Diagnosis of Congenital Portosystemic Shunt in Miniature Schnauzers 7 Years of Age or Older (1997–2006)

Introduction

Congenital portosystemic shunt (PSS) has been reported in dogs for over 30 years.¹ The frequency with which congenital PSS is diagnosed appears to be increasing as time progresses,² probably because of increased awareness and/or increased frequency of the problem. Affected dogs are typically diagnosed before 2 years of age, although scattered reports exist of dogs first being diagnosed with congenital PSS when they are older. One report² that utilized the Veterinary Medical Database stated that of 2400 dogs diagnosed with congenital PSS from 1980 to 2002, 3% were 7 years of age or older, which is consistent with three other manuscripts^3–5 that mention four (4.3%) out of 94 dogs with congenital PSS being 7 years of age or older at the time of diagnosis. A recent paper reported congenital PSS in five mature dogs, three of which were older than 7 years of age.⁶ None of the dogs in the latter report were miniature schnauzers.

Other reports mention finding congenital PSS in dogs 7 years of age or older, but they do not specify how many or if any of the affected dogs were miniature schnauzers.^7–12 A review of other studies published by or after 1987 revealed a total of 408 dogs^13–28 (assuming no dog was included in more than one report), all of which were first diagnosed with congenital PSS before 7 years of age and of which the vast majority were diagnosed before 2 to 3 years of age. A study by Niles et al²⁹ mentions 20 dogs under 7 years of age with extrahepatic congenital PSS. While this work originates from the same institution as that of Bright et al, the latter report only considered intrahepatic shunts.²⁵ A series of four reports with 17,³⁰ 90,³¹ 34,³² and 97³³ dogs diagnosed with congenital PSS from the same institution did not cite any dogs older than 7 years of age, although it is not certain whether the same dogs were used in more than one of these papers. Based on our review of the data, at least 97 dogs with congenital PSS had to be younger than 7 years of age at the time of diagnosis. Three studies included a reasonable number of cases^34–36 in which it was impossible to determine if any dogs were 7 years of age or older at the time of diagnosis.

We have diagnosed several animals with congenital PSS when they were 7 years of age or older, and miniature schnauzers appeared to be overrepresented in this group. Therefore, the purpose of this retrospective study was to determine if miniature schnauzers are more likely to be diagnosed with congenital PSS at an older age than are other breeds. Furthermore, we sought to determine if any serum biochemical markers were present that might help the clinician to suspect this diagnosis in older miniature schnauzers.

Materials and Methods

Medical records of dogs presented to our hospital between January 1, 1997 and December 31, 2006 were reviewed to identify all dogs that were diagnosed with congenital PSS. Diagnosis was based upon either a) visualizing a single shunting vessel with ultrasound, contrast portography, transabdominal splenic scintigraphy, surgery, or necropsy; or b) rectal scintigraphy in a dog that was 6 months of age or younger and that had hepatic histopathology confirming the absence of acquired hepatic disease. The medical records of dogs meeting these inclusion criteria were retrieved, and the breed, age at diagnosis, and presenting complaint were recorded. Selected serum biochemical parameters (i.e., albumin, cholesterol, blood urea nitrogen, alanine aminotransferase, serum alkaline phosphatase [SAP], glucose, fasting serum bile acids, postprandial serum bile acids, and blood ammonia) determined at or near the time of diagnosis were also recorded.

Descriptive statistics for clinical parameters were calculated for miniature schnauzers, dogs of other breeds, dogs at least 7 years of age at diagnosis, and dogs younger than 7 years of age at diagnosis. The distributions of clinical variables were assessed for normality by performing the Anderson-Darling test using commercially available software.^a Clinical laboratory values for miniature schnauzers were compared to values for all other breeds using Mann-Whitney U tests in available software.^b Median laboratory values were similarly compared between dogs 7 years of age or older at diagnosis and younger dogs. The association between miniature schnauzers and diagnosis of a congenital PSS at 7 years of age or older was assessed by estimating the prevalence ratio and its corresponding 95% confidence interval (CI) using available software.^c All statistical testing was interpreted at the 5% level of significance.

