Occurrence of bacteriuria in 18 catheterised cats with obstructive lower urinary tract disease: a pilot study

Abstract

The incidence of catheter-associated urinary tract infections in cats catheterised for an obstructive lower urinary tract disease (LUTD) has not previously been evaluated. The objective of this study was to evaluate the frequency of significant bacteriuria in cats with obstructive LUTD managed for 48 h with a closed urine collection system. Eighteen male cats admitted for a non-infectious obstructive LUTD were evaluated. This was a prospective study. A standard protocol was used for aseptic catheter placement and maintenance. Three urine samples were collected from each animal through the catheter immediately after placement, 24 h after placement and just before removal. All samples underwent complete urinalysis, including bacterial culture. Catheter tips were tested by bacterial culture. Six cats (33.3%) developed significant bacteriuria during catheterisation. The causative bacteria were common feline uropathogens (Escherichia coli, Staphylococcus species) in five cases, and Streptococcus bovis in one. One cat developed a fungal infection. The presence of bacteria in urinary sediment was correlated strongly with positive urine culture results. The catheter tips from 10/18 cats (55.5%) were positive for culture. The positive predictive value of a positive culture from the urinary catheter tip was 87.5%. The specificity was 53.8%. The same infectious agents were cultured from both urine and catheter tip in six cases. In summary, one-third of cats developed significant bacteriuria during catheterisation. Silent bacteriuria could not be clearly differentiated from true urinary tract infection. The presence of bacteria in the urinary sediment was strongly indicative of bacteriuria. The specificity of urinary catheter tip culture was low.

Introduction

Catheter-associated urinary tract infection (CAUTI) is a major health concern in humans. It is responsible for 40% of nosocomial infections, making it the most common type of nosocomial infection.¹ A recent study in dogs concluded that the placement of an indwelling urinary catheter to determine urinary output was associated with a low risk of CAUTI during the first 3 days of catheterisation, provided rules for aseptic catheter management were observed.²

Male cats are commonly affected by obstructive lower urinary tract disease (LUTD) requiring indwelling urinary catheterisation. However, few data are available on the risks of significant bacteriuria associated with this procedure in cats. In 1981, an experimental study of 51 normal male cats managed with an open indwelling urethral catheterisation system reported that these cats had a high risk (56%) of developing bacteriuria.³ Obstructive LUTD is a condition associated with compromised integrity of both the bladder and the urethral mucosa. Prevention of CAUTI is a major concern in these cats, but the use of prophylactic antibiotic treatment is still a matter for debate. No study has specifically addressed whether cats with obstructive LUTD managed aseptically with an indwelling urinary catheter are at risk of developing CAUTI. The primary aim of this prospective study was to evaluate the probability of bacteriuria among cats with non-infectious obstructive LUTD managed with a closed urine collection system; the secondary aim was to identify the causative infectious agents. A recent study reported a low positive predictive value (PPV) for bacterial culture of urinary catheter tips in dogs (25%);² our third aim was therefore to evaluate whether urine sample culture matched the catheter tip culture.

Material and methods

Cats

Male cats admitted for LUTD to the Intensive Care Unit of VetAgro Sup, Veterinary Campus of Lyon from 1 November 2006 to 31 July 2008, were eligible for inclusion. The owners provided consent for inclusion. The ethical committee of VetAgro Sup granted approval for this study. Cats that had undergone urinary catheterisation or that had received glucocorticoids or antibiotics in the month prior to admission were excluded, as were cats that tested positive for retrovirus(es). Cats were also excluded from the study if, during the protocol, there was a break in the closed urine collection system, the catheter was removed prematurely, the urine culture was positive on admission, or the clinical state led to the use of antibiotics and/or glucocorticoids during hospitalisation.

Data collection

The study was a prospective one. Signalment, medical history and clinical signs were collected on admission, and a complete biochemistry profile was obtained. All urinary catheters (Portex Jackson Cat Catheter 3 F; Smith Medical International) were placed by a clinician. The catheter was placed, in accordance with general rules of aseptic practice, under sedation or anaesthetic depending on the mental status of the cat. Briefly, the hair around preputial opening was clipped and the penis area was prepared with chlorhexidin. Surgical gloves and sterile lidocaine jelly were used for catheter placement. The time required to place the catheter was recorded. A sterile closed collection system (urine bag; Colèctor, SL) was connected to the catheter immediately following placement. The urine collection bag was kept at a level below the body to prevent reflux of urine into the bladder. The catheter was removed 48 h after placement.

