Risk factors for endometriosis in the rhesus monkey (Macaca mulatta): a case-control study
Abstract
The autopsy records between 1980 and 1995 of 399 female rhesus monkeys (Macaca mulatta) at the Wisconsin Regional Primate Research Center were examined. Spontaneous endometriosis was found in 81 (20%) of the animals. The mean (+/- SD) ages at death for animals with and without endometriosis were 20.7 +/- 5.5 (range 10-35) and 13.4 +/- 7.7 (range 4-37) years respectively. Many of the animals had been exposed to experimental procedures, including laparoscopies, hysterotomies and oestradiol implants, and these were examined as possible risk factors for endometriosis. Of the 81 affected animals, 62 were matched to unaffected controls for age at death (to within 1 year) and year of death (to within 2 years) and the effect of various factors on the development of endometriosis was determined using conditional logistic regression. Exposure to three or more oestradiol implants or one or more hysterotomies were both significant risk factors, with estimated relative risks of 9.7 (95% confidence interval 2.5-37.2) and 5.8 (95% confidence interval 1.6-20.2) respectively. Animals that had been exposed to one or more laparoscopies showed no increased risk for developing endometriosis. These findings provide insight into the aetiology of the disease in women. ?2P51 4RR00167
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Only a history of application of estrogen patches (in addition to a history of trauma by hysterotomy) showed a significant association with endometriosis.
“Only a history of application of estrogen patches (in addition to a history of trauma by hysterotomy) showed a significant association with endometriosis [67].”
From The pathophysiology of endometriosis and adenomyosis, tissue injury and repair (2009) · cites this paper as [67]
A history of hysterotomy in colonized rhesus monkeys showed a significant association with the later development of endometriosis in these animals.
“A history of hysterotomy in colonized rhesus monkeys showed a significant association with the later development of endometriosis in these animals [67].”
From The pathophysiology of endometriosis and adenomyosis, tissue injury and repair (2009) · cites this paper as [67]
Familial clustering of endometriosis is well established in humans and primates.
“Well established are familial clustering in humans (156) and primates (157).”
From Pathogenesis of deep endometriosis (2017) · cites this paper as [157]
Cites
Revised American Fertility Society Classification of Endometriosis: 1985
(1985) · Fertility and Sterility · doi:10.1016/s0015-0282(16)48430-x · Cited by 1,803 · see citing works
Rier, S. (1993) · Fundamental and Applied Toxicology · doi:10.1006/faat.1993.1119 · Cited by 502 · see citing works
Heritable aspects of endometriosis
Simpson, J. L., Elias, S., Malinak, L. R., & Buttram, V. C. (1980) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(80)90917-5 · Cited by 468 · see citing works
Endometriosis: Role of Ovarian Steroids in Initiation, Maintenance, and Suppression
diZerega, G. S., Barber, D. L., & Hodgen, G. D. (1980) · Fertility and Sterility · doi:10.1016/s0015-0282(16)44780-1 · Cited by 290 · see citing works
The familial risk of endometriosis
Moen, M. H., & Magnus, P. (1993) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016349309058164 · Cited by 248 · see citing works
(1980) · PubMed · Cited by 160 · see citing works
D’Hooghe, T. M., Bambra, C. S., Cornillie, F. J., ISAHAKIA, M. A., & Koninckx, P. R. (1991) · Biology of Reproduction · doi:10.1095/biolreprod45.3.411 · Cited by 100 · see citing works
Radiation-induced endometriosis in Macaca mulatta
Fanton, J. W., & Golden, J. G. (1991) · Radiation Research · doi:10.2307/3577812 · Cited by 84 · see citing works
Age of onset of pain symptoms in non-twin sisters concordant for endometriosis
Kennedy, S., Hadfield, R., Mardon, H., & Barlow, D. (1996) · Human Reproduction · doi:10.1093/humrep/11.2.403 · Cited by 63 · see citing works
Self-citationProton irradiation and endometriosis.
