Abstract
Background/Aim: Congenital portosystemic shunt (PSS) is a vascular anomaly forming a direct communication between portal and central venous systems, thus bypassing the liver. This condition is related to various clinical symptoms including those manifesting in the central nervous system, gastrointestinal tract, and urinary tract. Treatment of PSS includes medical management and surgery. When evaluating prognosis of dogs with PSS, serum biochemistry profiles including serum bile acid (SBA) and ammonia concentrations are routinely used as screening tests. However, the use of SBA concentration in Maltese is controversial because it can be measured above the reference range even in normal dogs of this breed. In addition, utilizing SBA levels to assess surgical prognosis of PSS is not widely understood in this breed. Thus, the present study evaluated whether SBA could be used as a screening test for PSS in Maltese dogs. Materials and Methods: Medical records of dogs in the Veterinary Teaching Hospital from 2018 to 2020 were retrospectively reviewed. Results: A total of 23 dogs with PSS and 30 Maltese dogs without PSS were analyzed. Although preoperative SBA levels were significantly higher in Maltese dogs (192 μmol/l) than in other dog breeds (137 μmol/l) with portocaval shunt, its concentrations were significantly decreased after surgery in both Maltese and other breeds of dogs. No significant difference was observed in postoperative SBA levels between Maltese and other dog breeds. The mean SBA levels for Maltese dogs without PSS (8 μmol/l) were within the reference interval (0-25 IU/l). Conclusion: Measuring pre- and post-operative SBA levels to evaluate prognosis of PSS might also be available for Maltese.
Congenital portosystemic shunt (PSS) is a vascular anomaly first reported in human medicine as Abernethy malformation in 1793 (1). An aberrant vessel occurs secondary to abnormal development of fetal vasculature, thus forming a communication between the portal vein and venous systemic circulation (2). This abnormal condition is related to significant complications such as encephalopathy and hepatopulmonary syndrome (1). PSS has also been reported in veterinary medicine (3, 4). Havanese, Yorkshire Terrier, and Maltese are known as PSS-predisposed breeds (5). Clinical signs of PSS are generally associated with the central nervous system, gastrointestinal tract, and urinary tract (3). Diagnosis of congenital PSS is routinely made by radiography and ultrasound combined with blood tests (4, 6). Computed tomography (CT) is a useful tool to identify insertion site of the shunt as prognosis varies between shunt types (6). Treatment of PSS includes medical treatment and surgery (7). Medical management consists of dietary, antimicrobial, and lactulose treatments (7, 8). Surgical attenuation or closure of the shunt is made by using ameroid ring constrictor (ARC), cellophane band, or silk suture (9, 10). When evaluating pre- and post-operative prognosis for surgically treated shunts, serum bile acid (SBA) and ammonia concentrations are useful screening tests (4). Although a previous study documented that dogs with PSS can show higher SBA levels than normal dogs despite surgical ligation of the shunt (11), SBA is generally identified as a sensitive factor in evaluation of PSS (4, 12). When utilizing SBA for PSS evaluation, Maltese can be an exception as normal Maltese often show SBA levels above the reference interval (RI) (13). SBA concentration is therefore often not used as a routine test for PSS in this breed (14). To the authors’ knowledge, measurement of SBA concentration for PSS prognosis evaluation in Maltese dogs has not been yet investigated. In order to determine whether SBA can be used to assess the surgical prognosis of PSS in Maltese, the present study evaluated pre- and post-operative serum biochemistry profiles including SBA concentrations in Maltese and other breeds of dogs with PSS.
Materials and Methods
Inclusion criteria. Medical records of Maltese dogs without PSS and Maltese dogs or other breeds of dogs with congenital PSS that underwent surgical attenuation of the shunt at the Veterinary Teaching Hospital in Cheongju, Korea, between 2018 and 2020 were retrospectively reviewed. Since the prognosis might differ depending on the shunt type (6), laboratory data of Maltese and other breed dogs with portocaval shunt were compared. Dogs received medications that could affect results of blood tests were excluded from this study.
