Evaluation of minimally invasive small intestinal exploration and targeted abdominal organ biopsy with use of a wound retraction device in dogs: 27 cases (2010–2017)

Shelly K. Shamir 1Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 5K2, Canada.

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Ameet Singh 1Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 5K2, Canada.

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Philipp D. Mayhew 2Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Jeffrey J. Runge 3Section of Surgery, Department of Clinical Studies–Philadelphia, Matthew J. Ryan Veterinary Hospital, School of Veterinary Medicine, University of Pennsylvania, Philadelphia, PA 19104.

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J. Brad Case 4Department of Small Animal Clinical Sciences, College of Veterinary Medicine, University of Florida, Gainesville, FL 32608.

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Michele A. Steffey 2Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Ingrid M. Balsa 2Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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William T. N. Culp 2Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Michelle A. Giuffrida 2Department of Surgical and Radiological Sciences, School of Veterinary Medicine, University of California-Davis, Davis, CA 95616.

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Jessica J. Kilkenny 1Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 5K2, Canada.

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Alex zur Linden 1Department of Clinical Studies, Ontario Veterinary College, University of Guelph, Guelph, ON N1G 5K2, Canada.

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Abstract

OBJECTIVE

To describe surgical technique, biopsy sample quality, and short-term outcome of minimally invasive small intestinal exploration and targeted abdominal organ biopsy (MISIETB) with use of a wound retraction device (WRD) in dogs.

ANIMALS

27 client-owned dogs that underwent MISIETB with a WRD at 1 of 4 academic veterinary hospitals between January 1, 2010, and May 1, 2017.

PROCEDURES

Medical records were retrospectively reviewed, and data collected included signalment; medical history; findings from physical, ultrasonographic, laparoscopic, cytologic, and histologic evaluations; surgical indications, procedures, duration, and complications; and short-term (14-day) outcomes. The Shapiro-Wilk test was used to evaluate the normality of continuous variables, and descriptive statistics were calculated for numeric variables.

RESULTS

Laparoscopic exploration was performed through a multicannulated single port (n = 18), multiple ports (5), or a single 6-mm cannula (4). Median length of the incision for WRD placement was 4 cm (interquartile [25th to 75th percentile] range, 3 to 6 cm). All biopsy samples obtained had sufficient diagnostic quality. The 2 most common histologic diagnoses were lymphoplasmacytic enteritis (n = 14) and intestinal lymphoma (5). Twenty-five of 27 (93%) dogs survived to hospital discharge, and 3 (12%) dogs had postsurgical abnormalities unrelated to surgical technique.

CONCLUSIONS AND CLINICAL RELEVANCE

Results indicated that MISIETB with WRD was an effective method for obtaining diagnostic biopsy samples of the stomach, small intestine, pancreas, liver, and mesenteric lymph nodes in dogs. Prospective comparison between MISIETB with WRD and traditional laparotomy for abdominal organ biopsy in dogs is warranted.

Abstract

OBJECTIVE

To describe surgical technique, biopsy sample quality, and short-term outcome of minimally invasive small intestinal exploration and targeted abdominal organ biopsy (MISIETB) with use of a wound retraction device (WRD) in dogs.

ANIMALS

27 client-owned dogs that underwent MISIETB with a WRD at 1 of 4 academic veterinary hospitals between January 1, 2010, and May 1, 2017.

PROCEDURES

Medical records were retrospectively reviewed, and data collected included signalment; medical history; findings from physical, ultrasonographic, laparoscopic, cytologic, and histologic evaluations; surgical indications, procedures, duration, and complications; and short-term (14-day) outcomes. The Shapiro-Wilk test was used to evaluate the normality of continuous variables, and descriptive statistics were calculated for numeric variables.

RESULTS

Laparoscopic exploration was performed through a multicannulated single port (n = 18), multiple ports (5), or a single 6-mm cannula (4). Median length of the incision for WRD placement was 4 cm (interquartile [25th to 75th percentile] range, 3 to 6 cm). All biopsy samples obtained had sufficient diagnostic quality. The 2 most common histologic diagnoses were lymphoplasmacytic enteritis (n = 14) and intestinal lymphoma (5). Twenty-five of 27 (93%) dogs survived to hospital discharge, and 3 (12%) dogs had postsurgical abnormalities unrelated to surgical technique.

CONCLUSIONS AND CLINICAL RELEVANCE

Results indicated that MISIETB with WRD was an effective method for obtaining diagnostic biopsy samples of the stomach, small intestine, pancreas, liver, and mesenteric lymph nodes in dogs. Prospective comparison between MISIETB with WRD and traditional laparotomy for abdominal organ biopsy in dogs is warranted.

Biopsy samples from abdominal organs are often obtained in small animal practice because histologic examination of such tissues is an integral diagnostic tool.1–3 Methods of collecting biopsy samples from the gastrointestinal tract include endoscopy for partial-thickness biopsy samples, ultrasonography for ultrasonographically guided needle biopsy samples, or traditional laparotomy or minimally invasive abdominal surgery for full-thickness biopsy samples.1–7 Flexible endoscopic gastrointestinal biopsy is commonly performed, and advantages of this method include its minimally invasive nature, lesion-targeted sampling, and short duration of anesthesia.1,8,9 However, disadvantages include the inability to safely sample deeper than the mucosa layer, limited range of access to portions of the gastrointestinal tract, additional skills required of the operator, and the potential for inadequate diagnostic quality of samples.1,8,9 Results from histologic evaluation of full-thickness biopsy samples are the gold standard in differentiation between infiltrative diseases of the gastrointestinal tract10; however, full-thickness biopsy samples of the gastrointestinal tract cannot be obtained with flexible endoscopy. Therefore, advantages of laparotomy include the ability to visually assess and palpate the entire gastrointestinal tract and other abdominal organs and to obtain full-thickness biopsy samples.

