DOI: 10.1542/peds.2013-1384; originally published online August 5, 2013; 2013;132;454Pediatrics

NaifehJay R. Malone, Sarah R. Durica, David M. Thompson, Amanda Bogie and Monique

InfectionsBlood Cultures in the Evaluation of Uncomplicated Skin and Soft Tissue

  

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located on the World Wide Web at: The online version of this article, along with updated information and services, is

 

of Pediatrics. All rights reserved. Print ISSN: 0031-4005. Online ISSN: 1098-4275.Boulevard, Elk Grove Village, Illinois, 60007. Copyright © 2013 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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Blood Cultures in the Evaluation of Uncomplicated Skinand Soft Tissue Infections

WHAT’S KNOWN ON THIS SUBJECT: Blood cultures are a commoninvestigation in children admitted to the hospital with skin andsoft tissue infections. The yield of blood cultures in this conditionis unknown.

WHAT THIS STUDY ADDS: Blood cultures are not useful inchildren admitted to the hospital with uncomplicated skin andsoft tissue infections, and they may be associated with increasedlength of hospital stay.

abstractBACKGROUND: Blood cultures are often obtained in children hospi-talized with skin and soft tissue infections (SSTIs). Because littleevidence exists to validate this practice, we examined the yield ofblood cultures in the evaluation of immunocompetent children withSSTIs.

METHODS: Medical records were reviewed for all children admittedbetween January 1, 2007 and December 31, 2009 after emergency de-partment evaluation and diagnosis of cellulitis or abscess. We com-pared patients with SSTIs (n = 482) with those with complicatedSSTIs (cSSTIs; n = 98). A cSSTI was defined as surgical or traumaticwound infection, need for surgical intervention, or infected ulcers orburns. The SSTI group included patients without complicating factors.

RESULTS: None of the patients in the SSTI group had a positive bloodculture. In the cSSTI group, 12.5% of blood cultures were positive. Themean length of hospital stay (LOHS) of children with SSTIs was shorterthan that of those with cSSTIs (P , .001). In the SSTI group, obtaininga blood culture was associated with a higher mean LOHS (P = .044).

CONCLUSIONS: Blood cultures are not useful in evaluating immuno-competent children who are admitted to the hospital with uncompli-cated SSTIs, and they are associated with a nearly 1-day increase inmean LOHS. Pediatrics 2013;132:454–459

AUTHORS: Jay R. Malone, MD, MS,a Sarah R. Durica, BA,b

David M. Thompson, PhD,a Amanda Bogie, MD,c andMonique Naifeh, MD, MPHa

Sections of aGeneral and Community Pediatrics and cEmergencyMedicine, Department of Pediatrics, The University of Oklahoma,Oklahoma City, Oklahoma; and bThe University of OklahomaCollege of Medicine, Oklahoma City, Oklahoma

KEY WORDSabscess, cellulitis, bacteremia, infant, child, adolescent, blood,culture, blood specimen collection

ABBREVIATIONSCA-MRSA—community-acquired methicillin-resistant StaphylococcusaureusCI—confidence intervalCRP—C-reactive proteincSSTI—complicated skin and soft tissue infectionED—emergency departmentLOHS—length of hospital stayMRSA—methicillin-resistant Staphylococcus aureusSSTI—skin and soft tissue infectionWBC—white blood cell

Dr Malone conceptualized and designed the study, participatedin data acquisition and initial data analysis, and drafted theinitial manuscript; Ms Durica performed data acquisition; DrThompson performed data analysis and interpretation; Dr Bogiecontributed to the conceptualization and design of the study; DrNaifeh contributed to study design and participated in datainterpretation; Ms Durica and Drs Thompson, Bogie, and Naifehcritically revised the manuscript; and all authors approved thefinal manuscript as submitted.

www.pediatrics.org/cgi/doi/10.1542/peds.2013-1384

doi:10.1542/peds.2013-1384

Accepted for publication Jun 20, 2013

Address correspondence to Monique Naifeh, MD, MPH,Department of Pediatrics, The University of Oklahoma, 1200Children’s Ave, Suite 14000, Oklahoma City, OK 73104. E-mail:monique-naifeh@ouhsc.edu

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

Copyright © 2013 by the American Academy of Pediatrics

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

FUNDING: No external funding.

