Introduction
Laparoscopic sterilization has become the standard of care in dogs,1 which is due to all the reported benefits, including improved visualization, less soft tissue trauma, less pain, shorter hospitalization times, and fewer postoperative complications compared to open surgery.2–6 Techniques in laparoscopic sterilization have been continuously modified in recent decades, starting with 3-port techniques and more recently description of several single-port techniques.3,7–12 Although laparoscopic-assisted ovariohysterectomy (LaOVH) has been described in several studies,5,10,11,13–16 ovariectomy is still the preferred technique and has been recommended to be the technique of choice, even in open surgery.15,17–20 Laparoscopic-assisted treatment of pyometra was first described in 1997 by Minami et al.21 Over the last 10 years, 3 additional reports were published on that topic. The publication by Adamovich-Rippe et al22 describes safe diameters for the enlarged uterus in dogs with pyometra and guidelines for selecting possible cases for LaOVH. According to their results, a diameter of < 2 cm was safe in dogs below 10 kg of body weight, and in larger dogs, the uterine diameter should be below 4 cm. Two more recent papers23,24 describe different single-port techniques, but so far, none of those studies did compare the minimally invasive approach to a standard open ovariohysterectomy in dogs with pyometra. Therefore, the objective of this study was to evaluate the effects of LaOVH in dogs presented with pyometra on surgery time, perioperative pain, need for rescue analgesia, recovery, C-reactive protein (CRP), and postoperative complications, compared to conventional surgery (ie, open surgery [OS]).
Methods
Study design and animals
Between June 1, 2016, and December 31, 2019, all dogs diagnosed with pyometra were prospectively enrolled in this study if the patients were stable and if the ultrasonographical (Logiq E9; GE) measured diameter of the uterus did fit into the following categories. Uterine diameter in dogs between 5 and 15 kg should be below 2 cm, in dogs between 15 and 35 kg should be below 3 cm, and in dogs above 35 kg of body weight should be < 4 cm. Results of the general physical examination were recorded, and CBC and biochemical profile as well as CRP were analyzed. Ethical approval was provided by the Jordbruksverket (Swedish Authority) with the diary No. C42/16. An informed owner consent form was signed by the owners at the time of inclusion. Thereafter, all suitable patients were randomly assigned to one of the treatment groups, LaOVH or OS, by a coin toss.
Anesthetic protocol
The same standardized anesthetic protocol was used in both groups. After preoxygenation, patients were premedicated IV with 0.5 mg/kg diazepam (Diazedor vet [5 mg/mL]) and 0.5 mg/kg methadone (Insistor vet [10 mg/mL]). Induction was performed IV with propofol (PropoVet Multidose [10 mg/mL]) to effect. Patients were endotracheally intubated, and anesthesia was maintained with isoflurane in oxygen using a rebreathing circuit. Meloxicam (Metacam för hund och katt [5 mg/mL]) was administered SC with a dose of 0.2 mg/kg shortly after induction. Intraoperative monitoring included capnography, pulse oximetry, ECG, noninvasive blood pressure, and temperature every 5 minutes. If deemed necessary by the attending anesthesiologist, intraoperative rescue analgesia could be provided in 0.1-mg/kg increments of methadone.
Surgery
All surgeries were performed by the same surgeon, experienced in both laparoscopic and OS. Different staff members were assisting with holding instruments in the LaOVH group, but they were not performing any active parts of the surgery. In both groups, the abdomen was aseptically prepared and patients were transferred to the surgical suite, where they were positioned in dorsal recumbency and connected to a ventilator (Care station 650; GE). Ventilation was set to a pressure-controlled mode, starting with an inspiratory pressure of 10 cm H2O. Frequency was adjusted to keep the end-tidal carbon dioxide between 35 and 45 mm Hg. Abdominal access was performed in the LaOVH by a visual entry technique described by Anderson and Fransson25 in the umbilicus with the help of a 6-mm Ternamian Endotip trocar (Karl Storz) in combination with a 5-mm, 30° laparoscope (Karl Storz). Insufflation was set to a pressure of 8 mm Hg and a flow rate of 1.5 L/min. After the selected pressure was reached, a second 6- or 12-mm Ternamian Endotip trocar (Karl Storz) was placed under direct visualization with the endoscope at the level of the bladder apex.
