OUP user menu

Epidemiology and Susceptibilities of Methicillin-Resistant Staphylococcus aureus in Northeastern Ohio

Thierry Delorme PhD, Stacy Rose MSN, Julie Senita MSN, Cynthia Callahan, Payman Nasr PhD
DOI: http://dx.doi.org/10.1309/AJCPQ46ZPQXVHHNC 668-677 First published online: 1 November 2009

Abstract

A retrospective survey was performed on all staphylococcal infections diagnosed by the Ashtabula County Medical Center (Ashtabula, OH) during 2006 and 2007. Of the 1,612 Staphylococcus aureus isolates evaluated for their antibiotic resistances, 947 were methicillin-resistant S aureus (MRSA). In 2007, MRSA infections reached 589 cases per 100,000 inhabitants, a 77% increase compared with 2006. The increase in MRSA infections was noticeable among youth (6–25 years old), middle-aged people (45–50 years old), and elderly people (86–90 years old). MRSA infections increased among inpatients by 58%, among outpatients by 43%, and among nursing home residents by 183%. More than 66% of MRSA infections were found among healthy people in the community with no apparent risk factors. More than 88.7% of the infections belong to only 9 profiles of antibiotic resistance indiscriminately distributed among inpatients, outpatients, and nursing home residents. This report sheds further light on the rapid spread of MRSA across Northeastern Ohio, stressing the need for better education in preventive measures and infection control at the level of community and health care settings.

Key Words:
  • Staphylococcus aureus
  • Methicillin resistance
  • MRSA
  • Community acquired
  • Hospital acquired
  • Epidemiology

Staphylococcus aureus is the most common cause of skin infections in the United States. When left untreated, these staphylococcal infections may result in a wide range of conditions such as endocarditis; pneumonia; wound, joint, and/or bone infections; and deep tissue abscess formation.1 Most staphylococcal infections can be effectively treated with antibiotics; however, in recent years, an increasing number of S aureus species have become resistant to wide arrays of antibiotics, including methicillin, β-lactams, macrolides, lincosamides, tetracyclines, and gentamicin.2

Methicillin-resistant S aureus (MRSA) was first identified in Europe in 1961, only 1 year after the introduction of methicillin.3,4 In the 1970s, MRSA was recognized as a serious nosocomial problem in the United States.5 Since then, MRSA has been an ever-growing problem in hospitals and nursing home settings. By the mid 1990s, hospital-acquired MRSA (HA-MRSA) had become one of the most prevalent nosocomial infections worldwide.6

Today, MRSA has expanded to the community, in addition to long-term health care facilities. Analysis of more than 3 million bacterial isolates from inpatients obtained from 300 laboratories across the United States between 1998 and March 2005 showed an S aureus prevalence of 18%.7 The worldwide emergence and spread of MRSA strains not associated with health care facilities have also been reported, which are commonly referred to as community-acquired MRSA (CA-MRSA). CA-MRSA is commonly implicated in skin and soft tissue infections and pneumonia, and is one of the most important public health concerns reaching endemic proportions.8

Molecular epidemiologic studies have shown that CA-MRSA differs phenotypically and genotypically from HA-MRSA.9 CA-MRSA strains have been shown to grow significantly faster than HA-MRSA strains.10 CA-MRSA resistance is usually limited to β-lactams, and the strains remain susceptible to clindamycin, gentamicin, sulfamethoxazole-trimethoprim, vancomycin, rifampin, tetracycline, and linezolid.1113 Most CA-MRSA strains also carry the Panton-Valentine leukocidin genes,10,11,13 leading to leukocyte destruction,11,14 skin abscesses, and necrotizing pneumonitis.10,11

The objective of the present study was to determine the extent of MRSA infections among the local population in Northeastern Ohio. We analyzed the rate of MRSA occurrence among the patients seeking medical attention at the Ashtabula County Medical Center (ACMC; Ashtabula, OH) during the 2006–2007 period. ACMC is a private, nonprofit hospital providing inpatient and outpatient services for northeastern Ohio. This 241-bed medical center is the largest in Ashtabula County and has been serving an estimated population of 102,70315 for more than a century.

Materials and Methods

A survey was performed on all cases of Staphylococcus infections diagnosed by the ACMC laboratory from February 2006 to December 2007. A total of 1,612 cases were included in this study after retrospective chart review. This study was reviewed and approved by Kent State University (Ashtabula, OH) Institutional Review Board (IRB 08-355).

