evaluacion de escalas para fiebre y tratamiento en niños.pdf

DOI: 10.1542/peds.2009-1070; originally published online January 18, 2010; 2010;125;228Pediatrics

Anna R. Huppler, Jens C. Eickhoff and Ellen R. WaldFever: Review of the Literature

Performance of Low-Risk Criteria in the Evaluation of Young Infants With

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of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.Boulevard, Elk Grove Village, Illinois, 60007. Copyright 2010 by the American Academy published, and trademarked by the American Academy of Pediatrics, 141 Northwest Pointpublication, it has been published continuously since 1948. PEDIATRICS is owned, PEDIATRICS is the official journal of the American Academy of Pediatrics. A monthly

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Performance of Low-Risk Criteria in the Evaluation ofYoung Infants With Fever: Review of the Literature

WHATS KNOWN ON THIS SUBJECT: Fever in neonates iscommon. The rate of SBIs in young infants may be as high as 12%.Low-risk criteria have been developed to aid in managementdecisions for well-appearing, febrile young infants.

WHAT THIS STUDY ADDS: Although the total risk of SBI in febrileyoung infants in this review was 10.9%, low-risk criteria allowed30% of these patients to be treated safely without empiricantibiotic therapy.

abstractOBJECTIVE: The goal was to determine the performance of low-riskcriteria for serious bacterial illnesses (SBIs) in febrile infants in pro-spective studies in which empiric antibiotic treatment was withheld,compared with studies (prospective and retrospective) in which em-piric antibiotic treatment was administered.

METHODS: A search of the English-language literaturewas undertakenby using a PubMed database and reference lists of relevant studies offever, low-risk criteria, and SBIs. Studies of infants 90 days of age,infants with specic infections, or infants with additional risk factorsfor infection were excluded. Publications were categorized as retro-spective, prospective with empiric antibiotic treatment for all patients,or prospective with antibiotics withheld. The relative risk of SBI inhigh-risk versus low-risk patients was determined for pooled data ineach category. The rates of SBIs in low-risk patients in each categorywere compared.

RESULTS: Twenty-one studiesmet the inclusion criteria. In prospectivestudies in which patients were cared for without empiric antibiotictreatment, 6 patients assigned to the low-risk category had SBIs; allrecovered uneventfully. The rate of SBIs in these low-risk patients was0.67%. The relative risk of SBIs in high-risk versus low-risk patients inthese studies was 30.56 (95% condence interval: 7.068.13). The rateof SBIs in low-risk patients in all studies was 2.23%. The rate of SBIs inlow-risk patients in the prospective studies without empiric antibiotictreatment was signicantly different from the rate in all other studies(0.67% vs 2.71%; P .01).

CONCLUSIONS: Low-risk criteria perform well in prospective studiesin which empiric antibiotic treatment is withheld. These criteria allow30% of young febrile infants to be observed without antibiotic treat-ment, thus avoiding unnecessary hospitalization, nosocomial infection,injudicious use of antibiotics, and adverse effects of antibiotics.Pediatrics 2010;125:228233

AUTHORS: Anna R. Huppler, MD,a Jens C. Eickhoff, PhD,b,c

and Ellen R. Wald, MDa

Departments of aPediatrics and bBiostatistics and MedicalInformatics, University of Wisconsin-Madison, Madison,Wisconsin; and cDepartment of Statistics and Clinical Sciences,Colorado State University, Fort Collins, Colorado

KEY WORDSfever, infant, bacteremia, meningitis, urinary tract infection

ABBREVIATIONSSBIserious bacterial illnessCIcondence intervalRRrelative riskUTIurinary tract infection

www.pediatrics.org/cgi/doi/10.1542/peds.2009-1070

doi:10.1542/peds.2009-1070

Accepted for publication Aug 28, 2009

Address correspondence to Anna R. Huppler, MD, University ofWisconsin-Madison, Department of Pediatrics, 600 Highland Ave,Madison, WI 53792. E-mail: [email protected]

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

Copyright 2010 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE: The authors have indicated they haveno nancial relationships relevant to this article to disclose.

