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Original Studies

Increasing Numbers of Staphylococcal Scalded Skin Syndrome Cases Caused by ST121 in Houston, Texas

Hultén, Kristina G. PhD*,†; Kok, Melissa BS*; King, Kathryn E. PA-C, MS*; Lamberth, Linda B. BS†; Kaplan, Sheldon L. MD*,†

Author Information

From the *Section of Infectious Diseases, Department of Pediatrics, Baylor College of Medicine

†Infectious Disease Service, Texas Children’s Hospital, Houston, Texas.

Accepted for publication September 4, 2019.

S.L.K. is the PI for a pneumococcal surveillance study sponsored by Pfizer for which K.G.H. is also a co-investigator.

The authors have no conflicts of interest to disclose.

Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal’s website (www.pidj.com).

Address for correspondence: Kristina Hultén, PhD, Department of Pediatrics, Baylor College of Medicine, Texas Children’s Hospital, Feigin Tower, 1102 Bates Ave, suite 1150, Houston, TX 77030. E-mail: [email protected].

The Pediatric Infectious Disease Journal: January 2020 - Volume 39 - Issue 1 - p 30-34
doi: 10.1097/INF.0000000000002499

Abstract

Staphylococcal scalded skin syndrome (SSSS) or, Ritter Disease, is primarily a disease of childhood, and of greatest concern to the neonate and the immunocompromised host.1,2 The disease has been associated with exfoliative toxin (ET)-producing Staphylococcus aureus strains and clinical manifestations range from blistering infections that affect confined body areas to more generalized and systemic infections.1,3,4 While mortality remains low, the extensive exfoliation and resulting loss of the protective skin barrier is especially concerning to the neonate where extensive fluid loss, hypothermia and secondary infections can occur.5

The epidermolytic activity of S. aureus isolates associated with SSSS in humans has been linked to the activity of ETs A and B while ETD was associated with cutaneous abscesses and furuncles.6,7 The ETs are serine proteases encoded by the genes eta, etb and etd. While eta is carried on a temperate phage (ϕeta),8etb is plasmid mediated9 and etd has been identified within a pathogenicity island on the bacterial chromosome.6 To date, the toxins have been associated with only certain strains of S. aureus, most of which have been methicillin-susceptible S. aureus (MSSA).10 In the past, the strains causing SSSS were commonly reported as belonging to phage group II.1 More recent studies have reported isolates belonging to sequence types (ST) 15, ST121, ST 2126, and ST2993, using multilocus sequence typing (MLST).11,12 Of these, ST121 has been most commonly reported as a cause of SSSS.

While the SSSS exfoliation has been mainly attributed to the effects of the ETs, studies have also reported the Panton-Valentine leukocidin (PVL) genes associated with SSSS isolates.13,14 PVL is encoded by the genes, lukSF-PV (pvl) and in the United States has been associated with the endemic USA300-ST8 MRSA clone. The presence of a few enterotoxin and enterotoxin-like genes have also been studied in SSSS isolates.11 Additionally agr group IV is the predominant accessory gene regulatory protein group among these isolates.11,15,16

While a few studies from Europe, Asia and Latin America include molecular analysis of scalded skin syndrome isolates, no similar contemporary data from the United States is available. One pediatric study reported current practice variations in diagnostic test use.17 A retrospective study from the Children’s Hospital of Philadelphia reported the SSSS epidemiology and antimicrobial susceptibility patterns of 21 patients and their isolates identified from 2005 to 2011. They found 86% of isolates to be MSSA among children 0.5 months to 6 years of age, but did not further characterize the isolates.10 One other study found increasing cases of SSSS around the United States from 2008 through 2012 based on data obtained from the Nationwide Inpatient Sample (NIS), but characteristics of isolates were not reported.18

At Texas Children’s Hospital (TCH) in Houston, Texas, we noticed an increase in the number of SSSS cases and S. aureus isolates that were collected through our prospective S. aureus surveillance study. We describe the increasing numbers of SSSS cases and the molecular characteristics of the S. aureus isolates and the clinical features of the patients from whom isolates were available.

METHODS

Patients and Study Design

All patients who were coded as SSSS by ICD9 (695.81) or ICD-10 (L00) codes at the time of hospital discharge, from 2008 to 2017, were identified through the Hospital Information System at TCH. Patients with S. aureus isolates available for study were retrospectively identified from the TCH S. aureus surveillance study database. The surveillance study has been ongoing since 2001 and was approved by the Institutional Review Board, Baylor College of Medicine, Houston, TX.19 For this subset of patients, medical records were reviewed for demographic data, clinical presentation and antimicrobial therapy. To delineate the reasons for the low number of available culture positive cases, the last consecutive 100 medical records from SSSS patients without isolates from the study period (1/1/2017–12/31/2017) were reviewed for whether cultures were performed or whether the cases were culture negative. This chart review focused on cultures pertinent to SSSS (eg, blood and body surface cultures), thus excluding urine and CSF cultures that were part of neonatal sepsis workups.