The diagnosis of MRSA vs methicillin-susceptible S aureus infection was determined based on clinical laboratory culture findings (antibiotic resistance screening) performed by the microbiology laboratory at ACMC. Antibiotic resistance results were interpreted in accordance with the Clinical and Laboratory Standards Institute.16 Isolates were routinely tested on ampicillin, amoxicillin clavulanate, ampicillin sulbactam, azithromycin, clindamycin, cephalothin, cefazolin, chloramphenicol, ciprofloxacin, cefoxitin, ceftriaxone, erythromycin, gentamicin, imipenem, levofloxacin, ofloxacin, oxacillin, penicillin G, rifampicin, sulfamethoxazole-trimethoprim, tetracycline, and vancomycin and for β-lactamases. The MicroScan WalkAway 96 Plus system (Siemens, New York, NY) served as the primary reference method for bacterial identification and antibiotic screening tests. Oxacillin-resistant S aureus isolates were defined as MRSA.

The cases of MRSA infections were classified on the basis of patient age, sex, and the sources of patient origin (inpatient, outpatient, physician office, and nursing home). Data were analyzed by using SAS 9.13 (SAS Institute, Cary, NC). Means of the different treatments were separated using the Waller-Duncan k-ratio t test after it was determined that there was a significant (P < .05) treatment effect using the general linear model procedure.

Results

A total of 1,612 staphylococcal infections were diagnosed in the ACMC laboratory from February 2006 to December 2007. The year 2007 showed a steady increase in MRSA infections Figure 1 . The monthly incidence of MRSA significantly increased from 30 cases per month on average in 2006 (for a total of 342) to 50.4 in 2007 (for a total of 605). When comparing data from 2006 with data from 2007, the monthly MRSA incidence increased across all population age groups Figure 2 . It was particularly significant among people 6 to 25 years old, middle-aged people (45–50 years old), and elderly people (86–90 years old). The MRSA incidence was not sex-linked; both males and females were equally vulnerable to the infection (data not shown). Figure 3 represents the monthly MRSA incidence related to patient origin (inpatient, outpatient, physician office, and nursing home). The MRSA increase in 2007 was not restricted to one particular patient population with increases of 58% among inpatients, 43% among outpatients, and 183% among nursing home residents.

Staphylococcal isolates were routinely tested and grouped based on their sensitivity or resistance to 22 different antibiotics and for β-lactamases. MRSA antibiotic resistance varied slightly between 2006 and 2007 in the studied population. Significant decreases in resistance were observed in 2007 for clindamycin, chloramphenicol, ciprofloxacin, levofloxacin, ofloxacin, and tetracycline Figure 4 . Antibiotic resistance was not affected by patient sex with the exception of resistance to ciprofloxacin, which was significantly higher in females than in males, with a frequency of 0.68 compared with 0.60, respectively. These differences were particularly remarkable for 26- to 30-year-old women, who were found to have more resistant strains to ciprofloxacin, levofloxacin, and ofloxacin than their male counterparts. The outpatient cases were correlated with the lowest levels of clindamycin, chloramphenicol, ciprofloxacin, levofloxacin, ofloxacin, rifampicin, azithromycin, erythromycin, and gentamicin resistance. The most resistant MRSA strains were found among nursing home residents Figure 5 .

MRSA infections were classified according to their profiles of antibiotic resistance. A total of 75 profiles were obtained, with 9 accounting for more than 88.7% of cases in 2007. The 9 major antibiotic profiles varied in their resistance and sensitivity to one or more of the following antibiotics: azithromycin, clindamycin, chloramphenicol, ciprofloxacin, erythromycin, gentamicin, levofloxacin, ofloxacin, and tetracycline Table 1 .

The distribution and incidence of each profile of antibiotic resistance varied with patient source Figure 6 and across all age groups. Profiles pa26, pa30, pa62, and pa80 were predominantly found among younger populations and outpatients, while pa127, pa152, and pa163 were more common in older populations and were evenly distributed among inpatients, outpatients, and nursing home residents Figure 7 . Profiles pa135 and pa97 were common among elderly people and were the most abundant profiles among inpatients and nursing home residents (Figure 7).

Figure 1

Total number of methicillin-resistant Staphylococcus aureus (MRSA) cases by month among patients seeking medical attention during the 2006–2007 period at Ashtabula County Medical Center and its affiliates (Ashtabula, OH).

Figure 2

Monthly incidence of methicillin-resistant Staphylococcus aureus cases by age among patients seeking medical attention during the 2006–2007 period at Ashtabula County Medical Center and its affiliates (Ashtabula, OH). Means of the different treatments were separated by using the Waller-Duncan k-ratio t test after it was determined that there was a significant (P < .05) treatment effect using the general linear model procedure. * Significant differences between 2006 and 2007 monthly incidences (P < .05).

Figure 3

Distribution of monthly total number of methicillin-resistant Staphylococcus aureus (MRSA) cases by patient sources in 2006 and 2007 at Ashtabula County Medical Center and its affiliates (Ashtabula, OH).