POTENTIAL CONFLICT OF INTEREST: The authors have indicatedthey have no conflicts of interest to disclose.

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Skin and soft tissue infections (SSTIs) areacommonpediatricproblem,accountingfor 1 in 500 to 1 in 150 pediatric emer-gency department (ED) visits.1,2 Somemanagement guidelines1,3,4 suggest ob-taining blood cultures to ensure earlyidentification of bacteremia and pre-vention of subsequent sepsis. Obtaininga blood culture during an episode of SSTIis common practice, particularly in chil-dren who are admitted to the hospitalfor treatment with intravenous anti-biotics.2,5

The rate of bacteremia in immunocom-petentchildrenwithSSTIs isnotknown. Inthe pre–Haemophilus influenzae vaccineera, the rate of SSTI-associated bacter-emia was ∼20%,6 but after introductionof the H. influenzae vaccine, the ratedecreased to 2%.7 In 1998, Sadow andChamberlain reported that bacteremiaduring SSTI was largely associated withsuperinfected lesions originating fromactive varicella infection,7 which is nowmuch less common because of routinechildhood vaccination.8 However, sincethat studywas published, thewidespreademergence of community-acquiredmethicillin-resistant Staphylococcus au-reus (CA-MRSA) has been implicated ininvasive infections and now accountsfor 45% to 75% of SSTIs.9–13 The numberof pediatric ED visits for SSTIs increasedmore than 170%between 1997 and 2005.14

It remains unclear how the introductionof varicella and pneumococcal vaccinesand the widespread emergence of CA-MRSA have affected rates of bacteremiain SSTIs.

We determined the prevalence of bac-teremia, defined as a blood culture thatyields a positive result, among immu-nocompetent children admitted to thehospital after ED evaluation and di-agnosis of SSTI.

METHODS

Subjects

This retrospective case series includedchildren aged 0 to 18 years who were

admitted to The Children’s Hospital ofOklahoma after diagnosis of SSTI dur-ing initial ED evaluation. The Children’sHospital of Oklahoma is an urban,university-affiliated pediatric hospitalat a tertiary medical center. The EDtreats ∼40 000 children annually, andduring the study period, patients wereevaluated by residents in pediatrics,emergency medicine, and family med-icine and attending physicians. Thisstudy was approved by the institutionalreview board of the University of Okla-homa Health Sciences Center.

A search of the hospital’s electronicmedical records listed all children whowere seen in the ED between January 1,2007 and December 31, 2009, diagnosedwith SSTIs using ICD-9-CM codes for cel-lulitis and abscess (682.X), and admittedto the hospital. Children who were dis-charged from the hospital from the EDwere excluded. Other exclusion criteriawere immunocompromise, missingmedical record, return ED visit for a sin-gle episode of cellulitis, diagnoses thatthe primary reviewer judged to be mis-coded upon detailed chart review, in-cidental diagnosis of cellulitis at the timeof admission for a reason other thanSSTI, and development of cellulitis whileadmitted to the hospital for a reasonother than SSTI.

Eligible patients were stratified intogroups that distinguished those withcomplicated skin and soft tissue in-fection (cSSTI) from those with un-complicated infections (SSTIs). ThecSSTI group included patients withsurgical or traumatic wound infection,need for surgical intervention, andinfected ulcers or burns.4 Routine in-cision and drainage was not consid-ered surgical intervention. The SSTIgroup included all children withoutthese complicating factors.

