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Evaluation of surveillance methods for Staphylococcal toxic shock syndrome.

Staphylococcal toxic shock syndrome (TSS) is a severe illness associated with toxin-producing Staphylococcus aureus. First named in 1978, TSS has been associated with tampon use, intravaginal contraceptive devices, and skin infections, particularly after surgical procedures (1,2). In January 1980, the Minnesota Department of Health (MDH) initiated surveillance for TSS with active and passive components. The national incidence of TSS decreased during 1980-1996 (3,4) after removal of high-absorbency tampons from the market and public awareness campaigns. In subsequent years, surveillance methods in Minnesota were changed to a solely passive surveillance system that relied on clinicians to report cases. MDH uses the 1997 case definition of the Centers for Disease Control and Prevention (CDC) (Atlanta, GA, USA) to determine case criteria for any probable TSS case ([greater than or equal to]4 clinical criteria and laboratory criteria) considered reportable (Table 1) (5). Given the complexity of the case definition, we suspected that TSS underreporting was likely.

Recently, several factors, including increasing prevalence of community-associated methicillin-resistant S. aureus that carries superantigens and the trend toward earlier menarche, suggested that the incidence of TSS might be increasing (6,7). Additionally, the number of requests for superantigen testing in the Minneapolis--St. Paul (MSP) area made to a reference microbiology laboratory that tests staphylococcal isolates from TSS cases increased during 2000-2003 (8). To determine the incidence of TSS, active surveillance was initiated at all MSP area hospitals using International Classification of Diseases, 9th Revision (ICD-9), codes assigned at hospital discharge. We compared passive surveillance reports with ICD-9 codes to determine an effective and efficient surveillance method for TSS.

The Study

The MSP area is composed of 7 counties with a population of 2,642,056 (2000 US Census) and 24 acute-care hospitals. Requests were sent to medical record departments of these hospitals for data on inpatients discharged from hospitals from January 1, 2000, through December 31, 2003, whose medical records indicated [greater than or equal to]1 of the select ICD-9 study codes. Medical records from all hospitalizations receiving the TSS-specific code (040.82 or 040.89) were reviewed (Figure), and a 20% random sample of medical records from hospitalizations that received [greater than or equal to]1 nonspecific TSS study code (Table 2) from within each hospital was reviewed. Each medical record was reviewed for TSS case criteria and pertinent epidemiologic and clinical information. Additionally, death certificates assigned the ICD-10 code for TSS (A48.3) and cases from the Minnesota Unexplained Critical Illness and Death of Possible Infectious Etiology project (UNEX) (9) during 2000-2003 were reviewed. TSS cases identified through ICD-9 code searches were compared with cases reported to MDH during 2000-2003. Data were analyzed with Stata version 9 (StataCorp, College Station, TX, USA). Statistical analyses included Pearson and McNemar [chi square] tests.

Of 7,414 hospitalizations with [greater than or equal to]1 study code, 116 (1.6%) were assigned the TSS-specific code and were reviewed (Figure). Of the remaining 7,298 hospitalizations assigned [greater than or equal to]1 nonspecific TSS code, 1,575 (21.6%) randomly selected hospitalizations were reviewed. Of these 1,691 hospitalizations, 55 had 5 or 6 criteria for TSS, of which 12 (22%) met the CDC case definition for streptococcal TSS, and 7 were non-MSP residents. The remaining 36 cases were probable or confirmed TSS. No cases from UNEX or death certificate searches met the TSS case definition. Of the 36 TSS cases, 17 (47%) were reported to MDH by passive surveillance. Thirty-one (86%) cases were found by using TSS-specific ICD-9 codes. Five cases were found by using non-TSS-specific ICD-9 codes. After adjusting for 20% random sampling for cases identified by non-TSS-specific codes, we identified the estimated number of cases by using non-TSS-specific codes to be 25. This analysis resulted in 56 estimated TSS cases identified in the surveillance area during 2000-2003 by using ICD-9 codes.

