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DOI: 10.1542/peds.2011-2856; originally published online April 2, 2012; 2012;129;885Pediatrics

Marie Gauthier, Serge Gouin, Vronique Phan and Jocelyn Gravel1 to 36 Months

Association of Malodorous Urine With Urinary Tract Infection in Children Aged

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Association of Malodorous Urine With Urinary TractInfection in Children Aged 1 to 36 Months

WHATS KNOWN ON THIS SUBJECT: The presence of malodorousurine is often mentioned as one of the clinical manifestations ofurinary tract infection (UTI) in young children, yet the few studieslooking at this symptom are contradictory.

WHAT THIS STUDY ADDS: Our study demonstrates thatmalodorous urine as reported by parents increases the likelihoodof UTI among young children evaluated for suspected UTI.However, this association is not strong enough to denitely rule inor out a diagnosis of UTI.

abstractOBJECTIVE: To determine whether parental reporting of malodorousurine is associated with urinary tract infection (UTI) in children.

METHODS:We conducted a prospective consecutive cohort study in theemergency department of a pediatric hospital from July 31, 2009 toApril 30, 2011. All children aged between 1 and 36 months for whoma urine culture was prescribed for suspected UTI (ie, unexplained fever,irritability, or vomiting) were assessed for eligibility. A standardizedquestionnaire was administered to the parents by a research assis-tant. The primary outcome measure was a UTI.

RESULTS: Three hundred ninety-six children were initially enrolled, but65 were excluded a posteriori either because a urine culture, althoughprescribed, was not done (11), was collected by bag (39), and/or showedgross contamination (25). Therefore, 331 children were included in thenal analysis. Their median age was 12 months (range, 136). Criteriafor UTI were fullled in 51 (15%). A malodorous urine was reported byparents in 57% of children with UTI and in 32% of children without UTI.On logistic regression, malodorous urine was associated with UTI (oddsratio 2.83, 95% condence interval: 1.545.20). This association remainedstatistically signicant when adjusted for gender and the presenceof vesicoureteral reux (odds ratio 2.73, 95% condence interval:1.465.08).

CONCLUSIONS: Parental reporting of malodorous urine increases theprobability of UTI among young children being evaluated for suspectedUTI. However, this association is not strong enough to denitely rule inor out a diagnosis of UTI. Pediatrics 2012;129:885890

AUTHORS: Marie Gauthier, MD,a Serge Gouin, MD,b

Vronique Phan, MD, MSc,c and Jocelyn Gravel, MD, MScb

aDivision of General Pediatrics, bDivision of Emergency Medicine,and cDivision of Nephrology, Department of Pediatrics, Sainte-Justine University Hospital Center, University of Montreal,Montreal, Canada

KEY WORDSurinary tract infection, child, odor, urine

ABBREVIATIONSCIcondence intervalEDemergency departmentFWSfever without sourceORodds ratioUTIurinary tract infectionVURvesicoureteral reux

All authors contributed substantially to the conception anddesign of the study; Dr Gravel performed the data analysis, andall authors were involved in the interpretation of the data;Dr Gauthier prepared the rst draft of the manuscript; and allthe authors participated in revising the article, and approvedthe nal version of the manuscript.

www.pediatrics.org/cgi/doi/10.1542/peds.2011-2856

doi:10.1542/peds.2011-2856

Accepted for publication Jan 18, 2012

Address correspondence to Marie Gauthier, MD, Department ofPediatrics, CHU Sainte-Justine, 3175 Cte Sainte-Catherine,Montreal, Canada, H3T 1C5. E-mail: [email protected]

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright 2012 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: The authors do not have nancialrelationships or conicts of interest relevant to this article todisclose.

FUNDING: This project was supported by the Fonds doprationpour les projets de recherche clinique applique, CHU Sainte-Justine, Montreal.

