Comparison of urine protein-to-creatinine ratio in urine samples collected by cystocentesis versus free catch in dogs

Laura Beatrice Sezione di Clinica Medica Veterinaria, Dipartimento di Salute Animale, University of Parma, 43100 Parma, Italy.

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Francesca Nizi Clinica Veterinaria Pirani, Via Majakowski 2/L,M,N, 42100 Reggio Emilia, Italy.

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Daniela Callegari Sezione di Clinica Medica Veterinaria, Dipartimento di Salute Animale, University of Parma, 43100 Parma, Italy.

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Saverio Paltrinieri Department of Veterinary Pathology, Hygiene and Public Health, University of Milan, 20133 Milan, Italy.

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Eric Zini Clinic for Small Animal Internal Medicine, Vetsuisse Faculty, University of Zürich, CH-8057 Zürich, Switzerland.

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Paola D'Ippolito Clinica Veterinaria Pirani, Via Majakowski 2/L,M,N, 42100 Reggio Emilia, Italy.

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Andrea Zatelli Clinica Veterinaria Pirani, Via Majakowski 2/L,M,N, 42100 Reggio Emilia, Italy.

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Abstract

Objective—To assess whether urine protein-to-creatinine (UPC) ratios determined in urine samples collected by cystocentesis versus those collected by free catch provide similar diagnostic information for dogs.

Design—Evaluation study.

Animals—115 client-owned dogs evaluated because of various health problems requiring urinalysis or to screen for proteinuria in an area endemic for leishmaniasis.

Procedures—230 paired urine samples, 1 collected by cystocentesis and 1 by free catch, were collected from the 115 dogs. The UPC ratio was determined in paired urine samples (n = 162) from 81 dogs with no indication of active inflammation according to urine sediment analysis. On the basis of the UPC ratio of urine sample collected by cystocentesis, dogs were classified as nonproteinuric (UPC ratio < 0.2), borderline proteinuric (UPC ratio of 0.2 to 0.5), or proteinuric (UPC ratio > 0.5), according to the International Renal Interest Society (IRIS).

Results—The correlation between UPC ratio in urine samples collected by cystocentesis and by free catch was strong (r2 = 0.90); 75 of 81 (92.6%) dogs had UPC ratios from both urine samples that resulted in classification in the same IRIS substage with a kappa coefficient of 0.83.

Conclusions and Clinical Relevance—The UPC ratio in dogs was minimally affected in urine samples collected by free catch, thus allowing correct grading of proteinuria with this method. The high reliability of the UPC ratio in free-catch urine samples coupled with the ease of collection should increase the use of this value for assessment of proteinuria.

Abstract

Objective—To assess whether urine protein-to-creatinine (UPC) ratios determined in urine samples collected by cystocentesis versus those collected by free catch provide similar diagnostic information for dogs.

Design—Evaluation study.

Animals—115 client-owned dogs evaluated because of various health problems requiring urinalysis or to screen for proteinuria in an area endemic for leishmaniasis.

Procedures—230 paired urine samples, 1 collected by cystocentesis and 1 by free catch, were collected from the 115 dogs. The UPC ratio was determined in paired urine samples (n = 162) from 81 dogs with no indication of active inflammation according to urine sediment analysis. On the basis of the UPC ratio of urine sample collected by cystocentesis, dogs were classified as nonproteinuric (UPC ratio < 0.2), borderline proteinuric (UPC ratio of 0.2 to 0.5), or proteinuric (UPC ratio > 0.5), according to the International Renal Interest Society (IRIS).

Results—The correlation between UPC ratio in urine samples collected by cystocentesis and by free catch was strong (r2 = 0.90); 75 of 81 (92.6%) dogs had UPC ratios from both urine samples that resulted in classification in the same IRIS substage with a kappa coefficient of 0.83.

Conclusions and Clinical Relevance—The UPC ratio in dogs was minimally affected in urine samples collected by free catch, thus allowing correct grading of proteinuria with this method. The high reliability of the UPC ratio in free-catch urine samples coupled with the ease of collection should increase the use of this value for assessment of proteinuria.