With both ports in position, patients were rotated manually into an about 45° right lateral recumbency to allow visualization of the left ovary. The proper ligament was grasped with an endoscopic grasping forceps (CLICKline Dissecting and Grasping Forceps; Karl Storz) and lifted toward the ventral abdominal wall. A needle-suture combination was percutaneously inserted under visual guidance through the bursa to allow temporary fixation of the left ovary toward the abdominal wall. The suture was fixated with a hemostat on the outside as close to the body wall as possible. The endoscopic grasping forceps was exchanged with a 5- or 10-mm Caiman handpiece (Aesculap), and the suspensory ligament, ovarian pedicle, and mesometrium were sealed and transected with the help of the vessel-sealing device (VSD). The mesometrium was transected as far caudally as the elevated uterus allowed. The suture was released and pulled out from the abdomen, allowing the left ovary and uterus to be free in the abdomen. The same procedure was performed on the right side after turning the patient into 45 degrees left lateral recumbency. After completing the right side, the patient was turned back into dorsal recumbency. In contrast to the left side, the ovary was still fixed to the abdominal wall with the help of the percutaneously placed needle-suture combination. The Caiman VSD was exchanged with the endoscopic grasping forceps, and the right ovary was grasped.
An Alexis wound retractor (AWR; Alexis Wound Retractor [small, 2.5 to 6.0 cm]; Applied Medical) was prepared by placing a mosquito forceps through both rings. A skin incision approximately the length of the preoperatively measured diameter of the uterus was made with a No. 10 blade starting at the level of the caudal port and extending cranially. Thereafter, the carbon dioxide insufflation was turned off; the caudal trocar was removed from the abdomen, leaving the endoscopic grasping forceps in place; and a full-thickness incision was performed at the level of the previous skin incision with the help of Mayo scissors along the endoscopic grasping forceps under visual guidance. The right ovary was exteriorized and grasped with the mosquito forceps, preplaced through the AWR. At that time point, the needle-suture combination was pulled out, the endoscopic grasping forceps was removed, and the green interior ring of the AWR was inserted into the abdominal cavity. The remaining device was rolled down on itself to expand the abdominal incision into a round opening. The entire uterus was then exteriorized through the AWR, and a modified Miller’s knot and 1 transfixing suture on each side were performed with poliglecaprone suture of appropriate size caudal to the cervix before transection of the uterine body. The abdominal incisions were routinely closed in 3 layers.
Open ovariohysterectomy was performed with the same anesthesia protocol and settings of the anesthesia machine. A standard midline skin incision was performed, starting slightly cranial to the umbilicus. Electrocautery was used for hemostasis of larger vessels in the subcutis, but held to a minimum. After entering the abdominal cavity, digital transection of the suspensory ligament of the left ovary was performed with a caudomedially directed force. A 2-clamp technique was used on the ovarian pedicle and ligation performed with 1 sliding knot and appropriately sized poliglecaprone suture material. This was followed by ligation and transection of the right pedicle in the same manner. The uterine body was ligated with the same technique as described for the LaOVH group, and abdominal closure was routine in 3 layers.
In both groups, the following variables of interest were monitored: time for placement of both ports in the LaOVH group or time for surgical incision in the OS group, both starting when the scalpel blade first touched the skin. Other variables were the time for sealing and transection or ligation of the left and right ovarian pedicles (including temporary percutaneous fixation in the LaOVH group and digital transection of the suspensory ligament in the OS group) and ligation and transection of the uterine stump (including placement of the AWR in the LaOVH group) as well as closure time. Total surgery time was defined as the time from the scalpel first touching the skin until the placement of the last suture was finished. All measurements were recorded in minutes. In addition, all intraoperative complications as well as technical difficulties in the LaOVH group were recorded. Finally, total incision length, combining both incisions in the LaOVH group, was measured in both groups with a linear ruler before protecting the surgical site with an absorbent dressing.