Minimally invasive surgery is commonly performed in veterinary practice11 and has many patient benefts.12–18 Recent reports4,5,19,20 describe minimally invasive laparoscopic-assisted abdominal organ biopsy as a less invasive option, compared with traditional laparotomy for biopsy. The purpose of the case series presented here was to retrospectively describe surgical technique, biopsy sample quality, and short-term outcome of MISIETB with use of a WRD in dogs.

Materials and Methods

Case selection criteria

Medical records of dogs that underwent MISIETB at 4 academic institutions between January 1, 2010, and May 1, 2017, were retrospectively reviewed. Dogs were included in the study if a laparoscopic procedure was performed with a single- or multiport technique and followed by the use of a WRD for abdominal organ biopsy. Dogs in which the surgery was converted from a laparoscopic or laparoscopic-assisted approach to a laparotomy approach were included.

Medical record review

Data collected from the medical records included signalment; medical history; owner's primary complaint; clinical signs; results of abdominal ultrasonography; laparoscopic and laparoscopic-assisted procedures and duration (time from initial skin incision to abdominal closure); number of laparoscopic ports used (single port vs multiport); port type, location, and size; reason for conversion to laparotomy; laparotomy incision length; WRD placement location and size; other extra-abdominal surgical procedures performed during the same anesthetic period; intra- and postoperative complications; and short-term outcome (14-day postsurgical follow-up period). Intraoperative complications were defined as complications during the surgical procedure that required considerable deviation from the planned procedure. Postoperative complications were defined as any adverse events attributed to surgery or anesthesia and recorded in the medical records from the time of surgery to the recheck examination when the skin staples or sutures were removed. Short-term follow-up information from the time of surgery to 14 days after surgery was obtained from the medical records and referring veterinarians.

Surgical preparation

For each dog, premedication and induction agents used were at the discretion of the attending veterinary anesthesiologist, and general anesthesia was maintained with isoflurane or sevoflurane delivered in oxygen. Cefazolin (22 mg/kg [10 mg/lb], IV) was administered 30 minutes before the initial incision and every 90 minutes thereafter until the surgery was completed.

The ventral aspect of each dog's abdomen was clipped and aseptically prepared for a standard laparotomy. All dogs were positioned in dorsal recumbency. The surgical procedure was performed either by a board-certified veterinary surgeon or a surgery resident under direct supervision of a board-certified veterinary surgeon.

Laparoscopy

The decision to perform laparoscopy with a multicannulated single port, with a 6-mm trocar and cannula assembly single port, or with multiple ports was made at the discretion of the primary surgeon. In dogs that underwent single-port laparoscopy with a multicannulated flexiblea or stainless steelb device, an initial 2- to 3-cm midline incision through skin, subcutaneous tissue, and linea alba was made approximately 1 cm caudal to the umbilicus. The surgeon inserted a gloved index finger into the incision to ensure no adhesions of abdominal viscera were present and to liberate the falciform ligament. Through the incision, a multicannulated single-port device was inserted as previously described.7 In dogs that underwent single-port laparoscopy without a multicannulated port, a 6-mm threaded trocarc was placed approximately 1 cm caudal to the umbilicus with a modified Hasson technique21 and was used for an abbreviated abdominal exploration followed by removal of the trocar, enlargement of the portal incision, and placement of the WRD.

In dogs that underwent laparoscopy with multiple ports, abdominal access was obtained with a modified Hasson technique, with a camera portal established through a 6-mm trocar and cannula assemblyd caudal to the umbilicus. A 6-mm instrument portal was placed cranial (between the endoscopic portal and xiphoid process) and either 2 to 4 cm lateral to the camera portal or on the ventral midline with direct endoscopic observation.

In all dogs, pneumoperitoneum was established with CO2 and a pressure-regulating mechanical insufflatore to a maximum intra-abdominal pressure between 8 and 12 mm Hg. Either a 5-mm 0°f or 30°g 29-cm laparoscope was inserted into the abdomen.

At the surgeon's discretion, laparoscopic exploration of the abdomen may have been performed.7 Briefly, if laparoscopic exploration occurred, it proceeded in a clockwise manner, starting at the liver and diaphragm, continuing to the left abdominal gutter (with the dog tilted 45° in left dorsaloblique recumbency), the caudal abdominal region, and the right abdominal gutter (with the dog tilted 45° in right dorsaloblique recumbency).7 Laparoscopic Babcock forceps,h DeBakey forceps,i or a blunt probej inserted alone or in combination through an instrument portal were used to help move organs for abdominal exploration.

When indicated, laparoscopic liver biopsy was performed with 5-mm laparoscopic biopsy cup forceps,k and cholecystoscentesis was performed under direct laparoscopic guidance with a 20-gauge needle inserted percutaneously into the abdomen.22 Kidney biopsy, when indicated, was performed with a 14-gauge side-notch biopsy needlel inserted percutaneously into the abdomen under direct laparoscopic guidance.23 When elected, laparoscopic-assisted ovariohysterectomy was performed with a vessel-sealing devicem as previously described,21 and the ovaries and uterine body were removed after placement of the WRD. Following laparoscopic abdominal exploration and biopsy of targeted tissues, the laparoscopic port or ports were removed, and the pneumoperitoneum was purged.

Use of WRDs

A small incision to access the abdomen was made on the ventral midline at the level of the previous subumbilical port or centered between the xiphoid process and umbilicus. On the basis of incision length, an appropriately sized WRDn (either a WRD for incisions 2 to 4 cm long or a WRD for incisions 5 to 9 cm long) was selected and applied in accordance with the manufacturer's instructions (Figure 1).