PEDIATRICS Volume 129, Number 5, May 2012 885

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Urinary tract infection (UTI) occurs in8%of girls and 2%of boys by the age of7 years.1 Acute pyelonephritis is themost common serious bacterial infec-tion in childhood.2 In younger children,fever without source (FWS) is often themode of presentation of UTI. The lack ofmore specic symptoms or signs maydelay the diagnosis in this age group.Moreover, appropriate methods to ob-tain urine culture in young children,namely suprapubic aspiration andbladder catheterization, are invasiveand should be ordered with care. Thereis some debate as to the timing andextent of investigations in this pop-ulation.3 Any additional clinical clue,with sufcient predictive ability, couldhelp practitioners decide when to eval-uate a young child for a possible UTI.

Malodorous urine has been reported in2% to 18% of children with UTI46 and isoften described in review articles as 1 ofthe clinical manifestations of UTI in youngchildren.714 However, 14% of parentsasked to answer a questionnaire onteething symptoms described malodor-ous urine as associated with teething.15

So far, only a fewauthors have studied thevalue of malodorous urine as a predictorof UTI.1618 Their results are contradictory.Shaw et al16 described higher prevalenceof UTI in young children with FWS havingmalodorous urine or hematuria. Coutureet al17 found foul-smelling urine as 1 of 4variables enabling prediction of UTI inchildren ,2 years of age, whereasStruthers et al18 did not nd any associ-ation between parental reporting ofa particular urine smell and a diagnosisof UTI in children,6 years of age.

The objective of this study was to de-termine whether parental reporting ofmalodorousurine isassociatedwithUTIin young children.

METHODS

Study Design and Subjects

We conducted a prospective cohortstudy in the emergency department

(ED) of a pediatric university-afliatedtertiary-care center (Sainte-JustineUniversity Hospital Center, Montreal,Canada) from July 31, 2009 to April 30,2011. This center has an annual EDcensus of 60 000 patient-visits.All children aged between 1 and 36months for whom a urine culture wasprescribed for suspected UTI (ie, FWS,unexplained irritability, or vomiting) bythe treating ED physician were as-sessed for eligibility. Fever was con-sidered present if parents reportedfever at home or if, in the ED, the childsbody temperature was .38.5C rec-tally. Exclusion criteria included anti-biotics other than for prophylaxis givenover the preceding 48 hours, diabetesor other metabolic disease, vesico/ureterostomy or urinary catheter inplace, patient already included in thestudy, person accompanying the childnot knowing the patient well enough toanswer the questionnaire (see below),and inability to administer the ques-tionnaire in either English or French.

Patients were recruited during theweekdays (Monday to Friday) from10:00 AM to 6:00 PM. For all eligiblepatients, a standardized questionnairewas administered to the parents (or tothe person accompanying the child) bya research assistant. The question-naire was administered as soon as theurine culture was prescribed and be-fore the result of the urine analysiswascommunicated to either the parents,the research assistant, or the physi-cian. It was available in both Englishand French. The rst part consistedof questions on past medical history(history of UTI and vesicoureteralreux [VUR], circumcision status),administration of antibiotics (prophy-lactic or not) over the last 48 hours,and the duration of fever, if present.The second part included 8 questionson symptoms presented by the childduring the 48 hours before the ED visit(see Table 1). For 7 of these questions,

the response was either yes or no. If therespondent was unable to answer, theresponse was considered negative.The eighth question requested the num-ber of episodes of vomiting.

Data obtained from the questionnairewere collected on standardized datacollection forms by the research as-sistant. Demographic data, why theurine culture was prescribed, and theresults of laboratory tests performedin the EDwere retrieved through reviewof medical records by the researchassistant and collected on the sameforms. According to the study protocol,there were 3 possible reasons to pre-scribeaurine culture for suspectedUTI:FWS, unexplained vomiting without fe-ver, or irritability in an afebrile child. Inthe case of a child who presented withvomiting or irritability, and who wasalso febrile, FWS was considered to bethe reason for urine sampling. Labo-ratory tests were ordered according tothe clinical judgment of the ED physi-cian. Results of urine cultures werecollected a posteriori from the patientschart by the principal investigator (M.G.)blinded to the exposure of interest.In the event where 2 urine cultureswere performed either by midstreamvoiding or bladder catheterization, andthe results were different from eachother, the urine culture with the lowerbacterial count was considered as thenal result for the patient concerned.

