Bacterial UTI is common in dogs. Previous investigations12 found the prevalence of UTIs to be as high as 27% in healthy dogs. More recently, the prevalence of SBU in healthy dogs has been found to be much lower, with values ranging between 2% and 9%.3,4 Creation of standards by human infectious disease specialists has led to greater efforts toward identification and characterization of SBU in dogs.4,5 Some studies6–8 have classified dogs as having occult UTIs on the basis of quantitative urine microbial culture results, regardless of the presence of clinical signs. It is possible that some of these dogs might be more appropriately classified as having SBU, since the term UTI, when used to describe bacterial cystitis, typically implies the presence of dysuria, pollakiuria, and urgency, in addition to bacteriuria.5 Except for pregnant women or people undergoing invasive urologic procedures, treatment is not recommended for human patients with SBU, even if they are immunosuppressed or are kidney transplant recipients.9,10 It is currently unknown whether dogs with CKD and SBU require antimicrobial treatment.
The authors of 1 retrospective study7 found that systemic diseases such as diabetes mellitus and hyperadrenocorticism were associated with a 37% to 46% prevalence of positive results for microbial culture of urine samples from dogs. However, in that investigation,7 40 of 42 (95%) dogs with a positive urine culture result lacked clinical signs of bacterial cystitis. The prevalence of positive urine culture results in cats with CKD has been reported as 17% to 22%; most cats in those studies11,12 also lacked clinical signs. To the authors’ knowledge, the prevalence of UTI and bacteriuria in dogs with CKD has not previously been reported.
The objectives of the study reported here were to retrospectively evaluate the prevalence of bacteriuria in a population of dogs with CKD; to further categorize these patients as having SBU, bacterial cystitis, or pyelonephritis; and to summarize bacterial isolates commonly identified by microbial culture of urine samples from these dogs.
Materials and Methods
Case selection criteria
Medical records of the Matthew J. Ryan Veterinary Hospital of the University of Pennsylvania were retrospectively reviewed to identify dogs with CKD that had urine samples submitted with urinalysis and microbial culture performed between January 1, 2010, and July 1, 2015. The diagnosis and staging of CKD was made on the basis of IRIS guidelines.13 Patients with stage 1 CKD were nonazotemic but had renal concentrating defects, renal proteinuria, or persistently rising serum creatinine concentration combined with minimally concentrated urine (urine specific gravity ≤ 1.030). Stages 2 through 4 were diagnosed on the basis of serum creatinine concentration after correction of any hypovolemia or dehydration causing prerenal reduction in glomerular filtration. To be included in the study, a dog was required to have a urine sample obtained via cystocentesis and submitted for aerobic microbial culture at the inhospital microbiology lab. Patients were excluded if they had conditions that could be expected to cause lower urinary tract signs or that are commonly associated with UTI. These included endocrine disease (eg, hyperadrenocorticism or diabetes mellitus), urolithiasis, urinary incontinence, urinary bladder neoplasia, or a potential nidus for infection (eg, ureteral stent or subcutaneous ureteral bypass). Patients receiving immunosuppressive drugs orally or by injection were also excluded from the study.
Medical records review
Data collected from the medical records included signalment; clinical signs; physical examination findings; results of clinicopathologic analyses, urinalysis, and urine microbial culture; urinary tract ultrasonographic findings; treatments administered; and outcome. Routine laboratory methods were used to perform serum biochemical analyses, CBCs, and urinalyses. Aerobic microbial culture procedures and antimicrobial susceptibility testing were performed in accordance with Clinical Laboratory Standards Institute guidelines.14 Quantitative culture results indicating presence of ≥ 1,000 colony-forming units of bacteria/mL were considered to represent clinically relevant growth (ie, a positive culture result).15 Urinary tract ultrasonography was performed by board-certified radiologists or by radiology residents under the supervision of board-certified radiologists; the images were not retrospectively reviewed.
