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Semin Reprod Med 2017; 35(03): 263-270
DOI: 10.1055/s-0037-1603582
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

The Systemic Effects of Endometriosis

Myles H. Alderman III   *
1   Department of Obstetrics and Gynecology and Reproductive Sciences, Yale School of Medicine, New Haven, Connecticut
,
Nicole Yoder   *
1   Department of Obstetrics and Gynecology and Reproductive Sciences, Yale School of Medicine, New Haven, Connecticut
,
Hugh S. Taylor
1   Department of Obstetrics and Gynecology and Reproductive Sciences, Yale School of Medicine, New Haven, Connecticut
› Author Affiliations
Further Information

Publication History

Publication Date:
28 June 2017 (online)

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Abstract

Endometriosis is a condition defined by the presence of endometrial glands and stroma in ectopic locations. While the most commonly seen symptoms of the disease are pelvic pain, dysmenorrhea, and infertility, endometriosis has also systemic effects in multiple organ systems. Here, we review literature describing closely associated comorbidities including cardiovascular disease, cancers, autoimmune disease, psychiatric conditions, and metabolism/body weight. We examine the pathophysiology and hypothesized mechanism by which endometriosis may lead to these systemic effects; mechanisms include cytokine and micro-RNA production as well as stem cell migration and dissemination. The broad systemic effects of endometriosis as well as correlated comorbidities are often overlooked in the treatment of patients with endometriosis. Increased awareness may lead to more effective treatment and prevention.

Keywords

endometriosis - pain - inflammation - miRNA - stem cells - CXCL12

* These authors contributed equally to the writing of this article.


 

  • References

  • 1 Cramer DW, Missmer SA. The epidemiology of endometriosis. Ann N Y Acad Sci 2002; 955 (01) 11-22 , discussion 34–36, 396–406
    CrossrefPubMedGoogle Scholar
  • 2 De Graaff AA, D'Hooghe TM, Dunselman GA, Dirksen CD, Hummelshoj L, Simoens S. ; WERF EndoCost Consortium. The significant effect of endometriosis on physical, mental and social wellbeing: results from an international cross-sectional survey. Hum Reprod 2013; 28 (10) 2677-2685
    CrossrefPubMedGoogle Scholar
  • 3 Sampson JA. Metastatic or embolic endometriosis, due to the menstrual dissemination of endometrial tissue into the venous circulation. Am J Pathol 1927; 3 (02) 93-110 , 43
    PubMedGoogle Scholar
  • 4 Goetz LG, Mamillapalli R, Taylor HS. Low body mass index in endometriosis is promoted by hepatic metabolic gene dysregulation in mice. Biol Reprod 2016; 95 (06) 115
    CrossrefPubMedGoogle Scholar
  • 5 Kvaskoff M, Mu F, Terry KL. , et al. Endometriosis: a high-risk population for major chronic diseases?. Hum Reprod Update 2015; 21 (04) 500-516
    CrossrefPubMedGoogle Scholar
  • 6 Gemmill JA, Stratton P, Cleary SD, Ballweg ML, Sinaii N. Cancers, infections, and endocrine diseases in women with endometriosis. Fertil Steril 2010; 94 (05) 1627-1631
    CrossrefPubMedGoogle Scholar
  • 7 Teng SW, Horng HC, Ho CH, Yen MS, Chao HT, Wang PH. ; Taiwan Association of Gynecology Systematic Review Group. Women with endometriosis have higher comorbidities: analysis of domestic data in Taiwan. J Chin Med Assoc 2016; 79 (11) 577-582
    CrossrefPubMedGoogle Scholar
