Single-Port Laparoscopic Treatment and Outcome of Dogs with Ovarian Remnant Syndrome: 13 Cases (2010–2018)
ABSTRACT
Ovarian remnant syndrome (ORS) is a condition resulting from incomplete removal of ovarian tissue during ovariectomy and/or ovariohysterectomy. Single-port laparoscopy (SPL) is an alternative to ventral midline laparotomy for treatment of ORS. Medical records of 13 client-owned female dogs who underwent SPL for the treatment of ORS were retrospectively reviewed to evaluate surgical technique and outcome. Dogs who had undergone a previous attempt at open ovariectomy or ovariohysterectomy were included. Major intraoperative complications did not occur and conversion to open laparotomy was not required. In 1 dog, an SPL + 1 technique was used, in which an additional port was placed cranial to the single-port device to aid in dissection and tissue manipulation. Median surgical time was 45 min (range, 30–90 min). Clinical signs related to estrus had resolved in 11 of 13 dogs with a median follow-up time of 18 mo. Two of 13 dogs were lost to follow-up at 3 mo postoperatively; however, signs of estrus had resolved at time of last follow-up. SPL treatment for ORS was feasible and successful in this cohort of dogs. Reduced surgical time was found in this study compared with previous reports investigating multiple-port laparoscopic treatment of ORS.
Introduction
Ovarian remnant syndrome (ORS) is a result of failure to completely remove ovarian tissue because of a complication of surgery, ectopic tissue, or autotransplantation.1–3 Typical clinical signs of ORS may include signs of estrus, diestrus, proestrus, or pseudocyesis including vulvar swelling, vulvar discharge, mammary engorgement, behavioral changes, and/or uterine stump pyometra.2,3 Dogs undergoing ventral midline laparotomy are more likely to develop ORS of their right ovary compared with the left as a result of difficulty isolating the more cranially located right ovary through a traditional midline ovariohysterectomy (OVH) incision.2,3 In addition, as the weight of bitches increases, so too does their risk for experiencing ORS.4 Surgical removal of the remaining ovarian tissue is the treatment of choice for ORS and is typically performed after vaginal cytology, hormonal assay, and/or confirmatory ultrasonography.2–6 Laparoscopic ovariectomy (OVE) is commonly performed in dogs and has been shown to result in a more rapid return to function compared with a ventral midline approach.7–10 Laparoscopic treatment of ORS has been described in dogs using multiple-port laparoscopy (MPL) and in a single dog using a single-port approach in the veterinary literature.11–14 Single-port laparoscopy (SPL) techniques have been described for several procedures such as OVE, gastropexy, and cryptorchidectomy.15–17 SPL techniques allow for all laparoscopic instruments and an endoscope to be passed through one multichanneled access port using a single incision. Although SPL has been demonstrated to reduce surgical time and complications (primarily splenic puncture) of elective surgical procedures (OVE and gastropexy) when compared with MPL, loss of triangulation can make single-port techniques challenging for advanced cases in which careful surgical dissection is required.18 The purpose of this study was to describe the technique for SPL treatment of ORS and the related long-term clinical outcomes.
Materials and Methods
Case Selection
The medical records of dogs who underwent SPL treatment for ORS between 2010 and 2018 at the University of Guelph (Ontario Veterinary College), University of California – Davis School of Veterinary Medicine, University of Florida College of Veterinary Medicine, Centre Veterinaire DMV, and University of Pennsylvania (Matthew J. Ryan Veterinary Hospital), were reviewed. Dogs were included if their medical records were complete and they received SPL surgical treatment for ORS using a commercially available single-port devicea. Data collected from the medical record included history, signalment, weight, clinical signs, operative details, time to presentation from initial sterilization surgery, preoperative vaginal cytology and hormonal assay testing, diagnostic imaging type, and results. Operative data recorded included surgical time (defined as time from first incision to final suture), size of the incision, location of port placement, need for additional port placement, surgical findings, complications, and histopathologic evaluation of resected tissue. Patient follow-up was performed via telephone interview with the owner and/or referring veterinarian.