Figure 4

Comparison of antibiotic resistance frequency of methicillin-resistant Staphylococcus aureus cases in 2006 and 2007 among patients seeking medical attention at Ashtabula County Medical Center and its affiliates (Ashtabula, OH). AMO, amoxicillin clavulanate; AZI, azithromycin; CD, clindamycin; CHLO, chloramphenicol; CIPRO, ciprofloxacin; ERY, erythromycin; GM, gentamicin; IMIP, imipenem; LEVO, levofloxacin; OFLOX, ofloxacin; RIF, rifampicin; SXT, sulfamethoxazole-trimethoprim; TE, tetracycline; VA, vancomycin. Means of the different treatments were separated by using the Waller-Duncan k-ratio t test after it was determined that there was a significant (P < .05) treatment effect using the general linear model procedure. *Significant differences between 2006 and 2007 antibiotic resistance (P < .05).

Figure 5

Influence of patient sources on antibiotic resistance frequency among patients seeking medical attention in 2007 at Ashtabula County Medical Center and its affiliates (Ashtabula, OH). AZI, azithromycin; CD, clindamycin; CHLO, chloramphenicol; CIPRO, ciprofloxacin; ERY, erythromycin; GM, gentamicin; LEVO, levofloxacin; OFLOX, ofloxacin; RIF, rifampicin. Means with the same letter are not significantly different (P < .05) for the same antibiotic.

View this table:
Table 1

Discussion

The northeastern Ohio area has experienced a steady increase in MRSA infections during the 2006–2007 period (Figure 1). In 2007, the ACMC identified and reported 605 MRSA infections for an estimated population of 102,703,15 a 77% increase compared with 2006. The observed MRSA rates were higher than those previously published by the Centers for Disease Control and Prevention, which reported more than 94,000 Americans (approximately 31.5 MRSA cases per 100,000 patients) became infected with MRSA in 2005.17 Furthermore, variations in MRSA antibiotic resistance between 2006 and 2007 with the decrease for clindamycin, chloramphenicol, ciprofloxacin, levofloxacin, ofloxacin, and tetracycline (Figure 4) suggest a fast and incessant change in MRSA epidemiology and support past observations, which indicate extreme heterogeneity of the genetic background in MRSA13 and suggest that any strain of methicillin-susceptible S aureus has the potential of becoming MRSA.2

Figure 6

Influence of patient sources on the monthly incidence for the 9 most common profiles of antibiotic resistance among patients seeking medical attention in 2007 at Ashtabula County Medical Center and its affiliates (Ashtabula, OH). Means of the different treatments were separated by using the Waller-Duncan k-ratio t test after it was determined that there was a significant (P < .05) treatment effect using the general linear model procedure. Means with the same letter are not significantly different (P < .05) for the same profile of antibiotic resistance.

In northeastern Ohio, MRSA has become the predominant isolate for S aureus infections, representing 61.3% of all staphylococcal infections in 2007 compared with 54.7% in 2006. Previous reports have indicated that up to 70% of all S aureus infections are found among people without apparent risk factors.18,19 These infections are commonly referred to as community-acquired MRSA.20 CA-MRSA infections are endemic and regarded as a major public health care concern worldwide.12,13,21,22 CA-MRSA demonstrates resistance to penicillin and methicillin but remains susceptible to non–β-lactam antimicrobials, such as clindamycin, sulfamethoxazole-trimethoprim, and tetracyclines.14 Our results confirmed such trends and indicated lower resistances to clindamycin, chloramphenicol, ciprofloxacin, levofloxacin, ofloxacin, rifampicin, azithromycin, erythromycin, and gentamicin compared with HA-MRSA isolates from inpatients and nursing home residents (Figure 5). General health decline with age, higher antibiotic regimens, lack of proper education, and less frequent visits to physicians are influential factors in the rapid evolution of antibiotic-resistant species.

The analysis of antibiotic resistance revealed that 88.7% of the infections were caused by strains belonging to only 9 profiles of antibiotic resistance (Table 1). Even though their respective frequency varied drastically, 7 of the 9 major profiles (pa127, pa135, pa152, pa163, pa30, pa80, and pa97) were commonly found between CA-MRSA (outpatients) and HA-MRSA (inpatients and nursing home residents) isolates. The other 2 profiles (pa26 and pa62) were predominantly found among outpatients and inpatients but not in nursing home residents (Figure 6). These results suggest that the traditional distinction between CA-MRSA and HA-MRSA based on antibiotic resistance (eg, current classification of CA-MRSA based on sensitivity to clindamycin) is a difficult task and increasingly ambiguous.23 Others have suggested a need to distinguish CA-MRSA from HA-MRSA while arguing that most nosocomial colonizations remain undetected and lead to infection many months after hospital discharge that are often erroneously referred to as CA-MRSA.2 They also point out that the current spread of drug resistance has made CA-MRSA strains evolutionarily more successful in replacing other MRSA strains in the hospital.

