Infertility caused by oophoritis in a dog resolved by hemiovariectomy
Keywords:
Canine oophoritis, infertility, ovarian nodule, hemiovariectomy
Abstract
Canine oophoritis is a rare ovarian pathology that has been reported to cause infertility. However, diagnostic work-up, treatment options, and prognosis of return to fertility after treatment for oophoritis were not reported. We report oophoritis in a dog that was diagnosed via histopathology after hemiovariectomy; diagnostic tests, treatment, and outcome of fertility are included and compared to other domestic species and women. Additionally, pathophysiology and prognostic outcome of oophoritis in women are discussed in the context of future directions and possible avenues of investigation in canine oophoritis.
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References
1. Hollinshead FK, Hanlon DW: Factors affecting the reproductive performance of bitches: a prospective cohort study involving 1203 inseminations with fresh and frozen semen. Theriogenology 2017;101:62-72. doi: 10.1016/j.theriogenology.2017.06.021
2. Maya-Pulgarin D, Gonzalez-Dominguez MS, Aranzazu-Taborda D, et al: Histopathologic findings in uteri and ovaries collected from clinically healthy dogs at elective ovariohysterectomy: a cross-sectional study. J Vet Sci 2017;18:407-414. doi: 10.4142/jvs.2017.18.3.407
3. Sasidharan JK, Patra MK, Singh LK, et al: Ovarian cysts in the bitch: an update. Top Companion Anim Med 2021;43:1-7. doi: 10.1016/j.tcam.2021.100511
4. Nickel R, Okkens AC, van der Gaag I, et al: Oophoritis in a dog with abnormal corpus luteum function. Vet Rec 1991;128: 333-334. doi: 10.1136/vr.128.14.333
5. Johnston S: Premature gonadal failure in female dogs and cats. J Reprod Fertil 1989;39:65-72.
6. Parker RF, Foley GL, Dangler CA, et al: Necrotic oophoritis in gilts associated with experimental inoculation of a viral gene-deletion mutant pseudorabies vaccine. Vet Pathol 1997;34:199-203. doi: 10.1177/030098589703400304
7. Smith P, Nusbaum KE, Kwapien RP, et al: Necrotic oophoritis in heifers vaccinated intravenously with infectious bovine rhinotracheitis virus vaccine during estrus. Am J Vet Res 1990;51:969-972. doi: 10.2460/ajvr.1990.51.07.969
8. Grooms DL, Brock KV, Ward LA: Detection of bovine viral diarrhea virus in the ovaries of cattle acutely infected with bovine viral diarrhea virus. J Vet Diagn Invest 1998;10:125-129. doi: 10.1177/104063879801000201
9. McGowan MR, Kafi M, Kirkland PD, et al: Studies of the pathogenesis of bovine pestivirus-induced ovarian dysfunction in superovulated dairy cattle. Theriogenology 2003;59:1051-1066. doi: 10.1016/S0093-691X(02)01136-6
10. Bogh IB, Brink P, Jensen HE, et al: Ovarian function and morphology in the mare after multiple follicular punctures. Equine Vet J 2003;35:575-579. doi: 10.2746/042516403775467243
11. Hawkins K: Bilateral salpingitis, hydrosalpinx and oophoritis in a mare. Cornell Vet 1986;76:38-48.
12. Velez IC, Arnold C, Jacobson CC, et al: Effects of repeated transvaginal aspiration of immature follicles on mare health and ovarian status. Equine Vet J 2012;44:78-83. doi: 10.1111/j.2042-3306.2012.00606.x
13. Jankowska K: Premature ovarian failure. Menopause Rev 2017;16:51-56. doi: 10.5114/pm.2017.68592
14. Alekberova Z, Goloeva R, Popkova T, et al: Pregnancy outcomes in systemic lupus erythematosus (SLE). BMJ Sci Abstr 2021; 9:1072 AB0086.
