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Epidemiology of Dermatitis and Skin Infections in United States Physicians' Offices, 1993–2005

  1. Daniel J. Pallin1,2,
  2. Janice A. Espinola3,
  3. Donald Y. Leung6,
  4. David C. Hooper5, and
  5. Carlos A. Camargo Jr.3,4
  1. 1Department of Emergency Medicine, Brigham and Women's Hospital, Boston, Massachusetts
  2. 2Division of Emergency Medicine, Children's Hospital Boston, Boston, Massachusetts
  3. 3Department of Emergency Medicine, Allergy, and Immunology, Boston, Massachusetts
  4. 4Division of Rheumatology, Allergy, and Immunology, Boston, Massachusetts
  5. 5Division of Infectious Diseases, Department of Medicine, Massachusetts General Hospital, Boston, Massachusetts
  6. 6Department of Pediatrics, National Jewish Medical Health, Denver, Colorado
  1. Reprints or correspondence: Dr. Daniel J. Pallin, 75 Francis St., Boston, MA 02115 (dpallin{at}partners.org).
 
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Abstract

Background.Since the discovery of community-associated methicillin-resistant Staphylococcus aureus (MRSA), the number of emergency department visits for skin and soft-tissue infection (SSTI) has increased, and one report suggested an increase in the much larger setting of physicians' offices. Dermatitis compromises the cutaneous barrier to microorganisms and may predispose to SSTI. Our objectives were to determine whether office visits for dermatitis or SSTI have become more frequent since the emergence of community-associated MRSA, to describe the age-specific frequency of visits for dermatitis and SSTI, and to determine whether dermatitis is associated with SSTI and whether the association strengthened over time.

Methods.We analyzed visits for the diagnoses of dermatitis and SSTI by means of codes from the International Classification of Diseases, Ninth Revision recorded in the National Ambulatory Medical Care Survey, 1993–2005. We calculated population estimates by year and age group, with 95% confidence intervals (CIs), and examined trends over time. Multivariate logistic regression quantified the association between dermatitis and SSTI and assessed for interaction between dermatitis and year in the prediction of SSTI.

Results.Dermatitis was diagnosed at 13 million office visits per year (95% CI, 12-14 million office visits per year) over the study period, and SSTI was diagnosed at 6.3 million office visits per year (95% CI, 5.8 million-6.8 million office visits per year). The frequency did not change for either diagnosis over time when expressed as a percentage of all visits (both, P>.60). Dermatitis was most common among infants (256 visits per 1,000 population per year; 95% CI, 216-293 visits per 1,000 population per year). The rate of diagnosis of SSTI did not vary importantly by age. Dermatitis was associated with SSTI (odds ratio, 2.54; 95% CI, 1.92-3.35). The association did not strengthen over time.

Conclusions.The rate of office visits for dermatitis or SSTI did not increase from 1993 through 2005. Dermatitis was associated with SSTI. This association did not strengthen as community-associated MRSA became prevalent.

Genetically unique strains of community-associated methicillin-resistant Staphylococcus aureus (CA-MRSA) were discovered in the mid-1990s and are now the most common identifiable cause of skin and soft-tissue infection (SSTI) in United States emergency department patients [1, 2]. An increase in the number of physicians' office visits for SSTI during this period has been claimed in one article [3]. This claim is important because ∼8 times as many patients are examined in physicians' offices as are examined in emergency departments each year.

Dermatitis is a disorder of cutaneous immunity that compromises the physical barrier to bacteria. Lesions of immunoglobulin E (IgE)-mediated atopic dermatitis commonly harbor S. aureus and MRSA, and such lesions may predispose to infection [4], although it is unknown whether this is true in other forms of dermatitis, largely cell-mediated. We used a large nationwide sample of physicians' office visits to test the hypothesis that dermatitis is associated with SSTI and to determine whether the strength of association increased during the emergence of CA-MRSA.

We also sought to clarify 2 areas of ambiguity in the current literature. Prior studies have provided strong evidence of an increase in the rate of SSTI visits to the emergency department but left unclear whether a similar increase occurred in physicians' offices [2, 3, 5]. We will answer this question by reporting the change over time in the frequency of diagnosis of SSTI in the office setting. Also, prior studies provided only cursory information about the influence of age on the likelihood of SSTI [2, 3]. Pediatricians and other clinicians want to know whether everyone is at increased risk during the era of CA-MRSA or whether the frequency of relevant infections is increasing more in infants, children, or adults. We therefore measured age-specific rates of dermatitis and SSTI.