Diagnosis categories
On the basis of previously described definitions, patients with positive urine culture results were retrospectively assigned by one of the study authors (JDF) to the following 3 categories according to data in the medical records: SBU, pyelonephritis, or bacterial cystitis.4,16–18 Findings that were consistent with a diagnosis of SBU included body temperature within the reference range, absence of dysuria (stranguria or pollakiuria), blood leukocyte count and leukogram results within the respective reference ranges (including absence of bands and neutrophilic toxic changes), no evidence of progressive azotemia or progressive azotemia that failed to improve despite appropriate antimicrobial treatment and negative culture results obtained ≥ 14 days after initiation of antimicrobial therapy, absence of cylindruria, and absence of ultrasonographic findings suggestive of pyelonephritis.4 Findings that were consistent with bacterial cystitis included all of the criteria for SBU, except that dysuria was present. Findings suggestive of pyelonephritis included high body temperature (rectal temperature ≥ 39.4°C [103°F]), signs of pain elicited by renal palpation, leukocytosis (> 19.8 × 103 leukocytes/μL) neutrophilia (> 14.4 × 103 neutrophils/μL) or neutropenia (≤ 3.1 × 103 neutrophils/μL), the presence of bands or ≥ 1+ toxic change, cylindruria (with the exception of hyaline casts), newly diagnosed renal tubular glucosuria, progressive azotemia that improved with appropriate antimicrobial treatment and follow-up culture results indicating eradication of infection (≥ 14 days after initiation of antimicrobial therapy), and ultrasonographic findings suggestive of pyelonephritis. Ultrasonographic findings potentially consistent with pyelonephritis included renal pelvis dilation, echogenic debris within the renal pelvis, a hyperechoic line in the wall of the renal pelvis, renomegaly, retroperitoneal effusion, hyperechoic fat adjacent to the kidney, increased echogenicity of the renal parenchyma relative to the echogenicity of the liver and spleen, and focal hyperechoic or hypoechoic cortical lesions not consistent with a cyst, infarct, neoplasm, or other noninfectious processes.19–21 The cumulative renal ultrasonographic findings were evaluated by the attending radiologist to establish a likely diagnosis.
Follow-up data (examination results, clinicopathologic data, and diagnostic imaging findings) were also recorded. This information was used to assess response to antimicrobials and further confirm the clinical diagnosis associated with a positive urine microbial culture result.
Statistical analysis
The frequencies of positive urine microbial culture results, SBU, pyelonephritis, and bacterial cystitis were compared among individual dogs through use of a contingency table where they were categorized by IRIS CKD stage and evaluated with Fisher exact tests. Because ≥ 1 urine culture was performed in many dogs and different diagnoses were identified in the same patient, the urine culture was regarded as the unit of interest of the study. Therefore, results were categorized for each patient as well as each culture. A statistical software program was used for all analyses.a Values of P ≤ 0.05 were considered significant for all comparisons.
Results
Two hundred eighty-two urine samples were submitted for microbial culture from 195 dogs with CKD during the study period. The median number of urine culture samples submitted per patient was 1 (range, 1 to 12). Results of 47 cultures performed for 13 patients were excluded because of the presence of ureteral stents (n = 5 patients), chemotherapeutic treatment (2), or diagnosis of diabetes mellitus (2), transitional cell carcinoma (2), urinary incontinence (1), or cystic calculi (1). A total of 235 culture samples submitted for 182 patients (8 sexually intact males, 52 castrated males, 5 sexually intact females, and 117 spayed females) were included in the final analysis.
Culture results were positive for 40 of 235 (17%) urine samples; these were obtained from 33 of 182 dogs, yielding a prevalence of 18.1% for ≥ 1 positive culture result. Twenty-five of these 33 dogs were spayed females, 7 were castrated males, and 1 was a sexually intact male. Of all cultures that tested positive for microbial growth, the most frequent retrospectively determined diagnosis was SBU (18/40 [45%] cultures), followed by pyelonephritis (16 [40%]) and bacterial cystitis (6 [15%]). Seventeen dogs were classified as having SBU, with 1 dog identified as having twice during the study period. Thirteen dogs had pyelonephritis, with 3 dogs identified with the condition twice during the study period. Six patients had a diagnosis of cystitis. One dog had SBU, pyelonephritis, and cystitis, and another dog had both pyelonephritis and cystitis during the study period. Twenty-one, 43, 113, and 58 samples submitted for culture were collected from dogs with IRIS stage 1, 2, 3, and 4 CKD, respectively. One dog had a diagnosis of SBU at IRIS stage 3 CKD and later at stage 4 CKD. The breakdown of negative results and diagnoses for dogs with positive results stratified according to IRIS CKD stage was summarized (Table 1). There was no significant (P = 0.635) association detected between IRIS stage and diagnosis category. The number of positive culture results, regardless of patient diagnosis, was not significantly (P = 0.432) different among IRIS stages.