Postoperative care and monitoring
At the time when the anesthesia gas was turned off, all patients received 0.1 mg/kg of methadone once IM, and the postoperative serum sample for CRP analysis was taken. Pain scoring according to a short form of the Modified University of Melbourne Pain Scale was started at 2, 4, 8, 12, 16, and 24 hours after surgery. Patients were housed in the intensive care unit during the 2 days after the surgical procedure to assure continuous monitoring by nurses trained in pain scoring. Rescue analgesia with 0.2 mg/kg of methadone IM was provided in case the patients scored higher than 6.26 Meloxicam was provided orally according to body weight once daily 24 and 48 hours postoperatively. Additional serum samples for CRP analysis were collected 24 and 48 hours after the initial sample, as a marker for surgical trauma and inflammation.
Furthermore, the recovery period was assessed, including time to standing and time to the first water and food intake. Water and food were provided when patients stood up the first time. All patients were discharged on day 2 after surgery, and a recheck examination was planned for the time of suture removal, to record for any medium-term complications postoperatively.
Statistical analysis
Statistical analysis was performed with Prism Windows 5 (Graph Pad Software). Normality was analyzed by the D’Agostino & Pearson normality test. Data are presented as median and range. Differences in results for variables of interest were compared between groups using the Mann-Whitney U test, except the number of dogs requiring rescue analgesia was analyzed via the Fisher exact test, and OR and 95% CIs were presented. Values of P ≤ .05 were considered statistically significant.
Results
Signalment and clinical presentation
In total, 12 female dogs could be included in the study. One dog from the LaOVH group was excluded from analysis, since there was a scant amount of free abdominal fluid leaking from the left salpinx tube and moderate peritonitis detected after insufflation was started. This patient was converted to OS to allow adequate lavage of the abdominal cavity and excluded from further analysis.
Median body weight of the remaining 5 dogs was 22.0 kg (range, 7.0 to 40.0 kg) in the LaOVH group and 17.9 kg (range, 7.6 to 39.0 kg) in the OS group (P = .792). Median age in the LaOVH group was 97.0 months (range, 90.0 to 104.0 months) and 99.5 months (range, 78.0 to 124.0 months) in the OS group (P = 1.000). Breeds included 9 purebred dogs and 3 mixed-breed dogs.
The most common clinical signs were vaginal discharge (n = 10), lethargy (8), anorexia (6), and polyuria/polydipsia (5). None of the patients presented due to fever.
Diagnostic evaluation
Results of a CBC before surgery showed mild to moderate leukocytosis in 6 patients (median, 25.5 X 103/μL; range, 22.5 X 103 to 34.7 X 103/μL; reference interval, 6 X 103 to 17 X 103/μL), monocytosis in 4 (median, 3.6 X 103/μL; range, 2.3 X 103 to 4.3 X 103/μL; reference interval, 0.2 X 103 to 1.4 X 103/μL), and mild thrombocytopenia in 1 (110 X 103/μL; reference interval, 150 X 103 to 500 X 103/μL). Results for serum biochemical profiles were unremarkable for all patients, except for 1 dog with high serum alanine aminotransferase activity (180.7 U/L; reference limit, < 84.4 U/L).
Abdominal ultrasonography confirmed a fluid-filled uterus in all dogs. Median uterine diameter was 2.2 cm (range, 0.9 to 3.5 cm) in the LaOVH group and 1.6 cm (range, 1.2 to 3.1 cm) in the OS group (P = .359).
Surgical time
Total surgery time in the LaOVH group was significantly longer, with a median surgery time of 37 minutes (range, 24 to 44 minutes) compared to 22.5 minutes (range, 18 to 26 minutes) in the OS group (P = .017). Looking into each step of surgery, there was a significant difference in the time needed for port placement in the LaOVH group (5 minutes; range, 3 to 9 minutes) compared to a median time for the surgical incision of 1 minute (range, 1 to 2 minutes) in the OS group (P = .007). Furthermore, the time for the ligation of the uterine body was significantly longer in the LaOVH group, with a median of 6 minutes (range, 4 to 8 minutes), compared to a median of 2 minutes (range, 2 to 4 minutes) in the OS group (P = .011). There was no significant difference between the time for ligation or respective sealing and transection of the ovarian pedicles and mesometrium, as well as for the closure time (Table 1).