15. Silva CA, Yamakami LYS, Aikawa NE, et al: Autoimmune primary ovarian insufficiency. Autoimmun Rev 2014;13:427-430. doi: 10.1016/j.autrev.2014.01.003
16. Luborsky JL, Tung KS: Oophoritis. In: Rose NR, Mckay IR: editors. The Autoimmune Diseases. 4th edition, Cambridge; Academic Press: 2006. p. 849-859. doi: 10.1016/B978-012595961-2/50064-0
17. Nelson LM, Covington SN, Rebar RW: An update: spontaneous premature ovarian failure is not an early menopause. Fertil Steril 2005;83:1327-1332. doi: 10.1016/j.fertnstert.2004.11.059
18. Welt CK: Autoimmune oophoritis in the adolescent. Ann NY Acad Sci 2008;1135:118-122. doi: 10.1196/annals.1429.006
19. Warren BD, Kinsey WK, McGinnis LK, et al: Ovarian autoimmune disease: clinical concepts and animal models. Cell Mol Immunol 2014;14:510-521. doi: 10.1038/cmi.2014.97
20. Welt CK, Falorni A, Taylor AE, et al: Selective theca cell dysfunction in autoimmune oophoritis results in multifollicular development, decreased estradiol, and elevated inhibin B levels. J Clin Endocrinol Metab 2005;90:3069-3076. doi: 10.1210/jc.2004-1985
21. Tong ZB, Otsuka N, Tu W, et al: P450 side-chain cleavage enzyme (P450-scc) is an ovarian autoantigen in a mouse model for autoimmune oophoritis. Reprod Sci 2022;29:2391-2400. doi: 10.1007/s43032-022-00970-7
22. Bagavant H, Adams S, Terranova P, et al: Autoimmune ovarian inflammation triggered by proinflammatory (Th1) T cells is compatible with normal ovarian function in mice. Biol Reprod 1999;61:635-642. doi: 10.1095/biolreprod61.3.635
23. Altuntas CZ, Johnson JM, Touhy VK: Autoimmune targeted disruption of the pituitary-ovarian axis causes premature ovarian failure. J Immunol 2006;177:1988-1996. doi: 10.4049/jimmunol.177.3.1988
24. Ebrahimi M, Asbagh FA: The role of autoimmunity in premature ovarian failure. Iran J Reprod Med 2015;13:461-472.
25. Bakalov VK, Anasti JN, Calis KA, et al: Autoimmune oophoritis as a mechanism of follicular dysfunction in women with 46, XX spontaneous premature ovarian failure. Fertil Steril 2005;84:958-965. doi: 10.1016/j.fertnstert.2005.04.060
26. Damjanovic MA, Jankovic BD: Experimental autoimmune oophoritis. I. Inhibition of fertility in rats isoimmunized with homogenates of ovary. Am J Reprod Immunol 1989;20:1-8. doi: 10.1111/j.1600-0897.1989.tb00628.x
27. Hunter AG: Immunology and fertility in the bovine. J Dairy Sci 1989;72:3353-3362. doi: 10.3168/jds.S0022-0302(89)79498-4
28. Farin PW, Estill CT: Infertility due to abnormalities of the ovaries in cattle. Vet Clin North Am Food Anim Pract 1993;9:291-308. doi: 10.1016/S0749-0720(15)30647-2
29. Summers PM, Campbell RSF, Dennett DP: Herd studies on the genital pathology of infertile beef cows. Aust Vet J 1974;50:150-154. doi: 10.1111/j.1751-0813.1974.tb06881.x
30. Nishizuka Y, Sakakura T: Thymus and reproduction: sex-linked dysgenesia of the gonad after neonatal thymectomy in mice. Science 1969;166:753-755. doi: 10.1126/science.166.3906.753
31. Taguchi O, Nishizuka Y, Sakakura T, et al: Autoimmune oophoritis in thymectomized mice: detection of circulating antibodies against oocytes. Clin Exp Immunol 1980;40:540-534.
32. Ledger WJ: Laparoscopy in diagnosing and managing patients with suspected salpingo-oophoritis. Am J Obstet Gynecol 1980;138:1012-1016. doi: 10.1016/0002-9378(80)91098-4
33. Piseddu E, Masserdotti C, Milesi C, et al: Cytologic features of normal canine ovaries in different stages of estrus with histologic comparison. Vet Clin Pathol 2012;41:396-404. doi: 10.1111/j.1939-165X.2012.00453.x
34. Ayala C, Celis ME: Experimental autoimmune oophoritis and ɑ-melanocyte-stimulating hormone. Expert Rev Endocr Metab 2010;5:539-547. doi: 10.1586/eem.10.11
35. Patrelli T, Franchi L, Gizzo S, et al: Can the impact of pelvic inflammatory disease on fertility be prevented? Epidemiology, clinical features and surgical treatment: evolution over 8 years. J Reprod Med 2013;58:425-433.