Diagnosis categories assigned on the basis of microbial culture results for 235 urine samples from 182 dogs with CKD stratified by IRIS stage.
| No clinically relevant growth | SBU | Pyelonephritis | Cystitis | |||||
|---|---|---|---|---|---|---|---|---|
| IRIS stage | No. of dogs | No. of samples | No. of dogs | No. of samples | No. of dogs | No. of samples | No. of dogs | No. of samples |
| 1 | 15 | 18 | 3 | 3 | 0 | 0 | 0 | 0 |
| 2 | 29 | 32 | 5 | 5 | 3 | 4 | 2 | 2 |
| 3 | 84 | 96 | 6 | 7 | 6 | 7 | 3 | 3 |
| 4 | 46 | 49 | 3 | 3 | 5 | 5 | 1 | 1 |
| Total | 174 | 195 | 17 | 18 | 14 | 16 | 6 | 6 |
Clinically relevant growth (a positive culture result) was defined as presence of ≥ 1,000 colony-forming units of bacteria/mL in quantitative culture. Results were positive for 40 cultures of urine samples from 33 dogs. The diagnosis categories were determined retrospectively on the basis of data collected from the medical records. Two dogs (1 with diagnoses of pyelonephritis, SBU, and cystitis, and 1 with diagnoses of pyelonephritis and cystitis) were included in ≥ 1 diagnosis category. One dog with progressive CKD that resulted in advancing IRIS stage was included in ≥ 1 IRIS stage (this dog had pyelonephritis at IRIS stage 3 and again at IRIS stage 4 CKD).
Bacterial isolates identified by culture of urine samples for dogs categorized as having SBU, pyelonephritis, and cystitis were summarized (Table 2). Escherichia coli was the most frequently observed isolate (29/40 [73%] cultures from 25/33 [76%] dogs). Two dogs had multiple cultures with growth of E coli and ≥ 1 clinical diagnosis associated with the positive culture result. One dog had diagnoses of SBU, pyelonephritis, and cystitis, and another dog had diagnoses of pyelonephritis and cystitis, all with E coli growth in urine during the study period. One dog was identified as having pyelonephritis caused by Staphylococcus pseudintermedius at 2 different times. One dog had 2 diagnoses of SBU; the first culture grew E coli, and the second grew a Klebsiella sp.
Bacterial isolates identified in 40 urine cultures from 33 dogs with CKD grouped by diagnosis category.
| SBU | Pyelonephritis | Cystitis | ||||
|---|---|---|---|---|---|---|
| Isolate | No. of dogs | No. of samples | No. of dogs | No. of samples | No. of dogs | No. of samples |
| Escherichia coli | 13 | 13 | 10 | 12 | 4 | 4 |
| Klebsiella pneumoniae | 1 | 1 | 1 | 1 | 1 | 1 |
| Staphylococcus pseudintermedius | 0 | 0 | 2 | 2 | 0 | 0 |
| β-Hemolytic Streptococcus spp | 0 | 0 | 1 | 1 | 1 | 1 |
| Enterococcus faecium | 1 | 1 | 0 | 0 | 0 | 0 |
| Proteus mirabilis | 1 | 1 | 0 | 0 | 0 | 0 |
| Citrobacter korseri | 1 | 1 | 0 | 0 | 0 | 0 |
| Pseudomonas spp | 1 | 1 | 0 | 0 | 0 | 0 |
Dogs (n = 4) with ≥ 1 positive culture result were included in ≥ 1 diagnosis category. Escherichia coli was identified in 1 dog with SBU, pyelonephritis, and cystitis and in a second dog that had pyelonephritis and cystitis (each at different times during the study period). One dog was determined to have SBU twice, once with growth of E coli and once with growth of K pneumoniae. One dog was determined to have pyelonephritis twice, with positive culture results for S pseudintermedius at both times.
All patients received systemic antimicrobial treatment on the basis of susceptibility test results obtained for each isolate. The duration of antimicrobial treatment ranged from 2 to 6 weeks at the discretion of the primary clinician. Dogs with SBU had no change in their urination habits after completing the prescribed course of antimicrobial treatment. Eight of 13 dogs with pyelonephritis were euthanized ≥ 1 month after diagnosis, and all of these dogs were still receiving antimicrobial treatment at the time of euthanasia. Four of the remaining 5 dogs with pyelonephritis survived for 2 to 8 months after the clinical diagnosis; recovery of renal function following completion of antimicrobial treatment varied among these patients, with improvements in serum creatinine concentration ranging from 0% to 37.9%. The remaining dog in this category was lost to follow-up. All dogs with bacterial cystitis had resolution of dysuria ≤ 72 hours after antimicrobial treatment was started. One dog developed a distal aortic thromboembolism and was euthanized 3 weeks after the diagnosis of bacterial cystitis; the remaining 5 dogs in this category lived ≥ 1 month after diagnosis and were subsequently lost to follow-up.
