Abstract
This retrospective report describes perioperative and short-term postoperative complications of gastrointestinal biopsies obtained via a laparoscopic-assisted technique compared with laparotomy in a population of 60 client-owned dogs and cats with naturally occurring gastrointestinal disease. The medical records were examined for patients that underwent surgery for diagnostic gastrointestinal biopsies. Data were collected regarding perioperative complications such as hypotension, hypercarbia, and hypoxemia, and short-term postoperative complications including seroma and incisional infection/inflammation. The perioperative complication rate was 17.6% for the laparoscopically assisted group and 16.6% for the control group. The short-term postoperative complication rate was 5.9% for the laparoscopically assisted group and 0% for the control group. There was a 0% rate of intestinal dehiscence. There were no statistically significant differences in complication rates between the 2 groups, showing that laparoscopic-assisted gastrointestinal biopsies can be performed with acceptable perioperative and short-term postoperative complication rates.
Résumé
Comparaison des complications péri-opératoires et postopératoires à court terme découlant des biopsies gastro-intestinales à l’aide d’une technique assistée par laparascopie par rapport à la laparotomie. Ce rapport rétrospectif décrit les complications péri-opératoires et postopératoires à court terme de biopsies gastro-intestinales obtenues à l’aide d’une technique assistée par laparascopie comparativement à une laparatomie dans une population de 60 chiens et chats appartenant à des clients présentant une maladie gastro-intestinale naturelle. Les dossiers médicaux ont été examinés pour les patients qui ont subi une chirurgie pour des biopsies gastro-intestinales de diagnostic. Les données ont été recueillies concernant les complications péri-opératoires, comme l’hypotension, l’hypercarbie et l’hypoxémie ainsi que les complications postopératoires à court terme, incluant le sérome et l’infection/inflammation de l’incision. Le taux de complication péri-opératoire était de 17,6 % pour le groupe assisté par laparoscopie et de 16,6 % pour le groupe témoin. Le taux de complication postopératoire à court terme était de 5,9 % pour le groupe assisté par laparascopie et de 0 % pour le groupe témoin. Le taux de déhiscence intestinale était de 0 %. Il n’y avait aucune différence statistique des taux de complication entre les deux groupes, ce qui indique que les biopsies gastro-intestinales assistées par laparoscopie peuvent être réalisées avec des taux acceptables de complications péri-opératoires et postopératoires.
(Traduit par Isabelle Vallières)
Introduction
Laparoscopy is gaining momentum as a standard of care for certain minimally invasive diagnostic and therapeutic procedures, including laparoscopic-assisted gastrointestinal and liver biopsies, gastropexy, ovariectomy, and other diagnostic biopsies. Other procedures such as laparoscopic adrenalectomy, cholecystectomy, and cystotomy are quickly gaining popularity among surgeons due to benefits including decreased morbidity and decreased hospital stays (1–11).
There is sparse information on the complication rates for laparoscopic procedures, specifically laparoscopically assisted gastrointestinal biopsies. Previous studies have focused on the description of techniques, post-operative pain scores, and complication rates in small numbers of patients (1–9). As far as perioperative complications are concerned, the rate of conversion to laparotomy has been reported to be 21% in one study of 54 dogs and 40 cats (10). A few studies have reported on short-term complication rates of ovariectomy, adrenalectomy, and gastropexy (3–6,8). Minimally invasive surgery has been reported to have a 1.7% surgical site infection rate compared to 5.5% for open surgery (11).
Gastrointestinal biopsies are routinely performed in small animal practice to obtain a definitive diagnosis of inflammatory, infectious, and neoplastic conditions by obtaining representative samples from multiple areas of the gastrointestinal tract. One previous study showed a 12% intestinal dehiscence rate in the immediate postoperative period for full-thickness diagnostic intestinal biopsies in dogs (12). Studies of full-thickness gastrointestinal surgeries of any kind have reported intestinal dehiscence rates of 0% to 15.7% with more recent studies reporting lower complication rates, especially in cats (13–16).