TABLE 1 Questions Asked on SymptomsPresented by the Child

1. Has your child vomited?2. If your child vomited, how often did this happen?3. Has your child had diarrhea (liquid stools or

stools much softer than usual)?4. Have you had the impression that your child had

a stomachache?5. Have you had the impression that it was difcult

for your child to pee?6. Have you had the impression that it was painful

for your child to pee?7. Have you noticed that your childs urine smelled

stronger than usual?8. Have you noticed that your childs urine smelled

offensive?

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Collection of urine specimenswas doneasusualby theEDnurses. Themethodofsampling was decided by the ED phy-sician. Patients for whom urine culturewas collected by bag were excludeda posteriori.

The primary independent variable ofinterest was the presence of malodor-ous urine as dened by urine thatsmelledstrongerand/ormoreoffensive,according to the parents. The primaryoutcome was a UTI dened as: $50 3106/L of a single identied pathogen inurine culture obtained through bladdercatheterization (excluding lactobacilli,corynebacteria, and coagulase-negativestaphylococci; urine cultures were alsoconsidered positive if they revealed$103 106/L of Pseudomonas species);$100 3 106 bacteria/L of a single iden-tied pathogen in urine culture collectedfrom clean-catch or midstream void(excluding lactobacilli, corynebacteria,and coagulase-negative staphylococci);or any amount of Gram-negative bacteriain urine culture obtained from supra-pubic aspiration (or $10 3 106 ofGram-positive bacteria/L). Patients witha urine culture not meeting these cri-teria were considered to not have a UTI.

Human Subjects Protection

This study received full approval fromSainte-Justine University Hospital Cen-ters Institutional Review Board. To par-ticipate in the study, parents had toprovide written informed consent fortheir child. To prevent bias in answeringthe questionnaire, the study was enti-tled Predictive factors of UTI in 1- to 36month-old children on the consent form,and parents were asked to participate ina research project that aimed to de-scribe certain symptoms that couldpredict a UTI in 1- to 36-month-old chil-dren, without being more specic.

Data Analysis

All data were entered in an Excel da-tabase (Microsoft Inc, Richmond, WA)

andwere analyzedwithSPSSversion 17(SPSS Inc, Rainbow Technologies). The95% condence intervals (CI) weremeasured forall comparisons.Baselinecharacteristics were measured forthose children included and excludedin the nal analysis. Clinical character-istics including the presence/absenceof malodorous urine were also mea-sured for childrenwith andwithout UTI.Theprimaryanalysis of interestwas theassociation between parental reportingof malodorous urine and UTI by usinglogistic regression analysis. Simple lo-gistic regression was used to evaluateotherpotential predictorsofUTI (gender,age, pastmedical history ofUTI, VUR, andother symptoms). In a second step,a multiple logistic regression analysiswas performed to evaluate the pre-dictive ability of malodorous urine ad-justed for the predictors identied in therst step. To evaluatewhether themodelaccurately predicted the outcome, aHosmer-Lemeshow goodness-of-t testwas performed.

The sensitivity of the reporting of mal-odorousurinewasmeasuredbydividingthe numberof patientswithmalodorousurine and UTI by the total number ofUTIs. The specicity was calculated bydividing the number of participantswith no malodorous urine and no in-fection by the total number of patientswith no infection. The positive and neg-ative likelihood ratios were calculated.

Finally, a secondary analysis was per-formed to evaluate the associationbetween malodorous urine and mark-ers that could be associated with theurine smell (nitrite, leukocyte esterase,ketone bodies, specic gravity).

RESULTS

Of 601 participants originally screened,396 were recruited over the study pe-riod (Fig 1). Sixty-ve patients wereexcluded a posteriori, either becausethe urine culture, although prescribed,was not done, or was collected by bag,

or showed gross contamination (poly-microbial ora). Three hundred thirty-one children were therefore includedin the analysis.