In this report, CA-MRSA infections reached 389.5 cases per 100,000. Such a rate is higher than previously reported by Fridkin et al,12 who described much lower CA-MRSA incidences in Atlanta (25.7 cases per 100,000) and Baltimore (18.0 cases per 100,000). Furthermore Crum et al24 also reported a lower rate of 155 cases per 100,000 in the San Diego military community. Such high rates of MRSA prevalence in northeast Ohio may be related to the poor socioeconomic situation characterized by lower median income ($37,628 compared with the US national average of $48,373), higher numbers of people living below poverty levels (16.7% vs the US national average of 13.3%), and a poorly educated population, with only 12.3% of the local population possessing a bachelor’s or higher degree compared with a national average of 27%.15 Similar socioeconomic conditions have previously been linked to MRSA outbreaks in African Americans,12 Native Americans,25 and homeless people.14,26

Figure 7

Monthly incidence for the 9 most prevalent methicillin-resistant Staphylococcus aureus profiles for antibiotic resistance by patient age in 2007 among patients seeking medical attention at Ashtabula County Medical Center and its affiliates (Ashtabula, OH).

In northeast Ohio, the MRSA increase was visible among all ages, especially among young people (6–25 years old), middle-aged people (45–50 years old), and elderly people (86–90 years old) (Figure 2). The uneven age distribution of the major antibiotic-resistance profiles (Figure 7) in this region suggests that each age group is more susceptible to only a few age-specific MRSA strains likely owing to a preponderance of transfers among people of the same age in schools, in the workplace, and/or in nursing homes. Differences between children and adults with CA-MRSA were previously reported.27 Children with CA-MRSA were more likely to be resistant to only β-lactams and sensitive to clindamycin. Similarly, in this study, strains with pa26, pa30, pa62, and pa80 profiles characterized by their sensitivity to clindamycin were also preferentially found among the younger populations. These results suggest that distinct CA-MRSA strains may colonize and infect children and adults. Similarly, David et al27 proposed that these MRSA differences may be linked to the following: (1) unique environmentally related risk factors for MRSA colonization in children, such as attendance at daycare centers, schools, and recreational facilities; (2) differences in children and adults as MRSA hosts; and (3) the possible presence of an MRSA reservoir that affects children and adults differently. Children may be more susceptible to particular CA-MRSA infections as a result of a different colonization of the skin or by undefined difference in host defense.

The current rate of MRSA infections and the presence of identical profiles of antibiotic resistance among isolates of HA-MRSA and CA-MRSA is of utmost concern because the increase of MRSA cases suggests that the current preventive measures are not successful and must be revisited. In 2003, Hamour et al28 reported that only 44% of surgical outpatients had heard of MRSA. In 2008, Trigg et al29 reported similar results. Similarly, Lugg and Ahmed30 also reported the overall level of knowledge of infection control, especially among pediatric nurses, to be “relatively inadequate,” with only 57% aware of MRSA transmission routes. Other studies highlight the lack of compliance with hand hygiene by hospital staff.3134 Even though hand washing is recognized as the crucial step to limit the spread of nosocomial diseases,35,36 hand-washing rates have been shown to be as low as 46% among nurses37 and 57% among physicians.38 In 2008, Trigg et al29 appropriately advocated a change in attitudes and behavior by health care workers to increase compliance in hand hygiene.

We report increased numbers of MRSA infection in northeastern Ohio. The current data suggest that CA-MRSA and HA-MRSA infections are rapidly spreading among the general population. Our findings emphasize the importance of education of the public and health care workers in MRSA epidemiology, infection control, and prevention measures as simple as hygienic hand washing, especially among school-aged people. In addition, data sheets and education focused on early identification of symptoms with prompt follow-up care will assist in the containment of MRSA outbreaks. This effort may require extensive research and curricular activities, as well as greater government and media involvement.

References

  1. 1.
  2. 2.
  3. 3.
  4. 4.
  5. 5.
  6. 6.
  7. 7.
  8. 8.
  9. 9.
  10. 10.
  11. 11.
  12. 12.
  13. 13.
  14. 14.
  15. 15.
  16. 16.
  17. 17.
  18. 18.
  19. 19.
  20. 20.
  21. 21.
  22. 22.
  23. 23.
  24. 24.
  25. 25.
  26. 26.
  27. 27.
  28. 28.
  29. 29.
  30. 30.
  31. 31.
  32. 32.
  33. 33.
  34. 34.
  35. 35.
  36. 36.
  37. 37.
  38. 38.
View Abstract