To the authors’ knowledge there are no studies evaluating the perioperative complication rate of laparoscopically assisted diagnostic gastrointestinal biopsies performed in animals with naturally occurring gastrointestinal disease. Nor is there any comparison of the complication rates of these minimally invasive techniques with those of conventional approaches. The objectives of this study were to determine the perioperative and short-term postoperative complication rates of laparoscopic-assisted gastrointestinal biopsies and compare these rates to those of dogs and cats that underwent gastrointestinal biopsies via a laparotomy. Our hypothesis was that a laparoscopically assisted technique for obtaining biopsy samples for gastrointestinal disease is associated with a lower complication rate than for biopsy samples obtained by laparotomy.
Materials and methods
Case selection
The electronic medical records of the Animal Specialty Center were retrospectively reviewed to identify dogs or cats that underwent gastrointestinal biopsies either via laparotomy or laparoscopic-assisted methods between August 1, 2008 and April 30, 2014. Cases were excluded if there were incomplete medical records including the anesthetic record, comprehensive gastrointestinal biopsies with histopathologic diagnosis, and lack of either telephone or in-hospital follow-up 10 to 14 d after surgery.
Medical records review
Retrieved data from medical and anesthetic records included signalment, weight, age, preoperative total protein level, surgical time for the gastrointestinal biopsies, and whether a second unrelated surgical procedure was performed during the same anesthetic event as the biopsies and the type of second procedure. The histopathologic diagnosis of the gastrointestinal biopsies, the lowest body temperature recorded during anesthesia, and perioperative and postoperative complications were also recorded. All surgeries were performed by an American College of Veterinary Surgeons (ACVS) diplomate or by a resident under direct supervision of an ACVS diplomate. Anesthetic drugs were used at the discretion of the surgeon, but consistently contained an opiate and benzodiazepate premedication prior to induction, propofol for induction, and isoflurane inhalant anesthetic. Perioperative complications assessed were hypotension [mean arterial pressure (MAP) < 60 mmHg for 3 consecutive readings 5 min apart], hypercarbia (end-tidal CO2 > 45 mmHg for 3 consecutive readings 5 min apart), and hypoxemia (oxygen saturation < 95% measured via pulse oximetry for 3 consecutive readings 5 min apart) during the anesthetic event. Perioperative complications were considered minor if they were resolved with routine intraoperative adjustments and major if there was conversion or alteration of the surgical procedure. Medical records were evaluated for follow-up information for at least 2 wk after surgery for any incisional or systemic short-term complications that could be attributed to the surgery. A complication was defined as minor if it was outside the realm of normal healing and included incisional complications such as infection or inflammation resolving without surgical intervention. A complication was defined as major if a second surgical procedure was required for treatment of the complication.
Laparoscopic-assisted exploratory surgery and biopsy
A 5-mm camera port was placed in the ventral midline 2 to 3 cm caudal to the umbilicus. A 5 mm × 29 cm zero degree laparoscope (Karl Storz Veterinary Endoscopy; Goleta, California, USA) was inserted into the camera port and 5-mm instrument ports were inserted in the right and left cranial quadrants at the approximate level of the 13th rib. Insufflation pressures were maintained under 10 mmHg for cats and under 15 mmHg for dogs as described previously (17,18). A full laparoscopic exploratory examination of the gastrointestinal tract was performed by examining the cranial and caudal aspects of each liver lobe and evaluating the stomach, pancreas, and mesenteric lymph node and running the length of the small intestine intracorporeally to evaluate for any abnormalities. If abnormalities were noted, the area of interest was biopsied. For diffuse or nonspecific disease the following biopsy protocol was performed. The stomach was exteriorized through the left cranial port and a full thickness biopsy was taken. The site was closed with 4-0 polydioxanone (PDS; Ethicon, Somerville, New Jersey, USA) in 2 layers using a simple interrupted inverting suture pattern of the surgeon’s preference and locally lavaged. Multiple biopsies were taken of the liver from multiple lobes with cup biopsy forceps (Karl Storz Veterinary Endoscopy). The pancreas was biopsied from a free edge of the right limb with the punch biopsy forceps. The left cranial port was enlarged by 2 to 5 mm to allow the jejunum to be exteriorized and biopsied using a 3-mm punch biopsy instrument. The site was closed with 4-0 polydioxanone in a simple interrupted suture pattern and was lavaged with saline. A biopsy was taken of a representative part of the ileum in a similar fashion. A wedge biopsy was taken of a representative mesenteric lymph node if it could be safely obtained. The portal sites were closed in 2 layers using 3-0 polydioxanone for deep subcutaneous layers/abdominal fascia and 3-0 poliglecaprone 25 (Monocryl; Ethicon) in an intradermal suture pattern to close the skin. No external sutures were placed.