Their baseline characteristics are de-scribed in Table 2. Their median agewas 12 months, and 58% were female.FWS was the reason for suspecting UTIin.90% of cases. Urine cultures wereperformed through bladder catheteri-zation in 297 (88%) children, throughclean voiding/midstream in 31 (9%),and through suprapubic bladder aspi-ration in 3 (1%). The questionnaire wasadministered to themother in 279 cases(84%), the father in 38 instances (12%),the 2 parents in 6 cases (2%), andpeople other than parents in 8 in-stances (2%).

UTI criteria were fullled in 51 children(15%) (Table 3). In these patients, theinfection was suspected because ofFWS; no UTI was found in afebrile chil-dren suspected of having this infectionbecause of unexplained vomiting orirritability. Urine cultures were positivefor Escherichia coli in 82% of cases(42/51).

A malodorous urine was reported byparents in 57% of children with UTI and32%of childrenwithout UTI (Table 3). Onsimple logistic regression, this symp-tom was associated with the risk of UTI(odds ratio [OR] 2.83, 95% CI: 1.545.20). Other risk factors for UTI werefemale gender (OR 2.82, 95% CI: 1.415.61), and presence of VUR (OR 2.39,95% CI: 1.045.53), whereas age andpast medical history of UTI were notstatistically associated with UTI. Onmultiple logistic regression, the asso-ciation between malodorous urine andUTI remained statistically signicantwhen adjusting for gender and pres-ence of VUR (OR 2.73, 95% CI: 1.465.08).Malodorous urine showed a sensitivityof 0.57 (95% CI: 0.420.70) and a speci-city of 0.68 (95% CI: 0.620.74) for UTIleading to a positive likelihood ratio of1.79 (95% CI: 1.332.40) and a negative

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likelihood ratio of 0.63 (95% CI: 0.230.45). The Hosmer-Lemeshow goodness-of-t test suggested that the model t-ted (x2: 2.726; degrees of freedom 4; P =.605).

Among symptoms commonly attributedto UTI looked at by the questionnaire(eg, vomiting, diarrhea, and dysuria),malodorous urine was the risk factorwith the strongest association with UTI(Table 3). Finally, malodorous urine wasmore frequently observed in childrenwhose urine analysis showed positive

nitrite and leukocyte esterase on dip-stick. There was no association betweenmalodorous urine and presence of ke-tone bodies, high urine specic gravity,or urine pH (Table 4).

DISCUSSION

Our study showed that parentalreporting of malodorous urine wasassociated with UTI in young children.The association between smelly urineandUTIwas at least as signicant as theassociation with female gender, past

medical history of UTI, and presence ofVUR. However, 40% of children with UTIin our series did not have malodorousurine and .30% of parents reportedmalodorous urine in children withoutUTI. Although parental reporting ofmalodorous urine increased the prob-ability of UTI, in particular, in childrenwith FWS, it did not have a sufcientlyhigh specicity or sensitivity to de-nitely rule in or rule out a UTI. This isalso the case for other symptomsconsidered as "classical" for this typeof infection in older children, namely,ank pain or painful urination. Despitethese limitations, and given the clearassociation between this symptom andUTI, reporting of malodorous urine byparents should make the clinicianmore suspicious of this type of in-fection in a young child with FWS. In ourstudy, parents were asked specicallyabout the presence of malodorousurine and otherwise may not havereported it. The discrepancy betweenthe rather low rate of smelly urinereported in previous studies in asso-ciation with UTI in children (see above)and the rate in this study is probablyexplained by this observation. It couldtherefore be useful for the clinician tosystematically ask about urine odor inchildren in whom UTI is suspected.