36. Singh N, Tripathi R, Mala YM, et al: Xanthomatous oophoritis following uterine artery embolization: successful conservative surgical management with favourable outcome. BMJ Case Rep 2013; 2013:1-5. doi: 10.1136/bcr-2013-010184
37. Torre A, Amado A, Joao D, et al: Xanthogranulomatous salpingo-oophoritis presenting as an ovarian tumor. BMJ Case Rep 2022;15:1-4. doi: 10.1136/bcr-2021-248197
38. Van Kasteren Y, Hoek A, Schoemaker J: Ovulation induction in premature ovarian failure: a placebo-controlled randomized trial combining pituitary suppression with gonadal stimulation. Fertil Steril 1995;64:273-278. doi: 10.1016/S0015-0282(16)57722-X
39. Gleicher N, Darmon S, Molinari E, et al: A form of secondary ovarian insufficiency (SOI) due to adrenal hypoandrogenism as new infertility diagnosis. Endocrine 2021;72:260-267. doi: 10.1007/s12020-020-02512-0
40. Bradbury R, McLean M, Smith H: Successful live birth following a short course of glucocorticoid suppression in a patient with autoimmune polyglandular syndrome type 2 and premature ovarian insufficiency: A case report. J Obstet Gynaecol Res 2023;49:2194-2198. doi: 10.1111/jog.15684
41. Kalantaridou SN, Braddock DT, Patronas NJ, et al: Treatment of autoimmune premature ovarian failure. Hum Reprod 1999;14:1777-1782. doi: 10.1093/humrep/14.7.1777
42. Morrison J, Givens JR, Wiser WL, et al: Mumps oophoritis: a cause of premature menopause. Fertil Steril 1975;26:655-659. doi: 10.1016/S0015-0282(16)41233-1
43. Caine EA, Scheaffer SM, Broughton DE, et al: Zika virus causes acute infection and inflammation in the ovary of mice without apparent defects in fertility. J Infect Dis 2019;220:1904-1914. doi: 10.1093/infdis/jiz239
44. Broughton DE, Schaeffer S, Halabi J, et al: Zika virus causes acute oophoritis mediated by T lymphocytes in a mouse model. Fertil Steril PCRS Abstracts 2018;109:e4-e5. doi: 10.1016/j.fertnstert.2018.02.019
45. Sokolowski JH, Stover DG, Van Ravenswaay OF: Seasonal incidence of estrus and interestrous interval for bitches of seven breeds. J Am Vet Med Assoc 1970;171:271-273.
46. Christie DW, Bell ET: Some observations on the seasonal incidence and frequency of oestrus in breeding bitches in Britain. J Small Anim Pract 1971;12:159-167. doi: 10.1111/j.1748-5827.1971.tb06213.x
47. Sokolowski JH: Reproductive patterns in the bitch. Vet Clin North Am 1977;7:653-666. doi: 10.1016/S0091-0279(77)50076-7
2. Maya-Pulgarin D, Gonzalez-Dominguez MS, Aranzazu-Taborda D, et al: Histopathologic findings in uteri and ovaries collected from clinically healthy dogs at elective ovariohysterectomy: a cross-sectional study. J Vet Sci 2017;18:407-414. doi: 10.4142/jvs.2017.18.3.407
3. Sasidharan JK, Patra MK, Singh LK, et al: Ovarian cysts in the bitch: an update. Top Companion Anim Med 2021;43:1-7. doi: 10.1016/j.tcam.2021.100511
4. Nickel R, Okkens AC, van der Gaag I, et al: Oophoritis in a dog with abnormal corpus luteum function. Vet Rec 1991;128: 333-334. doi: 10.1136/vr.128.14.333
5. Johnston S: Premature gonadal failure in female dogs and cats. J Reprod Fertil 1989;39:65-72.
6. Parker RF, Foley GL, Dangler CA, et al: Necrotic oophoritis in gilts associated with experimental inoculation of a viral gene-deletion mutant pseudorabies vaccine. Vet Pathol 1997;34:199-203. doi: 10.1177/030098589703400304
7. Smith P, Nusbaum KE, Kwapien RP, et al: Necrotic oophoritis in heifers vaccinated intravenously with infectious bovine rhinotracheitis virus vaccine during estrus. Am J Vet Res 1990;51:969-972. doi: 10.2460/ajvr.1990.51.07.969
8. Grooms DL, Brock KV, Ward LA: Detection of bovine viral diarrhea virus in the ovaries of cattle acutely infected with bovine viral diarrhea virus. J Vet Diagn Invest 1998;10:125-129. doi: 10.1177/104063879801000201
9. McGowan MR, Kafi M, Kirkland PD, et al: Studies of the pathogenesis of bovine pestivirus-induced ovarian dysfunction in superovulated dairy cattle. Theriogenology 2003;59:1051-1066. doi: 10.1016/S0093-691X(02)01136-6
10. Bogh IB, Brink P, Jensen HE, et al: Ovarian function and morphology in the mare after multiple follicular punctures. Equine Vet J 2003;35:575-579. doi: 10.2746/042516403775467243