Measurements

The primary reviewer evaluated medi-cal records from eligible patients using

a standard form. Data extracted in-cluded demographics, length of hospi-tal stay (LOHS), clinical presentation,past medical history, and laboratoryresults obtained in the ED includingblood and wound cultures, completeblood count with differential, and C-reactive protein (CRP). A second re-viewer independently checked 10% ofthemedical records to ensureaccuracyof data collection.

Protocol

During the study period, blood cultureswere collected in BACTEC Peds Plus/Fculture vials (Becton, Dickinson andCompany, Sparks, MD). One culture witha volume of 1 to 3 mL was drawn fromeach patient and incubated for 120hours. Cultures were categorized ascontaminated if they grew Staphylococ-cus epidermidis, viridans streptococci,diphtheroids, micrococcus, or propioni-bacterium species. Cultures containingany other organism were categorized aspositive. Cultures were categorized asnegative if no organism was found.

The primary reviewer judged medicalrecords to be miscoded and excludedthemfromthestudyif theclinicalhistory,physical examination, and physicianassessment and plan made no mentionof SSTI or symptoms of SSTI. All chartsexcluded for this reason were reviewedby a second reviewer. The primary re-viewer also excluded medical recordsfrom patients who were immunocom-promised, as evidenced by informationthat was available to the treating phy-sician in the ED that indicatedprimaryorsecondary immunodeficiency.

Data Analysis

Categorical variables are reported ascounts and percentages. Intergroupdifferences in percentages were testedby using Fisher’s exact tests. Continu-ous variables, including age, arereported as means with SDs, and in-tergroup differences in means were

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tested by using 2-sample t tests. Sta-tistical significance was determined byusing a critical a of .05.

A sample of 340 patientswasneeded toensure, with 90% certainty, that thewidth of the confidence interval (CI) onthe estimated rate of bacteremia inpatients with SSTI would be no morethan 2%. The sample size estimateassumes that 2% is the true preva-lence of bacteremia in children withSSTIs.7

RESULTS

The initial database search identified1812 children who were seen in the EDfor SSTI during the 3-year study period(Fig 1). Of those, 657 were admitted tothe hospital. Exclusion criteria weremet by 77 patients. The primary in-vestigator reviewed the remaining 580charts and judged 482 patients to haveuncomplicated SSTIs and 98 to meetcriteria for cSSTIs.

Table 1 lists patient demographics andclinical features. In the SSTI group (n =482), the mean age was 3.4 years (SD:3.8) with a range of 4 days to 16 years.Of these, 50% were male, and 56.2%had received at least 1 dose of anti-biotics before ED presentation. Themean temperaturewas 37.5°C (SD: 1.2),and 26.6% had temperatures.37.9°C.

In the cSSTI group (n = 98), the meanage of 5.8 years (SD: 4.7), with a rangeof 6 days to 16 years, was significantlyolder than the uncomplicated group(P , .001). The cSSTI group also hadmore males (64.2%; P = .011). Forty-ninepercent received at least 1 dose ofantibiotics before ED presentation, andmean temperature was 37.5°C (SD: 1.0)with 24.5% of temperatures.37.9°C.

In the uncomplicated SSTI group,patients with and without a blood cul-ture had similar presenting tempera-ture (37.5°C vs 37.1°C, P = .095), CRP(60 mg/L vs 47 mg/L, P = .39), and white

blood cell (WBC) count (17.7 vs 15.5,P = .15). Patients with a blood culturewere more likely to have a CRP drawn(97.8% vs 74.1%, P , .001).

Patients with uncomplicated SSTIs mostoften presented with infections locatedontheextremities(32.3%)or thebuttocksor perineum (26.8%) (Table 2). The mostcommon site of infection in the cSSTIgroup was the face or neck (39%), andno children in the cSSTI group hadinfections of the buttocks or perineum(P , .001). The cSSTI group also hada higher number of periorbital infectionsthan the SSTI group (11 vs 0, P, .001).