Exploratory celiotomy
A standard ventral abdominal approach to the peritoneal cavity was performed and the abdomen was thoroughly explored. Liver biopsy samples were obtained with either guillotine method or a punch biopsy and hemostasis was achieved with absorbable gelatin powder (Gelfoam; Pfizer, New York, New York, USA). An incisional biopsy of the pancreas and a mesenteric lymph node were obtained. A full-thickness gastric biopsy was obtained and closed in 2 layers with 4-0 polydioxanone using inverting suture patterns of the surgeon’s choice. Intestinal biopsies were obtained with a 3-mm punch and closed in 1 layer with 4-0 polydioxanone using a simple interrupted suture pattern. The laparotomy incision was closed in 3 layers using continuous suture patterns with appropriately sized polydioxanone for the ventral rectus sheath, and appropriately sized poliglecaprone 25 for the subcutaneous and intradermal layers. Skin staples were used at the discretion of the surgeon.
Statistical analysis
All statistical analyses were performed with commercially available statistical software (SPSS Statistics for Windows version 22; IBM Corp., Armonk, New York, USA). Continuous variables were tested for normality using the Shapiro-Wilk test. The mean and standard deviation were used to describe the variable if it had a normal distribution. The median and range were used if the variable was non-normally distributed. Categorical variables were described with frequencies and percentages. A comparison of the variables between laparoscopically assisted and laparotomy groups was made with a Student’s t-test or a Mann-Whitney U-test depending on whether the variable was normally distributed. Age, weight, anesthesia time, and preoperative total protein, presence of neoplasia, and surgical time were all compared. A comparison of perioperative and postoperative complications between laparoscopically assisted and laparotomy groups was assessed using a Mann-Whitney U-test. For all comparisons, significance was set at P ≤ 0.05.
Results
Laparoscopically assisted group
There were 39 patients that had laparoscopically assisted gastrointestinal biopsies during the study period. Five patients were excluded from analysis due to lack of anesthetic record or histopathologic diagnosis; 34 patients (29 feline and 5 canine) met the inclusion criteria for the laparoscopically assisted group. Demographic characteristics are given in Table 1. The breed distribution for the 29 cats was: 19 (66%) domestic short haired (DSH), 3 (10%) Persian, 2 (7%) each of Siamese and domestic long hair, and 1 (3%) each of Himalayan, Maine coon, and Bengal breeds. Of the 5 dogs, there were 1 each of the miniature dachshund, boxer, Havanese, standard poodle, and golden retriever breeds. A preoperative total protein of ≤ 60 g/L was noted in 7/32 (22%) cases. The mean surgical time for the procedure was 95.0 min (SD +/− 25.6 min). A second procedure was performed in 6/34 (18%) cases, all of which were placement of esophagostomy tubes. A diagnosis of neoplasia was made in 12/34 (35%) cases with small cell lymphoma comprising the majority of cases (10/12). One animal each was diagnosed with histiocytic sarcoma and lymphoblastic lymphoma. The most common intestinal diagnosis in cases without neoplasia was inflammatory bowel disease (IBD) (19/22). Liver biopsies revealed hepatic lipidosis (7/22) and cholangiohepatitis (4/22) with multiple animals having more than 1 histopathologic abnormality.
Table 1.
Clinical characteristics for patients that underwent laparoscopic-assisted surgery or laparotomy to obtain gastrointestinal biopsies.
| Laparoscopically assisted (n = 34) | Laparotomy (n = 24) | P-value | |
|---|---|---|---|
| Mean age (± SD) (y) | 9.3 (± 4.2) | 8.0 (± 5.0) | 0.36 |
| Median weight (range) (kg) | 4.4 (2.1 to 27) | 8.8 (2.3 to 26.6) | 0.27 |
| Mean total protein (± SD) (g/L) | 74 (± 14) | 72 (± 12) | 0.46 |
| Mean surgical time (± SD) (min) | 95 (± 25.6) | 74 (± 29.8) | 0.009 |
| Second procedure (n; %) | 6 (17%) | 12 (50%) | 0.009 |
| Neoplasia (n; %) | 12 (35.3%) | 8 (33.3%) | 0.88 |
SD — standard deviation.
