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PAPER

Comparison of three techniques for the diagnosis of urinary tract infections in dogs with urolithiasis
OBJECTIVES: To identify an appropriate sampling technique(s) to accurately detect the bacteria causing urinary tract infections in dogs with urolithiasis. METHODS: Twenty-one dogs with urolithiasis were included in the study. Three types of samples were taken from each dog. Urine was collected by cystocentesis, and a urinary bladder mucosal biopsy and urolith were retrieved during cystotomy. The samples were then cultured on blood agar and MacConkeys agar to identify the bacteria associated with urinary tract infections. RESULTS: Bacterial urinary tract infection was found in 16 cases (76 19 per cent). The most prevalent bacteria found to cause urinary


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I. S. GATORIA, N. S. SAINI, T. S. RAI P. N. DWIVEDI


Journal of Small Animal Practice (2006) 47, 727732

tract infection were Escherichia coli (n=7), followed by coagulasepositive Staphylococcus species (n=4), Klebsiella pneumoniae (n=2), Pseudomonas aeruginosa (n=2) and Proteus mirabilis (n=1). In the case of a positive urine culture, the same bacteria were also cultured from the urinary bladder mucosal biopsy alone or from both the urinary bladder mucosal biopsy and urolith. However, in the case of a negative urine culture, bacteria were found to be present in the urinary bladder mucosal biopsy or urolith cultures in 23 81 per cent of dogs. The uroliths that gave positive culture


results were either infection-induced uroliths composed of struvite and calcium carbonate phosphate, ammonium acid urate only or metabolic uroliths composed of calcium oxalate and calcium phosphate, or calcium phosphate only. All the uroliths that gave negative culture results were metabolic uroliths composed of calcium oxalate and/or calcium phosphate, and uric acid and calcium phosphate. CLINICAL SIGNIFICANCE: When the culture from the urine obtained by cystocentesis is negative, cultures of urinary bladder mucosal biopsy and urolith are recommended in dogs with urolithiasis in order to accurately assess the microbiological status of the urinary tract.
Department of Veterinary Surgery and Radiology, and Department of Veterinary Microbiology, Guru Angad Dev and Veterinary and Animal Sciences University, Ludhiana 141 004, Punjab, India

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INTRODUCTION
Bacterial urinary tract infections (UTIs) are a major clinical problem in dogs and occur in about 14 per cent of all dogs at some time in their life (Ling 1984). The bacteria most frequently involved in UTIs include Escherichia coli, Proteus, Staphylococcus, Streptococcus, Klebsiella, Enterobacter and Pseudomonas species (Jarvinen 2002). These bacterial UTIs frequently occur in association with canine urolithiasis, and the bacteria isolated are similar to those found in patients with UTIs without urolithiasis. The role of bacterial UTI varies with the type of urolith. Bacterial UTI, especially caused by urease-producing bacteria such as Staphylococcus intermedius and Proteus species is often an important predisposing factor in the initiation, growth and recurrence of struvite (magnesium ammonium phosphate) uroliths (Osborne and others 1999), whereas in patients with metabolic uroliths, such as calcium oxalate, cystine, urate or silica, the bacterial UTI is a frequent complication occurring secondarily (Klausner and Osborne 1979). However, calcium oxalate and other sterile uroliths in the urinary tract may become infected with urease-producing or nonurease-producing bacteria during a UTI (Thompson and Stamey 1973, Shortliffe and others 1984). Bacteria contained within uroliths probably represent those present at the time of the urolith formation (Osborne and others 1993). In cases of canine urolithiasis, it has been recommended that a bladder mucosal biopsy, as well as uroliths, should be retrieved aseptically during cystotomy for aerobic bacterial culture in order to identify UTIs that cannot be detected by urine culture (Ruby and Ling 1986, Waldron 1993, Hamaide and others 1998). These bacterial UTIs may cause problems of equal or greater severity than the uroliths (Stone and Barsanti 1992, Bartges and others 1999). It is therefore critical to identify the bacteria and to conduct antimicrobial sensitivity tests in order to completely eradicate the bacterial UTI. The present study was therefore conducted to compare the results of bacterial culture of urine, urinary bladder mucosal
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biopsies and uroliths in dogs treated for urolithiasis to identify an appropriate sampling technique(s) to accurately detect the bacteria causing UTIs in dogs with urolithiasis.