Wood, D. H., Yochmowitz, M. G., Salmon, Y. L., Eason, R. L., & Boster, R. A. (1983) · PubMed · Cited by 61 · see citing works
Endometriosis in rhesus monkeys
McCann, T. O., & Myers, R. E. (1970) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(70)90034-7 · Cited by 57 · see citing works
D’Hooghe, T. M., Bambra, C. S., Jonge, I. D., et al. (1996) · Acta Obstetricia Et Gynecologica Scandinavica · doi:10.3109/00016349609033298 · Cited by 56 · see citing works
Dierschke, D. J., Hutz, R. J., & Wolf, R. C. (1985) · Endocrinology · doi:10.1210/endo-117-4-1397 · Cited by 56 · see citing works
D’Hooghe, T. M., Bambra, C. S., ISAHAKIA, M. A., & Koninckx, P. R. (1992) · Fertility and Sterility · doi:10.1016/s0015-0282(16)55190-5 · Cited by 52 · see citing works
Gynecologic Pathology in the Rhesus Monkey ( Macaca mulatta )
DiGiacomo, R. F. (1977) · Veterinary Pathology · doi:10.1177/030098587701400601 · Cited by 48 · see citing works
Seasonal Effects on Ovarian Folliculogenesis in Rhesus Monkeys1
Hutz, R. J., Dierschke, D. J., & Wolf, R. C. (1985) · Biology of Reproduction · doi:10.1095/biolreprod33.3.653 · Cited by 41 · see citing works
Endometriosis in Cynomolgus Monkeys Retired from Breeding.
Ami, Y., Suzaki, Y., & Naoaki, G. O. T. O. (1993) · Journal of Veterinary Medical Science · doi:10.1292/jvms.55.7 · Cited by 37 · see citing works
Effect of pregnancy on surgically induced endometriosis in cynomolgus monkeys
Schenken, R. S., Williams, R. F., & Hodgen, G. D. (1987) · American Journal of Obstetrics and Gynecology · doi:10.1016/s0002-9378(87)80230-2 · Cited by 35 · see citing works
Laparoscopy in Macaca mulatta: Specialized Equipment Employed and Initial Observations
Dierschke, D. J., & Clark, J. R. (1976) · Journal of Medical Primatology · doi:10.1159/000459923 · Cited by 32 · see citing works
Provinciali, M., Stefano, G. D., Muzzioli, M., Garzetti, G. G., Ciavattini, A., & Fabris, Ν. (1995) · Journal of Endocrinological Investigation · doi:10.1007/bf03349783 · Cited by 31 · see citing works
Endometriosis in a baboon (Papio doguera).
Folse, D. S., & Stout, L. C. (1978) · PubMed · Cited by 29 · see citing works
Cornillie, F. J., ́Hooghe, T. D., Bambra, C. S., Lauweryns, J. M., ISAHAKIA, M. A., & Koninckx, P. R. (2010) · Gynecologic and Obstetric Investigation · doi:10.1159/000292766 · Cited by 28 · see citing works
Spontaneous endometriosis in a cynomolgus monkey (Macaca fascicularis).