Diagnostic Evaluation
ORS was diagnosed using serum progesteroneb, vaginal cytology, and/or abdominal ultrasonography prior to SPL surgery.
Patient Preparation
The dogs were routinely anesthetized with a nonstandardized protocol approved by the attending anesthesiologist and were placed in dorsal recumbency. The ventral abdomen was clipped from xiphoid to pubis and the skin aseptically prepared for surgery. The dog was draped as for an open ventral midline abdominal exploration.
Surgical Technique
All surgeries were performed or directly supervised by a board-certified veterinary surgeon with expertise in laparoscopic procedures. A 2–3 cm skin incision was made centered over or just caudal to the umbilicus. Using a combination of sharp and electrosurgical dissection, the incision was extended through the linea alba. Stay sutures with 2-0 polydioxanonec, or rat tooth thumb forceps, were placed in the lateral aspects of the exposed rectus sheath for traction, and a commercially available single-port devicea was inserted into the incision as previously described.17 The peritoneal cavity was insufflated to 8–10 mm Hg with CO2 using a mechanically regulated insufflator deviced. Visual exploration of the abdominal cavity was performed to assess for abnormalities. The patient was rotated 25–45° laterally either manually or using a motorized mechanical tilt table to allow for improved visualization of the right and left abdominal cavity to evaluate the previous surgical sites (ovarian pedicles). When abnormal tissue was identified, it was grasped using laparoscopic forceps. Once grasped, the abnormal tissue was dissected from its surrounding tissue using a bipolar vessel-sealing device or articulating J-hook monopolar cauterye. After the tissue was dissected, the patient was rotated into dorsal recumbency, and the single-port device was removed while simultaneously holding the abnormal tissue. The single-port device was then reinserted into the abdomen, and the contralateral side of the abdomen was explored in the same manner as previously described. In cases in which uterine stump pathology was suspected based on abdominal ultrasonography, the region of the uterine stump was explored and hysterectomy performed using the vessel-sealing device if required. The single port was removed, pneumoperitoneum was purged, and a routine three-layer closure of the surgical wound was performed.
Operative data including anesthetic time, surgical time, location of ovarian remnant tissue, and complications were recorded. Intraoperative complications were classified as either minor or major. Minor complications were those that did not require conversion to open laparotomy and resolved with minor adjustments to surgical approach. Major complications were those that required conversion to open laparotomy or intervention that prevented successful completion of SPL treatment of ORS. Tissue samples were fixed in 10% formalin and stained using hematoxylin and eosin according to standard protocol of the diagnostic pathology service at each institution. Histopathology of the resected tissues was reviewed.
Postoperative Care
All dogs received an analgesic protocol as determined by the attending clinician. All dogs received hydromorphone (0.025–0.1 mg/kg [0.01–0.045 mg/lb] IV or subcutaneously), buprenorphine (0.01 mg/kg [0.045 mg/lb] subcutaneously or IV), or methadone (0.2 mg/kg [0.09 mg/lb] IV) at 4–6 hr intervals for 12–24 hr postoperatively. Hospitalization time, medications dispensed, time until follow-up, postoperative clinical status, and diagnostics were obtained from the patients’ medical records.
Statistical Analysis
Descriptive statistics such as mean, median, and range were calculated for continuous variables (e.g., age at initial procedure, time to presentation, and surgical time), and frequency percentages were calculated for categorical variables (e.g., dogs with neoplastic tissues).
Results
Animals
Thirteen female dogs who had previously undergone open OVH (n = 11) or OVE (n = 2) were included in this study. Dog breeds included mixed-breed dog (n = 5), Labrador retriever (n = 2), dachshund (n = 1), greyhound (n = 1), Kerry blue terrier (n = 1), Pit bull terrier (n = 1), mastiff (n = 1), and Australian shepherd (n = 1). The median weight of the dogs was 28 kg (61.6 lbs; range, 5–48.7 kg [11–107 lbs]) with a median age of 28 mo (range, 12–100 mo).