Figure 1—
Figure 1—

Intraoperative image of a 24.0-kg (52.8-lb) dog undergoing MISIETB with a 5- to 9-cm WRD (arrow) in place in a 7-cm access incision made on the dog's ventral midline. A segment of the small intestine has been exteriorized through the WRD. Cranial is at the top of the image.

Citation: Journal of the American Veterinary Medical Association 255, 1; 10.2460/javma.255.1.78

A moistened, sterile gloved finger was inserted through the WRD, and a segment of bowel was grasped and exteriorized to facilitate exploration of the small intestine in a systematic manner. When indicated, full-thickness intestinal biopsy samples were taken from the antimesenteric aspect of the small intestine, and the site sampled was closed with 3–0 or 4–0 monofilament absorbable sutureo in a simple interrupted pattern. When indicated, a full-thickness incisional biopsy of the stomach was performed, and the biopsy site was closed with monofilament absorbable sutureo in a 2-layer, simple continuous (full-thickness) pattern followed by an inverting (seromuscular) pattern. Lymph node biopsy, when indicated, was performed by removing the desired lymph node en bloc with sharp and blunt dissection. When indicated, pancreatic biopsy was performed by grasping the pancreas and with sharp dissection removing the desired segment. Splenectomy, when indicated, was performed through the WRD as previously described.24

After intra-abdominal procedures were completed, the WRD was removed in accordance with manufacturer's instructions. The abdominal incision was closed routinely, with closure of the linea alba with a monofilament absorbable sutureo in a simple continuous suture pattern, closure of SC tissues with monofilament absorbable suturep in a continuous appositional suture pattern, and apposition of skin edges with monofilament nonabsorbable sutureq in a cruciate pattern or with skin staples.

Postoperative care

After surgery, all dogs were monitored and received hydromorphone (0.025 to 0.05 mg/kg [0.01 to 0.02 mg/lb], IV, q 4 to 6 h), methadone (0.1 mg/kg [0.045 mg/lb], IV, q 6 h), buprenorphine (0.01 to 0.02 mg/kg [0.005 to 0.009 mg/lb], IV, q 6 h), or fentanyl (2 to 6 μg/kg/h [0.9 to 2.7 μg/lb/h], IV, as a continuous rate infusion) for analgesia. In addition, dogs were discharged with prescriptions of tramadol (2.0 to 5.0 mg/kg [0.9 to 2.3 mg/lb], PO, q 8 to 12 h), buprenorphine (0.01 mg/kg, PO, q 8 to 12 h), or gabapentin (10 mg/kg [4.5 mg/lb], PO q 8 to 12 h), alone or in combination, for 3 to 5 days of postoperative analgesia.

Statistical analysis

The Shapiro-Wilk test was used to evaluate the normality of continuous variables. Descriptive statistics for numeric variables were calculated with computer software.r Results were reported as mean ± SD, median (IQR), and prevalence (95% CI).

Results

Animals

The search of medical records identified 27 dogs that underwent MISIETB at the involved academic institutions between January 1, 2010, and May 1, 2017, and that met the inclusion criteria. Mean ± SD age and body weight were 7.2 ± 3.2 years and 16 ± 11. 3 kg (7.2 ± 5.1 lb), respectively. There were 3 mixed breed dogs; 2 each of Cavalier King Charles Spaniels, German Shepherd Dogs, Havanese, Maltese, and Yorkshire Terriers; and 1 each of Portuguese Water Dog, Border Collie, Miniature Schnauzer, Norfolk Terrier, Golden Retriever, Soft-Coated Wheaten Terrier, Husky, Rottweiler, French Bulldog, Miniature Dachshund, Flat-Coated Retriever, Greyhound, Parson Russell Terrier, and Boston Terrier.

All dogs had clinical signs consistent with gastrointestinal disease before surgery. The most commonly observed clinical sign was diarrhea (19/27 [70%; 95% CI, 50% to 86%]), and other signs included inappetence (14 [52%; 95% CI, 33% to 70%]), weight loss (13 [48%; 95% CI, 29% to 68%]), and vomiting (11 [41%; 95% CI, 22% to 61%]). All dogs underwent abdominal ultrasonography performed by a board-certified veterinary radiologist or radiology resident under the supervision of a board-certified veterinary radiologist. Ultrasonographic findings included abnormal thickening of the gastrointestinal tract (n = 13/27 [48%; 95% CI, 29% to 68%]), regional lymphadenomegaly (9 [33%; 95% CI, 16% to 54%]), and scant to mild peritoneal effusion (8 [30%; 95% CI, 14% to 50%]). Of the 13 dogs with gastrointestinal tract wall thickening, 8 had the small intestines affected (focally or diffusely), 5 had the colon affected, and 1 had the stomach affected. Of the 9 dogs with lymphadenomegaly, 5 had mesenteric lymphadenomegaly, 2 had ileocolic lymphadenomegaly, 2 had hepatic lymphadenomegaly, and 1 had pancreaticoduodenal, jejunal, or medial iliac lymphadenomegaly.

Laparoscopy

Before WRD placement, laparoscopy was performed with a multicannulated single-port device (fexible device, n = 17; stainless steel device, 1) in 18 of 27 (67%) dogs, with multiple ports in 5 (19%) dogs, and with a 6-mm trocar and cannula assemblyd in 4 (15%) dogs. Procedures performed included liver biopsy (n = 20), cholecystocentesis (6), kidney biopsy (3), and total laparoscopic ovariohysterectomy (1). Mean ± SD surgical duration was 92 ± 23 minutes (range, 45 to 140 minutes). When grouped according to laparoscopy ports used, the mean ± SD surgical duration for procedures performed with a multicannulated single port, multiple ports, or a 6-mm trocar and cannula assembly was 86 ± 23 minutes, 116 ± 20 minutes, and 85 ± 9 minutes, respectively.