Three urine samples were collected from each animal during the study. They were obtained through the catheter immediately after placement (S0), 24 h after placement (S24) and just before removal (S48). The first millilitre of urine at each sampling was discarded. All urine samples were subjected to a complete urinalysis, including dipstick (Combur 10 Test and Cobas; Roche Diagnostics), specific gravity measurement with a refractometer (URC-Ne; Atago), sediment examination and bacterial culture. Urine samples were divided into two aliquots. One was used immediately for centrifugation. The sediment was Gram-stained and examined under the microscope by a clinician. Pyuria was defined as the presence of ≥8 white blood cells/high power field. The second aliquot was stored at 4°C in a sterile tube pending bacterial culture. In all instances, the urine culture was initiated less than 12 h after urine collection. The urinary catheter tip was collected aseptically at the time of catheter removal, and also submitted for bacterial culture by rolling it on agar plates (Columbia agar + 5% sheep blood; BioMérieux) and flushing it with enriched culture medium. Plates were incubated at 37°C and examined for bacterial growth q24h for 2 days. Colony counts were determined for all urine samples for which growth was obtained. Cats were considered to have a positive bacterial culture if the number of colony-forming units (CFU) in a urine sample was ≥1000/ml. Growth was scored as heavy (≥100,000 CFU/ml) or moderate (1000–10,000 CFU/ml). For samples with more than one isolate, the bacterial count was established using the most numerous isolate. A qualitative result was obtained for culture of the urinary catheter tip without determining colony counts. Microorganisms were identified by the Microbiological Diagnostic Laboratory, VetAgro Sup Antimicrobial susceptibility profiles were not determined.

Cats that developed significant bacteriuria were treated with antibiotics (b-lactamines).

Data analysis

R 2.13.1 (R Development Core Team, 2011) was used for statistical analysis. The Kaplan–Meier survival method was used to evaluate the probability of urine remaining sterile as a function of time. Urine culture was considered to be the gold standard for assessing the sterility of urine. The Wald test of survival analysis was used to evaluate the correlation between urine culture results and the duration of catheterisation. Fisher’s exact test was used to evaluate the correlation between urine culture results and bacteriuria or pyuria in the sediment on the one hand, and between urine culture results and hyperthermia on the other hand. This statistical test provided only an informal trend of signiﬁcance because the data points for a single individual at 24 h and 48 h were not independent. The sensitivity, specificity, PPV and negative predictive value (NPV) of using the presence or absence of germs in the urinary sediment to predict bacterial culture results were calculated with their 95% confidence intervals (CI), as described by Mercaldo et al.⁴ The sensitivity, specificity, PPV and NPV (95% CI) of using the presence or absence of germs on urinary catheter tip to predict bacterial culture results were similarly calculated.

Results

Fifty-eight cats were diagnosed with obstructive LUTD during the inclusion period. Twenty-seven cats met the inclusion criteria and were enrolled in the study. Among the 31 cats that were not included in the study, 12 had undergone urinary catheterisation, 20 had received antibiotics and 14 glucocorticoids in the month prior to inclusion. Moreover, six cats tested positive for retrovirus(es). Furthermore, eight cats were excluded during the protocol owing to premature catheter removal (five were self-removals and three were removed owing to loss of patency). Another cat did not complete the study because it developed phlebitis that required antibiotic treatment during the protocol. None of the cats were excluded because of positive bacterial culture on admission.

Eighteen male cats (two sexually intact and 16 neutered) completed the study. The ages of the animals were between 7 months and 7 years. The mean age was 3.6 years (SD 2.3 years). Fifteen cats were European shorthair cats, two were Chartreux cats and one a Norwegian Forest cat. The mean weight was 5.5 kg (SD 1.4 kg). None of the cats had diabetes mellitus. Some of them had azotaemia, which resolved in all cases after catheterisation and appropriate fluid therapy.

The time required to place the urinary catheter was less than 15 mins for 10 cats and exceeded 15 mins for eight cats. A urethral plug was removed in 11 cats. Two cats had urethral and cystic calculi confirmed by imaging. A urethral spasm was suspected in the five last ones. Haematuria (macroscopic and microscopic) was noted in all urine samples obtained immediately after catheterisation (S0). Glucosuria was found in 7/18 cats (38.9%). The microscopic examination of the urine sediment at admission revealed struvite crystalluria in 12 (66.7%) and pyuria in seven (38.9%) cats.