Preoperative Diagnostic Evaluation
The median age at the time of initial surgery was 7 mo (range, 2–48 mo). All initial surgical procedures were performed through a ventral midline laparotomy. The median time interval between the initial surgical procedure and surgical treatment of ORS was 19 mo (range, 8–94 mo). The median time interval between initial sterilization surgery and clinical presentation was 14 mo (range, 1–72 mo). Dogs were presented for suspicion of ORS, and the clinical signs described by the owners included hemorrhagic vaginal discharge (n = 12), vulvar swelling (n = 12), behavior changes (n = 8), and mammary enlargement (n = 5). Vaginal cytology was performed on five dogs revealing stages of the estrus cycle (cornified epithelial cells in four dogs and polymononuclear cells with a mixture of parabasal and intermediate cells signifying diestrus in another dog). Serum progesterone levels were performed in three dogs demonstrating elevated progesterone levels (1.8 [0.57], 3.9 [1.23], and 16 [5.0] nmol/L [ng/mL]; <1.5 nmol/L [<0.5 ng/mL] normal reference range for a spayed bitch). Ultrasonography was performed in nine dogs to identify the presence of an ovarian remnant. In all nine dogs, a hypoechoic nodular mass was identified at the region of the ovarian pedicle and suspected to be ovarian remnant tissue. In five dogs, evidence of remnant tissue was discovered on the right side, two dogs had remnant tissue on the left side, and two dogs had remnant tissue bilaterally. Additional ultrasound findings included three dogs with evidence of hydrosalpinx, two with evidence of uterine stump enlargement, and two with remnant uterine horns without mucometra. In one of these dogs, the uterine horn remnant developed into an 8 × 4.5 × 3.5 cm cystic structure associated with a histologically normal left ovarian remnant.
Operative Data
The median anesthetic and surgical times for the 13 dogs undergoing SPL treatment of ORS was 122 min (range, 80–200 min) and 45 min (range, 30–90 min), respectively. In 8 dogs, ovarian remnant tissue was right sided, 3 dogs were left sided, and 2 dogs were bilateral. The predicted location of the ovarian remnant in all dogs who underwent ultrasonography was confirmed at the time of surgery. Major intraoperative complications were not encountered in any dog. In 2 dogs, minor complications occurred. In 1 dog, an additional 6 mm trocar/cannula assemblyd was placed between the single port and the xiphoid process to help facilitate visualization and dissection of a dilated uterine horn remnant. In this dog, the uterine horn remnant was found to be markedly dilated (>5 cm) during abdominal ultrasonography. Following dissection and sealing of the ovarian pedicle, a 22-gauge hypodermic needle was inserted transcutaneously to aspirate the fluid present in the uterine horn remnant. This allowed for removal of the tissue through the single-port access incision. In another dog, a rigid, conical, reusable single-port devicef was initially placed; however, as a result of persistent insufflation leakage, the surgeon removed this port and placed the single port used in the remainder of the dogs in the studya.
Histopathology
All resected tissues were submitted for histopathological evaluation totaling 15 samples. Twelve samples were determined to be nonneoplastic ovarian remnant tissue and 3 were consistent with sex cord stromal cell tumors. In addition, three samples showed evidence of hydrosalpinx.
Outcome
The median hospitalization time postoperatively was 24 hr (range, 5–28 hr). All dogs were discharged from the hospital on either oral meloxicam (0.1 mg/kg [0.045 mg/lb] q 24 hr for 3–7 days) or carprofen (2.2 mg/kg [0.1 mg/lb] q 12 hr for 3–7 days), and 8 dogs were discharged with both meloxicam (0.1 mg/kg [0.045 mg/lb] q 24 hr for 3–7 days) and tramadol (4 mg/kg [1.8 mg/lb] q 8–12 hr for 3–7 days). Follow-up via telephone interview with the owner and/or referring veterinarian was available for all dogs included in the present study. The median follow-up time for dogs of this study was 17 mo (range, 3–48 mo). There was no report of postoperative complications following surgery in any dog, and all clinical signs relating to ORS had resolved. Two dogs were lost to follow-up 3 mo postoperatively. With these dogs removed from the analysis, the median follow-up time for the remaining 11 dogs was 18 mo (range, 7–48 mo). One dog who was diagnosed with a sex cord stromal tumor had repeat abdominal ultrasonography at 90 days postoperatively and had evidence of a 9.0 × 4.6 mm hypoechoic nodule in the region of the previous surgery site. A repeat abdominal ultrasound 8 mo postoperatively was performed and identified the hypoechoic nodule and had remained similar in size (8.6 × 2.2 mm) compared with the previous evaluation. This was suspected to be associated with the suture material (suture-related granuloma) from the initial open OVH at the ovarian pedicle, although recurrent neoplasia could not be excluded. A second dog diagnosed with a sex cord stromal tumor continued to have persistent urinary tract infections and vaginitis, although all signs of estrus had resolved. Abdominal ultrasonography performed 150 days after surgery revealed a thickened uterine stump with no evidence of ORS 23 mo following surgery.