Laboratory Methods

Antimicrobial susceptibilities were determined in the Clinical Microbiology laboratory at TCH by Vitek 2 (bioMérieux, Cambridge, MA), E-test (bioMérieux) and Kirby-Bauer using Clinical and Laboratory Standards Institute guidelines.20 E-tests for mupirocin were performed in the Dr. Edward O. Mason, Jr. Infectious Disease Research Laboratory. Molecular analysis was performed using PCR to detect the genes tst, pvl (lukSF-PV), eta and etb and to determine the agr group.16,21

All isolates underwent pulsed-field gel electrophoresis to determine strain relatedness and to identify clonal clusters (CCs) using previously described methods and criteria.22 MLST was used to further characterize all SSSS isolates. MLST allele and ST designation were obtained using the online MLST database (http://pubmlst.org/saureus/). SSSS CCs were grouped amidst database isolates using eBURST (based upon related sequence types).

Statistical Analysis

STATA11 (College Station, TX) was used to calculate χ2 for trend. Statistical significance was set at P < 0.05.

RESULTS

Patients With SSSS

Three hundred and eighty-seven patients were identified with SSSS from 2008 to 2017. The number of cases increased from 5 in 2008 to 116 in 2017 representing a 20-fold increase (2.3/10,000 admissions to 52.6/10,000 admissions) in the study period (P < 0.0001) (Fig. 1). Only 58 patients (15%) had isolates available for study. All of the isolates were obtained from 2013 to 2017 (Table 1; Fig. 1). To understand the low number of culture-positive cases, the last 100 consecutive cases within the study period that lacked isolates were reviewed. Among these 100 patients with SSSS by ICD9/10 code, 59 had a culture performed of which 50 had only blood cultures done, 5 had blood cultures plus SSTI (skin, nose or eye) cultures and 4 had a skin/nose or eye culture done. Four of 9 patients with a SSTI culture were only tested for MRSA. Of the remaining 5 patients with SSTI cultures, 1 had Gram-positive cocci in clusters plus Acinetobacter spp., 1 had Gram-positive cocci in pairs and 1 was on antibiotics at the time of culture.

T1
TABLE 1.:
Patient Demographics and Characteristics for Isolates From Patients With Staphylococcal Scalded Skin Syndrome
F1
FIGURE 1.:
The numbers of Staphylococcal scalded skin syndrome (SSSS) cases are presented for the study period by ICD 9/10 codes, ICD 9/10 cases/10,000 hospitalizations and the S. aureus isolates available from patients with SSSS for study (SSSS isolates).

Demographic and Clinical Characteristics of Children With SSSS and S. aureus Isolates

For the 58 children with S. aureus isolates available, the median age was 0.9 years (range 0.04–9.6 years; 10 were <2 months old) and 34 (59%) were males. All patients except 1 presented with SSSS to the TCH or to an outside hospital. One patient was initially admitted for severe hyponatremia and developed S. aureus bacteremia, thus meeting the criteria for a nosocomial infection. In all cases, the scalded skin presentation involved large portions of the body, from face/neck to trunk and extremities; percent body involvement was not frequently recorded in the medical records. Nikolsky’s sign was recorded in 20/58 (34%) of cases and clinical descriptions commonly involved denudation, erythroderma, crusting, blistering, and peeling. Other general symptoms included pain, weakness, irritability and a change in appetite. Only 13 patients had a temperature >100.4°F recorded at least once during their illness. Isolates were obtained most commonly from the face (precise site on face not specified) (n = 14), nose (n = 12), eye (n = 11), and neck/head (n = 11). Other cultures were mainly from the upper body. Five of 19 patients who had a rapid Strep A test performed had a positive result. These tests were frequently done at an urgent care clinic or outside hospital before seeking care at TCH. Blood cultures were obtained from 47 patients; 3 were positive for MSSA, 1 patient had septic shock. Ten patients had other pathogens isolated. Co-pathogens included Streptococcus pyogenes (n = 3, from face or eye), Streptococcus agalactiae (n = 2, from rectum or neck), Pseudomonas aeruginosa (n = 2, from nose or neck), Streptococcus pneumoniae (nose) and Escherichia coli and Enterobacter sp. (chin). Two patients had urinary tract infections with Citrobacter koseri and Enterococcus spp., respectively. The majority of patients had no underlying condition identified. Six patients had a skin condition (ie, eczema, contact dermatitis, atopic dermatitis, seborrheic infantile dermatitis) and one of these patients had P. aeruginosa cultured from the nose. One patient had DiGeorge syndrome (Streptococcus agalactiae and P. aeruginosa were cultured from the neck swab).