  • 8 Cosar E, Mamillapalli R, Ersoy GS, Cho S, Seifer B, Taylor HS. Serum microRNAs as diagnostic markers of endometriosis: a comprehensive array-based analysis. Fertil Steril 2016; 106 (02) 402-409
    CrossrefPubMedGoogle Scholar
  • 9 Monsanto SP, Edwards AK, Zhou J. , et al. Surgical removal of endometriotic lesions alters local and systemic proinflammatory cytokines in endometriosis patients. Fertil Steril 2016; 105 (04) 968-977.e5
    CrossrefPubMedGoogle Scholar
  • 10 Gazvani R, Templeton A. Peritoneal environment, cytokines and angiogenesis in the pathophysiology of endometriosis. Reproduction 2002; 123 (02) 217-226
    CrossrefPubMedGoogle Scholar
  • 11 Sakr S, Naqvi H, Komm B, Taylor HS. Endometriosis impairs bone marrow-derived stem cell recruitment to the uterus whereas bazedoxifene treatment leads to endometriosis regression and improved uterine stem cell engraftment. Endocrinology 2014; 155 (04) 1489-1497
    CrossrefPubMedGoogle Scholar
  • 12 Naqvi H, Mamillapalli R, Krikun G, Taylor HS. Endometriosis located proximal to or remote from the uterus differentially affects uterine gene expression. Reprod Sci 2016; 23 (02) 186-191
    CrossrefPubMedGoogle Scholar
  • 13 Wilson PW. Evidence of systemic inflammation and estimation of coronary artery disease risk: a population perspective. Am J Med 2008; 121 (10) (Suppl. 01) S15-S20
    CrossrefPubMedGoogle Scholar
  • 14 Roifman I, Beck PL, Anderson TJ, Eisenberg MJ, Genest J. Chronic inflammatory diseases and cardiovascular risk: a systematic review. Can J Cardiol 2011; 27 (02) 174-182
    CrossrefPubMedGoogle Scholar
  • 15 Agic A, Xu H, Finas D, Banz C, Diedrich K, Hornung D. Is endometriosis associated with systemic subclinical inflammation?. Gynecol Obstet Invest 2006; 62 (03) 139-147
    CrossrefPubMedGoogle Scholar
  • 16 Nothnick W, Alali Z. Recent advances in the understanding of endometriosis: the role of inflammatory mediators in disease pathogenesis and treatment. F1000 Res 2016; 5: F1000 Faculty Rev-186
    PubMedGoogle Scholar
  • 17 Mu F, Rich-Edwards J, Rimm EB, Spiegelman D, Missmer SA. Endometriosis and risk of coronary heart disease. Circ Cardiovasc Qual Outcomes 2016; 9 (03) 257-264
    CrossrefPubMedGoogle Scholar
  • 18 Dhalla NS, Temsah RM, Netticadan T. Role of oxidative stress in cardiovascular diseases. J Hypertens 2000; 18 (06) 655-673
    CrossrefPubMedGoogle Scholar
  • 19 Gupta S, Agarwal A, Krajcir N, Alvarez JG. Role of oxidative stress in endometriosis. Reprod Biomed Online 2006; 13 (01) 126-134
    CrossrefPubMedGoogle Scholar
  • 20 Van Langendonckt A, Casanas-Roux F, Donnez J. Oxidative stress and peritoneal endometriosis. Fertil Steril 2002; 77 (05) 861-870
    CrossrefPubMedGoogle Scholar
  • 21 Melo AS, Rosa-e-Silva JC, Rosa-e-Silva Ade S, Poli-Neto OB, Ferriani RA, Vieira CS. Unfavorable lipid profile in women with endometriosis. Fertil Steril 2010; 93 (07) 2433-2436
    CrossrefPubMedGoogle Scholar
  • 22 Brinton LA, Gridley G, Persson I, Baron J, Bergqvist A. Cancer risk after a hospital discharge diagnosis of endometriosis. Am J Obstet Gynecol 1997; 176 (03) 572-579
    CrossrefPubMedGoogle Scholar
  • 23 Melin A, Sparén P, Persson I, Bergqvist A. Endometriosis and the risk of cancer with special emphasis on ovarian cancer. Hum Reprod 2006; 21 (05) 1237-1242
    CrossrefPubMedGoogle Scholar
  • 24 Ness RB. Endometriosis and ovarian cancer: thoughts on shared pathophysiology. Am J Obstet Gynecol 2003; 189 (01) 280-294