Discussion
In this population of dogs with CKD, the prevalence of bacteriuria (determined on the basis of a positive culture result for ≥ 1 urine sample) was 18.1%. The most frequently observed diagnosis associated with a positive culture result was SBU (18/40 [45%] samples). The IRIS CKD stage was not associated with the frequency of diagnosis of SBU, pyelonephritis, or cystitis. The most commonly identified isolate was E coli (29/40 [73°%] samples).
The prevalence of a positive urine culture result for dogs with CKD in the present study was less than that previously identified for dogs with other systemic diseases such as diabetes mellitus and hyperadrenocorticism, but greater than that observed for healthy dogs.3,4,7,8,22 The prevalence of a positive culture result for dogs with CKD in our study was similar to that reported elsewhere for 86 (17%) cats with CKD.12 In that study,12 31 of 134 (23%) urine samples cultured had a positive result, a value that was only slightly greater than the 40 of 235 (17%) cultures with positive results in the present study. However, 18 of 25 (72%) cats with positive culture results in the aforementioned study12 were identified as having occult UTIs (and therefore likely had SBU), whereas only 17 of 33 (52%) dogs with positive culture results in the present study had SBU. Results of another study11 revealed that 17 of 77 (22%) cats with CKD had positive urine microbial culture results, with most cats having no clinical signs of UTI. The reason for the apparently greater prevalence of presumed SBU in cats than in dogs with CKD is unknown; however, this might be attributable to less direct owner observation of cats during micturition, leading to a possible underrepresentation of bacterial cystitis in this species. Alternatively, greater prevalence may result from a lesser pathogenic potential of the organisms that colonize the feline bladder. Further studies would be necessary to make this distinction.
The authors of some studies4,23 in human and veterinary medicine have defined SBU as the presence of the same bacterial species identified in serial urine cultures from patients without clinical signs of infection. Positive growth from 2 urine samples is recommended for diagnosis of bacteriuria in women to help exclude growth resulting from extra-urinary tract contamination, whereas 1 culture result will suffice in men. However, repeatability of positive urine culture results was not used as a criterion for diagnosis of SBU in the 2011 International Society for Companion Animal Infectious Diseases consensus statement.5 It is unknown how many patients in the present study might have spontaneously cleared the bacterial colonization or gone on to develop clinical signs at a later date. To the authors’ knowledge, there has been no research to date to evaluate whether dogs with CKD and SBU require antimicrobial treatment.
Our findings were similar to data reported by Wong et al24 revealing that E coli was the most commonly observed isolate of all urine cultures from dogs as well as among dogs with pyelonephritis. In the present study, E coli was also the most common isolate in dogs with SBU. Other studies3,4 of SBU in dogs have identified E coli and S pseudintermedius as the most common isolates. Many investigations of asymptomatic bacteriuria in people have also found E coli to be the most frequent isolate; however, others have identified Proteus mirabilis or Staphylococcus aureus most commonly.23
The relationship between canine CKD and bacteriuria is not fully understood. Chronic kidney disease has not been found to be a risk factor for the development of UTI in cats.25 Urinary tract infection has also not been found to be a variable that influenced the progression of CKD in cats.26 However, a literature search identified no investigations of these relationships in dogs.
Previous reports7,8,22 have described occult UTI in dogs with systemic disease. It is likely that many of these patients would have been characterized as having SBU. Authors have suggested that antimicrobial treatment may not be indicated for dogs with SBU.4,5 Some clinicians may administer antimicrobials to dogs with CKD and SBU because of concerns regarding progression to pyelonephritis. Renal disease may be considered a disease that compromises normal defense mechanisms against UTI,1 and it has been hypothesized that compromised host defenses might prevent the development of clinical signs.27 However, 1 study28 found that isosthenuria is not a risk factor for the development of UTI in cats with systemic disease, and another29 found that performing a urine culture on the basis of isosthenuria alone in dogs is not cost-effective. Recommendations from human infectious disease experts include not treating patients with asymptomatic bacteriuria, with specific exceptions such as pregnant women or people undergoing invasive urologic procedures.24 Asymptomatic bacteriuria was not associated with progression of renal disease in people with CKD, and antimicrobial treatment given to renal transplant recipients with SBU was associated with an increase (2.8-fold difference) in the OR for developing clinical UTI.30,31 Further studies are needed to determine whether SBU requires treatment in dogs with CKD. If treatment for SBU is not indicated, the data for the population of dogs in the present study would suggest that results of only 22 of 235 (9.4%) submitted urine cultures warranted systemic antimicrobial treatment. However, all dogs with SBU in this study received antimicrobials, and generalizations regarding these treatments could not be made, as some dogs may have had early infection and could have developed clinical signs of pyelonephritis or bacterial cystitis at a later time.