The hospital length of stay ranged from 1 to 11 days, with a median of 3 days; 7 children spent from 1 to 10 days in a critical care unit. One patient with extensive skin exfoliation was transferred on hospital day 3 to a burn unit at an outside hospital for further care.

All patients received intravenous antibiotics while in the hospital. Forty-seven patients received clindamycin, either alone or as part of initial combination treatment. Ten patients were initially given vancomycin alone or in combination with other antibiotics and 1 patient was given ampicillin-sulbactam. Of the 57 patients who completed treatment at TCH, definitive treatment constituted clindamycin alone for 37 patients, clindamycin plus another drug (vancomycin, nafcillin or cefazolin) for 7 patients, nafcillin (4 patients), cefazolin (4 patients), vancomycin (3 patients), ampicillin-sulbactam (1 patient) or nafcillin and vancomycin (1 patient). Seven patients completed their antibiotic regimen in the hospital. For the remaining patients, outpatient antibiotics included clindamycin (n = 38), cephalexin (n = 5), trimethoprim-sulfamethoxazole (n = 3), clindamycin and cephalexin (n = 2), and 1 patient each with amoxicillin-clavulanate or levofloxacin. Total antibiotic duration of treatment ranged from 7 to 17 days. In addition to systemic antibiotics, emollients, mupirocin, eye drops, pain medications ranging from acetaminophen to intravenous morphine and antihistamine drugs such as hydroxyzine or diphenhydramine were prescribed. Of the 15 patients with clindamycin-resistant isolates, 2 patients whose isolates had constitutive resistance were treated with vancomycin. Nine of 13 patients with inducibly resistant isolates were treated with intravenous clindamycin as inpatients and 8 completed outpatient treatment with oral clindamycin. Seven of these 8 patients were in the hospital 3 or fewer days. SSSS resolved in all 57 patients managed at TCH. However, 1 child with a MSSA-SSSS had a recurrence 2 weeks after 7 days of treatment with nafcillin.

Molecular and Antimicrobial Susceptibility Characteristics of SSSS Isolates

One MRSA and 57 MSSA isolates were divided into 10 STs (Table 2). Overall, 52 (90%) were agr group IV, 49/58 isolates carried eta and 57 of 58 carried etb; all isolates with eta also contained etb. Fifty-one (87.9%) of the SSSS isolates clustered together within the Clonal Complex 121 (CC121). These were ST121, ST51, ST 2276 and a new single locus variant (SLV) of ST2276. All of these were of agr group IV, pvl−, tst−, and carried eta and/or etb. Pulsed field gel electrophoresis showed differences by <4 bands within this CC. None of the SSSS isolates were of the USA300 clone by pulsed-field gel electrophoresis by established criteria, although one isolate was USA300-related, ST8, agr group 1 and pvl+. Two isolates carried the tst gene. Other STs included STs 5, 6, 8, 30, 88 and one new SLV of ST25). The eBURST in the Figure (Supplemental Digital Content, https://links.lww.com/INF/D665) illustrates the genetic diversity of these different STs. Of the STs not associated with the CC121 cluster, one of the ST5 isolates, an MRSA, was recovered from a patient with SSSS with no underlying condition other than asthma; the other ST5 isolate was from a child with contact dermatitis and “other eczema.” This patient had an isolate negative for both ETs and it is possible his infection was a superinfection of the eczema rather than SSSS. The ST6 isolate was from a 4-month old who was initially admitted for hyponatremia and subsequently developed MSSA bacteremia and scalded skin syndrome. The ST8 isolate was from a neonate. The ST25-SLV isolate was from a patient initially diagnosed as impetigo. The ST30 isolate was from a 3-year old and the ST88 isolate was recovered from a 2-month old; neither of these infections was associated with any differentiating presentations or underlying conditions.

T2
TABLE 2.:
Molecular Characteristics Per Multi Locus Sequence Type

Fifteen isolates (25.9%) were clindamycin resistant; 2 ST121 isolates displayed constitutive resistance. The 13 MLSB-resistant isolates included ST30, ST51, ST2276-SLV and all of the ST2276 isolates. Eight isolates (ST121) were tetracycline resistant, 24 were erythromycin resistant and one (ST121) was resistant to trimethoprim-sulfamethoxazole. Twelve ST121 isolates had mupirocin MIC>256 µg/mL.

