Elderly people who reside in nursing homes (NHs) for long-term care represent an important reservoir for Staphylococcus aureus, and residence in a NH is a well-established risk factor for S. aureus carriage and infection.Reference Yoshikawa and Bradley 1 A new livestock-associated MRSA clone (ST398), which is mostly linked to pig farms and people in contact with them but is also found in other animals, is spreading in many countries.Reference Becker, Ballhausen, Kahl and Köck 2 There have been few reports of transmission of MRSA ST398 in NH healthcare settings.Reference Verkade, Bosch, Hendriks and Kluytmans 3
Previous studies have established that tetracycline resistance (TetR) is a good marker for rapid identification of ST398 strains.Reference Lozano, Rezusta and Gómez 4 The county of Osona (Barcelona, Catalonia, Spain) is an area with a high density of pig farms, and a high nasal carriage rate of MRSA ST398 (all TetR) has been recently detected in pig-farm workers and farm animals in the Osona region.Reference Reynaga, Navarro and Vilamala 5 The aim of our study was to determine the prevalences of MRSA and MRSA-ST398 nasal carriage in NH residents in the Osona region.
MATERIAL AND METHODS
A prospective study was performed during January–July 2015 in 6 NHs in the county of Osona (Barcelona, Spain). Nursing homes 1, 2 and 3 are located in in urban areas and NHs 4, 5, and 6 are located in rural areas.
A questionnaire with the epidemiological details of each resident was completed during a personal interview with them or their family or legal representative. Residents who were colonized with MRSA were divided into 2 groups depending on whether the strains were tetracycline sensitive or resistant (TetS or TetR, respectively), and these groups were compared. Permission for the study was obtained from the Hospital Universitari de Vic (HUV) Ethics Committee.
Sample Processing and MRSA Detection and Characterization
Nasal samples were processed for culture and bacterial identification in the Microbiology Department of HUV. One strain per person was studied. Detailed microbiological methods can be found in the Supplementary material. All MRSA-TetR strains were analyzed using multilocus sequence typing (MLST) and spa typing.Reference Lozano, Aspiroz and Charlez 6 , Reference Harmsen, Claus and Witte 7
Statistical Analysis
Statistical analysis was performed using SPSS software version 23.0 (IBM, Armonk, NY).
Categorical variables were expressed as frequency (%) and continuous variables as mean ± standard deviation (SD). The prevalence of positive results in MRSA was estimated with a 95% confidence interval (CI). Statistical significance for intergroup differences was assessed by the Pearson χ2 or the Fisher exact test for categorical variables and the Student t test for continuous variables. A P value < 0.05 was considered statistically significant.
RESULTS
Of the 204 NH residents analyzed in this study, 32 were MRSA carriers (15.7%; 95% CI, 10.7%–20.7%). Of the 32 MRSA-positive residents, 8 (25%; 95% CI, 10.0%–40.0%) carried MRSA-TetR. Of these, 5 (15.6%; 95% CI, 3.0–28.0) carried MRSA-ST398.
Table 1 shows the epidemiological differences between residents colonized versus not colonized with MRSA and those colonized with MRSA-TetS versus those with MRSA-TetR (Table 1). Of the MRSA-TetS–positive residents, 87% were identified in urban NHs and 55% were identified in rural NHs (P=.023). A total of 26 (12.7%) residents had had contact with relatives of farm workers in the previous 12 months, all of them working on pig farms and none on cow or chicken farms. Of these residents, 7 (26.9%) were colonized with MRSA and 4 (57.1%) were colonized with MRSA-TetR-ST398 (P=.026). Furthermore, only 2 residents had direct contact with pig farms, and both were positive for MRSA-ST398 (P=.018).
TABLE 1 Epidemiological Differences for the Residents Colonized With MRSA Versus Not Colonized and MRSA-TetR Versus MRSA-TetS in the 6 Nursing Homes Studied.
NOTE. MRSA, methicillin-resistant Staphyloccus aureus; TetR tetracycline resistant; TetS tetracycline susceptible; NH, nursing home; BI, Barthel index; CI, cognitive impairment.
a Bold P values indicate statistical significance.
b Comorbidity includes cerebrovascular disease, chronic cardiovascular disease, liver disease, chronic lung disease, chronic renal disease, auto-immune disease, neurological comorbidity, diabetes, and malignancy.