Urine analysis, and especially the evaluation of proteinuria through determination of the UPC ratio, has gained considerable importance in veterinary medicine. The UPC ratio correlates well with daily protein excretion and is practical, as it can be assessed in a single urine sample.1–5 The UPC ratio is necessary to accurately quantify proteinuria and to stage renal diseases or to monitor the efficacy of specific treatments.1,6–11 Previous studies1,6–8,11 have revealed that the degree of proteinuria, when CRF is first diagnosed, is positively correlated with the progression of kidney disease and the chance of developing uremic crisis and death. Specifically, dogs affected by CRF and proteinuria with a UPC ratio ≥ 1 have a relative risk of developing uremic crises and death that is approximately 3 times as high as that of dogs with a UPC ratio < 1.6

On the basis of serum creatinine concentrations, systemic blood pressure, and the UPC ratio, the IRIS has elaborated guidelines to diagnose and stage chronic kidney disease and to monitor the course of the disease or treatment response.11 Specifically, according to the IRIS staging system, dogs can be classified as nonproteinuric, borderline proteinuric, or proteinuric on the basis of a UPC ratio < 0.2, a UPC ratio ≥ 0.2 and ≤ 0.5, or a UPC ratio > 0.5, respectively.11 Nonetheless, despite the potential diagnostic and prognostic importance of proteinuria, the widespread determination of the UPC ratio in clinical practice is limited by the difficulty of collecting appropriate urine samples. As a matter of fact, the UPC ratio is generally considered reliable only if urine samples are collected by cystocentesis.2,12–16 This technique of collecting urine samples, however, may have some drawbacks that limit the routine use of cystocentesis, including the risk of bladder tearing during puncture, the need for secure immobilization of the dog, and the difficulty of manually localizing the bladder in some dogs.14 For these reasons, cystocentesis is not accepted by a number of owners and some practitioners; as a result, urine sample collection by cystocentesis is not performed.

Although cystocentesis is generally considered the most reliable technique to provide an accurate UPC ratio,2,12–15 only a couple of studies15,16 about the effects of voiding on the urine protein measurement have been published, to our knowledge. In 1 report15 in dogs it was suggested that urine samples collected by free catch during the midstream phase of micturition, in particular in males, may result in a higher UPC ratio, compared with urine samples collected by cystocentesis.

The aim of the study reported here was to compare UPC ratios of paired urine samples collected by cystocentesis and by free catch from the same dog. If urine samples collected by free catch had similar protein concentrations as those of urine samples collected by cystocentesis, practitioners could safely determine the UPC ratio by use of the former collection technique, which is less demanding.

Materials and Methods

Animals—One hundred fifteen client-owned dogs were included in this study. All dogs were brought to a veterinarian because of a variety of health problems requiring urinalysis as part of the diagnostic workup or for vaccination. In the latter dogs, urinalysis was performed to screen for proteinuria in a region endemic for leishmaniasis. Informed consent was obtained from owners. For inclusion in the study, dogs had to have an absence of lower urinary tract disorders, including cystitis and bladder or urethral tumors, and genital disorders, including pyometra and vaginitis in females and prostatitis or preputial diseases in males. Females in estrus were also excluded from the study. Dogs were excluded from the study on the basis of combined information obtained from anamnesis, physical examination, abdominal ultrasonography, and urinalysis.

Urine sample–collection technique—For all dogs, the free-catch urine samples were collected in sterile containers for urinalysis. At least 5 mL of urine from the midstream phase of micturition was collected. Cystocentesis was performed 60 minutes later by use of a 5-mL syringe connected to a 23-gauge needle. The needle was inserted in the urinary bladder under ultrasound guidance to avoid a direct contact with the contralateral bladder wall. All urine samples were put in 10-mL, sterile, evacuated blood-collection tubes. Tubes were labeled with alphanumeric codes preassigned by simple randomization to ensure that laboratory personal were blind to urine sample source and collection technique.

Urine sediment analysis—The urine sediment of all urine samples was examined by the same individual (FN). The analysis was performed within 60 minutes of collection for urine samples stored at room temperature (approx 20°C) and within 4 hours for urine samples stored at 4° to 8°C. Urine sediment was obtained by centrifugation (10 minutes at 900 × g) of 5 mL of urine, followed by removal of 4.5 mL of supernatant, and by resuspension of the remaining 0.5 mL of urine. Twelve microliters of the resuspended urine was microscopically examined. The supernatant was transferred into separate tubes and stored at −20°C to determine urine protein concentration. Red blood cells and WBCs were expressed as mean number of cells/10 hpf (40X magnification). Cellularity, bacteriuria, spermaturia, lipiduria, and the presence of crystals were evaluated according to a semiquantitative scale (rare, moderate, abundant, and very abundant). Urine sediment with > 5 RBCs or WBCs/hpf, or increased cellularity or bacteriuria, was considered indicative of active inflammation. Urine samples with sediment suggesting active inflammation were excluded from the study.

