A 2-year-old 4.7-kg (10.3-lb) spayed female domestic shorthair cat was referred to the Foster Hospital for Small Animals at Tufts University because of suspected estrous behavior, including rolling, vulvar licking, and vocalizations occurring every 5 to 6 weeks. The cat was reported to have undergone ovariohysterectomy prior to its adoption from a local animal shelter 15 months before this examination.
Exploratory laparotomy was performed by a local veterinarian 4 months after the cat had been adopted by the owners; at that time, suspected ovarian tissue was identified and removed at the left ovarian pedicle. Histologic examination of excised tissue was not performed. Five weeks after surgery, signs consistent with estrus returned, and a second exploratory laparotomy was performed. Suspected ovarian tissue was identified near the dorsal aspect of the body wall adjacent to the right kidney, and the suspect tissue was removed. Histologic evaluation of this excised tissue was also not performed. The cat had not undergone hormonal testing or ultrasonography before either of the exploratory laparotomies. Estrous behavior continued to occur every 5 to 6 weeks after the second exploratory surgery, and the cat was referred for consultation.
Physical examination revealed no abnormalities, and PCV and concentrations of serum total solids, BUN, and blood glucose were within the respective reference ranges. Ovarian remnant syndrome was suspected and subsequently confirmed by a positive serum AMH testa result and a serum P4 concentrationa of 6.76 ng/mL (positive result, > 0.5 ng/mL).1 Abdominal ultrasonographic examination was performed, and amorphous, hyperechoic tissue was identified immediately caudal to the left kidney (Figure 1). It was concluded that this finding could represent scar tissue from any of the 3 previous surgeries or a possible ovarian remnant.
Ultrasonographic image of the abdomen of a 2-year-old 4.7-kg (10.3-lb) domestic shorthair cat that was evaluated because of signs of estrous behavior at regular intervals following ovariohysterectomy despite removal of suspected ovarian tissue remnants in 2 separate exploratory laparotomies. An oval, slightly hyperechoic structure is visible (arrows) caudal to the left kidney (LK) that could represent scar tissue or an ovarian remnant. Another structure, possibly a suture remnant, can be visualized within the structure (asterisk). A similar hyperechoic structure was not visible on the opposite side of the abdomen.
Citation: Journal of the American Veterinary Medical Association 257, 6; 10.2460/javma.257.6.631
Exploratory laparotomy was performed when the cat was showing estrous behavior (6 weeks after evaluation of circulating P4 concentration and AMH testing). The patient was premedicated with buprenorphine hydrochlorideb (0.02 mg/kg [0.009 mg/lb], IM) and acepromazine maleatec (0.03 mg/kg [0.01 mg/lb], IM), and general anesthesia was induced with alfaxaloned (1.5 mg/kg [0.68 mg/lb], IV). The patient was intubated, and anesthesia was maintained with isoflurane in oxygen.
A standard ventral midline abdominal approach was made. Tissues at the right and left ovarian pedicles and the uterine stump appeared grossly normal but were excised and submitted for histologic examination. Two 0.5 × 0.3 × 0.3-cm red and tan nodules associated with the omentum were identified (Figure 2). Both nodules were removed with an electrosurgical cutting and coagulation systeme and submitted for histologic examination. Prior to closure, the abdomen was lavaged with warm, sterile saline (0.9% NaCl) solution. The linea alba was closed with polydioxanone suturef in a simple continuous pattern. The subcutaneous tissue was closed with polydioxanone sutureg in a subcuticular pattern, and the skin was closed with nylon sutureh in a simple interrupted pattern. Total duration of surgery was 50 minutes. An antimicrobial barrier bandagei was placed over the closed incision. The patient recovered uneventfully from the procedure. The barrier bandage was removed the following morning, and the patient was discharged from the hospital 24 hours after surgery. The owner was instructed to administer buprenorphineb (0.01 mg/kg [0.005 mg/lb], PO, q 8 to 12 h) as needed for pain control and to return the cat to the primary care veterinarian for suture removal and follow-up examination 10 to 14 days later.
Intraoperative photograph of omentum from the cat in Figure 1. A suspected ovarian remnant (arrow) is visible as a red and tan nodule in the omentum.
Citation: Journal of the American Veterinary Medical Association 257, 6; 10.2460/javma.257.6.631
Histologic examination of tissue located at both ovarian pedicles revealed fibroadipose tissue with normal vasculature. Both ovarian pedicle samples had minimal hemorrhage and smudged, hyalinized, amorphous tissue. Histologic evaluation of the uterine stump revealed normal hyalinized uterine structures. One of the 2 nodules excised from the omentum consisted primarily of fibroadipose tissue with numerous lymphocytes and macrophages admixed with mature granulation tissue. The second abdominal nodule consisted of fibroadipose tissue surrounding an ovarian remnant with secondary and graafian follicles (Figures 3 and 4). No corpora lutea were found on histologic examination.
Photomicrograph obtained during histologic examination of a suspected ovarian remnant from the cat in Figure 1. Fibroadipose tissue (asterisk) was present surrounding the remnant. Notice the graafian follicle within the tissue remnant (arrow). H&E stain; bar = 500 μm.
Citation: Journal of the American Veterinary Medical Association 257, 6; 10.2460/javma.257.6.631
Photomicrographs of the ovarian remnant in Figure 3 viewed with higher magnification. A late-secondary follicle (solid arrow) and a mature graafian follicle (open arrow) can be seen. H&E stain; bar = 200 μm. Inset—Highermagnification image of the late-secondary follicle revealing its transition into a graafian follicle. H&E stain; bar = 100 μm.