Use of WRDs

The primary surgeon determined WRD incision length and location. Median incision length for WRD placement was 4 cm (IQR, 3 to 6 cm). Most often (25/27 [93%; 95% CI, 76% to 99%]), the WRD location was centered on the umbilicus after enlargement of the single-port incision or connecting 2 port incisions. From this location, the intestinal tract was easily exteriorized for exploration and biopsy when indicated; however, the stomach, proximal aspect of the duodenum, and distal aspect of the colon could not be thoroughly evaluated. In some dogs for which gastric biopsy was required, the WRD was placed in a more cranial location (centered between the xiphoid and umbilicus; 2/27 [7%]) to allow for exteriorization of a small portion of the stomach with the aid of stay sutures. Gastrointestinal organs from which biopsy samples were obtained in conjunction with use of a WRD included jejunum (26/27 [96%; 95% CI, 81% to 100%]), duodenum (24 [89%; 95% CI, 71% to 98%]), ileum (22 [81%; 95% CI, 62% to 94%]), and stomach (9 [33%; 95% CI, 16% to 54%]). In 1 dog, biopsy samples of the stomach were obtained with upper gastrointestinal endoscopy. Additional procedures completed through the WRD included biopsy of mesenteric lymph nodes (n = 8), splenectomy (5), guillotine biopsy of liver (2), biopsy of pancreas (1), and resection and anastomosis of jejunum for removal of a jejunal mass discovered during gastrointestinal exploration (1).

Intraoperative complications

Intraoperative complications were encountered in 1 dog (body weight, 9.4 kg [20.7 lb]) in which elective conversion from MISIETB with WRD to traditional laparotomy was performed because of a 7 × 4-cm mesenteric root mass discovered during surgery that could not be adequately visualized or exteriorized through the WRD. The mass had not been detected by abdominal ultrasonography performed before surgery.

Histopathologic findings

All biopsy specimens collected were fixed in neutral-buffered 10% formalin at the time of collection and submitted for histologic evaluation. All specimens were routinely processed, embedded in paraffn, cut at 3- to 5-μm thickness, and stained with H&E stain before being reviewed by a board-certified veterinary pathologist at each respective institution. On the basis of histologic analysis by a veterinary pathologist, all samples were of diagnostic quality. Results of histologic examination of gastrointestinal biopsy samples included lymphoplasmacytic enteritis (n = 14), lymphosarcoma (5), plasmacytic enteritis with lymphangiectasia (2), lymphangiectasia (2), and 1 each of plasmacytic enteritis, eosinophilic enteritis, metastatic adenocarcinoma, and normal small intestine. Results of histologic examination of liver biopsy samples included chronic hepatitis (n = 2), active hepatitis (2), increased pigmentation (2), hepatic glycogenosis and lipidosis (steroid hepatopathy; 2), lipogranulomas (2), cytoplasmic swelling and clearing (2), hepatocellular necrosis (2), normal liver (2), and 1 each of cholestasis, metastatic adenocarcinoma, chronic cholangitis, chronic fibrosis, extramedullary hematopoiesis, and nodular hyperplasia. Results of histologic examination of splenic biopsy samples included splenic hyperplasia (n = 2) and 1 each of hematoma, myelolipomas, and histiocytosis.

Outcome

Postoperative complications were not encountered in any dog. Median duration of postoperative hospitalization was 41 hours (IQR, 20 to 64 hours). Owners of 2 dogs in which lymphosarcoma was diagnosed elected to have their dogs euthanized before hospital discharge. These 2 dogs were not included in the calculation of median duration of hospitalization. The remaining 25 (93%; 95% CI, 76% to 99%) dogs survived to hospital discharge, and 22 of these 25 (88%; 95% CI, 69% to 98%) dogs were alive and responding to medical management when their skin sutures or staples were removed 10 to 14 days after surgery.

Three of 25 (12%; 95% CI, 3% to 31%) dogs had postoperative abnormalities reported that were unrelated to the surgical technique. One dog with a histologic diagnosis of lymphoplasmacytic enteritis responded favorably after surgery; however, 14 days after hospital discharge, the dog was reexamined because of acute onset of vomiting and fever. Results of medical evaluation, including abdominal ultrasonography, indicated septic peritonitis likely secondary to a ruptured duodenal ulcer (visualized with ultrasonography) that was presumed to have been caused by high-dose steroid treatment. The dog was subsequently euthanized; however, a definitive site of gastrointestinal leakage was not identified on necropsy. Interestingly, before MISIETB, this dog had 2 duodenal ulcerations and 1 focal proximal- to midjejunal ulceration with gas dissection to the serosal surface noted on abdominal ultrasonography, but no evidence of intestinal perforation on ultrasonography or during surgery. A different dog in which lymphoplasmacytic enteritis had been diagnosed on the basis of histologic results was reexamined 5 days postoperatively because of abdominal effusion. Results of serum biochemical analyses indicated that the dog had marked hypoproteinemia; therefore, the effusion was presumed to have been a transudate. Results of cytologic examination and bacterial culture performed on the effusion were negative, and this dog was lost to follow-up. A third dog was reexamined 6 days postoperatively because of hyporexia and diarrhea, which were determined to have been secondary to progression of gastrointestinal disease caused by a large-cell lymphoma. This dog was also lost to follow-up.