To date, 3 studies have reported thevalue of malodorous urine as predictorof UTI in young children.1618 Results arecontradictory, and, in these 3 articles,methodological aws do not allow anaccurate answer. The main objective ofthe rst study16 was to establish prev-alence of UTI in febrile infants ,12months and girls ,2 years of age pre-senting to the ED with a fever withouta denite source. Of the patients eligiblefor the study, 83% had a urine culture.The exact nature of the questionnaireadministered was not described, nor ifcaregivers had previous knowledge ofthe urinalysis result when the ques-tionnaire was administered. A history of

TABLE 2 Baseline Characteristics of Patients Recruited for the Study

Characteristic Included N = 331 Not Includeda N = 65

Age, median (range), mo 12 (136) 14 (135)Weight, median (range), kg 9.7 (3.716.6) 10.45 (3.623.0)Males, n (%) 142 (42) 40 (62)

Circumcision, n (%) 37 (26) 5 (13)Past history of UTI, n (%) 62 (19) 7 (11)VUR already identied, n (%) 32 (10) 2 (3)Grade 35 VUR, n (%) 25 (8) 1 (2)Antibiotic prophylaxis for VUR, n (%) 25 (8) 1 (2)FWS, n (%) 309 (93) 54 (83)a Excluded a posteriori.

FIGURE 1Flow diagram outlining the enrollment.


malodorous urine was noted in only 3%of UTI cases, which is a surprisingly lowrate, given our own results. Higher pre-valence of UTI occurred in those childrenwith malodorous urine or hematuria,but the authors did not describe specicdata for 1 or the other symptom.

Couture et al17 performed a retrospec-tive study of children ,2 years of agesuspected of having a UTI, who had aurine culture collected during a 12-month period in a university-afliatedhospital. Ten percent (55/545) of urinecultures were positive. In this study, themethod of urine collection was notdescribed, and the presence of foul-smelling urine was assessed by chartreview. It was present in 6.8% of chil-dren (37/545) and was identied as 1 of4 predictors of UTI in their population.Struthers et al18 studied children aged,6 years who had urine collected

routinely as part of their admission tohospital. Parents were asked to com-plete a questionnaire asking if theirchilds urine smelled differently fromusual or had a specic smell. Onehundred ten questionnaires and urinesamples were collected. The authorsdid not state what proportion of pa-tients treated over the study periodthat this number represented, and theydid not use consecutive patients. Fifty-two percent of parents thought thattheir childs urine smelled differentlyfrom usual or had a particular smell.The authors did not nd a signicantassociation between parental repo-rting of abnormal urine smell anda diagnosis of UTI. However, in theirstudy group, only 7 children werediagnosed with UTI, therefore, toosmall a number to obtain reliableconclusions.

Urine normally has a faintly aromaticodor caused by the presence of manyorganic and inorganic substances.19 Inour study, malodorous urine was as-sociated with the presence of nitritesand leukocyte esterase on the dipstick,but not with ketone bodies or specicgravity. This association between mal-odorous urine and nitrites/leukocyteesterase may be explained by the factthat nitrites and leukocyte esterase are,in themselves, good indicators for UTI,20

the UTI itself causing the bad smell ofthe urine. Our study was not designed toidentify what substance causes theurine to be malodorous in UTI. Thesmelly odor of infected urine may bedue to the production of ammonia fromurea split by bacterial ureases and mayvary with certain bacteria.21

There aresome limitations to this study.First, there isnostandardizeddenitionof malodorous urine. Malodorousurine is a subjective description ofodor. We chose to include 2 items inour denition, namely, a urine thatsmelled stronger and/or more offensive,according to the parents. Second, thepresence of malodorous urine was notdirectly observed, but was consideredpresent or absent according to paren-tal opinion. However, if this clinical clueis to be used by clinicians, it will beobtained by questioning caregivers, aswas the case in our study, more thanby direct observation, which does notappear feasible. Third, we did notevaluate the predictability of malodor-ous urine for UTI in children seen in theED at large, and, in particular, we didnot include children brought to the EDfor this symptom only, or for thissymptom associated with dysuria butwithout fever. Indeed, to be valid, ourstudy had to have a control groupwithout the symptomatology (so with-out malodorous urine) and all childrenhad to have urine cultures collectedwith an appropriate technique, whichis most often invasive in this age group.