Laparotomy group
There were 26 patients that had gastrointestinal biopsies via open laparotomy during the study period. Two patients were excluded due to lack of anesthetic records or histopathologic diagnosis, leaving 24 patients (13 feline and 11 canine) which met the inclusion criteria. Demographic characteristics are given in Table 1. Breed distribution for the 13 cats was: DSH 11 (85%) with 1 (8%) ragdoll and 1 domestic long-hair. Of the 11 dogs, 3 (27%) were mixed breed, 2 (18%) were shih tzu, and there were 1 (9%) of each of the following breeds: miniature poodle, golden retriever, Labrador retriever, dachshund, Great Pyrenees, and schnauzer. A preoperative total protein of ≤ 60 g/L was noted in 4/24 (17%) cases. The mean surgical time for the procedure was 76 min (SD +/− 29 min). Second procedures performed in 11/24 animals included: gastrostomy tube placement (n = 2), splenectomy (n = 2), esophagostomy tube placement (n = 2), cholecystectomy (n = 2), liver lobectomy (n = 1), enterotomy for foreign body removal (n = 1), and duodenal resection and anastomosis for treatment of an obstructive mass (n = 1). A diagnosis of gastrointestinal neoplasia was made in 6/24 cases, with small cell lymphoma (4/6) being the most common neoplastic diagnosis followed by histiocytic sarcoma (1/6), and mixed cell lymphoma (1/6). One dog was diagnosed with an undifferentiated splenic sarcoma and 1 dog with a well-differentiated hepatocellular carcinoma based on histopathology of samples taken during the secondary procedure. The most common intestinal diagnosis in the cases that did not have neoplasia was IBD (17/24). Liver biopsies revealed hepatic lipidosis (7/24) and cholangiohepatitis (4/24) with multiple animals containing more than one histopathologic abnormality.
There were no significant differences in age, weight, preoperative total protein, presence of neoplasia, or whether a second procedure was performed. Animals undergoing laparoscopically assisted gastrointestinal biopsies had a significantly longer surgical time than animals undergoing laparotomy and gastrointestinal biopsies (Table 1).
Complications
Minor perioperative complications occurred in 6/34 (18%) animals that had laparoscopically assisted gastrointestinal biopsies and 4/24 (17%) animals that had laparotomy with gastrointestinal biopsies (Table 2). For the laparoscopically assisted group, 3/34 (8%) animals developed hypotension and 3/34 (8%) developed hypercarbia. All of the complications were seen in cats. For the laparotomy group, 3/24 (13%) animals developed hypotension and 1/24 (4%) developed hypoxemia. For the hypoxemia patients, 2 were dogs and 2 were cats. No animals in the laparotomy group developed hypercarbia. There was no significant difference in complications between the groups. There were no major perioperative complications resulting in conversion or changes to planned surgical procedure in either group.
Table 2.
Frequency of complications for animals undergoing laparoscopic-assisted or laparotomy techniques to obtain gastrointestinal biopsies
| Laparoscopically assisted (n = 34) | Laparotomy (n = 24) | P-value | |
|---|---|---|---|
| Perioperative complications (n; %) | 6 (17.6%) | 4 (16.7%) | 0.92 |
| Post-operative complications (n; %) | 2 (5.9%) | 0 (0.0%) | 0.23 |
| Total complications (n; %) | 7 (20.6%) | 3 (12.5%) | 0.42 |
Immediate postoperative complications occurred in 2/34 (6%) animals undergoing laparoscopically assisted gastrointestinal biopsies. No animals undergoing laparotomy for gastrointestinal biopsies had postoperative complications. The 2 minor complications in the laparoscopically assisted group included 1 case of excessive bruising at the surgical site in a 7-year-old spayed female DSH cat diagnosed with IBD, and post-operative pancreatitis that required extended hospitalization in a 4-year-old spayed female DSH cat diagnosed with IBD but with a histologically normal pancreas at surgery. A 10-year-old spayed female DSH cat from the laparotomy group died 4 d after surgery from an unrelated disease. There were no major short-term postoperative complications.