UPC ratio—To calculate the UPC ratio, protein concentration (mg/dL) was measured with pyrogallol red,a and serum creatinine (mg/dL) was measured by use of the Jaffé methodb in undiluted urine that was thawed before the analysis. Analytes were measured in an automated spectrophotometer.c For the purpose of the present study, dogs were classified as nonproteinuric, borderline proteinuric, or proteinuric according to the IRIS staging system11; samples collected by cystocentesis were used as a reference irrespective of the presence or absence of kidney disease. Therefore, dogs with UPC ratios < 0.2 were classified as nonproteinuric, dogs with UPC ratios of 0.2 to 0.5 as borderline proteinuric, and those with UPC ratios > 0.5 as proteinuric.11

Statistical analysis—Data are expressed as mean ± SD, median, and range, and 95% CIs are calculated. All analyses were performed with computer spreadsheetd and softwaree programs. Results obtained for urine samples collected with the 2 collection techniques were compared by use of the Wilcoxon paired t test. The Spearman correlation test was used to assess a possible relationship between results obtained with the 2 methods of urine sample collection. As described, results obtained with urine samples collected by cystocentesis were used to classify the dogs as nonproteinuric, borderline proteinuric, and proteinuric, and the agreement between the results achieved with 2 methods was calculated with the Cohen kappa coefficient.17,18 Values of P < 0.05 were considered significant.

Results

Two hundred thirty urine samples were collected from 115 dogs (48 female, 18 of which were neutered, and 67 males, 1 of which was castrated) of various ages and breeds that fulfilled the inclusion criteria on the basis of anamnestic, physical examination, and abdominal ultrasonographic findings.

Urine sediment analysis—Data from 34 of the 115 dogs initially enrolled in the study were excluded from the comparison of the 2 urine sample collection techniques because of urine sediment indicative of active inflammation (ie, active urine sediment). Of these 34 dogs, 16 had an active urine sediment from both the samples collected by free catch and those collected by cystocentesis, 13 had an active urine sediment from only the urine sample collected by free catch (6 dogs each with high RBCs or WBCs, 1 dog with high RBCs and WBCs, and 1 dog with high WBCs and with bacteria), and 5 had an active urine sediment from the cystocentesis-collected sample only (4 dogs with high RBCs and 1 dog with high WBCs).

Eighty-one dogs, for a total of 162 urine samples, fulfilled the inclusion criteria after urine sediment analysis. Of the 81 dogs remaining in the study, 23 were azotemic with serum creatinine concentrations > 2.0 mg/dL; 2 had nontraumatic orthopedic problems; 4 had ocular disease; 7 had dermatologic disorders; 3 had acute self-limiting vomiting, diarrhea, or both; and 42 were admitted for routine vaccination and were considered clinically normal.

UPC ratios—Paired comparison between UPC ratios recorded for urine samples collected by free catch (mean, 0.92 ± 3.80 [95% CI, 0.08 to 1.76]; median, 0.04 [95% CI, 0.03 to 0.10]) and for those collected by cystocentesis (mean, 0.95 ± 3.99 [95% CI, 0.07 to 1.84]; median, 0.08 [95% CI, 0.05 to 0.11]) revealed no significant differences in UPC ratios (Figure 1). Also, the minimum and maximum range of UPC value distribution (0.00 to 30.56 and 0.00 to 31.82, respectively) and the first (lower) and third (upper) quartile ranges (0.00 to 0.24 and 0.01 to 0.21, respectively) were similar and largely overlapped. There was a significant (P < 0.001) strong correlation (r2 = 0.90; 95% CI, 0.84 to 0.93) between the UPC ratios of urine samples collected via the 2 techniques.

Figure 1—
Figure 1—

Correlation between UPC ratios for paired urine samples obtained from 81 dogs.

Citation: Journal of the American Veterinary Medical Association 236, 11; 10.2460/javma.236.11.1221

Results between the 2 sets of data according to the IRIS staging system11 were determined (Table 1). The kappa coefficient was 0.83 (95% CI, 0.70 to 0.95), corresponding to the highest level of agreement as reported by Landis and Koch17 and Glas et al.18 Specifically, 75 of 81 (92.6%) dogs had UPC ratios in paired urine samples that resulted in classification in the same category (ie, nonproteinuric, borderline proteinuric, or proteinuric).