Laboratory investigations were per-formed in themajority of cases (Table 3).Blood cultureswere performed in 94.4%of uncomplicated and 81.6% of compli-cated cases. No positive blood cultureswere detected in the SSTI group, whichsuggests that the chance of obtaininga positive blood culture during an epi-sode of uncomplicated SSTI is ,1%

FIGURE 1Study design diagram.

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(95% CI: 0%–0.81%). In the cSSTI group,10 positive cultures were observed(12.5%; 95% CI: 6.2%–22.0%; P, .001).

In theSSTIgroup,75.7%ofpatients (365/482) had a wound culture, of which68.4%(250/365)grewMRSA. In thecSSTIgroup, 67.3% of patients (66/98) had awound culture, and 37.9% (25/66) ofthose grew MRSA.

Mean LOHS differed significantly be-tween the 2 groups (P, .001, Table 4).Children admitted with SSTIs hada mean LOHS of 3.2 days (SD: 2.3, range1–21 days), whereas children withcSSTIs had amean LOHS of 6.6 days (SD:10.9, range 1–72 days). In the SSTIgroup (Table 4), patients in whoma blood culture was obtained hada mean LOHS that was 0.91 days longerthan patients without a blood culture(95% CI: 0.026–1.8 days; P = .044).

DISCUSSION

SSTIs are an increasingly commoncause of outpatient visits and pediatricED visits. This is the first study in theCA-MRSA era to specifically examinethe prevalence of bacteremia in chil-dren with SSTIs. More than 90% ofchildren admitted to the hospital forSSTIsundergo laboratory investigations,including blood cultures. However, ourstudy found that blood cultures arepositive in ,1% of patients with un-complicated SSTIs and so do not im-prove patient management.

In our cohort, 83% of patients werejudged to have uncomplicated SSTIs,and 94% of those had blood culturesobtained. Among those with uncom-plicated SSTIs, there were no positive but3 contaminated blood cultures. This

preponderanceofcontaminatedculturesparallels the findings of 2 recent studiesof antibiotic choice inSSTIs, bothofwhichnoted false-positive to true-positive cul-tures in a ratio of 3:1.2,15 Similar false-positive blood culture rates were alsonoted in the 1998 study by Sadow andChamberlain, who examined the utility ofblood cultures in the post–Haemophilusinfluenzae vaccination era.7 They col-lected data in 1994–1995, before the in-troduction of the varicella vaccine in1995 and the pneumococcal conjugatevaccine in 2000. They detected 5 cases ofbacteremia, of which 3 were associatedwith varicella and one was Streptococ-cus pneumoniae. Routine vaccinationagainst both of these pathogens is nowcommon practice.

Additionally, Sadow and Chamberlain’sstudy was performed just as CA-MRSAinfections were beginning to increasein incidence. Although CA-MRSA hasbeen implicated in a wide range of se-vere infections, including bacteremiaand sepsis, it remains unclear wheth-er CA-MRSA causes bacteremia ina higher percentage of cases thanmethicillin-sensitive Staphylococcusaureus. Despite a high prevalence ofMRSA (68.4%) detected in wound cul-tures in children with uncomplicatedSSTI, no cases of bacteremia weredetected. In the cSSTI group, 60% of thedetected cases of bacteremia wereMRSA, although this figure should beviewed cautiously because there wereonly 10 isolates.