Thus, our objectives were to quantify the age-specific frequency of office visits for dermatitis and SSTI, to determine whether any change in these frequencies occurred during the emergence of CA-MRSA, to determine whether dermatitis and SSTI were associated, and to determine whether the association strengthened as CA-MRSA became prevalent.

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Methods

We analyzed data from the National Ambulatory Medical Care Survey (NAMCS) for 1993–2005 [6–9]. The NAMCS is a 3-stage probability sample of visits to US office-based physicians in the 50 states and the District of Columbia that is conducted annually. The survey includes physician participants who are not federally employed and who are classified by the American Medical Association or the American Osteopathic Association as primarily engaged in office-based patient care. Physicians in the specialties of anesthesiology, pathology, and radiology are excluded. A random sample of visits is studied during a randomly selected week. From the pooled sample, we obtained national estimates via visit weights and a multistage estimation procedure that is described elsewhere [7–9]. Data on 361,697 physicians' office visits were collected in the sample, forming the basis for our study.

Unlike prior investigations of SSTI in the era of CA-MRSA, we used only the NAMCS database, because its sister database, the National Hospital Ambulatory Medical Care Survey, describes acute-care visits to emergency departments, at which codiagnosis of a chronic condition (eg, atopic dermatitis) probably is less likely in the face of an acute condition (infection) [2, 3]. The hospital database also includes data on outpatient department visits, but these account for a small proportion of all ambulatory visits (∼6%) [5].

We identified visits that had a diagnosis of dermatitis by the diagnostic codes shown in table 1. We also conducted separate analyses for atopic dermatitis (International Classification of Diseases, Ninth Revision [ICD-9] code 691.8). In accordance with a prior study, we defined SSTI as shown in table 1[ 2].

Figure 1
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Figure 1

Annual rates of United States physicians' office visits with diagnosis of skin and soft-tissue infection (SSTI) or dermatitis, 1993–2005.

Figure 2
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Figure 2

Estimated number of United States physicians' office visits with diagnosis of dermatitis or skin and soft-tissue infection (SSTI), 1993–2005, stratified by age. Although the odds ratios appear to vary by age group, this variation is well within the bounds of random variation because the 95% confidence intervals all overlap substantially (not shown).

Table 1
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Table 1

Case Definitions for Diagnosis of Dermatitis or Skin and Soft-Tissue Infection

We describe the frequency of diagnosis of dermatitis and SSTI by reporting absolute numbers of visits, visits as a percentage of all-cause visits, and visits on a population basis by means of civilian population estimates from the US Census Bureau [10]. Additionally, we report frequencies of diagnosis by year and by age.

We quantified the association of dermatitis and SSTI by means of logistic regression. To control for potential confounders, we used a multivariate logistic regression model with SSTI as the dependent variable and with the following independent variables: dermatitis diagnosis, age, sex, race, ethnicity, region, metropolitan location, payer, season, and presence of diabetes [2]. The presence of diabetes was ascertained by detection of any code for diabetes and also by a checkbox for a history of diabetes that was available during 5 years of the study (1993–1996 and 2005).

In addition to determining the association between dermatitis and SSTI, we were interested in whether CA-MRSA in particular predisposes to SSTI among dermatitis patients. In the early years of our data set, CA-MRSA was unknown, and by the end of our study period, it was widespread [1]. This change afforded an opportunity to seek evidence of an association between dermatitis and CA-MRSA. We constructed another multivariate logistic regression by adding to the model described above terms for year of office visit and interaction of year and dermatitis. A positive interaction would suggest that dermatitis was a greater risk factor for SSTI in the presence of CA-MRSA.

We used Stata, version 10.0 (StataCorp), for analyses, and we used NAMCS design variables to estimate variance [7]. To test for trends over time, we used logistic regression and a nonparametric Wilcoxon-based trend test, where appropriate, and we report rates and proportions with 95% confidence intervals (CIs). A 2-sided P value <.05 was considered statistically significant.

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Results

We estimate that 10.6 billion visits to physicians' offices (95% CI, 9.9 billion-11.3 billion) occurred in the United States from 1993 through 2005, on the basis of the sample of 361,697 physicians' office visits [6, 7]. Dermatitis was diagnosed at 5,737 of the visits in our sample, atopic dermatitis at 674, and SSTI at 2,495.