The TSS-specific ICD-9 code search identified 31 of the 56 estimated TSS cases (sensitivity 55%, specificity 99%). Seventeen cases were reported to MDH by passive surveillance (sensitivity 30%, specificity 99.9%); all were coded with the TSS-specific code. The TSS-specific ICD-9 code search was more sensitive than passive surveillance (p = 0.0005, McNemar [chi square] 12.25). Of those cases reported to MDH, more were likely to be associated with menstruation (14/17 vs. 5/19; p<0.001) and to have had a positive test result for S. aureus (16/17 vs. 11/19; p = 0.01). Twenty-seven of 36 TSS cases detected had a bacterial culture positive for S. aureus. The 3 TSS cases with methicillin-resistant S. aureus isolates were not reported to MDH. The positive predictive value of being a case among those coded with the TSS-specific code was 27% (31/116). In 68 of 116 cases that received the TSS-specific code, there was clinical suspicion of TSS, but these cases did not meet the clinical case definition (<5 criteria): 10 were streptococcal TSS and 7 were in non-MSP residents. All 17 cases reported to MDH were detected through the ICD-9 code search.



Surveillance for TSS is challenging given the lack of a diagnostic test and a case definition with multiple components. Under the current passive surveillance system, between one third and half of potential TSS cases were identified. Discrepancies were found in reporting, with menstruation-associated cases more likely to be reported to MDH than nonmenstrual-associated cases. This discrepancy was observed with prior active surveillance efforts (10).

Using ICD-9 codes, we found 12 TSS cases that were of streptococcal etiology. Accuracy may be improved by developing separate ICD-9 codes specific for staphylococcal, streptococcal, or unidentified TSS. In addition to the TSS-specific ICD-9 code, we selected 5 other ICD-9 codes on the basis of previous studies to address the concern that TSS cases may be classified under a staphylococcal infection or sepsis code, but not the TSS-specific code (8-10). These 5 additional non-TSS-specific ICD-9 codes required reviewing 1,575 medical records; only 5 (0.3%) additional TSS cases were identified. The non-TSS-specific ICD-9 codes detected 25 estimated cases. However, this detection required 8 trained staff and substantial resources with [approximately equal to]40 minutes required per medical record review.

Passive surveillance requires fewer public health resources because it relies on clinicians to report cases. Active surveillance involves public health resources in identifying cases. The disadvantage of passive surveillance is the potential for missed cases. Despite possible inaccuracies associated with the assignment of ICD-9 codes, these codes represent a standardized data source that may be readily available. In the absence of a specific diagnostic test, ICD-9 codes represent an efficient method for surveillance and following trends.

Medical record abstraction per hospitalization was labor- and resource-intensive and is not feasible for most health departments. With increasing use of automated electronic reporting for disease surveillance (11), querying hospital discharge data for the TSS-specific ICD-9 code is a feasible adjunct to passive surveillance to detect TSS trends over time. Consequently, it is imperative that clinicians and coders are thorough to ensure that ICD-9 codes are accurate.

We found it useful to add regular ICD-9 code searches for TSS-specific codes as an active surveillance adjunct to our passive surveillance system. This addition increases sensitivity of TSS surveillance with a minimal increase in resources. Use of this more sensitive system increases the ability to detect trends in TSS, which may develop because of changes in bacterial virulence characteristics, host characteristics such as the use of new devices or products, changes in human behavior, or changes in host susceptibility. Evaluation of this approach in other areas to assess sensitivity of TSS surveillance would be useful because coding practices may differ.

DOI: 10.3201/eid1505.080826


We thank Brenda Jewel, Craig Morin, Jean Rainbow, and Lori Triden for assistance with data collection; Elly Pretzel for graphics assistance; and Catherine Lexau and Tyson Rogers for statistical assistance.

This study was supported by grants from the National Institutes of Health (Ruth L. Kirschstein National Research Service Award T32 AI 055433-2), the Loan Repayment Program, the National Institute of Allergy and Infectious Disease (Extramural Clinical Research L30 AI 071582-01), and the Centers for Disease Control and Prevention (Emerging Infections Program CDC 5 R01 CI000209).

Use of trade names is for identification only and does not imply endorsement by the Public Health Service or by the U.S. Department of Health and Human Services.