DISCUSSION

We report an increasing number of patients with a primary diagnosis of SSSS at TCH since 2008. In this first study to detail the molecular characteristics of pediatric SSSS isolates in the United States, we found the majority of isolates to be MSSA and genetically part of the CC121 cluster. This finding is in contrast to other MSSA isolates among our patient population, where diverse genetic backgrounds have been described.23–26 Among patients seeking care at our hospital, the majority of the skin and soft tissue infections (SSTI) have been caused by MRSA since the early 2000’s. However, the numbers of patients with community-acquired (CA) MRSA SSTI declined by 60% between 2007 and 2014 (from 1461 infections in 2007 to 578 in 2014), while the number of children with CA-MSSA SSTI have remained virtually the same.19,24 USA300 has been the most common clone of S. aureus SSTI among our patient population for more than a decade, causing >95% of infections in CA-MRSA SSTIs and a portion of the CA-MSSA infections. An informal study of 84 MSSA isolates from SSTI (cellulitis and abscesses) obtained within the same time period as the scalded skin infection isolates revealed 44% to be USA300, 70% agr group 1, 62% pvl+, 16% eta+ with none of these isolates carrying etb (data not shown). Thus, the characteristics of scalded skin isolates are genetically distinct from contemporary MSSA strains causing other SSTI infections within our hospital population.

CA-MRSA strains have been reported as carriers of eta and etb and it has been speculated that MRSA strains carrying these genes might disseminate across the world to cause bullous impetigo and/or SSSS.27 Our study identified only one of 58 isolates to be a MRSA and is in agreement with other studies identifying ST121-MSSA as the most common cause of SSSS.28,29 All of the ST121 isolates in the study were pvl negative. Most recently, molecular investigation of strains from a Greek hospital from 2014 to 2017 reported 31 cases and an association with ST121 MSSA isolates; co-existence of both ET (eta/etb) genes and mupirocin- and fusidic acid-resistance was also noted.28 High mupirocin resistance was also observed for a third of our ST121 isolates, but not detected among any of the other strains causing SSSS. The implications of the high mupirocin resistance rates are difficult to interpret with respect to clinical effectiveness in patients with SSSS considering that mupirocin is often applied to affected skin in addition to the administration of systemic antibiotics.

Rao et al30 summarized the literature on ST121 in Africa, Asia and Europe. The authors found that >90% of the ST121 isolates carried the PVL genes while in our present study, none of the ST121 isolates was pvl+ and only one ST8 isolate, related to USA300 was pvl+. Rao et al further reported increases of ST121 in Africa and noted that this genotype also can be a carriage pathogen. A Chinese study reported 30.6% of the 147 carriage isolates were ST121 while a German study found that 13.7% of 51 nasal colonization isolates were ST121.31,32

In accordance with all previous literature on SSSS, the infections we observed were primarily in young children and neonates with a median age just below a year. We found only 3 patients to be bacteremic, in contrast to a retrospective study of 290 children with SSSS which reported that 20% were “septicemic” (no mention of blood culture results).33

Most patients were treated with clindamycin with medical record notes frequently stating the intention to inhibit S. aureus toxin production. Despite the high rate of clindamycin resistance (25.9%; 13/15 inducible isolates), no case of recurrent SSSS treated with clindamycin was identified. The only recurrence occurred in a patient treated with nafcillin for 7 days. This is consistent with the thought that inducible resistance is of lesser importance for S. aureus infections associated with a relatively low bacterial inocula. By the same token, the relatively high rate of clindamycin resistance is of concern and cultures should be performed for this patient population.

We speculate that the CC121 clone was recently introduced to our region but is now responsible for an increasing number of SSSS cases at TCH. In the United States, ST121 has been rarely reported among S. aureus isolates characterized in global and collaborative collections of isolates prior to 2008.13,34 The combined worldwide literature suggests this ST is not only associated with SSSS but also with colonization and clinical infections ranging from SSTI to invasive disease such as osteomyelitis. Thus, further characterization of its genetic makeup and its role in other MSSA infections is required to better understand its importance and the unique propensities of this strain.

Limitations of this study included the availability of only a portion of isolates from the patients coded as having SSSS and that isolates were obtained from the skin and could potentially not be the cause of the SSSS. On the other hand, SSSS is typically not associated with an invasive infection and the only isolates available are obtained from superficial sites. There is a possibility that some cases of SSSS were miscoded as another skin condition, thus leading to underreporting this presentation. Finally, this study only concerns isolates from a pediatric population at 1 hospital and the results cannot be broadly applied to other populations within or outside of the United States.

ACKNOWLEDGMENTS

We thank Andrea R. Forbes, RN, MS, Dr. J.J. Dunn and Dr. PA Revell, for their contributions to the S. aureus surveillance study. This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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Keywords:

Staphylococcus aureus; ST121; scalded skin syndrome; pediatric

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