There were limitations to the present study. As other authors have stated, it can be difficult to localize the site of UTI in dogs.16,17 Despite the use of rigorous criteria for defining SBU, pyelonephritis, and bacterial cystitis in the present study, it is possible that some patients were incorrectly categorized. For example, absence of lethargy, signs of renal pain, and cylindruria does not rule out pyelonephritis.18 Similarly, lack of expected ultrasonographic findings does not rule out pyelonephritis.17–19 The lethargy and anorexia observed in some patients could have been attributable to worsened uremia, which could have resulted from pyelonephritis or progression of CKD. As mentioned, it is possible that some dogs categorized as having SBU in this study might have developed clinical signs of bacterial cystitis or pyelonephritis if antimicrobials had not been administered. Because all cases of bacteriuria were treated in this manner on the basis of antimicrobial susceptibility test results, patients with azotemia that failed to improve despite resolution of bacteriuria were classified as having SBU with progressive CKD instead of pyelonephritis. Although these patients did not have any ultrasonographic evidence of pyelonephritis, it is possible that some might have had pyelonephritis without return of renal function. Additional diagnostic tests, such as measurement of circulating concentrations of renal injury biomarkers and cytokines, might have helped to provide a more accurate diagnosis of pyelonephritis; however, such biomarkers are not currently available for commercial testing. Further, many of the urine cultures included in this study were performed as part of the routine monitoring for progression of CKD, and the reason for performing a culture was not clearly stated in many patient records, making it difficult to ascertain the exact proportion of dogs that had clinical signs of UTI.
Prospective research is needed to determine whether antimicrobial treatment is indicated in dogs with CKD and SBU. Additionally, evaluation of biomarkers that can identify renal tubular injury may allow for better characterization of patients with SBU and occult pyelonephritis and thereby improve antimicrobial stewardship.
Acknowledgments
No third-party funding or support was received in connection with this study or the writing or publication of the manuscript. The authors declare that there were no conflicts of interest.
The authors thank Dr. Ken Drobatz for assistance with statistical analysis.
ABBREVIATIONS
| CKD | Chronic kidney disease |
| IRIS | International Renal Interest Society |
| SBU | Subclinical bacteriuria |
| UTI | Urinary tract infection |
Footnotes
Stata, version 12.0 for Mac, Stata Corp, College Station, Tex.
References
1. Bush BM. A review of the aetiology and consequences of urinary tract infections in the dog. Br Vet J 1976;132:632–641.
2. Kivistö AK, Vasenius H, Sandholm M. Canine bacteruria. J Small Anim Pract 1977;18:707–712.
3. McGhie JA, Stayt J, Hosgood GL. Prevalence of bacteriuria in dogs without clinical signs of urinary tract infection presenting for elective surgical procedures. Aust Vet J 2014;92:33–37.
4. Wan SY, Hartmann FA, Jooss MK, et al. Prevalence and clinical outcome of subclinical bacteriuria in female dogs. J Am Vet Med Assoc 2014;245:106–112.
5. Weese JS, Blondeau JM, Boothe D, et al. Antimicrobial use guidelines for treatment of urinary tract disease in dogs and cats: antimicrobial guidelines working group of the International Society for Companion Animal Infectious Diseases. Vet Med Int 2011;2011:263768.
6. Thomsen MK, Svane LC, Poulsen PH. Canine urinary tract infection. Detection, prevalence and therapeutic consequences of bacteriuria. Nord Vet Med 1986;38:394–402.
7. Forrester SD, Troy GC, Dalton MN, et al. Retrospective evaluation of urinary tract infection in 42 dogs with hyperadrenocorticism or diabetes mellitus or both. J Vet Intern Med 1999;13:557–560.