This allows us to estimate that, nationwide, during this period, dermatitis was diagnosed at 13 million office visits per year (95% CI, 12 million-14 million office visits per year), corresponding to 1.6% of all visits (95% CI, 1.5%-1.7%) and corresponding to 48 office visits per 1,000 US population per year (95% CI, 44-51 office visits per 1,000 US population per year).

From 1993 through 2005, the frequency of visits for dermatitis increased in absolute terms (P=.002) and on a per population basis (P=.02) but not when expressed as a percentage of all visits (P=.86; figure 1). This pattern suggests that people made more visits in general but not specifically for dermatitis. Atopic dermatitis was diagnosed at 16 million visits (95% CI, 14 million-19 million visits) or 0.15% of all office visits (95% CI, 0.13%-0.18%). On a population basis, there were 4.6 atopic dermatitis visits per 1,000 US residents (95% CI, 3.9-5.3 atopic dermatitis visits per 1,000 US residents).

We estimate that SSTI was diagnosed at 82 million office visits (95% CI, 75 million-89 million office visits) during the study period, corresponding to 0.8% of all office visits (95% CI, 0.7%-0.8%) and corresponding to 23 office visits per 1,000 US population per year (95% CI, 21-25 office visits per 1,000 US population per year). The annual frequency of visits to physicians' offices for SSTI increased in absolute terms (P=.04) but not when expressed as a per population rate (P=.18) or as a percentage of all visits (P=.62) (Figure 1). This pattern suggests that people made more visits in general but not specifically for SSTI. This finding contradicts a prior report [3].

A detailed breakdown of visit frequency by diagnosis and age is provided in table 2. Age is categorized by decade for adults but more finely for children to provide data on pediatric subgroups of interest. Grouping age by decade, instead of by the finer strata shown in figure 2. The frequency of visits for dermatitis varied by age category (P<.001) (figure 2; table 2). Among children, any dermatitis was most common among infants. Atopic dermatitis visits were less common with increasing age (P<.001), with a rate among infants of 29 visits per 1,000 US population per year (95% CI, 19-39 visits per 1,000 US population per year); among children aged 1-5 years, 17 visits per 1,000 US population per year (95% CI, 12-21 visits per 1,000 US population per year); among children aged 5-10 years, 7.9 visits per 1,000 US population per year (95% CI, 5.2-11 visits per 1,000 US population per year); among children aged 10-15 years, 6.1 visits per 1,000 US population per year (95% CI, 4.0-8.1 visits per 1,000 US population per year); and among those aged ⩾15 years, 2.8 visits per 1,000 US population per year (95% CI, 2.2-3.3 visits per 1,000 US population per year). The frequency of visits for SSTI varied by age category (P<.001) (figure 2; table 2). On a population basis, SSTI visits were most common among the elderly.

Table 2
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Table 2

Estimated Annual No. of Office Visits for Skin and Soft-Tissue Infection (SSTI) and for Dermatitis in the United States, by Age in Years, 1993–2005

We categorized dermatitis in infants to determine whether diagnoses for diaper dermatitis were skewing the results. Of infant dermatitis diagnoses, contact dermatitis and other eczema accounted for 50%; diaper dermatitis, 37%; atopic dermatitis, 11%; dermatitis attributable to substances taken internally, 4%; and >1 form of dermatitis, 2%.

SSTI was diagnosed at 2.0% (95% CI, 1.5%-2.5%) of visits with diagnosis of dermatitis, compared with 0.8% (95% CI, 0.7%-0.8%) of visits without diagnosis of dermatitis, for an odds ratio (OR) of 2.72 (95% CI, 2.06-3.58; P<.001). Multivariate logistic regression analysis (controlling for age, sex, race, ethnicity, region, metropolitan location, payer, season, and diabetes) produced a similar result (OR, 2.54; 95% CI, 1.92-3.35; P<.001). Age did not influence the association of dermatitis and SSTI (figure 2, in which the slight variation in the OR from category to category was well within the expectation of random variation because all 95% CIs overlapped substantially [not shown]). As described in Methods, we assessed the interaction of dermatitis and year in the prediction of SSTI. The interaction was not statistically significant (P=.14).

We also examined the association between atopic dermatitis and SSTI. We again observed a positive association, but this was not statistically significant (OR, 1.87; 95% CI, 0.73-4.80). Multivariate analysis did not change this result materially (OR, 1.61; 95% CI, 0.63-4.10).

