[en] Background/Aims: The aim of this study was to induce endometriosis in female rhesus macaques (Macaca mulatta) for research purposes. Methods: Three female monkeys from 4 to 4.5 years of age underwent three consecutive attempts at endometriosis induction over an 8-month period: (i) the first attempt involved intravaginal sampling of endometrial tissue and transplantation into the intrapelvic cavity; (ii) the second entailed surgical removal of endometrium after hysterotomy and intra-abdominal placement, and (iii) the third used endometrial mucosa obtained by scraping the uterus after hysterectomy, placed in a surgical pouch created in the retrovesical space (Retzius). In each case, the pelvic cavity was closely inspected after 7, 9, and 6 weeks respectively for the presence of endometriotic lesions, and peritoneal biopsies were performed. Results: Neither macroscopic observation nor histological analysis revealed any endometriotic lesions. Conclusion: This failure to induce endometriosis in female rhesus macaques suggests that this species is not the most efficient experimental model among primates to investigate endometriosis development or treatment.
Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique - Labo de biologie des tumeurs et du développement
Jérôme, Christine ; Université de Liège - ULiège > Département de chimie (sciences) > Centre d'études et de rech. sur les macromolécules (CERM) - Chimie des macromolécules et des matériaux organiques
Delattre, Luc ; Université de Liège - ULiège > Département de pharmacie > Département de pharmacie
Donnez, J.
Dehoux, J. P.
Language :
English
Title :
Unsuccessful Induction of Endometriosis in Female Rhesus Macaques (Macaca mulatta).
Giudice LC, Kao LC: Endometriosis. Lancet 2004;364:1789-1799.
Story L, Kennedy S: Animal studies in endometriosis: a review. ILAR J 2004;45:132-138.
Eskenazi B, Warner ML: Epidemiology of endometriosis. Obstet Gynecol Clin North Am 1997;24:235-258.
Zondervan KT, Cardon LR, Kennedy SH: The genetic basis of endometriosis. Curr Opin Obstet Gynecol 2001;13:309-314.
Sampson JA: Peritoneal endometriosis due to menstrual dissemination of endometrial tissue into the peritoneal cavity. Am J Obstet Gynecol 1927;14:422-469.
D'Hooghe TM, Debrock S: Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons. Hum Reprod Update 2002;8:84-88.
Eisenfeld AJ, Gardner WU, Van Wagenen G: Radioactive estradiol accumulation in endometriosis of the rhesus monkey. Am J Obstet Gynecol 1971;109:124-130.
DiGiacomo RF: Gynecologic pathology in the rhesus monkey (Macaca mulatta). II. Findings in laboratory and free-ranging monkeys. Vet Pathol 1977;14:539-546.
Binhazim AA, Tarara RP, Suleman MA: Spontaneous external endometriosis in a De Brazza's monkey. J Comp Pathol 1989;101:471-474.
D'Hooghe TM: Clinical relevance of the baboon as a model for the study of endometriosis. Fertil Steril 1997;68:613-625.
Donnez J, Wayembergh M, Casanas-Roux F, Karaman Y, Willems T, Ferin J: Effect on ovulation of surgically induced endometriosis in rabbits. Gynecol Obstet Invest 1987;24:131-137.
Vernon MW, Wilson EA: Studies on the surgical induction of endometriosis in the rat. Fertil Steril 1985;44:684-694.
Sharpe-Timms KL: Using rats as a research model for the study of endometriosis. Proc Natl Acad Sci USA 2002;955:318-327.
Cummings AM, Metcalf JL: Induction of endometriosis in mice: a new model sensitive to estrogen. Reprod Toxicol 1995;9:233-238.
Fang Z, Yang S, Lydon JP, DeMayo F, Tamura M, Gurates B, Bulun SE: Intact progesterone receptors are essential to counteract the proliferative effect of estradiol in a genetically engineered mouse model of endometriosis. Fertil Steril 2004;82:673-678.
Efstathiou JA, Sampson DA, Levine Z, Rohan RM, Zurakowski D, Folkman J, D'Amao RJ, Rupnick MA: Nonsteroidal anti-inflammatory drugs differentially suppress endometriosis in a murine model. Fertil Steril 2005;83:171-181.
Awwad JT, Sayegh RA, Tao XJ, Hassan T, Awwad ST, Isaacson K: The SCID mouse: an experimental model for endometriosis. Hum Reprod 1999;14:3107-3111.