Comparison (Mann-Whitney U test) of results for surgical variables for 11 dogs with pyometra treated with laparoscopic-assisted ovariohysterectomy (LaOVH; n = 5) versus open-surgery (OS; 6) ovariohysterectomy between June 1, 2016, and December 31, 2019.
| Variable | LaOVH | OS | P value |
|---|---|---|---|
| Total surgical time (min) | 37 (24–44) | 22.5 (18–26) | .017 |
| Time for surgical incision (min) | 5 (3–9) | 1 (1–2) | .007 |
| Time for left ovary removal (min) | 2 (2–9) | 2 (1–3) | .245 |
| Time for right ovary removal (min) | 3 (2–5) | 3.5 (1–4) | .777 |
| Time for ligation of the uterus (min) | 6 (4–8) | 2 (2–4) | .011 |
| Time for closure (min) | 8 (10–12) | 11 (9–12) | .497 |
| Length of incision (mm) | 38 (26–56) | 106 (85–142) | .004 |
Data reported as median and range.
Total incision length
Total incision length was significantly shorter in the LaOVH group, with a median of 38 mm (range, 26 to 56 mm) compared to 106 mm (range, 85 to 142 mm) in the OS group (P = .004).
Pain scores and rescue analgesia
Rescue analgesia during surgery was required by 2 dogs in the OS group at the time of digital transection of the left suspensory ligament and by 1 patient in the LaOVH while lifting the left ovary (P = .455; OR, 6.1; 95%CI, 0.2 to 162.9). Postoperative rescue analgesia due to pain scores > 6 was required for 3 dogs in the OS group at 4 time points; all of those had a pain score of 7, whereas none of the dogs in the LaOVH needed additional postoperative analgesia (P = .1818; OR, 11; 95%CI, 0.4 to 284.5). Nevertheless, pain scores including the dogs with rescue analgesia were not statistically significantly different between the 2 groups throughout all time points (Table 2).
Comparison (Mann-Whitney U test) of pain scores (Melbourne pain scale) after surgery for the dogs described in Table 1.
| Time after surgery (h) | LaOVH | OS | P value |
|---|---|---|---|
| 2 | 2 (0–6) | 0.5 (0–5) | .399 |
| 4 | 2 (0–6) | 4 (0–7) | .508 |
| 8 | 2 (0–2) | 2.5 (0–5) | .742 |
| 12 | 2 (0–2) | 5.5 (0–7) | .324 |
| 16 | 1.5 (1–2) | 3 (0–7) | .329 |
| 24 | 1.5 (0–3) | 2 (0–5) | .743 |
See Table 1 for key.
Recovery period
No significant difference between any of the recovery variables, including time to extubation, time to stand up, time to drink, and time to eat, was observed (Table 3).
Comparison (Mann-Whitney U test) of results for recovery variables for the dogs described in Table 1.
| Time from surgery completion to recovery variable (min) | LaOVH | OS | P value |
|---|---|---|---|
| Time to extubation | 22 (13–74) | 32.5 (17–62) | .783 |
| Time to stand | 116 (55–200) | 187.5 (59–455) | .537 |
| Time to drink | 210 (57–255) | 369 (110–1,650) | .082 |
| Time to eat | 140 (57–271) | 445 (74–1,060) | .421 |
See Table 1 for key.
Intra- and postoperative complications and technical difficulties
In 1 dog in the LaOVH group, problems occurred with insertion of the cranial portal, which prolonged the procedure time by 6 minutes. In another dog of the LaOVH group, it was not possible to reach the left ovary before the patient was positioned in nearly complete right lateral recumbency. In addition, leakage of carbon dioxide from the caudal portal was observed in 1 patient due to a defective rubber valve of the trocar. This was in the patient with the longest procedure time of 44 minutes.
The only reported complication was a surgical site infection in a dog in the OS group 4 days after surgery, which resolved after empirical antimicrobial treatment until the time of suture removal.