obtained in a sterile Petri dish. Urocystoliths were also retrieved during cystotomy in a sterile Petri dish. All three samples were immediately stored in a refrigerator at 4C for four to six hours before bacteriological analysis. Bacteriological processing and analysis of samples Both qualitative and quantitative cultures were conducted on the urine sample. Qualitative cultures were carried out for the isolation and identication of bacteria in urine, whereas quantitative cultures were carried out to determine the signicant bacteriuria (the number of bacteria per unit volume of urine). For the qualitative culture, a 5 ml urine sample was centrifuged in a sterile tube at 1700 g for 15 minutes. Supernatant was rejected and a loopful of sediment was inoculated to blood agar and MacConkeys agar plates. These plates were incubated at 37C for 24 hours. Following incubation, individual colonies were identied on the basis of colony morphology, Gram staining and standard biochemical reactions (Quinn and others 1994). For the quantitative culture, a spread plate method was performed. A serial dilution of the urine sample ranging from 1021 to 1026 was made, and a 01 ml inoculum of each dilution in duplicate was placed on the surface of each agar plate. It was then spread uniformly with the help of a ame-sterilised nichrome wire, bent in a L-shape. All agar plates were incubated at 37C for 24 hours. After incubation, appropriate plates with a dilution sufcient to produce non-conuent growth, that is, those giving rise to 30 to 300 colony forming units (CFU)/plate, were selected for colony counts (Quinn and others 1994). Average number of CFU/plate were calculated from this dilution, and after applying the dilution factor, the number of bacteria were expressed as CFU/ml of urine. Only qualitative culture of the urinary bladder mucosal biopsy was performed. The sample was macerated in 2 ml of brain-heart infusion broth and incubated at 37C for six to eight hours after which subcultures were inoculated to the blood agar and MacConkeys agar

MATERIALS AND METHODS


The study was conducted on 21 dogs with urolithiasis that were referred to the Punjab Agricultural University, Ludhiana, between January 1, 2002 and April 31, 2003. The dogs had a mean (sd) age of 735 (059) years. The study included the following breeds: spitzs (n=6), dobermanns (n=4), German shepherd dogs (n=3), boxers (n=2), dalmatians (n=2), Lhasa apsos (n=2), a sheepdog (n=1) and a crossbreed dog (n=1). Bacterial isolations were performed on the urine samples collected by cystocentesis and urinary bladder mucosal biopsies and uroliths collected during cystotomy. The uroliths were also analysed to determine their chemical composition. At the time of presentation, the signalment and history of the dogs were recorded, and they all underwent a complete physical examination. Plain abdominal radiographs, complete blood count and plasma urea nitrogen and plasma creatinine evaluation was conducted to assess the status of each animal. Any antimicrobials being administered were discontinued at least 48 hours before the collection of samples. Urine samples were submitted for gross and microscopic urinalysis. In 17 dogs (8095 per cent) cystotomy alone was performed, and in four dogs (1905 per cent) both urethrotomy and cystotomy were performed under general anaesthesia with a combination of 05 mg/kg diazepam and 10 to 15 mg/kg thiopental sodium. Preoperatively, 05 mg/kg meloxicam was administered as analgesic to each animal. Sample collection procedures Urine was collected either by prepubic cystocentesis before surgery or by direct cystocentesis during cystotomy in sterile syringes. During cystotomy, an incisional biopsy from the mucosal edges of the bladder (greater than 5 mm2 in size) was
Journal of Small Animal Practice

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Comparison of techniques for diagnosis of urinary tract infections in dogs