Table 1—

Classification of proteinuria in 81 dogs on the basis of UPC ratios of urine samples obtained by cystocentesis versus free catch during the midstream phase of micturition.

Free-catch sampleCystocentesis-collected sample
NonproteinuricBorderline proteinuric
Nonproteinuric57*1
Borderline proteinuric35*
Proteinuric01
Total60 

Concordant results for classification of dogs according to IRIS11 staging on the basis of UPC ratios of samples collected by cystocentesis versus samples collected by free catch.

Of the 81 dogs, 6 had discordant UPC ratios between cystocentesis-collected samples and free-catch urine samples. Of these 6 dogs, 1 had a cystocentesis-collected sample with a UPC ratio (0.5) indicative of proteinuria and a free-catch sample with a UPC ratio (0.37) indicative of borderline proteinuria (false-negative result), 1 had a cystocentesis-collected sample with a UPC ratio (0.21) indicative of borderline proteinuria and a free-catch sample with a UPC ratio (0.18) indicative of no proteinuria (false-negative result), 1 had a cystocentesis-collected sample with a UPC ratio (0.49) indicative of borderline proteinuria and a free-catch sample with a UPC ratio (0.59) indicative of proteinuria (false-positive result), and 3 had cystocentesis-collected samples with UPC ratios (0.16, 0.17, and 0.19) indicative of no proteinuria and free-catch samples with UPC ratios (0.29, 0.20, and 0.21, respectively) indicative of borderline proteinuria (false-positive results).

Discussion

The early and correct identification of proteinuria is essential to identify renal diseases, design appropriate treatment, and efficiently monitor treatment efficacy, thus positively influencing the quality of life and survival time.1,6–11 In clinical practice, it would be advisable to determine the UPC ratio in all dogs with suspected proteinuria on the basis of clinical signs, in those belonging to breeds predisposed to proteinuria, or in those exposed to infectious diseases potentially causing renal damage and proteinuria (eg, ehrlichiosis and leishmaniasis). The use of the UPC ratio, however, is still limited because of the fact that it is generally accepted that the analysis needs to be performed in urine samples collected by cystocentesis. Although it is recommended to collect urine by cystocentesis to avoid inaccurate results because of postrenal conditions and overestimation of proteinuria,2,12,14–16 results of the current study indicate that dogs with inactive urine sediment can also be correctly classified according to the IRIS staging system by use of urine samples collected by free catch. Specifically, no significant differences were found in mean and median UPC ratios recorded, and results obtained from both urine sample collection methods were highly correlated with each other. More important, none of the cystocentesis-collected samples that had UPC ratios indicative of proteinuria had a paired free-catch sample with UPC ratios indicative of no proteinuria. Equally important, none of the cystocentesis-collected samples that had UPC ratios indicative of no proteinuria had a paired free-catch sample with UPC ratios indicative of proteinuria. Therefore, all dogs were classified in the same IRIS substaging category regardless of which urine sample was evaluated (ie, cystocentesis-collected or free catch), thus permitting classification of the patient in the equivalent IRIS substaging category. In the same dog, the diagnostic information obtained by urinalysis on voided samples was equal to that obtained on samples collected by cystocentesis.

There were only 2 dogs in which the analysis of urine samples collected by free catch provided a false-negative result (ie, dogs classified as nonproteinuric and borderline proteinuric on the basis of analysis of urine samples collected by free catch instead of classified as borderline proteinuric and proteinuric, respectively, on the basis of analysis of urine samples collected by cystocentesis). Compared with false-positive results, false-negative results would have more severe consequences on health status because dogs with proteinuria would not undergo additional procedures to further classify the renal damage, thus leading to progression of their renal disease. Nonetheless, it should also be mentioned that none of the dogs that were classified as proteinuric on the basis of analysis of cystocentesis-collected urine samples was classified as nonproteinuric on the basis of analysis of urine samples collected by free catch.

The reason urine samples of 6 dogs had UPC ratios that would result in misclassification is not clear. It is unlikely that the 60-minute delay between the 2 urine sample collections could have influenced the results of the second test, as could have occurred if free-catch urine samples were collected after cystocentesis (eg, thus exposing the second urine sample collection to potential blood contamination or inducing a local inflammatory reaction). It is also possible that the misclassification depends on analytic imprecision in the measurement because most of the discordant results were close to the threshold between the different IRIS categories.