Zaino RJ, Satyaswaroop PG, Mortel R: Histologic response of normal human endometrium to steroid hormones in athymic mice. Hum Pathol 1985;16:867-872.
Aoki D, Katsuki Y, Shimizu A, Kakinuma C, Nozawa S: Successful heterotransplantation of human endometrium in SCID mice. Obstet Gynecol 1994;83:220-228.
Grümmer R, Schwarzer F, Bainczyk K, Hess-Stump H, Regidor P-A, Schindler AE, Winterhager: Peritoneal endometriosis: validation of an in vivo model. Hum Reprod 2001;16:1736-1743.
Zamah NM, Dodson MG, Stephens LC, Buttram VC, Besch PK, Kaufman RH: Transplantation of normal and ectopic human endometrial tissue into athymic nude mice. Am J Obstet Gynecol 1984;149:591-597.
Bruner KL, Matrisian LM, Hrodgers WH, Gorstein F, Osteen KG: Suppression of matrix metalloproteinases inhibits establishment of ectopic lesions by human endometrium in nude mice. J Clin Invest 1997;9912:2851-2857.
Defrère S, Van Langendonckt A, González Ramos R, Jouret M, Mettlen M, Donnez J: Quantification of endometriotic lesions in a murine model by fluorimetric and morphometric analyses. Hum Reprod 2006;21:810-817.
Greenberg LH, Slayden OD: Human endometriotic xenografts in immunodeficient RAG-2/γ(c)KO mice. Am J Obstet Gynecol 2004;190:1788-1795.
Hadfield RM, Yudkin PL, Coe CL, Scheffler J, Uno H, Barlow DH, Kemnitz JW, Kennedy SH: Risk factors for endometriosis in the rhesus monkey (Macaca mulatta): a case-control study. Hum Reprod Update 1997;3:109-115.
MacKenzie WF, Casey HW: Animal model of human disease. Endometriosis. Animal model: Endometriosis in rhesus monkeys. Am J Pathol 1975;80:341-344.
Zondervan KT, Weeks DE, Colman R, Cardon LR, Hadfield R, Schleffler J, Trainor AG, Coe CL, Kemnitz JW, Kennedy SH: Familial aggregation of endometriosis in a large pedigree of rhesus macaques. Hum Reprod 2004;19:448-455.
Colman R, Kemnitz J: Aging experiments using nonhuman primates; in Yu BP (ed): Methods in Ageing Research. Boca Raton, CRC Press, 1998, pp 249-267.
Fanton JW, Golden JG: Radiation-induced endometriosis in Macaca mulatta. Radiat Res 1991;126:141-146.
Rier SE, Martin DC, Bowman RE, Dmowski WP, Becker JL: Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam Appl Toxicol 1993;21:433-441.
Arnold DL, Nera EA, Stapley R, Tolnai G, Claman P, Hayward S, Tryphonas H, Bryce F: Prevalence of endometriosis in rhesus (Macaca mulatta) monkeys ingesting PCB (Aroclor 1254): review and evaluation. Fundam Appl Toxicol 1996;31:42-55.
Krugner-Higby L, Rosenstein A, Handschke L, Luck M, Laughlin NK, Mahvi D, Gendron A: Inguinal hernias, endometriosis, and other adverse outcomes in rhesus monkeys following lead exposure. Neurotoxicol Teratol 2003;25:561-570.
Te Linde RW, Scott RB: Experimental endometriosis. Am J Obstet Gynecol 1950;60:1147-1173.
Scott RB, Wharton LR Jr: The effect of estrone and progesterone on the growth of experimental endometriosis in rhesus monkeys. Am J Obstet Gynecol 1957;74:852-863.
Scott RB, Wharton LR Jr: The effect of testosterone on experimental endometriosis in rhesus monkeys. Am J Obstet Gynecol 1959;78:1020-1027.
Mann DR, Collins DC, Smith MM, Kessler MJ, Gould K: Treatment of endometriosis in monkeys: effectiveness of continuous infusion of a gonadotropin-releasing hormone agonist compared to treatment with a progestational steroid. J Clin Endocrinol Metab 1986;63:1277-1283.
Schleicher RL, Mann DR, Gould KG, Collins DC: Serum levels of cholesterol and lipoproteins in rhesus monkeys: comparison of the effect of gonadotropin-releasing hormone agonist and the progestin, levonorgestrel. Fertil Steril 1987;47:710-713.