    CrossrefPubMedGoogle Scholar
  • 25 Munksgaard PS, Blaakaer J. The association between endometriosis and gynecological cancers and breast cancer: a review of epidemiological data. Gynecol Oncol 2011; 123 (01) 157-163
    CrossrefPubMedGoogle Scholar
  • 26 Farland LV, Tamimi RM, Eliassen AH. , et al. Laparoscopically confirmed endometriosis and breast cancer in the Nurses' Health Study II. Obstet Gynecol 2016; 128 (05) 1025-1031
    CrossrefPubMedGoogle Scholar
  • 27 Mogensen JB, Kjær SK, Mellemkjær L, Jensen A. Endometriosis and risks for ovarian, endometrial and breast cancers: a nationwide cohort study. Gynecol Oncol 2016; 143 (01) 87-92
    CrossrefPubMedGoogle Scholar
  • 28 Pontikaki A, Sifakis S, Spandidos DA. Endometriosis and breast cancer: a survey of the epidemiological studies. Oncol Lett 2016; 11 (01) 23-30
    CrossrefPubMedGoogle Scholar
  • 29 Melin A, Sparén P, Bergqvist A. The risk of cancer and the role of parity among women with endometriosis. Hum Reprod 2007; 22 (11) 3021-3026
    CrossrefPubMedGoogle Scholar
  • 30 Borgfeldt C, Andolf E. Cancer risk after hospital discharge diagnosis of benign ovarian cysts and endometriosis. Acta Obstet Gynecol Scand 2004; 83 (04) 395-400
    CrossrefPubMedGoogle Scholar
  • 31 Olson JE, Cerhan JR, Janney CA, Anderson KE, Vachon CM, Sellers TA. Postmenopausal cancer risk after self-reported endometriosis diagnosis in the Iowa Women's Health Study. Cancer 2002; 94 (05) 1612-1618
    CrossrefPubMedGoogle Scholar
  • 32 Kvaskoff M, Mesrine S, Fournier A, Boutron-Ruault MC, Clavel-Chapelon F. Personal history of endometriosis and risk of cutaneous melanoma in a large prospective cohort of French women. Arch Intern Med 2007; 167 (19) 2061-2065
    CrossrefPubMedGoogle Scholar
  • 33 Kvaskoff M, Han J, Qureshi AA, Missmer SA. Pigmentary traits, family history of melanoma and the risk of endometriosis: a cohort study of US women. Int J Epidemiol 2014; 43 (01) 255-263
    CrossrefPubMedGoogle Scholar
  • 34 Sinaii N, Cleary SD, Ballweg ML, Nieman LK, Stratton P. High rates of autoimmune and endocrine disorders, fibromyalgia, chronic fatigue syndrome and atopic diseases among women with endometriosis: a survey analysis. Hum Reprod 2002; 17 (10) 2715-2724
    CrossrefPubMedGoogle Scholar
  • 35 Nielsen NM, Jørgensen KT, Pedersen BV, Rostgaard K, Frisch M. The co-occurrence of endometriosis with multiple sclerosis, systemic lupus erythematosus and Sjogren syndrome. Hum Reprod 2011; 26 (06) 1555-1559
    CrossrefPubMedGoogle Scholar
  • 36 Aguiar FM, Melo SB, Galvão LC, Rosa-e-Silva JC, dos Reis RM, Ferriani RA. Serological testing for celiac disease in women with endometriosis. A pilot study. Clin Exp Obstet Gynecol 2009; 36 (01) 23-25
    PubMedGoogle Scholar
  • 37 Jess T, Frisch M, Jørgensen KT, Pedersen BV, Nielsen NM. Increased risk of inflammatory bowel disease in women with endometriosis: a nationwide Danish cohort study. Gut 2012; 61 (09) 1279-1283
    CrossrefPubMedGoogle Scholar
  • 38 Petta CA, Arruda MS, Zantut-Wittmann DE, Benetti-Pinto CL. Thyroid autoimmunity and thyroid dysfunction in women with endometriosis. Hum Reprod 2007; 22 (10) 2693-2697
    CrossrefPubMedGoogle Scholar
  • 39 Yuk J-S, Ji H-Y, Lee JH, Park WI. Graves' disease is associated with endometriosis: 3-year population-based study. J Minim Invasive Gynecol 2015; 22 (6S): S29
    PubMedGoogle Scholar