Table 1. Comparative bacterial cultures of urine, bladder mucosal biopsy and urolith in 21 dogs
Dog Urine (CFU/ml) 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18-21 Escherichia coli (.102) Escherichia coli (.105) Escherichia coli (.103) Escherichia coli (.106) Klebsiella pneumoniae (.105) Klebsiella pneumoniae (.105) Pseudomonas aeruginosa (.103) Pseudomonas aeruginosa (.103) Staphylococcus intermedius (.105) Proteus mirabilis (.105) Staphylococcus intermedius (.105) No growth No growth No growth No growth No growth No growth No growth Comparative culture results Biopsy Escherichia coli Escherichia coli Escherichia coli Escherichia coli Klebsiella pneumoniae Klebsiella pneumoniae Pseudomonas aeruginosa Pseudomonas aeruginosa Staphylococcus intermedius Proteus mirabilis Staphylococcus intermedius Escherichia coli Escherichia coli Staphylococcus intermedius No growth No growth No growth No growth Chemical composition of urolith Urolith No growth No growth No growth No growth No growth No growth No growth No growth No growth Proteus mirabilis Staphylococcus intermedius No growth No growth No growth Escherichia coli Staphylococcus aureus No growth No growth CaOx CaPO4 CaOx and CaPO4 CaOx and CaPO4 CaPO4 CaOx and CaPO4 UA and CaPO4 CaOx and CaPO4 CaOx and CaPO4 MAP and CaCO3PO4 AMAU UA and CaPO4 CaOx and CaPO4 UA and CaPO4 CaOx and CaPO4 CaPO4 CaPO4 (n=1) CaOx and CaPO4 (n=4)

CFU Colony forming units, CaOx Calcium oxalate, CaPO4 Calcium phosphate, UA Uric acid, MAP Magnesium ammonium phosphate, CaCO3PO4 Calcium carbonate phosphate, AMAU Ammonium acid urate

plates. Thereafter, standard procedure as described by Quinn and others (1994) was followed. Only qualitative culture was also performed of the urocystoliths. Urocystoliths were placed in absolute alcohol for two hours, after which they were washed with sterile saline four to ve times and crushed with a sterilised pestle and mortar. Sterilised saline (1 ml) was added to the crushed urolith, and 1 ml of the salineurolith suspension was added to 4 ml sterilised trypticase soya broth. The broth tubes were incubated at 37C for six to eight hours, after which subcultures were inoculated to blood agar and MacConkeys agar plates. Thereafter, standard procedure as described by Quinn and others (1994) was again followed.

RESULTS
Bacterial UTI was found in 16 cases (7619 per cent). In seven of these 16 cases (4375 per cent), E coli was cultured either from both the urine and bladder mucosal biopsy or from the bladder mucosal biopsy or urolith alone. In three cases (1875 per cent), S intermedius was cultured either from all three samples or from the urine and bladder mucosal biopsy together or from the biopsy alone. In one case, Staphylococcus aureus was cultured from the urolith alone, but in two cases each, Klebsiella
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pneumoniae and Pseudomonas aeruginosa were cultured from both the urine and the bladder mucosal biopsy. In one case, Proteus mirabilis was cultured from all three samples. The results of the comparative study of bacterial cultures of the urine, urinary bladder mucosal biopsy and urolith are shown in Table 1. In ve of 21 cases (2381 per cent), no bacteria were cultured from the urine, bladder mucosal biopsy or urolith. In two cases (952 per cent), the three cultures revealed identical bacterial isolates. In nine cases (4286 per cent), the urine and bladder mucosal biopsy cultures revealed identical bacteria that were not cultured from the urolith. In three cases (1429 per cent), the bladder mucosal biopsy cultures revealed bacteria that were not cultured from the urine and urolith samples. In two cases (952 per cent), the urolith cultures revealed bacteria that were not cultured from the urine and

bladder mucosal biopsy. The urine samples that were positive for bacterial cultures quantitatively yielded a bacterial count of more than 102 CFU/ml (n=1, 909 per cent), more than 103 CFU/ml (n=3, 2727 per cent), more than 105 CFU/ml (n=6, 5455 per cent) or more than 106 CFU/ml (n=1, 909 per cent). The bacteria isolated from urine culture by the qualitative culture technique were identical to those isolated by the quantitative culture technique.

DISCUSSION
Bacterial UTI was found in 16 cases (7619 per cent). In seven cases (4375 per cent) E coli was cultured from the urinary tract, S intermedius was cultured from three cases (1875 per cent), K pneumoniae and P aeruginosa in two cases (125 per cent) each and P mirabilis and S aureus

Escherichia coli Staphylococcus intermedius Klebsiella pneumoniae Pseudomonas aeruginosa Proteus mirabilis Staphylococcus aureus

FIG 1. Bacteria isolated from the urinary tract of dogs (n516)