CRP—Serum CRP concentrations were initially high in all but 1 dog, with no difference between groups (P = .464). Also, postoperative CRP concentrations remained high without statistically significant differences between groups at the time of discharge (Table 4).
Comparison (Mann-Whitney U test) of results for perioperative serum C-reactive protein (CRP) concentration (μg/mL) for the dogs described in Table 1.
| Timing of CRP measurement | LaOVH | OS | P value |
|---|---|---|---|
| Preoperative | 114 (18–300) | 60 (10–412) | .464 |
| Immediately postoperative | 90 (19–280) | 59 (33–291) | .662 |
| 24 h postoperative | 144 (52–197) | 169 (72–306) | .410 |
| 48 h postoperative | 91 (33–182) | 96 (32–263) | .792 |
See Table 1 for key.
Outcome
All dogs survived to discharge, and all dogs were hospitalized for an additional 2 days postoperatively according to the study protocol. Besides 2 dogs, all returned for suture removal between 10 and 14 days; the remaining 2 dogs got the sutures removed at the local veterinarian. Both veterinarians provided images of the incision site at the time of suture removal for evaluation, and a telephone follow-up with the owner was undertaken a few days later.
Discussion
The results of this prospective case series confirm the results from the previous study that LaOVH can be safely performed in stable dogs affected by pyometra with a slight modification of the previously published recommendations by Adamovich-Rippe et al.22 Dogs were included if their maximal uterine diameter was below 2 cm in dogs between 5 and 15 kg and < 3 cm in dogs between 15 and 35 kg and if the uterine diameter was ≤ 4 cm in dogs above 35 kg. Uterine diameters were comparable in both groups. Compared to the previous 4-port, 3-port, and single-port techniques, a 2-port technique was successfully used in this study. But besides the fact that LaOVH can be safely performed in stable dogs with pyometra, none of the previous studies evaluated the benefits of a laparoscopic approach in terms of surgery time, pain, and recovery. Previously well-described benefits for routine laparoscopic sterilization are decreased postoperative pain and surgical stress4,5,27 as well as potentially fewer surgical site infections.28
All the procedures in this short case series were executed by the same specialized surgeon, with extensive experience in both open and laparoscopic procedures. In addition, the anesthetic protocol was identical, trying to keep all variables as comparable as possible in a clinical setting. While healthy dogs in earlier studies4,5 required less postoperative analgesia with LaOVH compared to open ovariohysterectomy, it was not possible with the current study to demonstrate a significant difference in postoperative pain or need for rescue analgesia in dogs with pyometra. This is similar to results from 2 more recent studies,29,30 where the authors also were not able to see a difference in the need for pain medication comparing open ovariohysterectomy to LaOVH in healthy dogs. Nevertheless, there was need for rescue analgesia at 4 time points in the OS group, compared to none in the LaOVH group. Possibly a larger cases series would be able to detect a significant difference between the 2 groups regarding postoperative pain and need for rescue analgesia.
As expected, the surgical incision was statistically significant longer in the OS group compared to the LaOVH group. On the other hand, the surgical time was statistically longer in the LaOVH group compared to the OS group. Although a median surgical time of 37 minutes in the LaOVH group is comparatively short, especially in comparison to the previously reported surgical times for LaOVH in pyometra with a median of 43, 85, and 107 minutes,22–24 it is still more than 50% of the median surgical time for OS. Time to access the abdomen was significantly longer in the LaOVH group, compared to a standard surgical incision. Furthermore, time for ligation of the uterine body took significantly longer in the LaOVH group compared to the OS group. Regardless, there were no significant differences between groups for other surgical or recovery variables.
No intraoperative complications were observed in the OS group. On the other hand, technical difficulties specifically related to the laparoscopy equipment occurred in the LaOVH group. None of those required an emergency conversion to OS. Similarly, more intraoperative complications were reported by Davidson et al27 comparing laparoscopic ovariohysterectomy to open ovariohysterectomy in healthy dogs.