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Fever in very young infants is a com-mon and important problem. Neonateshave unique vulnerabilities to infectionbecause of their immature immunesystems and incomplete barriers to in-vasion. The rate of serious bacterial ill-nesses (SBIs) in young febrile infantshas been reported to be between 8.5%and 12%.13

Before 1985, it was recommended thatall febrile infants (60 days of age) behospitalized and treated with paren-teral antibiotic therapy after a full sep-sis evaluation, because various crite-ria used to identify high-risk infantswere insufciently sensitive to identi-fy all infants with SBIs.46 However, theapproach of hospitalizing and treatingall febrile young infants with empiricantibiotic therapy had the disadvan-tages of unnecessary hospitalizations,nosocomial infections, injudicious useof antibiotics, emergence of resistantbacteria, and adverse effects ofantibiotics.7,8

During the late 1980s and early 1990s,investigators changed strategies andattempted to identify febrile infantswho were at low risk for SBIs andmight be treated with close observa-tion (inpatient or outpatient) withoutantibiotic treatment.3,916 After the de-velopment of various low-risk criteria,several groups undertook studies tovalidate the criteria in their own popu-lations.1727 The designs of those stud-ies alternated between retrospectiveand prospective, with variable ap-proaches to empiric use of ceftriax-one. We hypothesized that prospectivestudies that implemented a strategy ofobservation without antibiotic treat-ment for low-risk infants, thereby rely-ing on meticulous evaluation andcareful decision-making, would showsignicantly better performance oflow-risk criteria than would studiesthat continued to treat all patients(prospectively or retrospectively), re-gardless of risk stratication.

METHODS

We searched the English-language lit-erature for original articles studyinglow-risk criteria for SBIs in febrile in-fants between 0 and 90 days of age. ANational Library of Medicine PubMeddatabase search for articles was per-formed by using combinations of thefollowing search terms: low risk crite-ria, criteria, or risk; seriousbacterial illness, serious bacterialinfection, bacterial infection, orbacteremia; and fever or feverwithout source.Studies were limitedto humans, infants, and publication af-ter 1985.

The search criteria identied 740 arti-cles. Bibliographic references fromthe relevant studies (original researchand review articles) were reviewed foradditional citations. Articles were ex-cluded on the basis of abstracts if theyfocused on infants 90 days of age,patients with underlying conditions(such as patients with sickle cell dis-ease, neutropenia,malignancy, centralvascular catheters, or other immuno-compromised states), or patients witha single focus of bacterial infection(eg, urinary tract infection [UTI] ormeningitis). Sixty-three publicationswere reviewed carefully for inclusioncriteria, denition of SBIs, and evalua-tions performed for study patients.The components of the low-risk crite-ria used in each study were reviewedand compared with the original Roch-ester Criteria9 (Tables 1 and 2). Stud-ies with overlapping subjects wereexcluded.

Articles were grouped according totype of study, and total patients wereaggregated. The categories of studieswere prospective without antibiotictreatment of low-risk infants, prospec-tive with antibiotic treatment of low-risk infants, and retrospective.

Portions of studies using differentmanagement plans for low-risk infantswere classied accordingly. Data were

extracted from the tables and text ofeach study and included the number oflow-risk infants, the number of high-risk infants, the number of SBIs in eachgroup, types of SBIs, and the outcomesof low-risk infants with SBIs. Therandom-effects method described byDerSimonian and Laird28 was used toestimate overall relative risks (RRs)and corresponding 95% condence in-tervals (CIs). This method accounts forthe heterogeneity of studies through astatistical parameter representing in-terstudy variation.

Heterogeneity between studieswas as-sessed by using the Q statistic, as wellas graphic techniques. The -binomialmodel for overdispersed data29 wasused to estimate pooled rates of SBIsfor low- and high-risk patients. Com-parison of pooled rates betweengroups was performed by using a like-lihood ratio test. Linear regressionanalysis was used to evaluate thetrend in the proportions of infants des-ignated as being at low risk over time.

RESULTS

Twenty-one studies met inclusion cri-teria; 14 were prospective studies (Ta-bles 3 and 4) and 7 were retrospective(Table 5).3,927,30 Among the prospectivestudies, 9 treated low-risk patients em-pirically with antibiotics, 4 monitoredlow-risk patients without antibiotictreatment, and 1 used both strategies.

TABLE 1 Rochester Criteria for Infants at LowRisk of SBIs9,27

1. Previously healthy term infant withoutperinatal complications and with no previousantibiotic treatment

2. Normal physical examination ndings(including no otitis media)

3. White blood cell count: 500015 000 cells permm3

4. Band count:1500 cells per mm3

5. Urinalysis:10 white blood cells per high-power eld in centrifuged catheterizedspecimen

No comment about stool

Reference 9 established the original Rochester criteria.Reference 27 used identical laboratory criteria andslightly different inclusion criteria.