Discussion
Perioperative and short-term postoperative complications were not significantly different between the 2 groups. Although laparoscopic-assisted gastrointestinal biopsies were not associated with significantly lower complications, the overall complications of this technique were relatively low and comparable to those in the laparotomy group. It follows that a laparoscopic technique can be a safe and reasonable alternative to obtain full-thickness gastrointestinal biopsies in dogs and cats. The perioperative and short-term post-operative complication rates were relatively low and comparable to those in other studies. A prospective study by Rawlings et al (19) showed only 1 short-term incisional complication among 23 dogs undergoing gastropexy. Another prospective study revealed that minimally invasive surgery had a surgical site infection rate of 1.7%, significantly different from 5.5% for open laparotomy (11).
This study failed to support the hypothesis that laparoscopically assisted gastrointestinal biopsy techniques were associated with decreased complication rates compared with gastrointestinal biopsies via laparotomy. As a retrospective case series there can be inherent selection bias as clinicians recommended different surgical approaches for the gastrointestinal biopsies of their patients. The groups may therefore differ by unmeasured variables. Patients with concurrent morbidities that result in decreased healing potential or increased risk of other complications may have been preferentially placed into the laparoscopically assisted group. Additionally, patients that needed a second abdominal surgical procedure were preferentially placed into the laparotomy group. The laparoscopically assisted technique resulted in significantly longer surgery time compared to the laparotomy approach, which could have contributed to an increased risk of complications such as surgical site infection in the laparoscopically assisted group. Our experience supports data from human and veterinary literature that surgeon experience also affects surgical time (20). In this study, surgeons and surgical residents performing this procedure were at different stages in their training and it was not possible to discern whether increased surgical time was associated with experience. A recent study reported a learning curve of approximately 80 cases to become proficient in laparoscopic ovariectomy (20). The surgical time in this study could also have been confounded by the many secondary procedures performed in both groups. Univariable and multivariable statistical analysis to assess for factors contributing to complications was not performed due to the low incidence of complications, so it is not known if increased time was associated with increased complications in this study.
Laparoscopic and laparoscopic-assisted surgical approaches use smaller incisions and result in lower pain and faster return to function (3–7). Multiple controlled studies demonstrated a repeatable decrease in analgesic requirements and increased post-operative activity after laparoscopically assisted ovariohysterectomy compared with ovariohysterectomy via laparotomy (3–6). Two recent case series report that laparoscopic-assisted approaches and instrumentation for gastrointestinal procedures have potential benefits with regard to pain response (21,22); however, evaluation of pain response or complications was not within the scope of these case series. While there are no studies directly evaluating laparoscopically assisted gastrointestinal biopsies and response to pain, the same equipment and techniques are applied, thus it follows that these procedures are likely to be associated with decreased pain and improved outcome. Recent studies in human medicine on laparoscopic appendectomy and cholecystectomy report improved outcomes with the laparoscopic approach compared with laparotomy, further supporting this speculation (23,24).
To the author’s knowledge, this is the first study evaluating perioperative parameters during laparoscopic insufflations in patients with a natural disease. None of the animals included in the study experienced any major perioperative complications that precluded obtaining biopsies for histopathologic evaluation or resulted in premature conversion of the procedure. There was no significant difference in hypoxemia, hypercarbia, and hypotension during diagnostic laparoscopic insufflations with CO2 compared with laparotomy. These findings are consistent with previous reports on cats undergoing laparoscopic pancreatic biopsies (18) and dogs undergoing laparoscopic surgery (17).
The immediate postoperative complication rate for all animals included in this study was 3.4%, with the 2 minor complications including excessive bruising at the surgical site and post-operative pancreatitis. There were no complications that resulted in a second surgical procedure or any animal that showed clinical signs consistent with intestinal biopsy site dehiscence in either group. By defining immediate postoperative complication as within 2 wk of surgery, any evidence of intestinal biopsy site dehiscence should have been captured given that the common time frame for intestinal dehiscence is in the first 2 to 5 d following surgery (25). Shales et al (12) reported a dehiscence rate of 12% in dogs undergoing full-thickness biopsies for chronic intestinal disease, and there was a major complication in 3.8% of dogs undergoing intestinal biopsy in a report by Harvey et al (16). The absence of intestinal biopsy site dehiscence in this case series is consistent with more recent studies showing low numbers of animals experiencing intestinal biopsy site dehiscence (12–16).