Results

Between January 1, 1997 and December 31, 2006, 171 dogs were diagnosed with congenital PSS, including 33 Yorkshire terriers and 31 miniature schnauzers. Twelve (7.0%) dogs were 7 years of age or older at the time of diagnosis. Seven (23%) of the 31 miniature schnauzers were 7 years of age or older (mean age 10.33 years, range 7.42 to 15.00 years) at the time of diagnosis. Six of the seven miniature schnauzers that were 7 years of age had shunts from the portal vein to the vena cava; the type of shunt was not recorded for one of the seven dogs. Only five (3.4%) of the 140 nonminiature schnauzers diagnosed with congenital PSS during this time were 7 years of age or older (mean age 7.75 years, range 7.0 to 9.0 years). One of each of the following breeds was diagnosed with congenital PSS at 7 years of age or older: Lhasa apso, Pekingese, West Highland white terrier, shih tzu, and mixed-breed dog. As described in Table 1⇓, the mean ± standard deviation and median age for all miniature schnauzers diagnosed with congenital PSS were 3.75±4.71 years (median 1.67 years) compared to 1.6±1.85 years (median 0.83 years) for all other breeds combined (P=0.012).

Miniature schnauzers were 6.3 times more likely to be diagnosed with a congenital PSS when 7 years of age or older compared to all other breeds (95% CI 2.2 to 18.6; P=0.001). While not statistically significant, poodles, Maltese, Havanese, pugs, and Yorkshire terriers appeared to be less likely to be first diagnosed with congenital PSS when 7 years of age or older compared to all other breeds, excluding miniature schnauzers (0% versus 6.8%; P=0.059).

Of the biochemical parameters examined, preprandial bile acids were above the reference range in all dogs and were significantly higher in miniature schnauzers than in other breeds diagnosed with congenital PSS [Table 1⇑].

When all dogs first diagnosed with congenital PSS at 7 years of age or older were compared to all dogs first diagnosed before 7 years of age, dogs that were 7 years of age or older had significantly higher mean serum albumin and cholesterol concentrations [Table 2⇓]. Serum bilirubin concentrations were significantly higher in dogs that were 7 years of age or older (P=0.005), but the difference was not clinically relevant, as all mean and median measures were within normal limits. One dog was hyperbilirubinemic, but it had concurrent systemic histoplasmosis affecting the liver. In addition, five of the seven miniature schnauzers 7 years of age or older that were diagnosed with congenital PSS had no report of visible fasting hyperlipidemia, while one dog repeatedly had visible hyperlipemia, and one had intermittent visible hyperlipidemia.

Four of the seven older miniature schnauzers were diagnosed in an almost fortuitous fashion. One dog had a spontaneously resolving acute gastrointestinal upset that led to the diagnosis of a urinary tract infection (UTI) that in turn led to finding ammonium urate cystic calculi, which ultimately led to the diagnosis of congenital PSS. Two of these dogs were referred, because the referring veterinarian found high serum bile acid concentrations (although it is not clear why the serum bile acids were measured in the first place). One of these dogs required a pacemaker for cardiac syncope, and thoracic radiographs revealed marked microhepatica that ultimately led to the diagnosis of congenital PSS. The other three miniature schnauzers diagnosed with congenital PSS at 7 years of age or older had various central nervous system (CNS) signs that started within 6 months of diagnosis. The dog with the longest-standing signs (i.e., mental dullness) was diagnosed as having “cognitive dysfunction” 6 months earlier based upon computed tomography and cerebrospinal fluid analysis, and it was being treated with L-deprenyl.^d This dog was presented to our hospital because of a spontaneously resolving gastroenteritis, and the diagnosis of congenital PSS occurred because the owner insisted upon a complete set of diagnostic tests, which revealed high serum bile acid concentrations. The other two miniature schnauzers had CNS signs (i.e., circling, aggressive behavior) that were first recognized 2 months to 1 week prior to presentation.

Three of the miniature schnauzers diagnosed with congenital PSS at 7 years of age or older had UTIs, and three dogs were polyuric-polydipsic (one dog had both signs). Only one of the older miniature schnauzers was diagnosed with ammonium urate cystic calculi; however, since one of the miniature schnauzers without cystic calculi only had radiography instead of ultrasonography, the dog may have had an undetected stone. Five nonschnauzer dogs diagnosed with congenital PSS that were 7 years of age or older also had UTIs. Only one of these dogs had ammonium urate cystic calculi. None of the miniature schnauzers diagnosed with congenital PSS at 7 years of age or older had clinical signs persisting beyond 1 year that were clearly associated with the congenital PSS.