Discussion

Results indicated that the MISIETB technique combined with use of a WRD was successful for obtaining minimally invasive biopsy samples of the stomach, small bowel, pancreas, liver, and abdominal lymph nodes from dogs in the present study. The combined approach of laparoscopic or laparoscopic-assisted biopsy followed by exteriorization of the small intestine through a WRD for further evaluation or full-thickness biopsy, when indicated, yielded biopsy samples that were all of diagnostic quality. Furthermore, postoperative complications related to surgery, including dehiscence of intestinal biopsy sites, did not occur with this technique in dogs of the present study.

Use of WRDs provides atraumatic intraoperative retraction for visualization of abdominal contents by exerting a radial force against the incisional edges while simultaneously protecting the incisional edges from potential contamination (eg, from the gastrointestinal tract or neoplastic cells).6 In people, WRDs have been used in thoracic surgery, gastrointestinal surgery, and for minimally invasive cholecystectomy, with the main reported benefits including reduction in postoperative wound infection and improved cosmesis owing to reduced incision size.25–28 In addition, use of WRDs provides improved visualization of underlying structures in a variety of circumstances and may cause less postoperative pain, compared with traditional retractors.29,30

The use of a WRD in veterinary medicine for minimally invasive surgery has been reported, initially in laparoscopic-assisted intestinal resection and anastomosis performed for treatment of discrete intestinal masses in dogs and cats.6 More recently, WRDs have been used in thoracoscopic-assisted lung lobectomy,31 laparoscopic-assisted splenectomy,24 laparoscopic-assisted ovariohysterectomy for pyometra,32 and abdominal organ biopsy in cats.20,33 Placement of the WRD incision is important because it determines the accessibility of abdominal organs for exploration and biopsy. Mayhew et al33 compared access to organs for biopsy from 3 different WRD positions in cats and showed that a more cranially located WRD allows for biopsy of the stomach in cats, but a similar comparison has not yet been described in dogs.

Although laparoscopy aided in visualization of abdominal organs that could not be adequately visualized or exteriorized through the WRD, elective conversion from MISIETB with WRD to a traditional laparotomy was required in 1 dog because of the inability to adequately visualize and exteriorize a mesenteric root mass. Interestingly, this mass was not identified with abdominal ultrasonography performed before surgery. Findings in this dog underscored the importance of client education before surgery about the potential need for surgical conversion as well as the potential for other complications.

Ultrasonography is commonly performed on veterinary patients evaluated for chronic gastrointestinal disease; however, use of CT improves accuracy in detection of small intestinal obstruction34 and may be beneficial when evaluating dogs with chronic gastrointestinal disease.35 Furthermore, CT detects more abdominal lesions than ultrasonography in sedated dogs > 25 kg; however, there are no meaningful differences between CT and ultrasonography for detecting abdominal lesions in dogs < 25 kg.36 Given these findings, we believe that CT should be considered as a preoperative imaging modality in dogs > 25 kg if MISIETB is intended. However, a 9.4-kg dog in the present study had a mesenteric root mass that was not identified by ultrasonography before surgery.

Previous studies37,38 in dogs undergoing full-thickness intestinal biopsy show dehiscence rates of up to 12%; however, none of the dogs in the present study, including dogs with infiltrative disease, had confirmed gastrointestinal dehiscence, which most likely would have been identified during the 10- to 14-day follow-up period. Similarly, a 0% dehiscence rate following a laparoscopic-assisted technique for intestinal biopsy in dogs has also been reported by Mitterman et al.5 In the present study, the dog that was euthanized because of septic peritonitis 14 days after surgery and in which no cause of the condition was identified on necropsy could have had a small partial-thickness ulcer in an area of bowel not able to be visualized during MISIETB. Alternatively, dehiscence of a gastrointestinal biopsy site in this dog could have occurred but was not visualized on necropsy.

A limitation of MISIETB with WRD in dogs of the present study was that although the intestinal tract was easily exteriorized for exploration and biopsy when indicated, the stomach, proximal aspect of the duodenum, and distal aspect of the colon could not be thoroughly evaluated through the WRD. Therefore, when considering MISIETB, abdominal ultrasonography or CT should be performed as part of the preoperative evaluation to assess whether lesions are suspected in tissues that cannot be exteriorized through a WRD. Regarding the gastrointestinal tract, traditional laparotomy should be considered for further evaluation and biopsy of suspected lesions of the stomach, proximal aspect of the duodenum, and distal aspect of the colon. Further, MISIETB with WRD requires additional equipment and advanced training.

Our findings indicated that MISIETB with WRD was a feasible method for obtaining diagnostic-quality abdominal organ biopsy samples from dogs of the present study. This hybrid technique facilitated intra-abdominal evaluation and biopsy as well as further access and tissue exteriorization when needed for evaluation and biopsy of selected portions of the gastrointestinal tract. In addition, the MISIETB with WRD also allowed for concurrent abdominal procedures (eg, splenectomy) to be performed without need of a traditional laparotomy in 5 dogs of the present study. Further, we believe that dogs with chronic gastrointestinal disease in which collection of full-thickness gastrointestinal biopsy samples is indicated may benefit from MISIETB with WRD in regard to potentially reduced postoperative pain and surgical site complications, compared with traditional laparotomy. Because many dogs with chronic gastrointestinal disease also receive immunosuppressive treatment, we believe that such dogs likely could further benefit from the smaller incisions needed for MISIETB with WRD, compared with larger incisions for traditional laparotomy. Prospective evaluation between MISIETB with WRD and traditional laparotomy for abdominal organ biopsy in dogs is warranted. In addition, MISIETB with WRD can be combined with upper and lower gastrointestinal endoscopy to improve diagnostic sensitivity. A complete presurgical evaluation, including abdominal ultrasonography or CT, is essential for appropriate case selection for MISIETB with WRD.