The benefit of full-thickness biopsies has been demonstrated in multiple recent publications comparing endoscopic biopsies to surgical biopsies. In 1 study, a diagnosis of lymphoma was not achieved via endoscopic biopsies, indicating a need for thorough investigation and full-thickness biopsies of representative sites of the entire gastrointestinal tract (26). This study indicates that laparoscopically assisted exploratory surgery is acceptable to obtain these samples, as biopsies were attained in all patients and were all of diagnostic quality. In our institution, the same methods for obtaining all of the samples were used in laparoscopically assisted and laparotomy groups with the exception of the liver, for which a guillotine method was used for biopsies obtained via laparotomy and a cup biopsy forceps was used to obtain a similar volume in the laparoscopic procedure. The exception to obtaining all 6 biopsies (liver, pancreas, stomach, jejunum, ileum, and lymph node) in either group occurred when, at the discretion of the surgeon, the mesenteric and ileocolic lymph nodes were too small to safely sample without running a substantial risk of vascular compromise and obtaining a biopsy sample that was non-diagnostic.
Of the animals included in this study, 31% were diagnosed with a primary or metastatic neoplasia of the gastrointestinal tract. There were no major complications including intestinal biopsy site dehiscence, which throughout the older literature has been more prevalent in patients with neoplasia. The complication rate from this study was consistent with a recent study which evaluated full-thickness biopsies in cats with gastrointestinal lymphoma and reported no intestinal biopsy dehiscences in a population of 70 cats (13). Our data suggest that full-thickness small intestinal biopsies have a very low major complication rate in both dogs and cats with intestinal neoplasia.
There was no difference in complication rate and clinical healing related to protein level in this study. The overall protein level in this study was by refractometry. This is a limitation of the retrospective nature of this study when compared with historical data, as total protein comprises albumin and globulin and may be higher than albumin alone. Harvey et al (16) reported a 3.8% intestinal biopsy site dehiscence rate and a 40% minor complication rate in a population of hypoalbuminemic dogs undergoing intestinal biopsy, although the definition of normal concentration albumin varied throughout the study period. More recent studies also support the lack of relationship between complication rate and healing and hypoproteinemia in dogs and cats undergoing small intestinal biopsies, suggesting relative safety in obtaining full-thickness biopsies in the face of chronic gastrointestinal disease (13,15). Total protein level is routinely used in the preanesthetic workup in practice and is still of clinical relevance for patients with naturally occurring disease.
There are a few limitations to this study. This retrospective study relied on medical records for assessment of minor short-term complications, which may not have been recorded leading to underappreciation of these complications. Recheck visits were occasionally performed by different services in the hospital, which could have resulted in minor complications being overlooked. Furthermore, end tidal CO2 was not recorded in anesthesia records at our institution during the first year of data collection. This resulted in a decreased number of patients with these results to assess the effect of the laparoscopic-assisted approach on ventilation. While the hypercarbia present in the laparoscopy group was not significantly greater than in the laparotomy group, the sample size was low, potentially allowing for type 2 statistical errors on this and other statistics that were performed. The inclusion of both dogs and cats in this study may confound potential complications that may be unique to each of these species. Univariable and multivariable analyses were not performed due to the low numbers of patients that had complications. Prospective studies are needed to evaluate complications in naturally occurring disease states in patients receiving laparoscopic, laparoscopic-assisted, and open surgeries, as well as retrospective studies looking at dogs and cats separately.
This study showed that a laparoscopically assisted procedure to obtain gastrointestinal biopsies resulted in complication rates that were comparable to those for laparotomy gastrointestinal biopsies. Laparoscopic-assisted gastrointestinal biopsies are an alternative to laparotomy, providing a safe and effective method of obtaining full-thickness diagnostic samples of the stomach, small intestine, pancreas, liver, and lymph nodes. CVJ
Footnotes
Use of this article is limited to a single copy for personal study. Anyone interested in obtaining reprints should contact the CVMA office (hbroughton@cvma-acmv.org) for additional copies or permission to use this material elsewhere.
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