It should be emphasized, however, that the essential prerequisite to obtain the same result, independently of the method of urine sample collection, is the presence of inactive urine sediment. Urine samples should thus be collected directly by cystocentesis in dogs affected by conditions potentially inducing postrenal proteinuria. In any case, even in the absence of postrenal disorders, urine samples collected by free catch must always be microscopically examined before measurement of the UPC ratio and not used for UPC ratio measurement if the urine sediment is indicative of active inflammation. On the basis of the results of this study, urine samples collected by free catch could thus be recommended in the evaluation of proteinuria in dogs.

In conclusion, this study revealed that determining the UPC ratio in urine samples collected by free catch that have an inactive urine sediment provides similar results to the analysis performed in urine samples collected by cystocentesis, thus suggesting that the former collection technique can be safely used in clinical practice. Increasing the ease of urine sample collection may encourage practitioners to measure UPC ratios on a more regular basis in dogs, possibly leading to earlier diagnosis and treatment of proteinuria with consequent reduction of related morbidity and mortality rates.1,6,7,9–11

ABBREVIATIONS

CI

Confidence interval

CRF

Chronic renal failure

IRIS

International Renal Interest Society

UPC

Urine protein-to-creatinine

a.

Fluitest USP, Biocon Diagnostik, Vohl-Marienhagen, Germany.

b.

Real Time Diagnostic System, Viterbo, Italy.

c.

Cobas Mira, Roche Diagnostic, Basel, Switzerland.

d.

Excel, Microsoft Corp, Redmond, Wash.

e.

Analyse-it Software Ltd, Leeds, West Yorkshire, England.

References

  • 1.

    Lees GE, Brown SA & Elliot J, et al. Assessment and management of proteinuria in dogs and cats: 2004 ACVIM Forum consensus statement (small animal). J Vet Intern Med 2005;19:377385.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    DiBartola SP, Chew DJ, Jacobs G. Quantitative urinalysis including 24-hour protein excretion in the dog. J Am Anim Hosp Assoc 1980;16:537546.

    • Search Google Scholar
    • Export Citation
  • 3.

    Center SA, Wilkinson E & Smith CA, et al. 24-Hour urine protein/creatinine ratio in dogs with protein-losing nephropathies. J Am Vet Med Assoc 1985;187:820824.

    • Search Google Scholar
    • Export Citation
  • 4.

    Moore FM, Brum SL, Brown L. Urine protein determination in dogs and cats: comparison of dipstick and sulfosalicylic acid procedures. Vet Clin Pathol 1991;20:9597.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Zatelli A, Paltrinieri S & Nizi F, et al. Evaluation of a urine dipstick test for confirmation or exclusion of proteinuria in dogs. Am J Vet Res 2010;71:235240.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Jacob F, Polzin DJ & Osborne CA, et al. Evaluation of the association between initial proteinuria and morbidity rate or death in dogs with naturally occurring chronic renal failure. J Am Vet Med Assoc 2005;226:393400.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Lees GE. Early diagnosis of renal disease and renal failure. Vet Clin North Am Small Anim Pract 2004;34:867885.

  • 8.

    Grauer GF. Measurement, interpretation, and implications of proteinuria and albuminuria. Vet Clin North Am Small Anim Pract 2007;37:283295.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Grauer GF, Greco DS & Getzy DM, et al. Effects of enalapril versus placebo as a treatment for canine idiopathic glomerulonephritis. J Vet Intern Med 2000;14:526533.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Grodecki KM, Gains MJ & Baumal R, et al. Treatment of X-linked hereditary nephritis in Samoyed dogs with angiotensin converting enzyme (ACE) inhibitor. J Comp Pathol 1997;117:209225.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Elliot J, Watson ADJ. Chronic kidney disease: staging and management. In: Bonagura JD, Twedt DC, eds. Kirk's current veterinary therapy XIV. St Louis: Saunders, 2008;883892.

    • Search Google Scholar
    • Export Citation
  • 12.

    Willard HD, Tvedten H. Urinary disorders. In: Barsanti JA, Lees GE, Willard HD, et al., eds. Small animal clinical diagnosis by laboratory methods. 4th ed. St Louis: Saunders, 2004;140153.

    • Search Google Scholar
    • Export Citation
  • 13.

    Gregory CR. Urinary system. In: Latimer KS, Mahaffey EA, Prasse KW, eds. Clinical pathology. 4th ed. Ames, Iowa: Iowa State Press, 2003;231259.

    • Search Google Scholar
    • Export Citation
  • 14.