11. Hawkins K: Bilateral salpingitis, hydrosalpinx and oophoritis in a mare. Cornell Vet 1986;76:38-48.
12. Velez IC, Arnold C, Jacobson CC, et al: Effects of repeated transvaginal aspiration of immature follicles on mare health and ovarian status. Equine Vet J 2012;44:78-83. doi: 10.1111/j.2042-3306.2012.00606.x
13. Jankowska K: Premature ovarian failure. Menopause Rev 2017;16:51-56. doi: 10.5114/pm.2017.68592
14. Alekberova Z, Goloeva R, Popkova T, et al: Pregnancy outcomes in systemic lupus erythematosus (SLE). BMJ Sci Abstr 2021; 9:1072 AB0086.
15. Silva CA, Yamakami LYS, Aikawa NE, et al: Autoimmune primary ovarian insufficiency. Autoimmun Rev 2014;13:427-430. doi: 10.1016/j.autrev.2014.01.003
16. Luborsky JL, Tung KS: Oophoritis. In: Rose NR, Mckay IR: editors. The Autoimmune Diseases. 4th edition, Cambridge; Academic Press: 2006. p. 849-859. doi: 10.1016/B978-012595961-2/50064-0
17. Nelson LM, Covington SN, Rebar RW: An update: spontaneous premature ovarian failure is not an early menopause. Fertil Steril 2005;83:1327-1332. doi: 10.1016/j.fertnstert.2004.11.059
18. Welt CK: Autoimmune oophoritis in the adolescent. Ann NY Acad Sci 2008;1135:118-122. doi: 10.1196/annals.1429.006
19. Warren BD, Kinsey WK, McGinnis LK, et al: Ovarian autoimmune disease: clinical concepts and animal models. Cell Mol Immunol 2014;14:510-521. doi: 10.1038/cmi.2014.97
20. Welt CK, Falorni A, Taylor AE, et al: Selective theca cell dysfunction in autoimmune oophoritis results in multifollicular development, decreased estradiol, and elevated inhibin B levels. J Clin Endocrinol Metab 2005;90:3069-3076. doi: 10.1210/jc.2004-1985
21. Tong ZB, Otsuka N, Tu W, et al: P450 side-chain cleavage enzyme (P450-scc) is an ovarian autoantigen in a mouse model for autoimmune oophoritis. Reprod Sci 2022;29:2391-2400. doi: 10.1007/s43032-022-00970-7
22. Bagavant H, Adams S, Terranova P, et al: Autoimmune ovarian inflammation triggered by proinflammatory (Th1) T cells is compatible with normal ovarian function in mice. Biol Reprod 1999;61:635-642. doi: 10.1095/biolreprod61.3.635
23. Altuntas CZ, Johnson JM, Touhy VK: Autoimmune targeted disruption of the pituitary-ovarian axis causes premature ovarian failure. J Immunol 2006;177:1988-1996. doi: 10.4049/jimmunol.177.3.1988
24. Ebrahimi M, Asbagh FA: The role of autoimmunity in premature ovarian failure. Iran J Reprod Med 2015;13:461-472.
25. Bakalov VK, Anasti JN, Calis KA, et al: Autoimmune oophoritis as a mechanism of follicular dysfunction in women with 46, XX spontaneous premature ovarian failure. Fertil Steril 2005;84:958-965. doi: 10.1016/j.fertnstert.2005.04.060
26. Damjanovic MA, Jankovic BD: Experimental autoimmune oophoritis. I. Inhibition of fertility in rats isoimmunized with homogenates of ovary. Am J Reprod Immunol 1989;20:1-8. doi: 10.1111/j.1600-0897.1989.tb00628.x
27. Hunter AG: Immunology and fertility in the bovine. J Dairy Sci 1989;72:3353-3362. doi: 10.3168/jds.S0022-0302(89)79498-4
28. Farin PW, Estill CT: Infertility due to abnormalities of the ovaries in cattle. Vet Clin North Am Food Anim Pract 1993;9:291-308. doi: 10.1016/S0749-0720(15)30647-2
29. Summers PM, Campbell RSF, Dennett DP: Herd studies on the genital pathology of infertile beef cows. Aust Vet J 1974;50:150-154. doi: 10.1111/j.1751-0813.1974.tb06881.x
30. Nishizuka Y, Sakakura T: Thymus and reproduction: sex-linked dysgenesia of the gonad after neonatal thymectomy in mice. Science 1969;166:753-755. doi: 10.1126/science.166.3906.753
31. Taguchi O, Nishizuka Y, Sakakura T, et al: Autoimmune oophoritis in thymectomized mice: detection of circulating antibodies against oocytes. Clin Exp Immunol 1980;40:540-534.