  • 40 Matarese G, De Placido G, Nikas Y, Alviggi C. Pathogenesis of endometriosis: natural immunity dysfunction or autoimmune disease?. Trends Mol Med 2003; 9 (05) 223-228
    CrossrefPubMedGoogle Scholar
  • 41 Eisenberg VH, Zolti M, Soriano D. Is there an association between autoimmunity and endometriosis?. Autoimmun Rev 2012; 11 (11) 806-814
    CrossrefPubMedGoogle Scholar
  • 42 Nichols TR, Lamb K, Arkins JA. The association of atopic diseases with endometriosis. Ann Allergy 1987; 59 (05) 360-363
    PubMedGoogle Scholar
  • 43 Matalliotakis I, Cakmak H, Matalliotakis M, Kappou D, Arici A. High rate of allergies among women with endometriosis. J Obstet Gynaecol 2012; 32 (03) 291-293
    CrossrefPubMedGoogle Scholar
  • 44 Bungum HF, Vestergaard C, Knudsen UB. Endometriosis and type 1 allergies/immediate type hypersensitivity: a systematic review. Eur J Obstet Gynecol Reprod Biol 2014; 179: 209-215
    CrossrefPubMedGoogle Scholar
  • 45 Caserta D, Mallozzi M, Pulcinelli FM, Mossa B, Moscarini M. Endometriosis allergic or autoimmune disease: pathogenetic aspects--a case control study. Clin Exp Obstet Gynecol 2016; 43 (03) 354-357
    PubMedGoogle Scholar
  • 46 Chen LC, Hsu JW, Huang KL. , et al. Risk of developing major depression and anxiety disorders among women with endometriosis: a longitudinal follow-up study. J Affect Disord 2016; 190: 282-285
    CrossrefPubMedGoogle Scholar
  • 47 Sepulcri RP, do Amaral VF. Depressive symptoms, anxiety, and quality of life in women with pelvic endometriosis. Eur J Obstet Gynecol Reprod Biol 2009; 142 (01) 53-56
    CrossrefPubMedGoogle Scholar
  • 48 Lorençatto C, Petta CA, Navarro MJ, Bahamondes L, Matos A. Depression in women with endometriosis with and without chronic pelvic pain. Acta Obstet Gynecol Scand 2006; 85 (01) 88-92
    CrossrefPubMedGoogle Scholar
  • 49 Pope CJ, Sharma V, Sharma S, Mazmanian D. A systematic review of the association between psychiatric disturbances and endometriosis. J Obstet Gynaecol Can 2015; 37 (11) 1006-1015
    CrossrefPubMedGoogle Scholar
  • 50 Yi KW, Shin JH, Park MS, Kim T, Kim SH, Hur JY. Association of body mass index with severity of endometriosis in Korean women. Int J Gynaecol Obstet 2009; 105 (01) 39-42
    CrossrefPubMedGoogle Scholar
  • 51 Hediger ML, Hartnett HJ, Louis GM. Association of endometriosis with body size and figure. Fertil Steril 2005; 84 (05) 1366-1374
    CrossrefPubMedGoogle Scholar
  • 52 Ferrero S, Anserini P, Remorgida V, Ragni N. Body mass index in endometriosis. Eur J Obstet Gynecol Reprod Biol 2005; 121 (01) 94-98
    CrossrefPubMedGoogle Scholar
  • 53 Lafay Pillet MC, Schneider A, Borghese B. , et al. Deep infiltrating endometriosis is associated with markedly lower body mass index: a 476 case-control study. Hum Reprod 2012; 27 (01) 265-272
    CrossrefPubMedGoogle Scholar
  • 54 Vitonis AF, Baer HJ, Hankinson SE, Laufer MR, Missmer SA. A prospective study of body size during childhood and early adulthood and the incidence of endometriosis. Hum Reprod 2010; 25 (05) 1325-1334
    CrossrefPubMedGoogle Scholar
  • 55 McCann SE, Freudenheim JL, Darrow SL, Batt RE, Zielezny MA. Endometriosis and body fat distribution. Obstet Gynecol 1993; 82 (4, Pt 1): 545-549
    PubMedGoogle Scholar
  • 56 Shah DK, Correia KF, Vitonis AF, Missmer SA. Body size and endometriosis: results from 20 years of follow-up within the Nurses' Health Study II prospective cohort. Hum Reprod 2013; 28 (07) 1783-1792