Children with uncomplicated versuscomplicated SSTI differed with regard toseveral demographic and laboratorymeasures. Mean age was higher inchildrenwith cSSTIs (5.8 vs 3.4 years;P,.001), possibly because of the inclusionof infection secondary to traumatic in-jury in the definition of complicated in-fection. Blood cultures were performedmore frequently in children with un-complicated infection (94.4% vs 81.6%;P , .001). This could be a result of

TABLE 1 Patient Demographics and Clinical Features (N = 580)

SSTI (n = 482) cSSTI (n = 98) P

Age, mean (SD) 3.4 (3.8) 5.8 (4.7) ,.001Male gender, n (%) 241 (50) 63 (64.2) .011Temperature (°C), mean (SD) 37.5 (1.2) 37.5 (1.0) .99

Fever (.37.9°C), n (%) 128 (26.6) 24 (24.5) .9Heart rate, mean (SD) 138 (30) 133 (31) .1353Prior antibiotics (yes), n (%) 271 (56.2) 48 (49.0) .22

TABLE 2 Location of Cellulitis (N = 580)

SSTI (n = 482), n (%) cSSTI (n = 98), n (%) P

Extremity 155 (32.3) 23 (23.5) .09Buttock or perineum 129 (26.8) 0 (0) ,.001Face or necka 93 (19.3) 38 (38.8) ,.001Hand or foot 36 (7.5) 9 (9.2) .41Trunk 35 (7.3) 13 (13.3) .07Genitals 25 (5.2) 2 (2.0) .29Scalp 9 (1.9) 2 (2.0) .99Periorbital 0 (0) 11 (11.2) ,.001a Excluding periorbital.

TABLE 3 Laboratory Investigations (N = 580)

SSTI (n = 482) cSSTI (n = 98) P

Blood culture performed, n (%) 455 (94.4) 80 (81.6) ,.001Blood culture positive, n (%) 0 (0) 10 (12.5) ,.001Blood culture contaminant, n (%) 3 (0.7) 1 (1.3) .11Complete blood count performed, n (%) 477 (99.0) 96 (98.0) .1WBC count 3109/L, mean (SD) 17.6 (6.9) 15.2 (7.6) .0024Neutrophils, mean (SD) 10.6 (5.3) 9.9 (6.5) .26Bands, mean (SD) 0.2 (0.7) 0.37 (1.1) .052Band/neutrophil ratio, mean (SD) 0.02 (0.08) 0.05 (0.2) .015CRP performed, n (%) 465 (96.5) 83 (84.7) ,.001CRP, mean (SD) 59.4 (64.2) 87.1 (101.1) .0011

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a greater percentage of children withcSSTI being admitted to surgical servicesthat may perform laboratory investiga-tions less often than medical services.Differences between the 2 groups inWBC, band/neutrophil ratio, and CRP,though statistically significant, were notlarge enough to be clinically meaningful.

Mean LOHS differed significantly be-tween the SSTI and cSSTI groups andalso differed within the SSTI group.Among patients with SSTI, those whounderwent blood cultures stayed in thehospital nearly 1 day longer (3.2 days)than those who did not (2.3 days; P ,.044). It is possible that patients with-out a blood culture were initially less illappearing than those who did receivea blood culture. However, no differ-ences were detected in presentingtemperature, CRP, or WBC. Blood cul-tures were obtained in a large pro-portion of patients whose initialclinical appearance seems unlikely tohave affected the decision to obtaina culture and therefore the LOHS.Rather, it is more likely that the longermean LOHS was a result of blood cul-ture monitoring. Although a case se-ries design cannot prove causality, thisconclusion is clinically logical, becausecare providers are most comfortabledeclaring a culture negative after 48hours.

Our study had several limitations. First,its retrospective study design limitedour interpretation of history and clini-cal appearance to clinician reports inthe medical record. Therefore, we mayhave incorrectly assigned somepatients to the SSTI or cSSTI groups.Second, 56.2% of patients in the SSTIgroup had received at least 1 dose ofantibiotics before their blood culture.This may have caused some bloodcultures to be negative in childrenwho were bacteremic before receivingantibiotics. Third, blood cultures werenot obtained in 5.6%of theSSTI groupor18.4% of the cSSTI group, which limitsour ability to determine the preciseincidence of bacteremia during SSTIs.Fourth, although our cohort includedinfants,60 days old, we did not studyenough patients in this age range toextend our conclusions to this high-riskgroup. Dedicated research is needed todetermine the bacteremia risk inyoung infants with SSTIs. Finally, ourstudy examined only the 36.3% of chil-dren presenting to the ED with SSTIswho were admitted to the hospital. Al-though this allowed us to select forchildren whowere presumably more illappearing and had a greater numberof laboratory examinations performed,some of the children who were dis-charged from the hospital from the ED

may have been initially bacteremic.Though unlikely, this possibility limitsour ability to determine with certaintythe true incidence of bacteremia dur-ing SSTI. Therefore, the applicability ofour study is limited to hospitalizedpatients.