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Discussion

We studied temporal variation in the frequency of diagnosis of dermatitis and SSTI during the emergence of CA-MRSA, 1993–2005. We also studied the age dependence of these diagnoses. We tested the hypothesis that dermatitis was associated with SSTI and asked whether the association became stronger during the period of emergence of CA-MRSA.

We found dermatitis to be most common among infants, and this finding was not explained by diaper dermatitis. We found no change in the annual rate of dermatitis office visits.

In contrast to a prior study [3], we found no significant increase in office visits for SSTI relative to other diagnoses. We found no change in the rate of visits for SSTI from 1993 through 2005, but the prior report found a significant increase from 1997 through 2005. There are 2 likely explanations for this discrepancy. First, inspection of figure 1shows that there was a drop in the rate from 1996 to 1997, and thus the selection of 1997 as the start year, rather than 1996 or an earlier year, biased the prior study toward finding an increase [3]. To compare our study with the prior one, we analyzed visits from 1997 through 2005 and did find an apparent increase in the population rate (P=.02; data not shown). Second, the prior study pooled emergency department and office visits [3]. We know from another study that there was a large increase in the frequency of SSTI visits to the emergency department [2]. Combining data from the emergency department and office settings led to a finding of an increase overall [3], because the increase in the emergency department setting was large enough to outweigh the stability in the much larger office setting. This is important, because clinicians and policymakers need to know where SSTI patients are examined. Physicians' office visits represent a much larger segment of the healthcare industry than emergency department visits, with 10.6 billion versus 1.3 billion visits during the study period [2]. We are indeed in the midst of an epidemic of SSTI, but the healthcare impact of the epidemic appears to be limited to the emergency department setting [2].

Why would the epidemic's impact be limited to the emergency department setting? We propose that because CA-MRSA may be more likely to cause necrotizing and purulent infections (ie, abscesses) rather than indolent cellulitis, its victims may seek emergency care rather than scheduled care. Such a theory would be consistent with the production by CA-MRSA strains of necrotizing toxins, for example, Panton-Valentine leukocidin toxin [11].

Our a priori hypothesis was that dermatitis would be associated with SSTI. It seemed plausible that dermatitis would predispose to SSTI because these lesions constitute a breakdown in the physical barrier provided by intact epidermis and involve disarray of immune function. Lesions of atopic dermatitis, an IgE-mediated disorder, commonly harbor S. aureus and MRSA [4], although less is known about the bacteriology of other, cell-mediated dermatitides. Indeed, we found the odds of SSTI to be 2.54 times higher in the presence of a diagnosis of dermatitis than in the absence of a diagnosis of dermatitis. However, the association of SSTI and atopic dermatitis, in particular, was not statistically significant.

We sought evidence for an increasing risk of SSTI among patients with dermatitis in the presence of CA-MRSA by examining the interaction of year and dermatitis as predictors of SSTI, during a period that began before CA-MRSA was discovered and ended when it was widespread [1]. We found no statistically significant interaction; the absence of a statistically significant interaction suggests that the relationship between dermatitis and SSTI did not change in physicians' offices during the emergence of CA-MRSA.

Our study has limitations. The NAMCS data lack verification of diagnoses and microbiological data. It is possible that some cases of severe dermatitis-associated inflammation without purulence were diagnosed as infection even when there really was no infection. In other words, there may be diagnostic uncertainty when clinicians are faced with inflamed skin, and they may simply be likely to diagnose both infection and dermatitis in some cases; the diagnosis of both in cases where, in fact, only one were present, would exaggerate the observed association. However, proof of an infection is very difficult in the absence of purulence, given the low yield of needle aspiration and even skin biopsy in cellulitis, and such diagnoses continue to depend on clinicians' judgment [12]. Moreover, some people would see the lack of microbiological data as a strength of our approach because microbiological data carry the risk of evaluation bias [13]. These considerations mean that even a prospective cohort study would not ensure more-robust causal inference. Oversampling of patients who made multiple visits is a minor concern because the NAMCS samples for only one week at any given office.

We did not include the hospital outpatient department sample from the National Hospital Ambulatory Medical Care Survey, which accounts for a small proportion of all visits. It bears mentioning that this setting is a substantial source of ambulatory care for Medicaid patients and serves heavier caseloads of African American patients. Of ambulatory visits included in the NAMCS and the National Hospital Ambulatory Medical Care Survey, ∼78% are visits to physicians' offices, ∼16% to emergency departments, and ∼6% to hospital outpatient departments [5].