    CrossrefPubMedGoogle Scholar
  • 57 Pluchino N, Taylor HS. Endometriosis and stem cell trafficking. Reprod Sci 2016; 23 (12) 1616-1619
    CrossrefPubMedGoogle Scholar
  • 58 Punnonen J, Teisala K, Ranta H, Bennett B, Punnonen R. Increased levels of interleukin-6 and interleukin-10 in the peritoneal fluid of patients with endometriosis. Am J Obstet Gynecol 1996; 174 (05) 1522-1526
    CrossrefPubMedGoogle Scholar
  • 59 Harada T, Yoshioka H, Yoshida S. , et al. Increased interleukin-6 levels in peritoneal fluid of infertile patients with active endometriosis. Am J Obstet Gynecol 1997; 176 (03) 593-597
    CrossrefPubMedGoogle Scholar
  • 60 Sikora J, Mielczarek-Palacz A, Kondera-Anasz Z. Imbalance in cytokines from interleukin-1 family - role in pathogenesis of endometriosis. Am J Reprod Immunol 2012; 68 (02) 138-145
    CrossrefPubMedGoogle Scholar
  • 61 Eisermann J, Gast MJ, Pineda J, Odem RR, Collins JL. Tumor necrosis factor in peritoneal fluid of women undergoing laparoscopic surgery. Fertil Steril 1988; 50 (04) 573-579
    CrossrefPubMedGoogle Scholar
  • 62 Ahn SH, Edwards AK, Singh SS, Young SL, Lessey BA, Tayade C. IL-17A contributes to the pathogenesis of endometriosis by triggering proinflammatory cytokines and angiogenic growth factors. J Immunol 2015; 195 (06) 2591-2600
    CrossrefPubMedGoogle Scholar
  • 63 Kennedy S, Bergqvist A, Chapron C. , et al; ESHRE Special Interest Group for Endometriosis and Endometrium Guideline Development Group. ESHRE guideline for the diagnosis and treatment of endometriosis. Hum Reprod 2005; 20 (10) 2698-2704
    CrossrefPubMedGoogle Scholar
  • 64 Fagervold B, Jenssen M, Hummelshoj L, Moen MH. Life after a diagnosis with endometriosis - a 15 years follow-up study. Acta Obstet Gynecol Scand 2009; 88 (08) 914-919
    CrossrefPubMedGoogle Scholar
  • 65 Fourquet J, Gao X, Zavala D. , et al. Patients' report on how endometriosis affects health, work, and daily life. Fertil Steril 2010; 93 (07) 2424-2428
    CrossrefPubMedGoogle Scholar
  • 66 Bruner-Tran KL, Herington JL, Duleba AJ, Taylor HS, Osteen KG. Medical management of endometriosis: emerging evidence linking inflammation to disease pathophysiology. Minerva Ginecol 2013; 65 (02) 199-213
    PubMedGoogle Scholar
  • 67 Vercellini P, Viganò P, Somigliana E, Fedele L. Endometriosis: pathogenesis and treatment. Nat Rev Endocrinol 2014; 10 (05) 261-275
    CrossrefPubMedGoogle Scholar
  • 68 Barcena de Arellano ML, Arnold J, Vercellino F, Chiantera V, Schneider A, Mechsner S. Overexpression of nerve growth factor in peritoneal fluid from women with endometriosis may promote neurite outgrowth in endometriotic lesions. Fertil Steril 2011; 95 (03) 1123-1126
    CrossrefPubMedGoogle Scholar
  • 69 McKinnon BD, Bertschi D, Bersinger NA, Mueller MD. Inflammation and nerve fiber interaction in endometriotic pain. Trends Endocrinol Metab 2015; 26 (01) 1-10
    CrossrefPubMedGoogle Scholar
  • 70 Barcena de Arellano ML, Arnold J, Lang H. , et al. Evidence of neurotrophic events due to peritoneal endometriotic lesions. Cytokine 2013; 62 (02) 253-261
    CrossrefPubMedGoogle Scholar
  • 71 Quiñones M, Urrutia R, Torres-Reverón A, Vincent K, Flores I. Anxiety, coping skills and hypothalamus-pituitary-adrenal (HPA) axis in patients with endometriosis. J Reprod Biol Health 2015; 3 (01) 2
    CrossrefPubMedGoogle Scholar
