levy G, Catherino WH. Leiomyoma fibrosis inhibited by liarozole, a retinoic acid metabolic blocking agent. Fertil Steril 2012; 98 (6) 1557-1562
77 Bulun SE, Lin Z, Imir G , et al. Regulation of aromatase expression in estrogen-responsive breast and uterine disease: from bench to treatment. Pharmacol Rev 2005; 57 (3) 359-383
78 Simpson ER, Clyne C, Rubin G , et al. Aromatase—a brief overview. Annu Rev Physiol 2002; 64: 93-127
79 Folkerd EJ, Newton CJ, Davidson K, Anderson MC, James VH. Aromatase activity in uterine leiomyomata. J Steroid Biochem 1984; 20 (5) 1195-1200
80 Pasqualini JR, Cornier E, Grenier J, Vella C, Schatz B, Netter A. Effect of Decapeptyl, an agonistic analog of gonadotropin-releasing hormone on estrogens, estrogen sulfates, and progesterone receptors in leiomyoma and myometrium. Fertil Steril 1990; 53 (6) 1012-1017
81 Sumitani H, Shozu M, Segawa T , et al. In situ estrogen synthesized by aromatase P450 in uterine leiomyoma cells promotes cell growth probably via an autocrine/intracrine mechanism. Endocrinology 2000; 141 (10) 3852-3861
82 Imir AG, Lin Z, Yin P , et al. Aromatase expression in uterine leiomyomata is regulated primarily by proximal promoters I.3/II. J Clin Endocrinol Metab 2007; 92 (5) 1979-1982
83 Shozu M, Sumitani H, Segawa T , et al. Overexpression of aromatase P450 in leiomyoma tissue is driven primarily through promoter I.4 of the aromatase P450 gene (CYP19). J Clin Endocrinol Metab 2002; 87 (6) 2540-2548
84 Ishikawa H, Reierstad S, Demura M , et al. High aromatase expression in uterine leiomyoma tissues of African-American women. J Clin Endocrinol Metab 2009; 94 (5) 1752-1756
85 Norman AW, Bouillon R. Vitamin D nutritional policy needs a vision for the future. Exp Biol Med (Maywood) 2010; 235 (9) 1034-1045
86 McDonnell DP, Mangelsdorf DJ, Pike JW, Haussler MR, O'Malley BW. Molecular cloning of complementary DNA encoding the avian receptor for vitamin D. Science 1987; 235 (4793) 1214-1217
87 Vienonen A, Miettinen S, Bläuer M , et al. Expression of nuclear receptors and cofactors in human endometrium and myometrium. J Soc Gynecol Investig 2004; 11 (2) 104-112
88 Baker AR, McDonnell DP, Hughes M , et al. Cloning and expression of full-length cDNA encoding human vitamin D receptor. Proc Natl Acad Sci U S A 1988; 85 (10) 3294-3298
89 Wang QM, Jones JB, Studzinski GP. Cyclin-dependent kinase inhibitor p27 as a mediator of the G1-S phase block induced by 1,25-dihydroxyvitamin D3 in HL60 cells. Cancer Res 1996; 56 (2) 264-267
90 Simboli-Campbell M, Narvaez CJ, van Weelden K, Tenniswood M, Welsh J. Comparative effects of 1,25(OH)2D3 and EB1089 on cell cycle kinetics and apoptosis in MCF-7 breast cancer cells. Breast Cancer Res Treat 1997; 42 (1) 31-41
91 Zhuang SH, Burnstein KL. Antiproliferative effect of 1alpha,25-dihydroxyvitamin D3 in human prostate cancer cell line LNCaP involves reduction of cyclin-dependent kinase 2 activity and persistent G1 accumulation. Endocrinology 1998; 139 (3) 1197-1207
92 Colston KW, Hansen CM. Mechanisms implicated in the growth regulatory effects of vitamin D in breast cancer. Endocr Relat Cancer 2002; 9 (1) 45-59
93 Sharan C, Halder SK, Thota C, Jaleel T, Nair S, Al-Hendy A. Vitamin D inhibits proliferation of human uterine leiomyoma cells via catechol-O-methyltransferase. Fertil Steril 2011; 95 (1) 247-253
94 Nesby-O'Dell S, Scanlon KS, Cogswell ME , et al. Hypovitaminosis D prevalence and determinants among African American and white women of reproductive age: third National Health and Nutrition Examination Survey, 1988-1994. Am J Clin Nutr 2002; 76 (1) 187-192
95 Sabry M, Halder SK, Allah AS, Roshdy E, Rajaratnam V, Al-Hendy A. Serum vitamin D3 level inversely correlates with uterine fibroid volume in different ethnic groups: a cross-sectional observational study. Int J Womens Health 2013; 5: 93-100
96 Halder SK, Sharan C, Al-Hendy A. 1,25-dihydroxyvitamin D3 treatment shrinks uterine leiomyoma tumors in the Eker rat model. Biol Reprod 2012; 86 (4) 116
97 Othman EE, Al-Hendy A. Molecular genetics and racial disparities of uterine leiomyomas. Best Pract Res Clin Obstet Gynaecol 2008; 22 (4) 589-601
98 Jacoby VL, Fujimoto VY, Giudice LC, Kuppermann M, Washington AE. Racial and ethnic disparities in benign gynecologic conditions and associated surgeries. Am J Obstet Gynecol 2010; 202 (6) 514-521
99 Laughlin SK, Stewart EA. Uterine leiomyomas: individualizing the approach to a heterogeneous condition. Obstet Gynecol 2011; 117 (2, Pt 1) 396-403
100 Wechter ME, Stewart EA, Myers ER, Kho RM, Wu JM. Leiomyoma-related hospitalization and surgery: prevalence and predicted growth based on population trends. Am J Obstet Gynecol 2011; 205 (5) e1-e5