Acknowledgments

The authors declare that there were no conflicts of interest. Presented in part at the 14th Annual Veterinary Endoscopy Society Conference, Cabo San Lucas, Mexico, June 2017.

ABBREVIATIONS

CI

Confidence interval

IQR

Interquartile (25th to 75th percentile) range

MISIETB

Minimally invasive small intestinal exploration and targeted abdominal organ biopsy

WRD

Wound retraction device

Footnotes

a.

SILS port, Covidien Inc, Mansfeld, Mass.

b.

EndoCone, Karl Storz Endoscopy, Goleta, Calif.

c.

Ternamian Endotip, Karl Storz Endoscopy, Goleta, Calif.

d.

6-mm trocar-cannula assembly, Karl Storz Endoscopy, Goleta, Calif.

e.

Endofator, Karl Storz Endoscopy, Goleta, Calif.

f.

0° rigid telescope, Karl Storz Endoscopy, Goleta, Calif.

g.

30° rigid telescope, Karl Storz Endoscopy, Goleta, Calif.

h.

Clickline, 5 mm, Straight Babcock Forceps, Karl Storz Endoscopy, Goleta, Calif.

i.

Clickline, 5 mm, DeBakey grasping forceps, Karl Storz Endoscopy, Goleta, Calif.

j.

Palpation probe, Karl Storz Endoscopy, Goleta, Calif.

k.

5-mm biopsy cup forceps, Karl Storz Endoscopy, Goleta, Calif.

l.

Tru-Cut biopsy needle, BD CareFusion Corp, St Albans, England.

m.

LigaSure, Covidien Inc, Mansfield, Mass.

n.

Alexis wound retractor, Applied Medical Resources Corp, Rancho Santa Margarita, Calif.

o.

PDS II, Ethicon US LLC, Cincinnati, Ohio.

p.

Monocryl, Ethicon US LLC, Cincinnati, Ohio.

q.

Prolene, Ethicon US LLC, Cincinnati, Ohio.

r.

Stata Statistical Software, release 14, StataCorp LLC, College Station, Tex.

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  • 8. Slovak JE, Wang C, Morrison JA, et al. Endoscopic assessment of the duodenum in dogs with inflammatory bowel disease. J Vet Intern Med 2014;28:14421446.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Willard MD, Mansell J, Fosgate GT, et al. Effect of sample quality on the sensitivity of endoscopic biopsy for detecting gastric and duodenal lesions in dogs and cats. J Vet Intern Med 2008;22:10841089.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Kleinschmidt S, Meneses F, Noltr I, et al. Retrospective study on the diagnostic value of full-thickness biopsies from the stomach and intestine of dogs with chronic gastrointestinal disease symptoms. Vet Pathol 2006;43:10001003.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Bleedorn JA, Dykema JL, Hardie RJ. Minimally invasive surgery in veterinary practice: a 2010 survey of diplomates and residents of the American College of Veterinary Surgeons. Vet Surg 2013;42:635642.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Polymeneas G, Theodosopoulos T, Stamatiadis A, et al. A comparative study of postoperative adhesion formation after laparoscopic vs open cholecystectomy. Surg Endosc 2001;15:4143.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Hewett PJ, Allardyce RA, Bagshaw PF, et al. Short-term outcomes of the Australasian randomized clinical study comparing laparoscopic and conventional open surgical treatments for colon cancer: the ALCCaS trial. Ann Surg 2008;248:728738.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Davidson EB, Moll HD, Payton ME. Comparison of laparoscopic ovariohysterectomy and ovariohysterectomy in dogs. Vet Surg 2004;33:6269.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Culp WT, Mayhew PD, Brown DC. The effect of laparoscopic versus open ovariectomy on postsurgical activity in small dogs. Vet Surg 2009;38:811817.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Devitt CM, Cox RE, Hailey JJ. Duration, complications, stress, and pain of open ovariohysterectomy versus a simple method of laparoscopic-assisted ovariohysterectomy in dogs. J Am Vet Med Assoc 2005;227:921927.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Mayhew PD, Freeman L, Kwan T, et al. Comparison of surgical site infection rates in clean and clean-contaminated wounds in dogs and cats after minimally invasive versus open surgery: 179 cases (2007–2008). J Am Vet Med Assoc 2012;240:193198.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Pope JF, Knowles TG. Retrospective analysis of the learning curve associated with laparoscopic ovariectomy in dogs and associated perioperative complication rates. Vet Surg 2014;43:668677.

    • Search Google Scholar
    • Export Citation
  • 19. McClaran JK, Skerrett SC, Currao RL, et al. Comparison of laparoscopic-assisted technique and open laparotomy for gastrointestinal biopsy in cats. Vet Surg 2017;46:821828.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Baron J, Giuffrida M, Mayhew PD, et al. Minimally invasive small intestinal exploration and targeted abdominal organ biopsy with a wound retraction device in 42 cats (2005–2015). Vet Surg 2017;46:925932.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Mayhew PD, Brown DC. Comparison of three techniques for ovarian pedicle hemostasis during laparoscopic-assisted ovariohysterectomy. Vet Surg 2007;36:541547.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. McDevitt HL, Mayhew PD, Giuffrida MA, et al. Short-term clinical outcome of laparoscopic liver biopsy in dogs: 106 cases (2003–2013). J Am Vet Med Assoc 2016;248:8390.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Rawlings CA, Diamond H, Howerth EW, et al. Diagnostic quality of percutaneous kidney biopsy specimens obtained with laparoscopy versus ultrasound guidance in dogs. J Am Vet Med Assoc 2003;223:317321.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Wright T, Singh A, Mayhew PD, et al. Laparoscopic-assisted splenectomy in dogs: 18 cases (2012–2014). J Am Vet Med Assoc 2016;248:916922.