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The type of low-risk criteria was cate-gorized, with 10 studies using varia-tions of the Rochester criteria, 6 stud-ies using Philadelphia criteria (2comparing Rochester criteria withPhiladelphia criteria), 2 studies usingBoston criteria, 1 study using Pitts-burgh criteria, 1 study using Milwau-kee criteria, and 3 studies using clin-ical impression of sepsis or not illdescriptions (Tables 1 and 2). Studieswere performed between 1979 and1999. One study12 included only chil-dren in the low-risk category, without ahigh-risk comparison group. Fever

was dened as a temperature of38.2C in 1 study,1138.1C in 3 stud-ies,15,20,27 and38.0C in the rest of thestudies.

SBIs included bacteremia, meningitis,bacterial diarrhea, pneumonia, andUTIs.31 The dening characteristics foreach type of infection varied slightlybetween the studies, most notably inthe denition of UTI. Two studies ac-cepted bagged urine specimens forculture, resulting in 8 diagnoses ofUTIs in low-risk patients.13,19 Ten stud-ies diagnosed UTIs in patients with

catheterized urine cultures with50 000 colony-forming units of a singleorganism per milliliter.11,12,14,17,18,2023,25

Four studies provided no microbio-logic denition of UTI or description ofurine collection methods.3,15,16,30 An-other variation was the inclusion ofpneumonia as a SBI without microbio-logic documentation. All infants stud-ied were between 0 and 90 days of age.Six studies included only infants in therst month of life, and 4 studies ex-cluded infants in the rst month of life.The majority of studies were limited tothe rst 2 months of life, with 6 studiesextending to 3 months.

A summary of the prospective studiesin which patients underwent observa-tion alone is shown in Table 3.10,11,18,19,22

A total of 1858 patients were included,and 870 were classied as being at lowrisk. Six patients with SBIs weremissed, including 2 patients with bac-teremia and 4 patients with UTIs. Therst child with bacteremia receivedparenteral antibiotic treatment within24 hours after presentation and recov-ered uneventfully.11 The identity of theorganism was not noted. The secondchild had a blood culture positive forYersinia enterocolitica and fared wellafter treatment.18 The authors notedthat a conrmatory culture was notperformed before initiation of treat-ment. Three urine specimens obtainedwith sterile technique yielded eithergroup B streptococcus or Escherichiacoli.18 Those patients fared well withtreatment. One urine specimen col-lected by bag yielded E coli.19

TABLE 2 Variations of Rochester Criteria

Type of Low-Risk Criteria Differences From Original Rochester Criteria References

Rochester 2 If diarrhea,510 WBCs per high-power eld instool

10, 17, 18, 20, 30

Modied Rochester Normal inammatory markers (C-reactive proteinlevels or ESR)

13, 19, 21

Milwaukee CSF:10 WBCs per mm3; WBC count:15 000cells per mm3 (no band criteria); urinalysis:510 WBCs per high-power eld, no bacteria;urine dipstick: negative LE/nitrite

14

Philadelphia Infant observation score33:10; WBC count:15 000 cells per mm3 (no band criteria);urinalysis:10 WBCs per high-power eld, fewor no bacteria; CSF:8 WBCs per mm3, nobacteria, nonbloody

11

Philadelphia 2 WBC count:15 000 cells per mm3; band/neutrophil ratio:0.2; CSF:8 WBCs per mm3,no bacteria, nonbloody

20, 2225

Boston WBC count:20 000 cells per mm3 (no bandcriteria); CSF:10 WBCs per mm3; urinalysis:10 WBCs per high-power eld, no LE

12, 24

Pittsburgh Enhanced urinalysis:9 WBCs per mm3, negativeGram stain results; CSF:5 WBCs per mm3,negative Gram stain results (if6 wk)

26

Impression of sepsis Not ill or negative clinical impression of sepsis(history, physical examination, ESR of30mm/h, WBC count of15 000 cells per mm3)

3, 15, 16

WBC indicates white blood cell; ESR, erythrocyte sedimentation rate; CSF, cerebrospinal uid; LE, leukocyte esterase. Theinfant observation score includes 5 observations, that is, quality of cry, reaction to parent stimulation and state variation,color, hydration, and response to social overtures, each scored on a scale of 1 to 5.31

TABLE 3 Prospective Studies of Performance of Low-Risk Criteria for SBIs in Young Infants in Which Antibiotics Were Withheld From Low-Risk Patients