32. Ledger WJ: Laparoscopy in diagnosing and managing patients with suspected salpingo-oophoritis. Am J Obstet Gynecol 1980;138:1012-1016. doi: 10.1016/0002-9378(80)91098-4
33. Piseddu E, Masserdotti C, Milesi C, et al: Cytologic features of normal canine ovaries in different stages of estrus with histologic comparison. Vet Clin Pathol 2012;41:396-404. doi: 10.1111/j.1939-165X.2012.00453.x
34. Ayala C, Celis ME: Experimental autoimmune oophoritis and ɑ-melanocyte-stimulating hormone. Expert Rev Endocr Metab 2010;5:539-547. doi: 10.1586/eem.10.11
35. Patrelli T, Franchi L, Gizzo S, et al: Can the impact of pelvic inflammatory disease on fertility be prevented? Epidemiology, clinical features and surgical treatment: evolution over 8 years. J Reprod Med 2013;58:425-433.
36. Singh N, Tripathi R, Mala YM, et al: Xanthomatous oophoritis following uterine artery embolization: successful conservative surgical management with favourable outcome. BMJ Case Rep 2013; 2013:1-5. doi: 10.1136/bcr-2013-010184
37. Torre A, Amado A, Joao D, et al: Xanthogranulomatous salpingo-oophoritis presenting as an ovarian tumor. BMJ Case Rep 2022;15:1-4. doi: 10.1136/bcr-2021-248197
38. Van Kasteren Y, Hoek A, Schoemaker J: Ovulation induction in premature ovarian failure: a placebo-controlled randomized trial combining pituitary suppression with gonadal stimulation. Fertil Steril 1995;64:273-278. doi: 10.1016/S0015-0282(16)57722-X
39. Gleicher N, Darmon S, Molinari E, et al: A form of secondary ovarian insufficiency (SOI) due to adrenal hypoandrogenism as new infertility diagnosis. Endocrine 2021;72:260-267. doi: 10.1007/s12020-020-02512-0
40. Bradbury R, McLean M, Smith H: Successful live birth following a short course of glucocorticoid suppression in a patient with autoimmune polyglandular syndrome type 2 and premature ovarian insufficiency: A case report. J Obstet Gynaecol Res 2023;49:2194-2198. doi: 10.1111/jog.15684
41. Kalantaridou SN, Braddock DT, Patronas NJ, et al: Treatment of autoimmune premature ovarian failure. Hum Reprod 1999;14:1777-1782. doi: 10.1093/humrep/14.7.1777
42. Morrison J, Givens JR, Wiser WL, et al: Mumps oophoritis: a cause of premature menopause. Fertil Steril 1975;26:655-659. doi: 10.1016/S0015-0282(16)41233-1
43. Caine EA, Scheaffer SM, Broughton DE, et al: Zika virus causes acute infection and inflammation in the ovary of mice without apparent defects in fertility. J Infect Dis 2019;220:1904-1914. doi: 10.1093/infdis/jiz239
44. Broughton DE, Schaeffer S, Halabi J, et al: Zika virus causes acute oophoritis mediated by T lymphocytes in a mouse model. Fertil Steril PCRS Abstracts 2018;109:e4-e5. doi: 10.1016/j.fertnstert.2018.02.019
45. Sokolowski JH, Stover DG, Van Ravenswaay OF: Seasonal incidence of estrus and interestrous interval for bitches of seven breeds. J Am Vet Med Assoc 1970;171:271-273.
46. Christie DW, Bell ET: Some observations on the seasonal incidence and frequency of oestrus in breeding bitches in Britain. J Small Anim Pract 1971;12:159-167. doi: 10.1111/j.1748-5827.1971.tb06213.x
47. Sokolowski JH: Reproductive patterns in the bitch. Vet Clin North Am 1977;7:653-666. doi: 10.1016/S0091-0279(77)50076-7
Published
2025-01-10
How to Cite
Nebel-Karp A., Mahoney D., Whitacre M., Bauer B., & Lyle S. (2025). Infertility caused by oophoritis in a dog resolved by hemiovariectomy. Clinical Theriogenology, 17. https://doi.org/10.58292/CT.v17.10638
Section
Case Reports
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