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was cultured in one case each (Fig 1). It implies that in the present study, E coli followed by coagulase-positive Staphylococcus species were found to be the most common bacteria causing UTIs. Similar ndings have previously been reported in dogs (Weaver and Pillinger 1975, Brown and others 1977, Klausner and Osborne 1979, Jarvinen 2002) and bovines (Singh and others 1982). Kogika and others (1995) also isolated E coli (prevalence of infection 353 per cent) followed by Staphylococcus species (235 per cent), Proteus species (157 per cent), Streptococcus species (137 per cent), Klebsiella species (98 per cent), P aeruginosa (39 per cent), Enterobacter cloacae (20 per cent), Citrobacter freundii (20 per cent) and Providencia rettgeri (20 per cent) from the urine of 51 dogs with UTI in which urolithiasis was a common predisposing factor. In the present study, the organism distribution was similar to some extent to the distribution commonly listed in the literature, with E coli being the most common and coagulase-positive Staphylococcus species being the second most common organism. Ling (1984) reported that approximately 75 per cent of UTIs in dogs were caused by a single species of pathogen, 18 per cent by two species and 6 per cent by three species. However, in the present study, in the 16 cases (7619 per cent) cultured positive, UTI was caused by a single species of pathogen. In this study, all the urine samples that were positive for bacterial cultures quantitatively yielded a bacterial count between 102 and 106 CFU/ml. Comer and Ling (1981) reported that isolation of more than 102 bacteria/ml in a urine sample obtained by cystocentesis was considered to be indicative of UTI. It has been reported that any bacterial growth developed from samples collected under aseptic conditions would be considered signicant (Lulich and Osborne 1995, Hamaide and others 1998). In some dogs it appears that antibiotic use before sample collection had an impact on the results of urolith culture, such as in the dogs in which no bacteria were isolated by any sampling technique (n=5, 2381 per cent) (amoxicillin [n=3] and cefalexin [n=2]). These ndings suggest that antibiotic use before collection
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of samples had an inhibitory effect on bacterial growth. The uroliths in these dogs were found to be composed of calcium oxalate and calcium phosphate (n=4), or calcium phosphate only (n=1). UTI is often absent in patients with metabolic uroliths such as calcium oxalate, apatite, urate, cystine or silica. However, these metabolic uroliths might be associated with UTI, although not as a cause of these uroliths but developing secondarily in the presence of these uroliths in the urinary tract where the organisms isolated were often urease negative (Klausner and Osborne 1979). In dogs, where identical bacteria were cultured from all three sampling techniques (n=2, 952 per cent), the uroliths were found to be composed of struvite (magnesium ammonium phosphate) and calcium carbonate phosphate (n=1), or ammonium acid urate only (n=1). In the dog with struvite and calcium carbonate phosphate uroliths, P mirabilis, a urease-producing bacterium, was isolated from the urine, bladder mucosal biopsy and urolith sample. Infection by ureaseproducing bacteria was often an important predisposing factor in the initiation, growth and recurrence of struvite (magnesium ammonium phosphate) uroliths (Klausner and Osborne 1979, Osborne and others 1999). Infection-induced struvite uroliths often contained some quantity of calcium phosphate and calcium carbonate phosphate (Osborne and others 1999). Ruby and Ling (1986) isolated predominantly coagulase-positive Staphylococcus (47 per cent) followed by Streptococcus (10 per cent) and P mirabilis (3 per cent) from the struvite uroliths in dogs. S intermedius and Proteus species (potent urease producers) were commonly isolated from the dogs with infection-induced struvite uroliths (Osborne and others 1999). In the dog with ammonium acid urate uroliths, S intermedius was isolated from the urine, bladder mucosal biopsy and urolith sample. Since urate uroliths are metabolic uroliths, when infection develops with this type of urolith, it is a sequelae rather than a predisposing cause. But infection with urease-producing bacteria might be an important factor in the formation of urate uroliths due to the producJournal of Small Animal Practice