Year andReference

Criteria Type Age, d No. ofPatients

No. ofHigh-RiskPatients

Cases of SBI inHigh-RiskPatients

Rate of SBIs inHigh-RiskPatients, %

No. of Low-RiskPatients

Cases of SBI inLow-RiskPatients

Rate of SBIs inLow-RiskPatients, %

198810 Rochester 2 056 236 88 21 23.9 148 0 0.00199311 Philadelphia 2956 747 460 64 13.9 287 1 0.35199418 Rochester 2 060 203 203 4 1.97199719 Modied Rochester 428 250 119 40 33.6 131 1 0.76199922 Philadelphia 2 2960 422 321 43 13.4 101 0 0.00Total 1858 988 168 20.6 870 6 0.67


In the rest of the studies summa-rized in Tables 4 and 5 (prospectivestudies in which patients received em-piric antibiotic treatment and retro-spective studies), 89 low-risk infants(2.71%) were diagnosed as havingSBIs. This total included 2 cases ofmeningitis (1 with UTI and 1 with bac-teremia), 22 cases of bacteremia (1with gastroenteritis and 1 with osteo-myelitis), 39 cases of UTI, and 14 casesof gastroenteritis. Twelve cases of SBIdid not have a source identied.

Table 6 shows a comparison of the per-formance of the low-risk criteria forSBIs in young infants according tostudy design. The overall validity of thelow-risk criteria in pooled studies wasassessed by calculating the RR for SBIin high-risk versus low-risk infants.The RR reached statistical signicancein all 3 categories of studies. In pro-spective studies with no empiric anti-biotic treatment, the RR was 30.56(95% CI: 7.068.13). In prospectivestudies with empiric antibiotic treat-

ment, the RR was 8.75 (95% CI: 2.2915.21). In retrospective studies, the RRwas 6.93 (95% CI: 3.1010.75). Of im-portance, there was a statistically sig-nicant difference in the rates of SBIsin low-risk patients in the prospectivestudies with no empiric antibiotictreatment, compared with all otherstudies (P for difference .010). Whenprospective studies with no empiricantibiotic treatment were comparedwith all other studies, no signicantdifference in the rate of SBIs in high-

TABLE 4 Prospective Studies of Performance of Low-Risk Criteria for SBIs in Young Infants With Empiric Use of Antibiotics for All Patients

Year andReference








19859 Rochester 090 233 89 22 24.7 144 1 0.69198716 Impression of sepsis 056 97 36 5 13.9 61 2 3.28198815 Impression of sepsis 014 35 11 4 36.4 24 2 8.33199212 Boston 2889 503 503 27 5.37199314 Milwaukee 2856 534 391 23 5.9 143 1 0.70199418 Rochester 2 060 802 494 61 12.3 308 1 0.32199413 Modied Rochester 031 254 120 37 30.8 134 8 5.97200430 Rochester 2 090 1378 922 118 12.8 456 12 2.63200520 Rochester 2 and

Philadelphia 2056 259 186 63 33.9 73 2 2.74

200721 Modied Rochester Neonate 386 220 107 48.6 166 1 0.60Total 4481 2469 440 23.8 2012 57 2.71

TABLE 5 Retrospective Studies of Performance of Low-Risk Criteria for SBIs in Young Infants

Year andReference








198627 Rochester 090 117 47 4 8.5 70 3 4.2919903 Impression of sepsis 091 443 222 48 21.6 221 5 2.26199717 Rochester 2 029 119 71 19 26.8 48 3 6.25199725 Philadelphia 2 390 492 196 52 26.5 296 8 2.70199923 Philadelphia 2 328 254 145 27 18.6 109 5 4.59200024 Boston and

Philadelphia 2128 372 141 37 26.2 231 8 3.46

200126 Pittsburgh 060 404 277 41 14.8 127 0 0.00Total 2201 1099 228 19.8 1102 32 2.70

TABLE 6 Comparison of Performance of Low-Risk Criteria for SBIs in Young Infants, According to Study Design

Type of Study Total No.of Patients

No. ofPatients With

SBIs


Pooled Rate of SBIs inHigh-Risk Patients,Estimate (95% CI), %a


Pooled Rate of SBIs inLow-Risk Patients,Estimate (95% CI), %a

RR of SBI in High-Riskvs Low-Risk Patients

(95% CI)

Prospective, no antibiotictreatment

1858 174 988 20.6 (9.431.8) 870 0.67 (0.041.30) 30.56 (7.068.13)

Prospective, empiric antibiotictreatment

4481 497 2469 23.8 (13.434.1) 2012 2.71 (0.934.50) 8.75 (2.2915.21)

Retrospective 2201 260 1099 19.8 (14.525.1) 1102 2.70 (0.405.02) 6.93 (3.1010.75)Retrospective and prospective,empiric antibiotic treatment

6682 757 3568 22.3 (15.828.3) 3114 2.71 (1.44.0) 7.74 (3.8211.67)

a Estimated by using the -binomial model for overdispersed data.29

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risk patients was found (RR: 1.10;P .75).