Fanton, J. W., & Hubbard, G. B. (1983) · PubMed · Cited by 26 · see citing works
Markers of Atresia in Ovarian Follicular Components from Rhesus Monkeys Treated with Estradiol-17β1
Hutz, R. J., Dierschke, D. J., & Wolf, R. C. (1986) · Biology of Reproduction · doi:10.1095/biolreprod34.1.65 · Cited by 24 · see citing works
The relationship between endometriotic lesions and the disease endometriosis
Bergqvist, A. (1995) · Human Reproduction · doi:10.1093/humrep/10.1.11 · Cited by 22 · see citing works
Fetal Lung Development in Male and Female Nonhuman Primates
PERELMAN, R. H., Engle, M. J., Palta, M., et al. (1986) · Pediatric Research · doi:10.1203/00006450-198610000-00019 · Cited by 20 · see citing works
Endometriosis in rhesus monkeys
Bertens, A. P. M. G., Helmond, F. A., & Hein, P. R. (1982) · Laboratory Animals · doi:10.1258/002367782780891660 · Cited by 20 · see citing works
Radioactive estradiol accumulation in endometriosis of the rhesus monkey
Eisenfeld, A. J., GARDNER, W. U., & WAGENEN, G. V. (1971) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(71)90846-5 · Cited by 19 · see citing works
Endometrioma in a cesarean scar: Case report and review of the literature
Kale, S., Shuster, M., & Shangold, J. (1971) · American Journal of Obstetrics and Gynecology · doi:10.1016/0002-9378(71)90479-0 · Cited by 19 · see citing works
Is mild endometriosis a disease?: Why do women develop endometriosis and why is it diagnosed?
Moen, M. H. (1995) · Human Reproduction · doi:10.1093/humrep/10.1.8 · Cited by 19 · see citing works
Spontaneous External Endometriosis in a Gorilla (Gorilla gorilla).
Doré, M., & Lagacé, A. (1985) · PubMed · Cited by 16 · see citing works
Ectopic Endometrium in a Macacus Rhesus.
Fraser, A. D. (1929) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1929.tb06706.x · Cited by 16 · see citing works
Pre‐operative treatment of an abdominal wall endometrioma with nafarelin acetate. Case report
Kennedy, S., Brodribb, J., Barlow, D. H., et al. (1988) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/j.1471-0528.1988.tb12810.x · Cited by 12 · see citing works
Pomerantz, S. M., Roy, M. M., & Goy, R. W. (1988) · Hormones and Behavior · doi:10.1016/0018-506x(88)90068-2 · Cited by 9 · see citing works
An experimental model for studies of fetal maldevelopment in the diabetic pregnancy.
Kemnitz, J. W., PERELMAN, R. H., Engle, M. J., et al. (1986) · PubMed · Cited by 8 · see citing works
Endometriosis and stromal tumor in a baboon (Papio hamadryas).
Shalev, M., Ciurea, D. V., & Deligdisch, L. (1992) · PubMed · Cited by 8 · see citing works
Use of leuprolide to treat endometriosis in a rhesus macaque.
Kd, M., Dh, P., Ma, P., et al. (1991) · PubMed · Cited by 7 · see citing works
Endometriosis in a Gray-Cheeked Mangaby [Cercocebus albigena]
Schmidt, R. E., & Hartfiel, D. A. (1978) · The Journal of Zoo Animal Medicine · doi:10.2307/20460204 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Caloric restriction improves health and survival of rhesus monkeys
Mattison, J. A., Colman, R. J., Beasley, T. M., Allison, D. B., Kemnitz, J. W., Roth, G. S., Ingram, D. K., Weindruch, R., de Cabo, R., & Anderson, R. M. (2017) · Nature Communications · doi:10.1038/ncomms14063 · Cited by 838 · see citing works
Macer, M. L., & Taylor, H. S. (2012) · Obstetrics and Gynecology Clinics of North America · doi:10.1016/j.ogc.2012.10.002 · Cited by 681 · see citing works
Pathogenesis of endometriosis: The genetic/epigenetic theory
Koninckx, P. R., Ussia, A., Adamyan, L., Wattiez, A., Gomel, V., & Martin, D. C. (2019) · Fertility and Sterility · doi:10.1016/j.fertnstert.2018.10.013 · Cited by 427 · see citing works
The pathophysiology of endometriosis and adenomyosis, tissue injury and repair