tion of increased amounts of ammonium that enhance the precipitation of ammonium urate (Porter 1963, Klohn and others 1986, Kruger and Osborne 1986, Hamaide and others 1998). Case and others (1993) also reported three urate-containing uroliths to be positive for coagulase-positive Staphylococcus. Bacteria harboured inside the uroliths might not always be the same species as those present in the urine (Osborne and others 1993). However, in the present study, two dogs revealed identical bacteria from the urine, bladder mucosal biopsy and urolith. In dogs, where bacteria were cultured from the urine, the same organism was also cultured from the bladder mucosal biopsy but not from the urolith (n=9, 4286 per cent). The uroliths were found to be composed of calcium oxalate and calcium phosphate (n=5), calcium phosphate only (n=2), calcium oxalate only (n=1) or uric acid and calcium phosphate (n=1). Since these were metabolic uroliths, their initiation and growth were not associated with bacteria. However, these uroliths might predispose the dog to the development of UTI by damaging the urothelium and/or by impeding the urine ow (Klausner and Osborne 1979). So, the cultures from the inside of these uroliths were negative whereas the urine and bladder mucosal biopsies were found to be positive for bacterial growth. In dogs, where bacteria were cultured from the urolith only, but not from the urine and bladder mucosal biopsy (n=2, 952 per cent), the uroliths were found to be composed of calcium oxalate and calcium phosphate (n=1), or calcium phosphate only (n=1). Even though these were metabolic uroliths, the cultures from inside the uroliths were positive for S aureus and E coli, both of which are non-ureaseproducing bacteria. Klausner and Osborne (1979) reported that cultures of the inside of such metabolic uroliths are usually sterile. However, calcium oxalate and other sterile stones in the urinary tract might become infective with urease-producing or non-urease-producing bacteria during the UTI (Thompson and Stamey 1973, Shortliffe and others 1984). Radostits and others (2000) also reported that a nidus favoured the deposition of crystals around itself to form a urolith,

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Comparison of techniques for diagnosis of urinary tract infections in dogs

and this nidus might be a group of desquamate epithelial cells or necrotic tissue that was occasionally formed as a result of local infection in the urinary tract. Bacteria contained within the uroliths probably represented those present at the time that urolith was formed (Osborne and others 1993). These bacteria might embed within the interstices of the urolith, thereby becoming impervious to treatment by antibiotics (Shortliffe and Spigelman 1986). Negative culture of the urine and bladder mucosal biopsy may be due to host defence mechanisms. Clark (1974) reported Staphylococcus epidermidis and Streptococcus faecalis from the culture of a urolith composed of uric acid and phosphate. Singh and others (1982) also isolated E coli from the interior of two metabolic uroliths out of the 30 urolith nuclei examined from bovines. Ruby and Ling (1986) also isolated coagulasepositive Staphylococcus from 14 per cent of the non-struvite uroliths. In dogs, where bacteria were cultured from the bladder mucosal biopsy only, but not from the urine and urolith (n=3, 1429 per cent), the uroliths were found to be composed of uric acid and calcium phosphate (n=2), or calcium oxalate and calcium phosphate (n=1). Isolation of bacteria from the urinary tract tissue (such as bladder wall or renal biopsy) obtained under aseptic conditions would be indicative of UTI, regardless of the number of bacteria present (Lulich and Osborne 1995, Hamaide and others 1998). Bacteria isolated were E coli in two dogs and S intermedius in one dog. Collins and others (1998) isolated Pseudomonas species from the bladder wall of a dog in which urine culture was negative. Similarly, Hamaide and others (1998) also isolated S intermedius from the bladder mucosal biopsy of two dogs in which urine and urolith cultures were negative. In the present study, negative urolith culture from these cases suggested that the dietary and/or metabolic factors might have been involved in the genesis of these sterile uroliths, as reported by Osborne and others (1999). The negative urine cultures might also be due to host defence mechanisms or presurgical antimicrobial