Discussion
In 13 canine cases of ORS presenting to five veterinary referral centers, SPL was successfully used for treatment without major perioperative complications in any dog. Postoperatively, all 13 dogs had resolution of clinical signs associated with ORS and complications were not reported. Based on the results of this study, SPL is a viable alternative to open laparotomy and/or MPL for the treatment of dogs with ORS.
Clinical signs were typical of estrus or historical estrus in all dogs. Abdominal ultrasonography was performed in 9 out of 13 dogs and was accurate in describing the location of the ovarian remnant in all dogs. Although serum progesterone level is considered highly sensitive for the presence of ovarian tissue, the authors recommend performing abdominal ultrasonography prior to SPL for the treatment of ORS. Ultrasonography can provide an accurate location of the remnant tissue (side and uni- versus bilateral) and whether abnormal uterine tissue is present. One of the disadvantages of the laparoscopic approach (single- or multiport) is that abdominal exploration is limited and ovarian remnant tissue can be missed if not in the location of the ovarian pedicles. Ultrasonography can provide confidence to the surgeon as to the localization of abnormal tissue when considering a minimally invasive approach.
Compared with traditional open laparotomy in dogs, the benefits of single-port, multiple-port, and laparoscopic-assisted OVH have been previously reported and include reduced surgical time, reduced surgical trauma and postoperative pain, possible reduction in surgical site infections, and reduced hospitalization time.7–10,19 In addition, the illumination and magnification provided during laparoscopy may be particularly beneficial in the surgical treatment of ORS allowing for improved visualization of the remnant tissue with an endoscope. As a further evolution of laparoscopic surgery, SPL has been developed to decrease number of incisions, reduce postoperative pain, and improve cosmesis.15–17,19,20 In veterinary laparoscopy, single-port approaches have been described for OVE, OVE and gastropexy, cryptorchidectomy, and several laparoscopic-assisted procedures including splenectomy and enterotomy/enterectomy.15–18,21,22 Furthermore, in a recent study, SPL resulted in reduced complications and surgical time when compared with MPL in which elective OVE, gastropexy, and combination of OVE with gastropexy were studied.18 The reduced surgical time for elective SPL procedures in the previously discussed study was attributed to lack of requirement for a Veress needle and ovarian hook or transabdominal suspension sutures and the minimal approach needed for gastropexy when the single port was already placed in the right paramedian location.18 Although surgical time ranged between 30 and 90 min for the dogs of this study undergoing SPL for the treatment of ORS, the median surgical time of 45 min was less than previously reported surgical times in two studies using a multiport approach for the treatment of ORS (80.5 and 90 min).11,12 Among the dogs of this study, the longest surgical time of 90 min was the only procedure >60 min. This dog was one of three cases diagnosed as having a sex cord stromal tumor on histopathology, and marked adhesions were noted at the time of surgery. The variability in surgical time is likely multifactorial considering patient variation, reproductive pathology, and surgeon experience. As laparoscopic surgery has become more widely practiced, it is conceivable to expect that surgical efficiency has improved as surgeons develop improved laparoscopic technique.23 This may be reflected when comparing surgical times of contemporary procedures with prior studies that were performed when the learning curve for a particular laparoscopic procedure was being traversed.