Leyendecker, G., Wildt, L., & Mall, G. (2009) · Archives of Gynecology and Obstetrics · doi:10.1007/s00404-009-1191-0 · Cited by 418 · see citing works
Genetic influences on endometriosis in an Australian twin sample
Treloar, S. A., O’Connor, D. T., O’Connor, V. M., & Martin, N. G. (1999) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00540-8 · Cited by 353 · see citing works
Endometriotic disease: the role of peritoneal fluid
Koninckx, P. (1998) · Human Reproduction Update · doi:10.1093/humupd/4.5.741 · Cited by 252 · see citing works
Pathogenesis of deep endometriosis
Gordts, S., Koninckx, P., & Brosens, I. (2017) · Fertility and Sterility · doi:10.1016/j.fertnstert.2017.08.036 · Cited by 241 · see citing works
Endometriosis, retrograde menstruation and peritoneal inflammation in women and in baboons
D'Hooghe, T. M. (2002) · Human Reproduction Update · doi:10.1093/humupd/8.1.84 · Cited by 231 · see citing works
Genetic factors contribute to the risk of developing endometriosis
Stefansson, H., Geirsson, R. T., Steinthorsdottir, V., Jonsson, H., Manolescu, A., Kong, A., Ingadottir, G., Gulcher, J., & Stefansson, K. (2002) · Human Reproduction · doi:10.1093/humrep/17.3.555 · Cited by 228 · see citing works
Update on biomarkers for the detection of endometriosis
Fassbender, A., Burney, R. O., F. O, D., D’Hooghe, T., & Giudice, L. (2015) · BioMed Research International · doi:10.1155/2015/130854 · Cited by 195 · see citing works
Uterine peristaltic activity and the development of endometriosis
LEYENDECKER, G., KUNZ, G., HERBERTZ, M., BEIL, D., HUPPERT, P., MALL, G., KISSLER, S., NOE, M., & WILDT, L. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1335.036 · Cited by 162 · see citing works
A new concept of endometriosis and adenomyosis, tissue injury and repair (TIAR)
Leyendecker, G., & Wildt, L. (2011) · hmbci · doi:10.1515/hmbci.2011.002 · Cited by 147 · see citing works
Familial aggregation of endometriosis in a large pedigree of rhesus macaques
Zondervan, K. T. (2004) · Human Reproduction · doi:10.1093/humrep/deh052 · Cited by 99 · see citing works
Leyendecker, G., Kunz, G., Kissler, S., & Wildt, L. (2006) · Best Practice & Research Clinical Obstetrics & Gynaecology · doi:10.1016/j.bpobgyn.2006.01.008 · Cited by 94 · see citing works
- Authors
- Hadfield, R.
- Affiliations
- John Radcliffe Hospital (GB)
- Corresponding author
- Hadfield, R.
- ORCID
- Hadfield, R.
- Venue
- Human Reproduction Update
- Publisher
- Oxford University Press (OUP)
- Published
- 1997-03-01
- Volume
- 3
- Issue
- 2
- Pages
- 109-115
- ISSN
- 1355-4786 (ISSN-L)
- 1460-2369
- OpenAlex
- W2125954943
- Cited by
- 86
- References
- 38
- Citations by year
- 2025: 1 · 2023: 1 · 2022: 1 · 2021: 2 · 2020: 2 · 2019: 4 · 2018: 3 · 2017: 5 · 2016: 1 · 2015: 5 · 2014: 1 · 2013: 1 · 2012: 6
- FWCI
- 3.03
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Human Reproduction Update (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- Medical Research Council
- Topics
- Health Sciences › Medicine › Reproductive Medicine › Endometriosis Research and Treatment
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Ectopic Pregnancy Diagnosis and Management
- Health Sciences › Medicine › Obstetrics and Gynecology › Gynecological conditions and treatments
- Keywords
- endometriosis, rhesus monkeys, risk factors, estradiol implants, hysterotomy, laparoscopy, spontaneous endometriosis, etiology, female primates, age at death
- MeSH terms
- Aging, Animals, Drug Implants, Endometriosis, Estradiol, Female, Macaca mulatta, Postoperative Complications, Risk Factors, Uterus, Logistic Models, Case-Control Studies
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review