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Lindsey Lesher, Aaron DeVries, Richard Danila, and Ruth Lyn eld

Author affiliations: Minnesota Department of Health, St. Paul, Minnesota, USA (L. Lesher, A. DeVries, R. Danila, R. Lynfield); and University of Minnesota, Minneapolis, Minnesota, USA (A. DeVries)

Ms Lesher is an epidemiologist in the Emerging Infections Program at the Minnesota Department of Health. Her research interests include epidemiologic methods and disease caused by S. aureus.

Address for correspondence: Lindsey Lesher, Minnesota Department of Health, 625 Robert St N, PO Box 64975, St. Paul, MN 55164-0975, USA; email:
Table 1. Staphylococcal toxic shock syndrome case definitions*

Criteria Definition


 Fever Temperature [greater than or equal
 to]38.9[degrees]C (102.0[degrees]F)

 Rash Diffuse macular erythroderma

 Desquamation 1-2 weeks after onset of illness,
 particularly on the palms
 and soles

 Hypotension Systolic blood pressure [less than
 or equal to]90 mm Hg for adults or
 <5th percentile by age for
 children <16 years of age;
 orthostatic decrease in diastloc
 blood pressure [greater than or
 equal to]5 mm Hg from lying to
 sitting, orthostatic syncope,
 or orthostatic dizziness

 Multisystem organ involvement

 Gastrointestinal Vomiting or diarrhea at onset of

 Muscular Severe myalgia or creatine
 phosphokinase level at least twice
 the upper limit of normal

 Mucous membrane Vaginal, oropharyngeal, or
 conjunctival hyperemia

 Renal Blood urea nitrogen or creatinine
 at least twice the upper limit of
 normal for laboratory or urinary
 sediment with pyuria ([greater
 than or equal to]5 leukocytes by
 high-power field) in the absence
 of urinary tract infection

 Hepatic Total bilirubin, alanine
 aminotransferase, or aspartate
 aminotransferase levels at least
 twice the upper limit of normal

 Hematologic Platelet counts [less than or
 equal to]100 x [10.sup.9]/L

 Central nervous system Disorientation or alterations in
 consciousness with focal neurologic
 signs when fever and
 hypotension are absent


 Culture If obtained, negative results on
 blood, throat, or cerebrospinal
 fluid cultures (blood culture may
 be positive for Staphylococcus

 Titer If obtained, no increase in titer
 for Rocky Mountain spotted fever,
 leptospirosis, or measles

Case classification

 Probable Meets laboratory criteria and in
 which 4 of 5 clinical findings
 described above are present

 Confirmed Meets laboratory criteria and in
 which all 5 of the clinical
 findings described above are
 present, including desquamation,
 unless the patient dies before
 desquamation occurs

* From the US Centers for Disease Control and Prevention (5).

([dagger]) Involving [greater than or equal to]3 organ systems.

Table 2. ICD-9 study codes used for staphylococcal toxic shock
syndrome case ascertainment *

Code Associated diagnosis

Specific toxic shock syndrome

040.89 or 040.82 ([dagger]) Toxic shock syndrome

Nonspecific toxic shock
syndrome codes

038.11 Staphylococcus aureus septicemia
038.19 ([double dagger]) Other staphylococcal septicemia
038.9 Unspecified sepsis
785.5 Shock without mention of trauma
785.59 or 785.52 ([dagger]) Sepsis

* ICD-9, International Classification of Diseases, 9th Revision.

([dagger])The code assigned to toxic shock syndrome changed from
040.89 to 040.82 on October 1, 2002, and the code assigned to
sepsis changed from 785.59 to 785.52 on October 1, 2003. Although
the codes changed, their associated diagnoses remained unchanged
and are considered mutually exclusive.

([double dagger]) Code eliminated after interim analysis of 627
medical records at 14 of 24 hospitals. Of 122 records receiving
only this code, 40% had 0 case criteria, all had [less than or
equal to]3 criteria, and 88% had bacteremia with a staphylococcal
species other than S. aureus.
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Title Annotation:DISPATCHES
Author:Lesher, Lindsey; DeVries, Aaron; Danila, Richard; eld, Ruth Lyn
Publication:Emerging Infectious Diseases
Date:May 1, 2009
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