8. Hess RS, Saunders HM, Van Winkle TJ, et al. Concurrent disorders in dogs with diabetes mellitus: 221 cases (1993–1998). J Am Vet Med Assoc 2000;217:1166–1173.
9. Nicolle LE, Bradley S, Colgan R, et al. Infectious Diseases Society of America guidelines for the diagnosis and treatment of asymptomatic bacteriuria in adults. Clin Infect Dis 2005;40:643–654.
10. Fiorante S, López-Medrano F, Lizasoain M, et al. Systematic screening and treatment of asymptomatic bacteriuria in renal transplant recipients. Kidney Int 2010;78:774–781.
11. Mayer-Roenne B, Goldstein RE, Erb HN. Urinary tract infections in cats with hyperthyroidism, diabetes mellitus and chronic kidney disease. J Feline Med Surg 2007;9:124–132.
12. White JD, Stevenson M, Malik R, et al. Urinary tract infections in cats with chronic kidney disease. J Feline Med Surg 2013;15:459–465.
13. International Renal Interest Society Staging of Chronic Kidney Disease. Available at www.iris-kidney.com/guidelines/staging.html. Accessed Jul 15, 2015.
14. Clinical Laboratory Standards Institute. Performance standards for antimicrobial susceptibility disk and dilution susceptibility tests for bacteria isolated from animals. Approved standard. CLSI document M31-A3. 3rd ed. Wayne, Pa: Clinical and Laboratory Standards Institute, 2008.
15. Barsanti JA, Finco DR. Laboratory findings in urinary tract infections. Vet Clin North Am Small Anim Pract 1980;9:729–748.
16. Finco DR, Shotts EB, Crowell WA. Evaluation of methods for localization of urinary tract infection in the female dog. Am J Vet Res 1979;40:707–712.
17. Finco DR, Barsanti JA. Localization of urinary tract infection in the dog. Vet Clin North Am Small Anim Pract 1980;9:775–781.
18. Finco DR, Barsanti JA. Bacterial pyelonephritis. Vet Clin North Am Small Anim Pract 1980;9:645–660.
19. Neuwirth L, Mahaffey M, Crowell W, et al. Comparison of excretory urography and ultrasonography for detection of experimentally induced pyelonephritis in dogs. Am J Vet Res 1993;54:660–669.
20. Choi J, Jang J, Choi H, et al. Ultrasonographic features of pyonephrosis in dogs. Vet Radiol Ultrasound 2010;51:548–553.
21. D'Anjou MA, Bédard A, Dunn ME. Clinical significance of renal pelvic dilatation on ultrasound in dogs and cats. Vet Radiol Ultrasound 2011;52:88–94.
22. McGuire NC, Schulman R, Ridgway MD, et al. Detection of occult urinary tract infections in dogs with diabetes mellitus. J Am Anim Hosp Assoc 2002;38:541–544.
23. Nicolle LE. Asymptomatic bacteriuria. Curr Opin Infect Dis 2014;27:90–96.
24. Wong C, Epstein SE, Westropp JL. Antimicrobial susceptibility patterns in urinary tract infections in dogs (2010–2013). J Vet Intern Med 2015;29:1045–1052.
25. Martinez-Ruzafa I, Kruger JM, Miller R, et al. Clinical features and risk factors for development of urinary tract infections in cats. J Feline Med Surg 2012;14:729–740.
26. Chakrabarti S, Syme HM, Elliott J. Clinicopathological variables predicting progression of azotemia in cats with chronic kidney disease. J Vet Intern Med 2012;26:275–281.
27. Bartges JW. Diagnosis of urinary tract infections. Vet Clin North Am Small Anim Pract 2004;34:923–933, vi.
28. Bailiff NL, Westropp JL, Nelson RW, et al. Evaluation of urine specific gravity and urine sediment as risk factors for urinary tract infections in cats. Vet Clin Pathol 2008;37:317–322.
29. Tivapasi MT, Hodges J, Byrne BA, et al. Diagnostic utility and cost-effectiveness of reflex bacterial culture for the detection of urinary tract infection in dogs with low urine specific gravity. Vet Clin Pathol 2009;38:337–342.
30. Tencer J. Asymptomatic bacteriuria-a long-term study. Scand J Urol Nephrol 1988;22:31–34.
31. Green H, Rahamimov R, Goldberg E, et al. Consequences of treated versus untreated asymptomatic bacteriuria in the first year following kidney transplantation: retrospective observational study. Eur J Clin Microbiol Infect Dis 2013;32:127–131.