  • 72 Petrelluzzi KF, Garcia MC, Petta CA, Grassi-Kassisse DM, Spadari-Bratfisch RC. Salivary cortisol concentrations, stress and quality of life in women with endometriosis and chronic pelvic pain. Stress 2008; 11 (05) 390-397
    CrossrefPubMedGoogle Scholar
  • 73 Brawn J, Morotti M, Zondervan KT, Becker CM, Vincent K. Central changes associated with chronic pelvic pain and endometriosis. Hum Reprod Update 2014; 20 (05) 737-747
    CrossrefPubMedGoogle Scholar
  • 74 Winter J, Jung S, Keller S, Gregory RI, Diederichs S. Many roads to maturity: microRNA biogenesis pathways and their regulation. Nat Cell Biol 2009; 11 (03) 228-234
    CrossrefPubMedGoogle Scholar
  • 75 Bartel DP. MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 2004; 116 (02) 281-297
    CrossrefPubMedGoogle Scholar
  • 76 Ohlsson Teague EM, Van der Hoek KH, Van der Hoek MB. , et al. MicroRNA-regulated pathways associated with endometriosis. Mol Endocrinol 2009; 23 (02) 265-275
    CrossrefPubMedGoogle Scholar
  • 77 Cho S, Mutlu L, Grechukhina O, Taylor HS. Circulating microRNAs as potential biomarkers for endometriosis. Fertil Steril 2015; 103 (05) 1252-60.e1
    CrossrefPubMedGoogle Scholar
  • 78 Seifer BJ, Su D, Taylor HS. Circulating miRNAs in murine experimental endometriosis. Reprod Sci 2017; 24 (03) 376-381
    PubMedGoogle Scholar
  • 79 Teague EM, Print CG, Hull ML. The role of microRNAs in endometriosis and associated reproductive conditions. Hum Reprod Update 2010; 16 (02) 142-165
    CrossrefPubMedGoogle Scholar
  • 80 Ramón LA, Braza-Boïls A, Gilabert-Estellés J. , et al. microRNAs expression in endometriosis and their relation to angiogenic factors. Hum Reprod 2011; 26 (05) 1082-1090
    CrossrefPubMedGoogle Scholar
  • 81 Braza-Boïls A, Salloum-Asfar S, Marí-Alexandre J. , et al. Peritoneal fluid modifies the microRNA expression profile in endometrial and endometriotic cells from women with endometriosis. Hum Reprod 2015; 30 (10) 2292-2302
    CrossrefPubMedGoogle Scholar
  • 82 Braza-Boïls A, Marí-Alexandre J, Gilabert J. , et al. MicroRNA expression profile in endometriosis: its relation to angiogenesis and fibrinolytic factors. Hum Reprod 2014; 29 (05) 978-988
    CrossrefPubMedGoogle Scholar
  • 83 Braza-Boïls A, Gilabert-Estellés J, Ramón LA. , et al. Peritoneal fluid reduces angiogenesis-related microRNA expression in cell cultures of endometrial and endometriotic tissues from women with endometriosis. PLoS One 2013; 8 (04) e62370
    CrossrefPubMedGoogle Scholar
  • 84 Hawkins SM, Creighton CJ, Han DY. , et al. Functional microRNA involved in endometriosis. Mol Endocrinol 2011; 25 (05) 821-832
    CrossrefPubMedGoogle Scholar
  • 85 Burney RO, Hamilton AE, Aghajanova L. , et al. MicroRNA expression profiling of eutopic secretory endometrium in women with versus without endometriosis. Mol Hum Reprod 2009; 15 (10) 625-631
    CrossrefPubMedGoogle Scholar
  • 86 Chen S, Yang L, Jie Q. , et al. MicroRNA‑125b suppresses the proliferation and osteogenic differentiation of human bone marrow‑derived mesenchymal stem cells. Mol Med Rep 2014; 9 (05) 1820-1826
    CrossrefPubMedGoogle Scholar
  • 87 Wang H, Tan G, Dong L. , et al. Circulating MiR-125b as a marker predicting chemoresistance in breast cancer. PLoS One 2012; 7 (04) e34210
    CrossrefPubMedGoogle Scholar
  • 88 Sasson IE, Taylor HS. Stem cells and the pathogenesis of endometriosis. Ann N Y Acad Sci 2008; 1127 (01) 106-115
    CrossrefPubMedGoogle Scholar