    Reine NJ, Langston CE. Urinalysis interpretation: how to squeeze out the maximum information from a small sample. Clin Tech Small Anim Pract 2005;20:210.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Barsanti JA, Finco DR. Protein concentration in urine of normal dogs. Am J Vet Res 1979;40:15831588.

  • 16.

    White JV, Olivier NB & Reimann K, et al. Use of protein-to-creatinine ratio in a single urine specimen for quantitative estimation of canine proteinuria. J Am Vet Med Assoc 1984;185:882885.

    • Search Google Scholar
    • Export Citation
  • 17.

    Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159174.

  • 18.

    Glas AS, Lijmerb JG & Prinsc MH, et al. The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 2003;56:11291135.

  • Figure 1—

    Correlation between UPC ratios for paired urine samples obtained from 81 dogs.

  • 1.

    Lees GE, Brown SA & Elliot J, et al. Assessment and management of proteinuria in dogs and cats: 2004 ACVIM Forum consensus statement (small animal). J Vet Intern Med 2005;19:377385.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 2.

    DiBartola SP, Chew DJ, Jacobs G. Quantitative urinalysis including 24-hour protein excretion in the dog. J Am Anim Hosp Assoc 1980;16:537546.

    • Search Google Scholar
    • Export Citation
  • 3.

    Center SA, Wilkinson E & Smith CA, et al. 24-Hour urine protein/creatinine ratio in dogs with protein-losing nephropathies. J Am Vet Med Assoc 1985;187:820824.

    • Search Google Scholar
    • Export Citation
  • 4.

    Moore FM, Brum SL, Brown L. Urine protein determination in dogs and cats: comparison of dipstick and sulfosalicylic acid procedures. Vet Clin Pathol 1991;20:9597.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 5.

    Zatelli A, Paltrinieri S & Nizi F, et al. Evaluation of a urine dipstick test for confirmation or exclusion of proteinuria in dogs. Am J Vet Res 2010;71:235240.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 6.

    Jacob F, Polzin DJ & Osborne CA, et al. Evaluation of the association between initial proteinuria and morbidity rate or death in dogs with naturally occurring chronic renal failure. J Am Vet Med Assoc 2005;226:393400.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 7.

    Lees GE. Early diagnosis of renal disease and renal failure. Vet Clin North Am Small Anim Pract 2004;34:867885.

  • 8.

    Grauer GF. Measurement, interpretation, and implications of proteinuria and albuminuria. Vet Clin North Am Small Anim Pract 2007;37:283295.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Grauer GF, Greco DS & Getzy DM, et al. Effects of enalapril versus placebo as a treatment for canine idiopathic glomerulonephritis. J Vet Intern Med 2000;14:526533.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Grodecki KM, Gains MJ & Baumal R, et al. Treatment of X-linked hereditary nephritis in Samoyed dogs with angiotensin converting enzyme (ACE) inhibitor. J Comp Pathol 1997;117:209225.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Elliot J, Watson ADJ. Chronic kidney disease: staging and management. In: Bonagura JD, Twedt DC, eds. Kirk's current veterinary therapy XIV. St Louis: Saunders, 2008;883892.

    • Search Google Scholar
    • Export Citation
  • 12.

    Willard HD, Tvedten H. Urinary disorders. In: Barsanti JA, Lees GE, Willard HD, et al., eds. Small animal clinical diagnosis by laboratory methods. 4th ed. St Louis: Saunders, 2004;140153.

    • Search Google Scholar
    • Export Citation
  • 13.

    Gregory CR. Urinary system. In: Latimer KS, Mahaffey EA, Prasse KW, eds. Clinical pathology. 4th ed. Ames, Iowa: Iowa State Press, 2003;231259.

    • Search Google Scholar
    • Export Citation
  • 14.

    Reine NJ, Langston CE. Urinalysis interpretation: how to squeeze out the maximum information from a small sample. Clin Tech Small Anim Pract 2005;20:210.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Barsanti JA, Finco DR. Protein concentration in urine of normal dogs. Am J Vet Res 1979;40:15831588.

  • 16.

    White JV, Olivier NB & Reimann K, et al. Use of protein-to-creatinine ratio in a single urine specimen for quantitative estimation of canine proteinuria. J Am Vet Med Assoc 1984;185:882885.

    • Search Google Scholar
    • Export Citation
  • 17.

    Landis JR, Koch GG. The measurement of observer agreement for categorical data. Biometrics 1977;33:159174.

  • 18.

    Glas AS, Lijmerb JG & Prinsc MH, et al. The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 2003;56:11291135.

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