Discussion

Congenital PSS is generally sought for and diagnosed in relatively young dogs (younger than 2 to 3 years of age) with classic signs that include intermittent vomiting, polyuria-polydipsia, poor condition, and/or postprandial encephalopathy. Therefore, the vast majority of cases reported in the literature are, not surprisingly, relatively young at the time of diagnosis. In general, the more aware the practicing community becomes of a particular disease, the more cases are diagnosed and the more our appreciation of the range of clinical presentations grows. This appears to be the situation with congenital PSS, in that awareness is growing that congenital PSS may be first diagnosed in older dogs that would more typically be thought to have acquired hepatic disease as opposed to congenital hepatic disease.⁶

Compared to findings in the published literature, our findings revealed approximately twice as many dogs diagnosed with congenital PSS when they were 7 years of age or older (12 [7.0%] of 171 dogs in our study versus approximately 3% to 4% in the published literature).^2–5 In several of the cases described herein, congenital PSS was not initially considered a likely differential diagnosis. Those miniature schnauzers with signs suggestive of hepatic disease had a relatively recent onset of neurological dysfunction or polyuria-polydipsia, which prompted consideration of acquired rather than congenital hepatic disease. The diagnosis was especially unexpected in some of the miniature schnauzers that had signs not particularly suggestive of hepatic disease. These findings raise the question as to how many mature or geriatric dogs have congenital PSS and are never diagnosed. One can reasonably speculate that some dogs with congenital PSS live lives that are normal enough for the owners and veterinarians never to suspect a congenital shunt is present. We could not detect any particular disease or reason why some miniature schnauzers developed clinical signs at such an advanced age. No clear evidence was seen of other hepatic disease or other systemic diseases that could have caused hepatic decompensation and subsequent manifestations of hepatic disease.

Miniature schnauzers have been reported as commonly being affected with congenital PSS.^2,7,10,19,36 We found that 31 of our 171 dogs with congenital PSS were miniature schnauzers. Only Yorkshire terriers (n=33) were more commonly diagnosed with congenital PSS than miniature schnauzers in our series. Therefore, it could be argued that we diagnosed congenital PSS in more old miniature schnauzers simply because more miniature schnauzers had this disease. Nonetheless, even though more Yorkshire terriers than miniature schnauzers were diagnosed with congenital PSS, the Yorkshire terriers appeared more likely to be diagnosed before 7 years of age. Therefore, finding many older miniature schnauzers with congenital PSS does not appear to be simply due to the high number of miniature schnauzers diagnosed with PSS. We speculate that miniature schnauzers may not necessarily show signs of hepatic insufficiency as obviously and/or as readily as other breeds, or maybe these dogs experienced less hepatic insufficiency than other dogs with congenital PSS.

Examination of select clinicopathological data did not identify changes that would be particularly useful in raising suspicion of congenital PSS in an older dog. In fact, the serum albumin and cholesterol concentrations were higher, and the means were normal in the older dogs with congenital PSS [Table 2⇑]. In our study, only one of the miniature schnauzers that was over 7 years of age at the time of diagnosis consistently had fasting hyperlipidemia, so this is not a reasonable explanation for the higher cholesterol values in older dogs. We believe that the higher serum albumin and cholesterol values in the older dogs of all breeds are most consistent with the idea that dogs that are first diagnosed when older are those that compensate better because they have a lesser degree of hepatic insufficiency. Therefore, looking for hypoalbuminemia and hypocholesterolemia does not appear to be a good screening tool when considering congenital PSS in dogs over 7 years of age. The significantly higher serum bilirubin concentrations in the older dogs were still well within the reference range, making such a finding of questionable diagnostic value. Serum alkaline phosphatase was not useful in suspecting congenital PSS in these dogs. Finding an increased SAP is so common in older dogs that it is of doubtful diagnostic value in this situation. The differences in the preprandial serum bile acids are not diagnostically helpful, because unlike serum albumin concentrations, serum bile acid concentrations can vary markedly from day to day.

Conclusion

In this study, miniature schnauzers, in comparison to other breeds, were more likely to be diagnosed with congenital PSS when they were 7 years of age or older. Clinical signs of congenital PSS may not manifest sufficiently to cause an owner to seek veterinary care until the dog is older, and even then the signs may be vague. Routine serum biochemical panel results are not helpful in screening for congenital PSS in older dogs. Congenital PSS should be considered in mature dogs, particularly miniature schnauzers, that are presented with signs potentially consistent with hepatic insufficiency. Also, screening tests (e.g., blood ammonia concentrations) should be employed to look for evidence of congenital PSS.