Zong LL, Li YL, Wang LX, Zou J, Li J, Li T: Establishment of animal models of endometriosis in rhesus monkeys. Di Yi Jun Yi Da Xue Xue Bao 2003;23:1006-1009.
Noyes RW, Hertig AT, Rock J: Dating the endometrial biopsy. Fertil Steril 1950;1:3-25.
Paris JM, Williams KJ, Hermsmeyer KR, Delansorne R: Nomegestrol acetate and vascular reactivity: nonhuman primate experiments. Steroids 2000;65:621-627.
Pecins-Thompson M, Bethea CL: Ovarian steroid regulation of serotonin-1A autoreceptor messenger RNA expression in the dorsal raphe of rhesus macaques. Neuroscience 1999;89:267-277.
Baskin GB, Smith SM, Marx PA: Endometrial hyperplasia, polyps, and adenomyosis associated with unopposed estrogen in rhesus monkeys (Macaca mulatta). Vet Pathol 2002;39:572-575.
Resko JA, Goy RW, Robinson JA, Norman RL: The pubescent rhesus monkey: some characteristics of the menstrual cycle. Biol Reprod 1982;27:354-361.
Downs JL, Urbanski HF: Neuroendocrine changes in the aging reproductive axis of female rhesus macaques (Macaca mulatta). Biol Reprod 2006;75:539-546.
Pittaway DE, Klimek M, Koritnik DR: CA-125 antigen in rhesus monkeys with spontaneous endometriosis. Fertil Steril 1986;46:967-969.
Sternfeld MD, West NB, Brenner RM: Immunocytochemistry of the estrogen receptor in spontaneous endometriosis in rhesus macaques. Fertil Steril 1988;49:342-348.
D'Hooghe TM, Bambra CS, Suleman MA, Dunselman GA, Evers HL, Koninckx PR: Development of a model of retrograde menstruation in baboons (Papio anubis). Fertil Steril 1994;62:635-638.
D'Hooghe TM, Bambra CS, Raeymaekers BM, De Jonge I, Lauweryns JM, Koninckx PR: Intrapelvic injection of menstrual endometrium causes endometriosis in baboons (Papio cynocephalus and Papio anubis). Am J Obstet Gynecol 1995;173:125-134.
Lebovic DI, Mwenda JM, Chai DC, Mueller MD, Santi A, Fisseha S, D'Hooghe T: PPAR-γ receptor ligand induces regression of endometrial explants in baboons: a prospective, randomized, placebo- and drug-controlled study. Fertil Steril 2007;88:1108-1119.
Falconer H, Mwenda JM, Chai DC, Wagner C, Song XY, Mihalyi A, Simsa P, Kyama C, Cornillie FJ, Bergqvist A, Fried G, D'Hooghe TM: Treatment with anti-TNF monoclonal antibody (c5N) reduces the extent of induced endometriosis in the baboon. Hum Reprod 2006;21:1856-1862.
D'Hooghe TM, Nugent NP, Cuneo S, Chai DC, Deer F, Debrock S, Kyama CM, Mihalyi A, Mwenda JM: Recombinant human TNFRSF1A (r-hTBP1) inhibits the development of endometriosis in baboons: a prospective, randomized, placebo- and drug-controlled study. Biol Reprod 2006;74:131-136.
Schenken RS, Asch RH, Williams RF, Hodgen GD: Etiology of infertility in monkeys with endometriosis: luteinized unruptured follicles, luteal phase defects, pelvic adhesions, and spontaneous abortions. Fertil Steril 1984;41:122-130.
Schenken RS, Williams RF, Hodgen GD: Effect of pregnancy on surgically induced endometriosis in cynomolgus monkeys. Am J Obstet Gynecol 1987;157:1392-1396.
Sillem M, Hahn U, Coddington CC 3rd, Gordon K, Runnebaum B, Hodgen GD: Ectopic growth of endometrium depends on its structural integrity and proteolytic activity in the cynomolgus monkey (Macaca fascicularis) model of endometriosis. Fertil Steril 1996;66:468-473.
Einspanier A, Lieder K, Brüns A, Husen B, Thole H, Simon C: Induction of endometriosis in the marmoset monkey (Callithrix jacchus). Mol Hum Reprod 2006;12:291-299.