TABLE 3 Clinical Characteristics of Patients Included in the Final Analysis (N = 331)

Characteristic With UTI N = 51 Without UTIN = 280

P a

Age, median (range), mo 13 (236) 12 (136) .182Wt, median (range), kg 9.1 (3.816.5) 9.8 (3.715.8) .125Males, n (%) 12 (23) 130 (46) .002

Circumcision, n (%) 0 37 (29) .003Past history of UTI, n (%) 13 (27) 49 (18) .179VUR already identied, n (%) 9 (18) 27 (8) .036Grade 35 VUR, n (%) 9 (18) 17 (6) .017Antibiotic prophylaxis for VUR, n (%) 7 (14) 18 (6) .07Presence of fever, n (%) 51 (100) 258 (92) .038Duration of fever $72 h, n (%) 25 (49) 100 (56) .072Symptomsb

Smelly urine, n (%) 29 (57) 89 (32) .001Vomiting, n (%) 16 (31) 107 (38) .352Diarrhea, n (%) 14 (27) 68 (24) .630Abdominal pain, n (%) 21 (41) 127 (45) .58Dysuria, n (%) 10 (19) 61 (22) .727Painful urination, n (%) 13 (26) 40 (14) .045

a By using a Pearson x2 for categorical variable and analysis of variance for continuous variables.b According to the information given by parents.

TABLE 4 Association Between Smelly Urine and Results of Urine Analysis (N = 328)a

Variable Smelly Urine N = 117 Nonsmelly Urine N = 211 P b

Presence of ketone bodies, n (%) 35 (30) 60 (28) .777Ketone bodies $3.9 mmol/L, n (%) 16 (14) 22 (10) .380Nitrite, n (%) 11 (9) 8 (4) .037Leukocyte esterase, n (%) 26 (22) 25 (12) .013Specic gravity $1025, n (%) 31 (27) 60 (28) .707pH $7, n (%) 31 (27) 47 (22) .390a No urine analysis was available in 3 patients.b By using a Pearson x2 test.

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We considered that it was not ethicallypossible to obtain proper urine cul-tures in all patients included in a con-trol group without malodorous urine,and with no clinical manifestations likeFWS that would necessitate per sea urine culture. Fourth, it is possiblethat the presence of malodorous urinewas reported spontaneously by someparents to the ED physician and initi-ated a urine culture. Fifth, our studyinvolved only 51 children with UTI. Thislow number limits the possibility ofsecondary analysis for afebrile chil-dren suspected of UTI because of un-explained vomiting or irritability, and forchildren aged between 1 and 3 months

of age. It was therefore not possibleto describe the predictability of mal-odorous urine in these 2 subgroupsof patients.

CONCLUSIONS

Parental reporting ofmalodorousurineis associatedwithUTI in young children.Although it increases the probability ofUTI, in particular, in childrenwith FWS, itdoes not have a sufciently high spec-icity or sensitivity to denitely rule inor out a diagnosis of UTI. However, itshould make the clinician more suspi-cious of this type of infection in a youngchild with FWS. In a child.3 months, it

should encourage the physician to askfor a urine culture more rapidly thanif the child had not had this symptom.In future, a clinical decision rule forUTI, incorporating malodorous urine,could be developed and validated pro-spectively to verify if this more accu-rately predicts UTI than the decisionrules already reported.22,23

ACKNOWLEDGMENTSWe thank Ms Alexia Messier and MsMarie-Andre Robert for their helpwith patient recruitment. We also thankDrs Barbara Cummings-Mc Manusand Claire Mattimoe for review of themanuscript.

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DOI: 10.1542/peds.2011-2856; originally published online April 2, 2012; 2012;129;885Pediatrics

Marie Gauthier, Serge Gouin, Vronique Phan and Jocelyn Gravel1 to 36 Months

Association of Malodorous Urine With Urinary Tract Infection in Children Aged

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