  • 25. Kusafuka J, Yamataka A, Okazaki T, et al. Gastroschisis reduction using “Applied Alexis,” a wound protector and retractor. Pediatr Surg Int 2005;21:925927.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Tsunezuka Y, Oda M, Moriyama H. Wound retraction system for lung resection by video-assisted mini-thoracotomy. Eur J Cardiothorac Surg 2006;29:110111.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Horiuchi T, Tanishima H, Tamagawa K, et al. Randomized, controlled investigation of the anti-infective properties of the Alexis retractor/protector of incision sites. J Trauma 2007;62:212215.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Hong TH, You YK, Lee KH. Transumbilical single-port laparoscopic cholecystectomy: scarless cholecystectomy. Surg Endosc 2009;23:13931397.

  • 29. Beresford T, Misselhom D. Wound protector/retractor for improved access in infrainguinal vascular surgery. Ann R Coll Surg Engl 2014;96:169.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. Dessy LA, Fallico N, Serrate F, et al. The use of the Alexis device in breast augmentation to improve outcomes: a comparative randomized case-control survey. Gland Surg 2016;5:287294.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Wormser C, Singhal S, Holt DE, et al. Thoracoscopic-assisted pulmonary surgery for partial and complete lung lobectomy in dogs and cats: 11 cases (2008–2013). J Am Vet Med Assoc 2014;245:10361041.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Adamovich-Rippe KN, Mayhew PD, Runge JJ, et al. Evaluation of laparoscopic-assisted ovariohysterectomy for treatment of canine pyometra. Vet Surg 2013;42:572578.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Mayhew PD, Mayhew KN, Shilo-Benjamini Y, et al. Prospective evaluation of access incision position for minimally invasive surgical organ exposure in cats. J Am Vet Med Assoc 2014;245:11291134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Winter MD, Barry KS, Johnson MD, et al. Ultrasonographic and computed tomographic characterization and localization of suspected mechanical gastrointestinal obstruction in dogs. J Am Vet Med Assoc 2017;251:315321.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Fitzgerald E, Lam R, Drees R. Improving conspicuity of the canine gastrointestinal wall using dual phase contrast-enhanced computed tomography: a retrospective cross-sectional study. Vet Radiol Ultrasound 2017;58:151162.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Fields EL, Robertson ID, Osborne JA, et al. Comparison of abdominal computed tomography and abdominal ultrasound in sedated dogs. Vet Radiol Ultrasound 2012;53:513517.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37. Harvey HJ. Complications of small intestinal biopsy in hypoalbuminemic dogs. Vet Surg 1990;19:289292.

  • 38. Shales CJ, Warren J, Anderson DM, et al. Complications following full-thickness small intestinal biopsy in 66 dogs: a retrospective study. J Small Anim Pract 2005;46:317321.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • Figure 1—

    Intraoperative image of a 24.0-kg (52.8-lb) dog undergoing MISIETB with a 5- to 9-cm WRD (arrow) in place in a 7-cm access incision made on the dog's ventral midline. A segment of the small intestine has been exteriorized through the WRD. Cranial is at the top of the image.

  • 1. Jergens AE, Willard MD, Allenspach K. Maximizing the diagnostic utility of endoscopic biopsy in dogs and cats with gastrointestinal disease. Vet J 2016;214:5060.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2. Vignoli M, Saunders JH. Image-guided interventional procedures in the dog and cat. Vet J 2011;187:297303.

  • 3. Craven M, Simpson JW, Ridyard AE, et al. Canine inflammatory bowel disease: retrospective analysis of diagnosis and outcome in 80 cases (1995–2002). J Small Anim Pract 2004;45:336342.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 4. Mayhew P. Techniques for laparoscopic and laparoscopic-assisted biopsy of abdominal organs. Compend Contin Educ Vet 2009;31:170176.

    • Search Google Scholar
    • Export Citation
  • 5. Mitterman L, Bonczynski J, Hearon K, et al. Comparison of perioperative and short-term postoperative complications of gastrointestinal biopsies via laparoscopic-assisted technique versus laparotomy. Can Vet J 2016;57:395400.