Preoperative evaluation. Data included breed, age, sex, body weight, shunt type, and results of laboratory tests. Serum biochemistry profiles included alanine aminotransferase (ALT) activity, alkaline phosphatase (ALP) activity and concentrations of albumin, ammonia, SBA, and blood urea nitrogen (BUN). Blood tests were performed pre- and post-operatively. Short-term follow-up was conducted within a month after surgery. Dogs with follow-up periods of more than 6 months were defined as having a long-term follow-up.
Imaging. CT images of each dog were taken using a four-row multi-detector CT scanner (HiSpeed QX/i; GE Medical Systems, Milwaukee, WI, USA). A CT angiography was performed following previous literature (Figure 1A and B) (15). Shunt types were classified according to the insertion site (portocaval, portophrenic, and portoazygos shunt) (6). Data were analyzed using a digital image measurement program (eFilm Workstation 4.1; Merge Healthcare, Hartland, WI, USA).
Transverse (A) and sagittal (B) computed tomography images of a dog with portosystemic shunt.
Surgical procedure. Animals were pre-medicated with midazolam (0.2 mg/kg, IV) and butorphanol (0.2 mg/kg, IV). Anesthesia was induced with propofol (6 mg/kg, IV) and maintained by isoflurane. After anesthetic stabilization, a ventral midline celiotomy was performed and the shunt was visualized. After dissection of the perivascular fascia, the decision to use ARC or cellophane band was made based on the surgeon’s preference. The ARC of 3.5 or 5 mm in diameter was used and placed as previously recommended (16). When using a cellophane band, a strip of the cellophane band (12 mm in width) was folded in triple layers (4 mm in final width) (17). It was placed around the shunt and secured using surgical clips. Peri- and post-operative pain were managed by butorphanol or fentanyl transdermal patch (2 μg/kg/h).
Statistical analysis. Data between two groups were analyzed by Mann-Whitney U-test. All statistical analyses were performed using GraphPad Prism version 6.01 for Windows and a p-value <0.05 was considered significant. Data are expressed as mean±standard deviation.
Results
Demographics. A total of 23 dogs were reviewed. Breeds included Maltese (n=10), Pomeranian (n=3), Bichon Frise (n=3), Italian Greyhound (n=2), Poodle (n=1), White Terrier (n=1), and mixed (n=3). No significant differences were observed in age or body weight between Maltese and other breeds of dogs. Among Maltese dogs, the portocaval shunt was identified in 8 dogs. The portophrenic and portoazygos shunts were identified in one dog each. Depending on types of shunts in other breeds of dogs, portocaval shunt (n=9) was the most common, followed by portophrenic shunt (n=3) and portoazygos shunt (n=1) (Table I). Subsequent laboratory results were conducted for dogs with portocaval shunt (8 Maltese dogs and 9 non-Maltese dogs, respectively).
Demographics of Maltese and non-Maltese dogs with portosystemic shunt.
Serum bile acid concentrations in Maltese dogs without PSS. Medical records of 30 Maltese dogs without PSS were reviewed. Maltese dogs without PSS were significantly older than Maltese dogs with PSS in this study. There was no significant difference in body weight between the two groups. According to SBA concentration in the present study, 25 out of 30 Maltese dogs without PSS showed SBA levels within the RI (Table II).
Demographics and serum bile acid concentrations of Maltese dogs without portosystemic shunt (PSS).
Preoperative evaluation. Both Maltese and non-Maltese dogs with portocaval shunt showed ALT, ALP, and SBA levels above RIs. Preoperative ALP and SBA levels were significantly higher in Maltese dogs than in non-Maltese dogs. There was no significant difference in albumin, ALT, ammonia, or BUN level between the two groups.