Previous studies2,28 have suggested a decreased risk for surgical site infections with minimally invasive surgery. One medically treated surgical site infection was observed in the OS group, and none were observed in the LaOVH group. Due to the small number of patients in this case series, it is not possible to draw any general conclusions from this finding.
CRP is an acute-phase protein synthesized in the liver. In general, CRP has been used as a marker for the severity of inflammation and surgical trauma in several previous studies.31 A previous study32 has shown that CRP is a useful biomarker in differentiating dogs with pyometra from dogs with cystic endometrial hyperplasia. Furthermore, a study by Krzyzanowski et al33 could demonstrate that CRP was increased in all dogs with pyometra. In contrast to the results from a study34 comparing open prophylactic gastropexy in dogs to laparoscopic-assisted prophylactic gastropexy, it was not possible in the current case series to use CRP as a marker for the severity of surgical trauma. One explanation might be the fact that CRP is already elevated at the beginning of the procedure due to the primary disease, and this overlaps with the surgical trauma, making separate evaluations impossible. On the other hand, CRP was not different in a previous study29 comparing open OVH versus LaOVH in healthy dogs.29 Similarly, contradictory results were reached in 2 studies comparing CRP concentrations at the time of presentation in dogs with pyometra. The initial CRP concentration was not associated with a prolonged hospitalization in the study by Jitpean et al,35 whereas in the study by Fransson et al,36 a clear relationship between the severity of systemic inflammatory response syndrome and prolonged hospitalization and initial CRP concentration was detected. Unfortunately, in the latter studies, CRP was not monitored throughout hospitalization. The results from the present case series suggested that CRP is not an optimal marker for predicting time of hospitalization, since none of the patients had normal CRP at the time of discharge 48 hours after surgery. Furthermore, CRP concentration did not differ significantly between the 2 groups of this study, calling into question the reliability of that variable for monitoring the severity of postoperative inflammation and surgical trauma in clinical patients with pyometra.
The biggest limitation of this study is the low number of patients. This is owed to the challenge of acquiring cases fitting the inclusion criteria and having supportive staff available for anesthesia and laparoscopy equipment as well as postoperative care. Due to the fact that all patients with pyometra are presented as an emergency, it was difficult to free the same specialized surgeon with a busy surgical schedule in a nonteaching hospital in combination with a limited number of staff. This made the acquisition of patients very challenging. In addition, many patients had to be excluded since they were not deemed stable, had free abdominal fluid, or were on concurrent medication due to coexisting disease, which would have made equal comparison of all required variables impossible. A further limitation is the fact that the ovarian pedicles were ligated in the OS group, instead of sealed and transected with a Caiman VSD. The use of a VSD in both groups would have dramatically increased the costs of the study. Another limitation is the fact that pain scoring was performed by different personnel, which might have influenced the results. This is unfortunately inevitable in a clinical setting and with an observational period of 48 hours. On the other hand, this did account similarly for both groups and reflects the reality in the best possible way. In addition, none of the observers were blinded to the type of surgery, since they had full access to the journal records at the time patients were hospitalized. A final limitation is that all surgeries were performed by a specialist surgeon already very experienced in laparoscopic surgery. Therefore, the surgical times and complications might actually be higher than reported in this study in less experienced hands.
In summary, this prospective study was not able to clearly demonstrate the same benefits for LaOVH in dogs presented with pyometra as previously reported in elective sterilization in dogs. Although less patients in the LaOVH group required rescue analgesia, this was not statistically significant, and surgical time was more than 50% longer. In addition, LaOVH required an assistant, which dramatically increases the costs for that procedure. Furthermore, technical difficulties occurred in the LaOVH group, all specifically related to the equipment. Even though LaOVH is an equally safe and effective procedure for treatment of pyometra in dogs, it does not seem to be superior over traditional OS in clinical patients with pyometra at this point. Further studies with a larger caseload including surgeons with different levels of experience are necessary to evaluate the potential benefits of LaOVH in dogs with pyometra.
Acknowledgments
Part of the study was presented at the Veterinary Endoscopy Society Congress in Sorrento, Italy, July 2023.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.
Funding
The authors have nothing to disclose.
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