therapy given to the dogs (Brodey 1955, Weaver and Pillinger 1975, Singh and others 1982). Adherence of bacteria to the urothelium could explain positive bladder mucosal biopsy culture results in the presence of negative urine and urolith culture or only negative urolith culture results. It has previously been reported that these urothelial cells normally produce a layer of glycosaminoglycan that coats their surface (Parsons and others 1977, Balish and others 1982). The surface coating of glycosaminoglycan and water non-specically inhibits bacterial adherence to urothelial cells and therefore enhances the mechanical washout of bacteria during micturition. But when these urocystoliths cause damage to the urothelium, they might alter the anti-adherence activity of the glycosaminoglycan layer, enhancing the adherence of bacteria to the urothelium, which further results in positive biopsy cultures. A further explanation of the positive biopsy culture might be the production of urease by urease-producing bacteria, which has also been known to alter the anti-adherence activity of the glycosaminoglycan layer at the transitional cell surface (Parsons and others 1984). In 11 cases (5238 per cent) where bacteria were isolated from urine obtained by cystocentesis, the same bacteria were also isolated either from the bladder mucosal biopsy alone (4286 per cent) or from both the bladder mucosal biopsy and uroliths (952 per cent). In 10 cases (4762 per cent), no bacteria were isolated from the urine. In ve (2381 per cent) of these 10 cases, bacteria were isolated either from the bladder mucosal biopsy or the urolith. Therefore, the results of this study suggest that if bacteria are isolated from urine culture before surgery, it is not necessary to culture bladder mucosal biopsy or urolith. On the other hand, if no bacteria are isolated from urine samples, bacteria can be isolated by the other two sampling methods in 25 per cent of cases. Therefore, one sampling method cannot be recommended above the others. So, to rule out an underlying UTI following a negative urine culture, bladder mucosal biopsy and urolith cultures should be performed in dogs with urolithiasis.

Conclusions If urine culture obtained by cystocentesis is positive before surgery, it is not necessary to culture bladder mucosal biopsy or urolith. However, when the culture from the urine obtained by cystocentesis is negative, cultures of bladder mucosal biopsy and urolith are recommended in dogs with urolithiasis in order to accurately assess the microbiological status of the urinary tract. The results of this study also suggest that for urine samples both qualitative and quantitative culture techniques should be undertaken.

References
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in dogs. Brazilian Journal of Veterinary Research and Animal Science 32, 31-36 KRUGER, J. M. & OSBORNE, C. A. (1986) Etiopathogenesis of uric acid and ammonium urate uroliths in non-Dalmatian dogs. Veterinary Clinics of North America: Small Animal Practice 16, 87-126 LING, G. V. (1984) Therapeutic strategies involving antimicrobial treatment of the canine urinary tract. Journal of the American Veterinary Medical Association 185, 1162-1164 LULICH, J. P. & OSBORNE, C. A. (1995) Bacterial infections of the urinary tract. In: Textbook of Veterinary Internal Medicine: Diseases of Dogs and Cats. Eds S. J. Ettinger and E. C. Feldman. W. B. Saunders, Philadelphia, PA, USA. pp 1775-1787 OSBORNE, C. A., LULICH, J. P., POLZIN, D. J., ALLEN, T. A., KRUGER, J. M., BARTGES, J. W., KOEHLER, L. A., ULRICH, L. K., BIRD, K. A. & SWANSON, L. L. (1999) Medical dissolution and prevention of canine struvite urolithiasis: twenty years of experience. Veterinary Clinics of North America: Small Animal Practice 29, 73-111 OSBORNE, C. A., LULICH, J. P., UNGER, L. K., BARTGES, J. W. & FELICE, L. J. (1993) Canine and feline urolithiasis: relationship of etiopathogenesis with

treatment and prevention. In: Disease Mechanisms in Small Animal Surgery. Ed M. J. Bojrab. Lea & Febiger, Philadelphia, PA, USA. pp 476478 PARSONS, C. L., GREENSPAN, C., MOORE, S. W. & MULHOLLAND, S. G. (1977) Role of surface mucin in primary antibacterial defence of bladder. Urology 9, 48-52 PARSONS, C. L., SKANFFER, C., MULHOLLAND, S. G. & GRIFFITH, D. P. (1984) Effect of ammonium on bacterial adherence to bladder transitional epithelium. Journal of Urology 132, 365-366 PORTER, P. (1963) Urinary calculi in the dog. II. Urate stones and purine metabolism. Journal of Comparative Pathology 73, 119-135 QUINN, P. J., CARTER, M. E., MARKEY, B. K. & CARTER, G. R. (1994) Clinical Veterinary Microbiology. Mosby Ltd: London, UK RADOSTITS, O. M., GAY, C. C., BLOOD, D. C. & HINCHCLIFF, K. W. (2000) Diseases of urinary system. In: Textbook of the Diseases of Cattle, Sheep, Pigs, Goats and Horses. W. B. Saunders, Philadelphia, PA, USA. pp 465-500 RUBY, A. L. & LING, G. V. (1986) Bacterial culture of uroliths: techniques and interpretation of results.

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