Six of the 18 cats (33.3%) had at least one positive urine bacterial culture. One cat (cat 18) had negative bacterial urine cultures throughout study, but exhibited fungal growth in all urine samples except that collected on admission. All urine samples from 11/18 cats (61.1%) were sterile for the entire study.

Urine cultures were negative for all cats at admission. Bacterial urine culture was positive for 3/18 cats (16.7%) 24 h after catheterisation (S24) and for 6/18 cats (33.3%) 48 h after catheterisation (S48). Among the six positive S48 urine samples, three were new positives. The three cats with positive S24 urine samples also had positive S48 urine samples. For those three cats, the same bacterial isolate was found in the two urine samples and at a concentration ≥100-fold higher in the second. Among the six cats with positive bacterial urine samples, five had single isolates and one (cat 15) had multiple isolates both at S24 and S48. Four of the nine (S24 and S48 combined) bacterial culture-positive urine samples showed heavy growth (≥100,000 CFU/ml). Results for each cat with culture-positive urine are detailed in Table 1. The probability of urine remaining sterile 24 h after catheter placement was 83.3% (95% CI: 57–94%) and 66.7% (95% CI: 40–83%) 48 h after placement.

Table 1

Bacterial isolates and degree of growth for the 18 cats

	S24 urine sample^*	S48 urine sample^†	Urinary catheter^‡
Cat 1	Sterile	Sterile	Sterile
Cat 2	Sterile	Sterile	Sterile
Cat 3	Sterile	Sterile	Sterile
Cat 4	Sterile	Sterile	Streptococcus species SI
Cat 5	Streptococcus bovis SI, HG	Streptococcus bovis SI, HG	Streptococcus bovis MI
Cat 6	Sterile	Coagulase-negative Staphylococcus species SI, MG	Sterile
Cat 7	Sterile	Sterile	Sterile
Cat 8	Sterile	Sterile	Sterile
Cat 9	Sterile	Sterile	Streptococcus species MI
Cat 10	Sterile	Coagulase-negative Staphylococcus species SI, HG	Coagulase-negative Staphylococcus species SI
Cat 11	Sterile	β-haemolytic Escherichia coli SI, HG	β-haemolytic Escherichia coli SI
Cat 12	Coagulase-positive Staphylococcus species SI, MG	Coagulase-positive Staphylococcus species SI, HG	Coagulase-positive Staphylococcus species SI
Cat 13	Sterile	Sterile	Streptococcus species SI
Cat 14	Sterile	Sterile	Sterile
Cat 15	β-haemolytic Escherichia coli MI, MG	β-haemolytic Escherichia coli MI, HG	β-haemolytic Escherichia coli MI
Cat 16	Sterile	Sterile	Sterile
Cat 17	Sterile	Sterile	Streptococcus canis SI
Cat 18	Fungal growth	Fungal growth	Fungal growth

S24 urine sample: urine sample obtained through the catheter 24 h after placement

†

S48 urine sample: urine sample obtained through the catheter 48 h after placement, just before its removal

‡

Urinary catheter: urinary catheter tip collected aseptically at the time of catheter removal and used for bacterial culture

SI = single isolate; HG = heavy growth; MG = moderate growth; MI = multiple isolates (predominant germ indicated when possible)

We compared cats for which urinary catheterisation required less than 15 mins to those for which it took longer than 15 mins and found no significant correlation between the time required to place the catheter and the probability of developing a positive urine culture (P >0.05).

The catheter tips of 10/18 cats (55.5%) were culture positive. Compared with the urine culture results at 48 h, urinary catheter tip culture results had a sensitivity of 85.7% (95% CI: 47.9–100%), a specificity of 53.8% (95% CI: 28.7–100%), a PPV of 87.5% (95% CI: 16.5–99.6%) and a NPV of 91.3% (95% CI: 79.7–96.5%). The infectious agents isolated from the catheter tips were the same as those found in the urine samples for 6/10 cats (60%).

Fifty-four urine samples were collected during the study. Bacteriuria was present in the urinary sediment of 4/9 samples (44%) found to have positive bacterial culture results and in that of 1/45 samples (2.2%) found to have negative bacterial culture results. The presence or absence of bacteria in the urine sediment correlated with the bacteriological results (P = 0.002). Compared with the urine culture results, the presence or absence of bacteria in the urinary sediment had a sensitivity of 44.4% (95% CI: 17–100%), a specificity of 97.7% (95% CI: 90–100%), a PPV of 80% (95% CI: 33–97%) and a NPV of 89.8% (95% CI: 83–94%). The presence or absence of pyuria did not correlate with culture results (P >0.05).