Major intraoperative complications were not encountered in the dogs of this study. Minor complications did occur in two dogs. In one dog, a rigid, conical, reusable single-port devicef was replaced with the single porta used in the dogs in the remainder of the study as a result of persistent insufflation leakage. Insufflation leakage using this rigid, reusable single-port device has been previously reported during elective gastropexy.24 The authors of that study suggested that accurate incision length is required to minimize this complication as the nonmalleable nature of the rigid, conical port allows for gas leakage through an ovoid incision.24 Additional complications related to the single-port device were not seen in the dogs of this study. In another dog of the present study, an additional 6 mm port was placed halfway between the single port and the xiphoid process to aid in retraction. Upon initial SPL evaluation, markedly distended uterine horn remnants were visualized that were connected to the ovarian remnant. Retraction with laparoscopic Babcock forceps did not provide adequate visualization, and the decision was made to insert a 6 mm port to aid in retraction. This operative maneuver allowed for successful resection of the remnant tissue in a surgical time of 60 min. Consideration could have been made for insertion of a 3 mm trocar/cannula assembly and blunt probe; however, the morbidity of a 6 mm port insertion on ventral midline was thought to be minimal. Regardless, when performing SPL, surgeons should not hesitate to place additional ports should additional retraction or triangulation for dissection be required. A single-port +1 port technique has been described for cholecystectomy, for which the additional port was used for indirect retraction of the gall bladder.25
Following histopathology, three dogs were diagnosed with a sex cord stromal tumor. One of these dogs had the longest operating time of 90 min, whereas the other two dogs had surgical times of 45 and 55 min, respectively. Also, two of these patients had the longest time intervals between initial sterilization surgery and clinical presentation for ORS (72 mo for both dogs). Two of these three cases are consistent with previous findings that demonstrated increased time intervals between sterilization surgery and ORS evaluation in patients with neoplastic tissue when compared with those with nonneoplasic tissues.2,3 In previous studies, it has been suggested that animals with ovarian neoplasms may not secret adequate concentrations of hormones to cause clinical signs until malignant transformation.2 However, it may be that veterinarians and owners do not recognize clinical signs as readily with the information that the dog had previously undergone OVH.3 In all three of the dogs in this report, intraoperative or postoperative complications were not reported and clinical signs of ORS had resolved. Upon follow-up at 5 and 9 mo postoperatively, one of these dogs continued to display signs of persistent urinary tract infections but did not display further clinical signs related to ORS 23 mo following SPL treatment of ORS. Additionally, one of these dogs showed evidence of a hypoechoic nodule suspected to be associated with the suture material from the initial open sterilization procedure at the location of the ovarian pedicle on repeat ultrasound postoperatively.
An oncologic consideration for future laparoscopic treatment of ORS (single- or multiport) is how the resected tissue is removed from the dog. In all cases of this study, the resected tissue was withdrawn through the single-port incision after the port was removed. Because 23% (3/13) of dogs in this study were diagnosed with neoplastic tissue, consideration should be given to the use of a specimen retrieval bag or placement of a wound retraction device to prevent neoplastic seeding of tissue during extraction. This may be of particular importance where neoplasia may be suspected in dogs that had a prolonged period of time between initial surgery and development of clinical signs.
Conclusion
The results of the present study suggest that SPL surgery is a viable option for the treatment of dogs with ORS as a result of either benign or neoplastic ovarian tissue. Despite the specialized training and equipment required to perform laparoscopic surgery, reduced surgical time and previously reported reduction in postoperative pain, complications, and incisions should be considered in patients with ORS. Median surgical time (45 min) was improved when compared with previous studies. Perioperative complications were not observed, and all patients were discharged from the hospital within 28 hr of surgery. Complete resolution of clinical signs relating to ORS was noted in all dogs upon follow-up. Further studies are required to investigate and compare the benefits of SPL with MPL and open laparotomy for the treatment of ORS.
Contributor Notes
MPL (multiple-port laparoscopy); ORS (ovarian remnant syndrome); OVE (ovariectomy); OVH (ovariohysterectomy); SPL (single-port laparoscopy)