A practical limitation of the present and prior [2, 3] investigations is the inability to differentiate purulent from nonpurulent infections. The World Health Organization's ICD-9 is problematic because of its pooling of these disparate diseases. The tenth edition lacks this problem but has not come into wide use. CA-MRSA is known to have unique virulence factors that might predispose to purulent infections [11].

Despite these limitations, the following conclusions seem justified from this observational study: Dermatitis accounts for twice as many office visits as SSTI. Office visits for dermatitis are most common in infants and toddlers and not only because of diaper dermatitis. Office visits for SSTI are most common among children but occur in all age groups, representing 0.8% of all office visits. Office visits for SSTI did not increase from 1993 through 2005, during the emergence of CA-MRSA, despite prior assertions to the contrary [3]. Dermatitis is significantly associated with SSTI, but this association appears to have not changed as CA-MRSA became prevalent.

  • Received March 19, 2009.
  • Accepted April 29, 2009.
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References

  1. ↵
    1. Moran GJ,
    2. Krishnadasan A,
    3. Gorwitz RJ,
    4. et al
    . Methicillin-resistant S. aureus infections among patients in the emergency department. N Engl J Med 2006;355:666-674.
    CrossRefMedline
  2. ↵
    1. Pallin DJ,
    2. Egan DJ,
    3. Pelletier AJ,
    4. Espinola JA,
    5. Hooper DC,
    6. Camargo CA Jr
    . Increased US emergency department visits for skin and soft tissue infections, and changes in antibiotic choices, during the emergence of community-associated methicillin-resistant Staphylococcus aureus. Ann Emerg Med 2008;51:291-298.
    CrossRefMedlineWeb of Science
  3. ↵
    1. Hersh AL,
    2. Chambers HF,
    3. Maselli JH,
    4. Gonzales R
    . National trends in ambulatory visits and antibiotic prescribing for skin and soft-tissue infections. Arch Intern Med 2008;168:1585-1591.
    Abstract/FREE Full Text
  4. ↵
    1. Chung HJ,
    2. Jeon HS,
    3. Sung H,
    4. Kim MN,
    5. Hong SJ
    . Epidemiological characteristics of methicillin-resistant Staphylococcus aureus isolates from children with eczematous atopic dermatitis lesions. J Clin Microbiol 2008;46:991-995.
    Abstract/FREE Full Text
  5. ↵
    1. McCaig LF,
    2. McDonald LC,
    3. Mandal S,
    4. Jernigan DB
    . Staphylococcus aureus- associated skin and soft-tissue infections in ambulatory care. Emerg Infect Dis 2006;12:1715-1723.
    MedlineWeb of Science
  6. ↵
    National Ambulatory Medical Care Survey list of NCHS reports. Available at: http://www.cdc.gov/nchs/ahcd/ahcd_reports.htm#Physician. Accessed March 2007.
  7. ↵
    1. Tenney JB
    . Information for developing national statistics on ambulatory medical care. Med Care 1973;11(Suppl):87-95.
    Medline
    1. Tenney JB,
    2. White KL,
    3. Williamson JW
    . Ambulatory medical care survey: background and methodology. National Center for Health Statistics. Vital Health Stat 1974;2:61.
  9. ↵
    CDC. National Ambulatory Medical Care Survey: background and methodology. United States, 1967–72. Vital and Health Statistics. Data Evaluation and Methods Research. 1974, Series 2, No. 61. Available at: http://www.eric.ed.gov. Accessed 15 April 2008.
  10. ↵
    National Center for Health Statistics. Population information. 2008. Available at: http://wonder.cdc.gov/population.html. Accessed 9 September 2008.
  11. ↵
    1. Lina G,
    2. Piemont Y,
    3. Godail-Gamot F,
    4. et al
    . Involvement of Panton-Valentine leukocidin-producing Staphylococcus aureus in primary skin infections and pneumonia. Clin Infect Dis 1999;29:1128-1132.
    Abstract/FREE Full Text
  12. ↵
    1. Swartz MN
    . Clinical practice: cellulitis. N Engl J Med 2004;350:904-912.
    CrossRefMedlineWeb of Science
  13. ↵
    1. Talan DA
    . MRSA: deadly super bug or just another staph? Ann Emerg Med 2008;51:299-302.
    CrossRefMedlineWeb of Science
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  1. Clin Infect Dis. (2009) 49 (6): 901-907. doi: 10.1086/605434
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