Cats with a body temperature exceeding 39.2°C were considered hyperthermic. Hyperthermia did not correlate with a positive urine culture result (P >0.05). Only one cat (cat 15) infected with a b-haemolytic Escherichia coli (heavy growth) exhibited hyperthermia associated with signs of systemic illness. Hyperthermia was not significantly correlated with pyuria (P ≥0.05).

Discussion

In this study, about one-third [6/18 (33.3%)] of the cats developed significant bacteriuria during catheterisation with adequate precautions being taken in urinary catheter management. A closed urine collection system was used and urine sampling was performed through the catheter. The incidence of bacteriuria in our study was lower than that reported by Lees et al³ [20/36 (55.6%)], using an open system drainage and urine sampling by cystocentesis, for healthy male cats catheterised for a mean duration of 3 days. This previous report is the only published study in cats with which our results can be compared even if our case series was smaller. Three studies have investigated CAUTI in dogs. In the first, 4/39 dogs (10.3%) with a mean duration of 2.2 days of catheterisation developed a bacterial urinary tract infection (UTI).² Urine was collected through the catheter. In another, 67/147 dogs (45.6%) catheterised for a median of 3 days and managed with a closed collection system developed a UTI.⁵ Urine was collected by cystocentesis. In the last, 5/51 dogs (9.8%) managed with either an open or a closed collection system for a median duration of 2 days of catheterisation developed a UTI.⁶ Urine was collected through the catheter. In this third, the type of urine collection system (open versus closed) had no identifiable effect on the incidence of nosocomial bacteriuria.⁶ In our study, all cats were managed with a closed system. Sullivan et al⁶ suggest that aseptic catheter placement and maintenance are more important than the type of urine collection system for minimising the incidence of CAUTI.

There are differences in urine sampling procedures between institutions, and feline LUTD is a particular medical context, being associated with marked pre- existing inflammation of the urinary tract, such that our results cannot be strictly compared with those of the canine studies cited earlier. We did not sample urine by cystocentesis because repeated cystocentesises are relatively contraindicated for weakened bladders. Nevertheless, cystocentesis is regarded as the method of choice for urine collection.^7,8 Catheter sampling may overestimate the incidence of significant bacteriuria,⁷ although a recent report in cats found no significant difference in bacteriuria results between urine collected by cystocentesis and that collected by catheterisation.⁹

In our study, the number of cats with significant bacteriuria doubled between 24 h and 48 h of catheterisation. The prevalence of bacterial UTI in catheterised dogs and humans is reported frequently to increase with the duration of catheterisation.^5,6,10 Indwelling bladder catheters can also predispose to urinary fungal colonisation,¹¹ as was observed in one cat in our study. Therefore, it would appear to be beneficial to limit the duration of catheterisation whenever possible. In our study, the duration of catheterisation was fixed arbitrarily at 48 h. It would be informative to investigate the incidence of bacteriuria in cats with obstructive LUTD that are catheterised for shorter periods (24 or 36 h). Another good reason for limiting catheterisation time in cats with obstructive LUTD is to minimise the risk of catheter self-removal, which increased in our study as clinical status improved (five catheter self-removals between 24 h and 48 h after catheter placement). Surprisingly, the probability of developing bacteriuria was not linked to the time required to place the catheter.