  • 89 Cassina PC, Hauser M, Kacl G, Imthurn B, Schröder S, Weder W. Catamenial hemoptysis. Diagnosis with MRI. Chest 1997; 111 (05) 1447-1450
    CrossrefPubMedGoogle Scholar
  • 90 Van Schil PE, Vercauteren SR, Vermeire PA, Nackaerts YH, Van Marck EA. Catamenial pneumothorax caused by thoracic endometriosis. Ann Thorac Surg 1996; 62 (02) 585-586
    CrossrefPubMedGoogle Scholar
  • 91 Gruenwald P. Origin of endometriosis from the mesenchyme of the celomic walls. Am J Obstet Gynecol 1942; 44 (03) 470-474
    CrossrefPubMedGoogle Scholar
  • 92 Du H, Taylor HS. Contribution of bone marrow-derived stem cells to endometrium and endometriosis. Stem Cells 2007; 25 (08) 2082-2086
    CrossrefPubMedGoogle Scholar
  • 93 Figueira PG, Abrão MS, Krikun G, Taylor HS. Stem cells in endometrium and their role in the pathogenesis of endometriosis. Ann N Y Acad Sci 2011; 1221 (01) 10-17
    CrossrefPubMedGoogle Scholar
  • 94 Wang X, Mamillapalli R, Mutlu L, Du H, Taylor HS. Chemoattraction of bone marrow-derived stem cells towards human endometrial stromal cells is mediated by estradiol regulated CXCL12 and CXCR4 expression. Stem Cell Res (Amst) 2015; 15 (01) 14-22
    CrossrefPubMedGoogle Scholar
  • 95 Taylor HS. Endometrial cells derived from donor stem cells in bone marrow transplant recipients. JAMA 2004; 292 (01) 81-85
    CrossrefPubMedGoogle Scholar
  • 96 Moridi I, Mamillapalli R, Cosar E, Ersoy GS, Taylor HS. Bone marrow stem cell chemotactic activity is induced by elevated CXCl12 in endometriosis. Reprod Sci 2017; 24 (04) 526-533
    CrossrefPubMedGoogle Scholar
  • 97 Liu Y, Gao S, Wang Z, Yang Y, Huo H, Tian X. Effect of stromal cell-derived factor-1 on myocardial apoptosis and cardiac function recovery in rats with acute myocardial infarction. Exp Ther Med 2016; 12 (05) 3282-3286
    CrossrefPubMedGoogle Scholar
  • 98 Kao A-P, Wang K-H, Chang C-C. , et al. Comparative study of human eutopic and ectopic endometrial mesenchymal stem cells and the development of an in vivo endometriotic invasion model. Fertil Steril 2011; 95 (04) 1308-15.e1
    CrossrefPubMedGoogle Scholar
  • 99 Kidd LJ, Stephens AS, Kuliwaba JS, Fazzalari NL, Wu AC, Forwood MR. Temporal pattern of gene expression and histology of stress fracture healing. Bone 2010; 46 (02) 369-378
    CrossrefPubMedGoogle Scholar
  • 100 Toksoy A, Müller V, Gillitzer R, Goebeler M. Biphasic expression of stromal cell-derived factor-1 during human wound healing. Br J Dermatol 2007; 157 (06) 1148-1154
    CrossrefPubMedGoogle Scholar
  • 101 Tögel F, Isaac J, Hu Z, Weiss K, Westenfelder C. Renal SDF-1 signals mobilization and homing of CXCR4-positive cells to the kidney after ischemic injury. Kidney Int 2005; 67 (05) 1772-1784
    CrossrefPubMedGoogle Scholar
  • 102 Wang Y, Deng Y, Zhou G-Q. SDF-1α/CXCR4-mediated migration of systemically transplanted bone marrow stromal cells towards ischemic brain lesion in a rat model. Brain Res 2008; 1195: 104-112
    CrossrefPubMedGoogle Scholar
  • 103 Imitola J, Raddassi K, Park KI. , et al. Directed migration of neural stem cells to sites of CNS injury by the stromal cell-derived factor 1alpha/CXC chemokine receptor 4 pathway. Proc Natl Acad Sci U S A 2004; 101 (52) 18117-18122
    CrossrefPubMedGoogle Scholar
  • 104 Santamaria X, Massasa EE, Taylor HS. Migration of cells from experimental endometriosis to the uterine endometrium. Endocrinology 2012; 153 (11) 5566-5574
    CrossrefPubMedGoogle Scholar