Short-term clinical outcomes (within a month). Follow-up blood tests were mainly performed at two weeks after surgery. Both Maltese and non-Maltese dogs showed significantly lower ammonia and SBA levels than preoperative values. ALT and ALP activities were significantly decreased in Maltese dogs (Table III). In non-Maltese dogs, BUN levels were significantly increased (Table IV). During the short-term follow-up, no significant difference was identified in serum biochemistry profiles between the two groups.
Comparison of pre- and post-operative serum biochemistry in Maltese dogs with portocaval shunt.
Comparison of pre- and post-operative serum biochemistry in non-Maltese dogs with portocaval shunt.
Long-term clinical outcomes (more than 6 months). Long-term follow-up was available for 2 Maltese dogs and 3 non-Maltese dogs. Serum biochemistry profiles including SBA concentrations in both groups were within RI. ALP activities were above RI. The mean ALP was 269 IU/l (RI, 29-97 IU/l) in Maltese dogs and 308 IU/l in non-Maltese dogs.
Discussion
A previous study documented female over-representation of PSS in Maltese (11 out of 15 dogs) (18). However, another study reported a similar ratio between sexes (8 females and 11 males) (14). The present study revealed that male Maltese dogs were predisposed to PSS (9 out of 10 dogs). However, as numbers of dogs evaluated in previous and present studies were small, it was difficult to describe whether distribution of PSS in Maltese had a difference according to sex. When shunt types were evaluated according to the site of insertion, a shunt that was inserted into the vena cava was the most prevalent in both Maltese and other breeds of dogs, similar to previous literatures (6, 17). Surgical attenuation of a portocaval shunt was conducted using ARC or cellophane band. As both ARC and cellophane band have already been verified through various studies (10, 16, 17, 19, 20), these two methods were used according to the surgeon’s preference. Although cellophane band was applied in only 3 out of 17 dogs in the present study, both methods were effective considering resolution of preoperative clinical signs and postoperative normalization of serum biochemistry profiles of dogs. Between serum biochemistry profiles in evaluating pre- and post-operative prognosis of dogs with PSS, previous studies have suggested not to use SBA concentration for diagnosis of PSS in Maltese dogs as high levels can be seen in normal dogs of this breed (13, 14). However, the authors also mentioned that these investigations might result in not using SBA concentration as a routine test for diagnosis and monitoring the response to surgery of PSS. In addition, diagnosis between normal and PSS Maltese dogs mainly relied on ammonia tolerance test and/or visual confirmation of the shunt in previous studies (13, 14). Among various liver diseases, portal vein hypoplasia may reveal similar clinical presentation and laboratory finding, although those are generally less pronounced than those in PSS (21). Furthermore, the ammonia tolerance test can also give false-negative results for portal vein hypoplasia or residual shunting (21, 22). Recently, it has been reported that such hepatic disorders might not be revealed through laboratory testing alone. However, these hepatic disorders can be diagnosed when laboratory testing is combined with other diagnostic methods such as scintigraphy or CT angiography (21, 23). Unlike results of previous studies (13, 14), SBA concentrations in Maltese dogs without PSS were generally within RI in the present study.
Taken together, it is presumed that Maltese dogs with portal vein hypoplasia might have been included in normal groups at that time. Consequently, although it is not recommended to diagnose PSS based only on SBA levels (12, 13, 24), evaluating the prevalence and surgical prognosis of PSS through SBA concentration combined with other serum biochemistry factors is useful in Maltese dogs.
Footnotes
Authors’ Contributions
DK, DP, K-JN and GK designed the study. DK, HA and BA analyzed the data. The manuscript was written by DK, HO and GK. All Authors critically revised the manuscript and approved the final version.
Funding
This research was supported by the Chungbuk National University Korea National University Development Project (2022).
Conflicts of Interest
The Authors declare no conflicts of interest in relation to this study.
- Received January 9, 2023.
- Revision received January 25, 2023.
- Accepted February 3, 2023.
- Copyright © 2023, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved
This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY-NC-ND) 4.0 international license (https://creativecommons.org/licenses/by-nc-nd/4.0).
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