As cats managed for obstructive LUTD frequently display haematuria, pyuria and a painful bladder on palpation,^12,13 the occurrence of CAUTI may not be clinically obvious. This issue could be further explored by considering the pathogenicity of the isolates, in terms of their proliferation evaluated by colony counts and by the growth of a single type of bacteria, rather than the presence of a mixed population. In our study, the urine samples of 5/6 cats with a bacteriuria contained single isolates, with heavy growth for four of them. In addition to the number of CFU/ml, the type of pathogen is an important determinant of pathogenicity. Commensal colonic Gram-negative bacteria, especially E coli, are among the principal causative pathogens of spontaneous symptomatic bacterial UTIs in cats, dogs and humans.^9,14,15 Haemolytic E coli is considered to be potentially harmful¹⁵ and was encountered in two of our six cats. One of them (cat 15) exhibited systemic signs of illness and developed sepsis, as defined by Brady et al.¹⁶ Staphylococcus species isolates were obtained from three cats. The Staphylococcus species isolates from two cats were coagulase negative and one was coagulase positive. Coagulase-positive Staphylococcus species are occasional causative agents of spontaneous UTIs in cats, but coagulase-negative species are not widely known to be feline uropathogens.¹⁵ In a recent report, however, 19.8% of the isolates obtained from cats with clinical signs of LUTD¹⁵ were the coagulase-negative Staphylococcus felis, suggesting that this species may be a common, but previously neglected, feline uropathogen. After E coli, pathogenic Gram-positive Enterococcus species are the next most frequently implicated pathogens in felines.^9,15 However, none were identified in our study. Streptococcus bovis was isolated from one cat. Although Streptococcus species are encountered occasionally in feline and canine UTIs,^9,15,17 their pathogenicity in the urinary tract is questionable.

In our study, the presence of bacteria in the urinary sediment was correlated strongly with bacterial culture results despite a low sensitivity (44.4%). The presence of bacteria in the urinary sediment appears to be a useful marker for bacteriuria and should prompt bacterial culture. By contrast, a positive bacterial culture result for the urinary catheter tip was not a reliable predictor of bacteriuria: the specificity was only 53.8%, although the PPV (87.5%) was satisfactory and notably higher than that (25%) reported in a study on catheterised dogs.² Among the 10 cats with a positive catheter tip culture, six had the same infectious agent in urine and on the catheter tip. Four cats had a positive bacterial culture of the catheter tip although urine was sterile. In these four cases, the isolate on the catheter tip was a species of Streptococcus. As discussed previously, Streptococcus species are not common uropathogens,^9,15,17 but are members of the commensal bacterial flora of the genital tract of adult cats.¹⁴ The large proportion (4/10) of catheter tips that were culture positive for Streptococcus species and associated with sterile urine suggested that these isolates were contaminants or opportunistic pathogens favoured by urethritis secondary to the presence of an indwelling urinary catheter. Further investigations with larger numbers of animals are needed to determine whether culturing urinary catheter tips can be used to predict bacteriuria.

To our knowledge, practical guidelines for managing bacteriuria in catheterised cats have not been established. In humans, CAUTI is defined strictly as the presence of signs consistent with UTI with no other identified source of infection, plus counts of >1000 CFU/ml of one or more bacterial species in a catheter urine specimen.^10,18
–20 Only patients fulfilling this strict definition of CAUTI warrant antibiotic treatment.^10,18
–20 CAUTI is distinguished from catheter-associated asymptomatic bacteriuria (CA-ASB), defined as the presence of >100,000 CFU/ml of one or more bacterial species in a catheter urine specimen from patients without symptoms consistent with UTI.^10,19,20 CA-ASB does not warrant antibiotics.^10,19,20 In humans, pyuria is not used to differentiate CAUTI from CA-ASB.²⁰ In our study population, the urinary clinical signs potentially associated with bacteriuria are indistinguishable from those of LUTD.^12,13 Moreover, in our study, hyperthermia and pyuria are not correlated with a positive urine culture and therefore cannot be considered as suggestive of CAUTI. For these reasons, the sole relevant terminology in our study population is ‘significant bacteriuria’. Our results don’t enlighten the necessity of using antibiotics in catheterised cats with significant bacteriuria. However, the benefits of systemic antimicrobial prophylaxis have not been established and this practice may contribute to increasing antibiotic resistance.^2,10,20 In our opinion, antimicrobial prophylaxis should not be used routinely.

Conclusions

Short-term indwelling urinary catheterisation for obstructive LUTD was associated with significant bacteriuria in one-third of cats. Bacterial culture of urinary catheter tips was a poor indicator of urine bacterial culture results. The probability of developing bacteriuria increased with the duration of catheterisation, as has been reported previously for dogs and humans.^5,6,10 Except for one cat with S bovis, the bacteria involved were common uropathogens. Distinguishing CAUTI from CA-ASB in cats, as is performed for humans, would be helpful in determining practical guidelines for antibiotic therapy in catheterised cats, but this remains particularly challenging in the context of LUTD. The extent to which bacteriuria resolves spontaneously after catheter removal is unknown. Further studies including urine sampling a few days after catheter removal may be warranted to address this issue and clarify the need for systematic screening for bacteriuria during catheterisation.