    • Search Google Scholar
    • Export Citation
  • 6. Gower SB, Mayhew PD. A wound retraction device for laparoscopic-assisted intestinal surgery in dogs and cats. Vet Surg 2011;40:485488.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7. Case JB, Ellison G. Single incision laparoscopic-assisted intestinal surgery (SILAIS) in 7 dogs and 1 cat. Vet Surg 2013;42:629634.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 8. Slovak JE, Wang C, Morrison JA, et al. Endoscopic assessment of the duodenum in dogs with inflammatory bowel disease. J Vet Intern Med 2014;28:14421446.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9. Willard MD, Mansell J, Fosgate GT, et al. Effect of sample quality on the sensitivity of endoscopic biopsy for detecting gastric and duodenal lesions in dogs and cats. J Vet Intern Med 2008;22:10841089.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10. Kleinschmidt S, Meneses F, Noltr I, et al. Retrospective study on the diagnostic value of full-thickness biopsies from the stomach and intestine of dogs with chronic gastrointestinal disease symptoms. Vet Pathol 2006;43:10001003.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11. Bleedorn JA, Dykema JL, Hardie RJ. Minimally invasive surgery in veterinary practice: a 2010 survey of diplomates and residents of the American College of Veterinary Surgeons. Vet Surg 2013;42:635642.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12. Polymeneas G, Theodosopoulos T, Stamatiadis A, et al. A comparative study of postoperative adhesion formation after laparoscopic vs open cholecystectomy. Surg Endosc 2001;15:4143.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 13. Hewett PJ, Allardyce RA, Bagshaw PF, et al. Short-term outcomes of the Australasian randomized clinical study comparing laparoscopic and conventional open surgical treatments for colon cancer: the ALCCaS trial. Ann Surg 2008;248:728738.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14. Davidson EB, Moll HD, Payton ME. Comparison of laparoscopic ovariohysterectomy and ovariohysterectomy in dogs. Vet Surg 2004;33:6269.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15. Culp WT, Mayhew PD, Brown DC. The effect of laparoscopic versus open ovariectomy on postsurgical activity in small dogs. Vet Surg 2009;38:811817.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16. Devitt CM, Cox RE, Hailey JJ. Duration, complications, stress, and pain of open ovariohysterectomy versus a simple method of laparoscopic-assisted ovariohysterectomy in dogs. J Am Vet Med Assoc 2005;227:921927.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17. Mayhew PD, Freeman L, Kwan T, et al. Comparison of surgical site infection rates in clean and clean-contaminated wounds in dogs and cats after minimally invasive versus open surgery: 179 cases (2007–2008). J Am Vet Med Assoc 2012;240:193198.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18. Pope JF, Knowles TG. Retrospective analysis of the learning curve associated with laparoscopic ovariectomy in dogs and associated perioperative complication rates. Vet Surg 2014;43:668677.

    • Search Google Scholar
    • Export Citation
  • 19. McClaran JK, Skerrett SC, Currao RL, et al. Comparison of laparoscopic-assisted technique and open laparotomy for gastrointestinal biopsy in cats. Vet Surg 2017;46:821828.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20. Baron J, Giuffrida M, Mayhew PD, et al. Minimally invasive small intestinal exploration and targeted abdominal organ biopsy with a wound retraction device in 42 cats (2005–2015). Vet Surg 2017;46:925932.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21. Mayhew PD, Brown DC. Comparison of three techniques for ovarian pedicle hemostasis during laparoscopic-assisted ovariohysterectomy. Vet Surg 2007;36:541547.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 22. McDevitt HL, Mayhew PD, Giuffrida MA, et al. Short-term clinical outcome of laparoscopic liver biopsy in dogs: 106 cases (2003–2013). J Am Vet Med Assoc 2016;248:8390.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 23. Rawlings CA, Diamond H, Howerth EW, et al. Diagnostic quality of percutaneous kidney biopsy specimens obtained with laparoscopy versus ultrasound guidance in dogs. J Am Vet Med Assoc 2003;223:317321.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24. Wright T, Singh A, Mayhew PD, et al. Laparoscopic-assisted splenectomy in dogs: 18 cases (2012–2014). J Am Vet Med Assoc 2016;248:916922.

  • 25. Kusafuka J, Yamataka A, Okazaki T, et al. Gastroschisis reduction using “Applied Alexis,” a wound protector and retractor. Pediatr Surg Int 2005;21:925927.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 26. Tsunezuka Y, Oda M, Moriyama H. Wound retraction system for lung resection by video-assisted mini-thoracotomy. Eur J Cardiothorac Surg 2006;29:110111.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27. Horiuchi T, Tanishima H, Tamagawa K, et al. Randomized, controlled investigation of the anti-infective properties of the Alexis retractor/protector of incision sites. J Trauma 2007;62:212215.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28. Hong TH, You YK, Lee KH. Transumbilical single-port laparoscopic cholecystectomy: scarless cholecystectomy. Surg Endosc 2009;23:13931397.

  • 29. Beresford T, Misselhom D. Wound protector/retractor for improved access in infrainguinal vascular surgery. Ann R Coll Surg Engl 2014;96:169.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 30. Dessy LA, Fallico N, Serrate F, et al. The use of the Alexis device in breast augmentation to improve outcomes: a comparative randomized case-control survey. Gland Surg 2016;5:287294.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31. Wormser C, Singhal S, Holt DE, et al. Thoracoscopic-assisted pulmonary surgery for partial and complete lung lobectomy in dogs and cats: 11 cases (2008–2013). J Am Vet Med Assoc 2014;245:10361041.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32. Adamovich-Rippe KN, Mayhew PD, Runge JJ, et al. Evaluation of laparoscopic-assisted ovariohysterectomy for treatment of canine pyometra. Vet Surg 2013;42:572578.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 33. Mayhew PD, Mayhew KN, Shilo-Benjamini Y, et al. Prospective evaluation of access incision position for minimally invasive surgical organ exposure in cats. J Am Vet Med Assoc 2014;245:11291134.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34. Winter MD, Barry KS, Johnson MD, et al. Ultrasonographic and computed tomographic characterization and localization of suspected mechanical gastrointestinal obstruction in dogs. J Am Vet Med Assoc 2017;251:315321.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35. Fitzgerald E, Lam R, Drees R. Improving conspicuity of the canine gastrointestinal wall using dual phase contrast-enhanced computed tomography: a retrospective cross-sectional study. Vet Radiol Ultrasound 2017;58:151162.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36. Fields EL, Robertson ID, Osborne JA, et al. Comparison of abdominal computed tomography and abdominal ultrasound in sedated dogs. Vet Radiol Ultrasound 2012;53:513517.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37. Harvey HJ. Complications of small intestinal biopsy in hypoalbuminemic dogs. Vet Surg 1990;19:289292.

  • 38. Shales CJ, Warren J, Anderson DM, et al. Complications following full-thickness small intestinal biopsy in 66 dogs: a retrospective study. J Small Anim Pract 2005;46:317321.

    • Crossref
    • Search Google Scholar
    • Export Citation

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