Despite these limitations, several find-ings of this large case series areimportant. First, blood cultures per-formed in patients admitted to thehospital with uncomplicated SSTIs yieldan extremely low number of positiveresults. Second, although some labo-ratory findings differ between patientswith uncomplicated and complicatedSSTIs, these differences do not provideuseful clinical predictive value. Giventhe limited value of these tests, physi-cians might reasonably limit their useto childrenwith complicated infections.Third, patients with cSSTIs have a highrate of bacteremia, and blood culturesare important in treating those pati-ents. However, obtaining blood culturesin children with uncomplicated SSTIis seldom useful and may be harmful,as we found that obtaining a blood cul-ture is associated with a longer meanLOHS.

This is the first study to examine theyield of blood cultures in patients withSSTIs since the introduction of thevaricella and pneumococcal vaccines,and it is the first to do so in the CA-MRSAera. We agree with recent research onpediatric SSTIs that has called for ad-ditional prospective research to definecriteria forhospitalization.Weconcludethat blood cultures are not useful in themanagement of uncomplicated SSTI inhospitalized children, and cliniciansshould discontinue their use in thissetting.

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TABLE 4 LOHS (N = 580)

SSTI (n = 482) cSSTI (n = 98) P

LOHS (days),mean (SD)

3.18 (2.3) 6.62 (10.9) ,.001

Blood CultureDrawn

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3.24 (2.31) 2.33 (1.47) .044 7.30 (11.89) 3.61 (2.17) .194

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TRADEWINDS:Mywife and I lived in Hawaii for several years. We loved everythingabout the islands, including theweather. Other than a short period early each fall,we could always count on the trade winds to keep the sky clear and the tem-perature and humidity perfect for outdoor activities. We even had an expressionabout living in Hawaii: that there were “trade winds and tradeoffs.” Alas, thetrade winds, such a constant in island life, may be diminishing. As reported in theHonolulu Star-Advertiser (News: June 4, 2013), researchers using data from fourairports and four ocean buoys have concluded that there has been a 28% drop innortheast trade wind days since the early 1970s. Why the trade winds have di-minished is not known. While the weather remains lovely and the humidity stillcomfortable, other effects have been seen. Without the winds to generate waves,outrigger paddlers can no longer ride the waves and now need to prepare to raceover flat water. If the winds are weak, sulfur dioxide from the Kilauea volcano onthe island of Hawaii is no longer blown out to sea, leaving a haze hanging overHonolulu. The biggest issue, however, is decreased rainfall. The trade winds bringrain clouds that bump into the mountains and release their water. It is thisrainfall, along with the rain associated with winter storms, which supplies theislands with water. Residents report less water in streams fed by the rains, andseveral parts of Hawaii are even reporting drought conditions. If the trendscontinue, farmers may have to change when they plant or use more drought-tolerant crops. While it is unclear if the trade winds will continue to diminish, I amtrying to convince my wife that we should visit and conduct our own investigationfor a week or two.

Noted by WVR, MD

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DOI: 10.1542/peds.2013-1384; originally published online August 5, 2013; 2013;132;454Pediatrics

NaifehJay R. Malone, Sarah R. Durica, David M. Thompson, Amanda Bogie and Monique

InfectionsBlood Cultures in the Evaluation of Uncomplicated Skin and Soft Tissue

  

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