Footnotes

Acknowledgements

The authors wish to thank Charlye Guyet, Serge Angelier and Xavier Henry for their technical assistance, and Professor Jacques Croize for scientific assistance.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Conflict of interest

The authors do not have any potential conflicts of interest to declare.

Accepted: 11 January 2013

Parts of this study were presented as an abstract at the 18th ECVIM-CA congress, Ghent, Belgium, 4–6 September 2008 and as an abstract at the 7th EVECCS congress, Gothenburg, Sweden, 29 May–1 June 2008

References

Mittal

Aggarwal

Sharma

, et al. Urinary tract infections caused by Pseudomonas aeruginosa: a minireview. J Infect Public Health 2009; 2: 101–111.

Smarick

Haskins

Aldrich

, et al. Incidence of catheter-associated urinary tract infection among dogs in a small animal intensive care unit. J Am Vet Med Assoc 2004; 224: 1936–1940.

Lees

Osborne

Stevens

, et al. Adverse effects of open indwelling urethral catheterization in clinically normal male cats. Am J Vet Research 1981; 42: 825–833.

Mercaldo

Lau

Zhou

. Confidence intervals for predictive values with an emphasis to case-control studies. Statist Med 2007; 26: 21070–21083.

Bubenik

Hosgood

Waldron

, et al. Frequency of urinary tract infection in catheterized dogs and comparison of bacterial culture and susceptibility testing results for catheterized and non-catheterized dogs with urinary tract infections. J Am Vet Assoc 2007; 231: 893–899.

Sullivan

Campbell

Onuma

. Evaluation of open versus closed urine collection systems and development of nosocomial bacteriuria in dogs. J Am Vet Med Assoc 2010; 237: 187–190.

Van Duijkeren

van Laar

Houwers

. Cystocentesis is essential for reliable diagnosis of urinary tract infections in cats. Tijdschr Diergeneeskd 2004; 129: 394–396.

Eggertsdottir

Saevik

Halvorsen

, et al. Occurrence of occult bacteriuria in healthy cats. J Feline Med Surg 2011; 13: 800–803.

Eggertsdottir

Lund

Krontveit

, et al. Bacteriuria in cats with feline lower urinary tract disease: a clinical study of 134 cases in Norway. J Feline Med Surg 2007; 9: 458–465.

10.

Tenke

Kovacs

Bjerklund Johansen

, et al. European and Asian guidelines on management and prevention of catheter-associated urinary tract infections. Int J Antimicrob Agents 2008; 31 (Suppl. 1): S68–S78.

11.

Jin

Lin

. Fungal urinary tract infections in the dog and cat: a retrospective study (2001–2004). J Am Anim Hosp Assoc 2005; 41: 373–381.

12.

Gerber

Boretti

Kley

, et al. Evaluation of clinical signs and causes of lower urinary tract disease in European cats. J Small Anim Pract 2005; 46: 571–577.

13.

Saevik

Trangerud

Ottesen

, et al. Causes of lower urinary tract disease in Norwegian cats. J Feline Med Surg 2011; 13: 410–417.

14.

Ström Holst

Bergström

Lagerstedt

, et al. Characterization of the bacterial population of the genital tract of adult cats. Am J Vet Res 2003; 64: 963–968.

15.

Litster

Moss

Honnery

, et al. Prevalence of bacterial species in cats with clinical signs of lower urinary tract disease: Recognition of Staphylococcus felis as a possible feline urinary tract pathogen. Vet Microbiol 2007; 121: 182–188.

16.

Brady

Otto

Winkle

, et al. Severe sepsis in cats: 29 cases (1986–1998). J Am Vet Med Assoc 2000; 217: 531–535.

17.

Seguin

Vaden

Altier

, et al. Persistent urinary tract infections and reinfections in 100 dogs (1989–1999). J Vet Intern Med 2003; 17: 622–631.

18.

Sedor

Mulholland

. Hospital-acquired urinary tract infections associated with the indwelling catheter. Urol Clin North Am 1999; 26: 821–828.

19.

Tambyah

Maki

. Catheter-associated urinary tract infection is rarely symptomatic. A prospective study of 1497 catheterized patients. Arch Intern Med 2000; 160: 678–682.

20.

Hooton

Bradley

Cardenas

, et al. Diagnosis, prevention, and treatment of catheter-associated urinary tract infection in adults: 2009 International Clinical Practice Guidelines from the Infectious Diseases Society of America. Clin Infect Dis 2010; 50: 625–663.