Citation: Journal of the American Veterinary Medical Association 257, 6; 10.2460/javma.257.6.631
The owner was contacted by telephone 25 weeks after surgery and reported that clinical signs of estrus had not returned. Serum collected from a venous blood sample obtained 28 weeks after surgery tested negative for AMHa and had a P4 concentrationa of < 0.06 ng/mL (negative result, < 0.2 ng/mL).
Discussion
Ovarian remnant syndrome is caused by the presence of residual functional ovarian tissue after gonadectomy.2–10 Residual ovarian tissue produces endogenous hormones, resulting in clinical signs of estrus in a presumably spayed animal.11 This syndrome has been associated with poor visibility of the ovarian pedicles, friable ovarian tissue, improper placement of ligatures or clamps, and the use of small (so-called keyhole) incisions to perform the gonadectomy5–8,12; it can also be caused by the presence of accessory ovarian tissue in the proper ligament.5–8,12 Whereas most cases of ORS result from surgical error, no correlation has been found between the incidence of ORS and surgeon experience.2,6 To our knowledge, in previous clinical reports of ORS in dogs and cats, ovarian remnant tissue has been located at or adjacent to an ovarian pedicle.2,3,6 Residual tissue is more frequently found at the right ovarian pedicle, presumably because it is located more cranially and subsequently more difficult to exteriorize.2,13,14 We could identify no previous clinical report of ORS in a cat or dog secondary to ovarian tissue not directly associated with an ovarian pedicle. Although ORS has been produced experimentally in cats by suturing ovaries to a lateral aspect of the abdominal wall or to the mesentery, neither of these procedures completely mimics a clinical situation in which devitalized tissue is dropped freely into the abdomen.5,15
Preoperative suspicion of ORS requires additional diagnostic testing to confirm clinical observations of estrous behavior. Vaginal cytologic evaluation can be performed during presumed estrus, but changes are less specific in queens than in bitches.4,13 Challenge testing by administration of gonadotropinreleasing hormone or human chorionic gonadotropin with subsequent measurement of P4 concentration provides further evidence of ORS, as increases in serum P4 concentration in response to these products suggest presence of a functional corpus luteum.4 Qualitative testing of serum for AMH alone is often adequate for confirming ORS in cats because AMH values are generally intermediate between spayed and sexually intact animals.16 Measurement of serum P4 concentration is sometimes useful, but these values will be high only in cats that have been bred, have ovulated spontaneously, or have been stimulated to ovulate.8 Baseline testing of AMH and P4 concentrations was chosen in this case to avoid having to perform multiple blood sample collections from a very fractious cat.
No corpora lutea were found on histologic evaluation of the excised tissues, despite a high preoperative serum P4 concentration. Cats are considered to be induced ovulators, but 35% to 65% of queens ovulate spontaneously without physical contact from a male.17–19 The cat of the present report was kept indoors with no other animal housemates, so it was likely that the cat ovulated spontaneously and the corpora lutea had regressed in the 6 weeks between hormonal testing and surgery.17,20
Revascularization and return of endocrine function have previously been shown for pancreas and parathyroid gland grafts.21–24 Angiogenesis is a normal physiologic process associated with ovarian tissue and is under the control of the gonadotropins follicle-stimulating hormone and luteinizing hormone.25 The granulosa and theca layers of ovarian follicles become the source of angiogenesis in transplanted tissue.25 Regeneration is improved in ovarian grafts of larger size and those with a greater number and size of follicles.26 Revascularization of transplanted ovarian tissue may be improved when all other ovarian tissue has been completely removed because lack of negative feedback from the gonads results in higher circulating gonadotropin concentrations in this situation.26 The gold standard for proving revascularization of transplanted endocrine tissue is the use of direct electron microscopy and microangiography; however, these methods have been shown to provide similar results to hormonal testing,24,25,27 as was done for the cat of this report.
The recommended treatment of ORS is surgical removal of the remnant tissue.4,11,13 If possible, surgery should be performed while the animal is in estrus because ovarian tissue is more likely be hyperemic, simplifying visual identification of the remnant.17 Exploratory laparotomy should focus on the ovarian pedicles, but the entire abdominal cavity should be examined carefully.4 All suspected tissue located at and adjacent to the ovarian pedicles should be excised and submitted for histologic examination.28 In this case, the lack of previous histologic assessment made it impossible to know whether the tissue previously removed from 1 or both pedicles contained ovarian tissue in addition to the remnant found in the omentum.
Acknowledgments
No third-party funding or support was received in connection with this case or the writing or publication of the manuscript. The authors declare that there were no conflicts of interest.
Presented in part at the 18th Annual Meeting of the Society of Soft Tissue Surgery, Asheville, NC, June 2019.
The authors thank Drs. Dominique G. Penninck and Nicholas Robinson, Tufts University Cummings School of Veterinary Medicine, for their respective contributions of ultrasonographic and histologic images included in this publication.
ABBREVIATIONS
| AMH | Anti-Müllerian hormone |
| ORS | Ovarian remnant syndrome |
| P4 | Progesterone |
Footnotes
Cornell University Animal Health Diagnostic Center, Ithaca, NY.
Par Pharmaceutical, Chestnut Ridge, NY.
MWI Animal Health, Boise, Idaho.
Jurox Pty Ltd, Rutherford, Australia.
Force Triad Energy Platform, Medtronic, Minneapolis, Minn.
2-0 PDS, Ethicon Inc, Summerville, NJ.
3-0 PDS, Ethicon Inc, Summerville, NJ.
4-0 Nylon, Ethicon Inc, Summerville, NJ.
Bioguard Island Dressing, Derma Sciences, Toronto, Canada.
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