101 Wilcox LS, Koonin LM, Pokras R, Strauss LT, Xia Z, Peterson HB. Hysterectomy in the United States, 1988-1990. Obstet Gynecol 1994; 83 (4) 549-555
102 Roth TM, Gustilo-Ashby T, Barber MD, Myers ER. Effects of race and clinical factors on short-term outcomes of abdominal myomectomy. Obstet Gynecol 2003; 101 (5, Pt 1) 881-884
103 Abenhaim HA, Azziz R, Hu J, Bartolucci A, Tulandi T. Socioeconomic and racial predictors of undergoing laparoscopic hysterectomy for selected benign diseases: analysis of 341487 hysterectomies. J Minim Invasive Gynecol 2008; 15 (1) 11-15
104 Baird DD. Invited commentary: uterine leiomyomata-we know so little but could learn so much. Am J Epidemiol 2004; 159 (2) 124-126
105 Marshall LM, Spiegelman D, Goldman MB , et al. A prospective study of reproductive factors and oral contraceptive use in relation to the risk of uterine leiomyomata. Fertil Steril 1998; 70 (3) 432-439
106 Wise LA, Palmer JR, Harlow BL , et al. Reproductive factors, hormonal contraception, and risk of uterine leiomyomata in African-American women: a prospective study. Am J Epidemiol 2004; 159 (2) 113-123
107 Faerstein E, Szklo M, Rosenshein N. Risk factors for uterine leiomyoma: a practice-based case-control study. I. African-American heritage, reproductive history, body size, and smoking. Am J Epidemiol 2001; 153 (1) 1-10
108 D'Aloisio AA, Baird DD, DeRoo LA, Sandler DP. Early-life exposures and early-onset uterine leiomyomata in black women in the Sister Study. Environ Health Perspect 2012; 120 (3) 406-412
109 Wegman HL, Stetler C. A meta-analytic review of the effects of childhood abuse on medical outcomes in adulthood. Psychosom Med 2009; 71 (8) 805-812
110 Felitti VJ, Anda RF, Nordenberg D , et al. Relationship of childhood abuse and household dysfunction to many of the leading causes of death in adults. The Adverse Childhood Experiences (ACE) Study. Am J Prev Med 1998; 14 (4) 245-258
111 Goodwin RD, Stein MB. Association between childhood trauma and physical disorders among adults in the United States. Psychol Med 2004; 34 (3) 509-520
112 Boynton-Jarrett R, Rich-Edwards JW, Jun HJ, Hibert EN, Wright RJ. Abuse in childhood and risk of uterine leiomyoma: the role of emotional support in biologic resilience. Epidemiology 2011; 22 (1) 6-14
113 Baird D, Wise LA. Childhood abuse and fibroids. Epidemiology 2011; 22 (1) 15-17
114 Kant AK, Graubard BI. Ethnicity is an independent correlate of biomarkers of micronutrient intake and status in American adults. J Nutr 2007; 137 (11) 2456-2463
115 Timbo BB, Ross MP, McCarthy PV, Lin CT. Dietary supplements in a national survey: prevalence of use and reports of adverse events. J Am Diet Assoc 2006; 106 (12) 1966-1974
116 Rock CL. Multivitamin-multimineral supplements: who uses them?. Am J Clin Nutr 2007; 85 (1) 277S-279S
117 Wise LA, Radin RG, Palmer JR, Kumanyika SK, Boggs DA, Rosenberg L. Intake of fruit, vegetables, and carotenoids in relation to risk of uterine leiomyomata. Am J Clin Nutr 2011; 94 (6) 1620-1631
118 Wise LA, Palmer JR, Harlow BL , et al. Risk of uterine leiomyomata in relation to tobacco, alcohol and caffeine consumption in the Black Women's Health Study. Hum Reprod 2004; 19 (8) 1746-1754
119 Wickett RR. Permanent waving and straightening of hair. Cutis 1987; 39 (6) 496-497
120 Hauser R, Calafat AM. Phthalates and human health. Occup Environ Med 2005; 62 (11) 806-818
121 Weuve J, Hauser R, Calafat AM, Missmer SA, Wise LA. Association of exposure to phthalates with endometriosis and uterine leiomyomata: findings from NHANES, 1999-2004. Environ Health Perspect 2010; 118 (6) 825-832
122 Huang PC, Tsai EM, Li WF , et al. Association between phthalate exposure and glutathione S-transferase M1 polymorphism in adenomyosis, leiomyoma and endometriosis. Hum Reprod 2010; 25 (4) 986-994
123 Wise LA, Palmer JR, Reich D, Cozier YC, Rosenberg L. Hair relaxer use and risk of uterine leiomyomata in African-American women. Am J Epidemiol 2012; 175 (5) 432-440
124 Thoits PA. Stress, coping, and social support processes: where are we? What next?. J Health Soc Behav 1995; (Spec No): 53-79
125 Nepomnaschy PA, Welch K, McConnell D, Strassmann BI, England BG. Stress and female reproductive function: a study of daily variations in cortisol, gonadotrophins, and gonadal steroids in a rural Mayan population. Am J Hum Biol 2004; 16 (5) 523-532
126 Vines AI, Ta M, Esserman D, Baird DD. A comparison of the occurrence and perceived stress of major life events in black and white women. Women Health 2009; 49 (5) 368-380
127 Williams DR, Mohammed SA. Discrimination and racial disparities in health: evidence and needed research. J Behav Med 2009; 32 (1) 20-47
128 Vines AI, Ta M, Esserman DA. The association between self-reported major life events and the presence of uterine fibroids. Womens Health Issues 2010; 20 (4) 294-298