An analysis examining the proportionof infants designated as low risk in allstudies showed a signicant trend to-ward assigning fewer infants to thelow-risk category over time ( 0.67; P .001). The slope parameterof the linear regression model of theproportions of infants designated aslow risk by time (year) was 0.015(P .001). Early studies placed60%of children in the low-risk category. Bythe middle 1990s, only 30% of childrenwere considered at low risk, as illus-trated in Fig 1.

DISCUSSION

The impetus for this study was theapparent discrepancy in the rate ofSBIs among low-risk febrile infantsreported in the literature. Previousstudies reported a range of rates ofSBIs in low-risk infants of 0% to

8.3%.10,15,22,26 This can be explained, inpart, by the different sets of criteriaused by various investigators (Table2).3,926,30 We showed that the rates ofSBIs in low-risk patients in both ret-rospective studies and prospectivestudies using empiric antibiotictreatment were the same (2.7%) andwere signicantly different from therate of SBIs in low-risk patients inprospective studies in which antibi-otics were withheld (0.67%). We hy-pothesized that the low-risk criteriawould function best when used inprospective studies in which low-risk patients underwent observationalone. Without reliance on empiricantibiotic treatment, it would be es-sential to capture all infants at riskof early deterioration in the high-riskgroup. Careful sample collection, aswell as meticulous physical examina-tion, excluded infants with SBIs fromthe low-risk group.

For physicians to rely on clinical al-gorithms, they must be convincedthat patients will not be placed injeopardy. The clinical predictabilityprovided by low-risk criteria will bedeemed satisfactory if the childrenidentied as being at low risk eitherdo not have a SBI or remain in stablecondition until the SBI is recognized.In prospective trials that treated low-risk infants with observation alone,the low-risk criteria missed SBIs in6 patients (bacteremia in 2 patientsand UTIs in 4 patients). One of thecases involved a positive urine cul-ture from a bagged specimen, whichmay represent a contaminant. Thesepatients were treated with appropri-ate antibiotics when the culturesyielded positive results, and allrecovered uneventfully. Therefore,careful application of these low-riskcriteria was very effective in identify-ing children from whom empiric an-tibiotic therapy could be withheld.

Overall, data from 8540 infants wereanalyzed in this study. The total num-ber of SBIs was 931, that is, 10.9%,consistent with rates commonly re-ported in the literature. With the useof low-risk criteria, 30% of febrileinfants can be identied as being atlow risk for SBIs and can be treatedwith observation alone. These pa-tients can be spared the negative ef-fects that may be associated withempiric use of antibiotics, includingcost, adverse effects of medications,development of resistant organisms,and psychosocial stresses on familydynamics. The criteria must be ap-plied carefully to avoid misassign-ment of infants. Special attentionshould be given to the physical exam-ination and medical history.

This study represents a comprehen-sive review of the literature that hasevaluated the effectiveness of low-riskcriteria in the identication of infantsunlikely to have SBIs over the previous

FIGURE 1Proportions of infants assigned to the low-risk category according to year of study initiation, with astatistically signicant trend toward assignment of fewer infants to the low-risk category over time(P .001).


23 years. The major weakness of thisanalysis is that the studies demon-strated minor variations in the low-risk criteria used and the age groupsincluded. Although these small differ-

ences in demographic characteristicsprohibit a clean comparison of all ofthe studies, we conclude that the ob-served difference in the performanceof low-risk criteria was a function of

the study design. When low-risk crite-ria are applied prospectively aftercareful evaluation, clinicians shouldbe condent in withholding empiric an-tibiotic treatment.

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DOI: 10.1542/peds.2009-1070; originally published online January 18, 2010; 2010;125;228Pediatrics

Anna R. Huppler, Jens C. Eickhoff and Ellen R. WaldFever: Review of the Literature

Performance of Low-Risk Criteria in the Evaluation of Young Infants With

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