A rural NH showed the highest prevalence of MRSA-TetR (3 of 3 residents, 100%; 2 carried ST398), and an urban NH had the lowest prevalence (1 of 13 residents, 7.7%; typed as ST398).
Table 2 shows the characteristics for residents colonized with MRSA TetR as well as the antibiotic resistance phenotype of the isolates. Of 8 isolates, 5 were typed as ST398-t011, although the lineages ST1, ST9, and ST146 were also detected.
TABLE 2 Molecular Typing and Resistance Phenotypes for the 8 MRSA-TetR Strains Recovered From the Residents of the 6 Nursing Homes Analyzed
NOTE. MRSA, methicillin-resistant Staphylococcus aureus; TetR tetracycline resistant; CC, Clonal Complex; ST, Sequence Type; NH, nursing home; TET, tetracycline; ERY, erythromycin; CLI, clindamycin; GEN, gentamicin; TOB, tobramycin; CIP, ciprofloxacin; SXT, trimethoprim-sulfamethoxazole; LEV, levofloxacin.
a Nursing homes 1, 2, and 3 are in urban areas and nursing homes 4, 5, and 6 are in rural areas.
b In the previous 12 months.
DISCUSSION
In our study, the prevalence of MRSA in NHs (15.7%) was similar to that described in other studies carried out in Spain.Reference Manzur, Gavalda and Ruiz De Gopegui 8 The prevalence rate of MRSA-ST398 detected in our study in NHs in the region of Osona is significant (15.6% among MRSA-colonized residents and 2.5% of all NH residents). This is the first study to describe the presence of MRSA-ST398 in NHs in Catalonia and in Spain.
The NH with the highest prevalence of MRSA-TetR was in a rural area, and the NH with the lowest prevalence was in an urban area. This difference may be due to the rural character of NH-6, which generally admits people straight from their homes, whereas urban NH-3 regularly admits patients referred from hospital.
In our study, 4 of the 5 residents colonized with MRSA-ST398 had direct or indirect contact with pig farms. This finding suggests that acquisition of MRSA-ST398 could be from relatives and not the nursing home itself. It is well known that nursing homes are a reservoir for MRSA, and they could also be reservoir for MRSA-ST398. Two residents in the same NH were identified as carriers of MRSA-ST398 with the same spa-type (t011) and a similar though not identical resistance phenotype (Table 2). Both had contact with relatives of farm workers but not directly with the farms. We ascertained that the residents and the farm workers’ relatives were not related and that they only had occasional contact at mealtimes. Even though this could have constituted an outbreak, it was not possible to confirm this hypothesis because neither the relatives nor the health workers were screened.
The first outbreak of MRSA-ST398 in a NH was described in the Netherlands, in which 1 of 7 residents and 2 of 4 healthcare workers were MRSA-ST398 carriers. They had contact either with pig farms or with relatives of pig-farm workers.Reference Verkade, Bosch, Hendriks and Kluytmans 3 Another study performed in China detected MRSA-ST398 carriage in 21 of 491 residents from 7 NHs, although no information about potential contact with farmers or the type of transmission was included.Reference Zhang, Gu and Zhao 9
The county of Osona has one of the highest pig densities in Spain.Reference Reynaga, Navarro and Vilamala 5 In a recent study in this same area of Osona, 57.8% of pig-farm workers were carriers of MRSA-ST398Reference Reynaga, Navarro and Vilamala 5 , and approximately 45% of patients diagnosed with MRSA in the hospital of this county in 2015 had the ST398 lineage.Reference Reynaga, Torres and Garcia-Nuñez 10 These data suggest that the MRSA-ST398 clone plays a significant role both in colonization and in infections in the population of the Osona region.
Although the current prevalence of MRSA-ST398 in our study is moderate compared to other MRSA lineages, the characteristics of the region (with a high density of pigs) suggest that MRSA-ST398 might have greater prevalence in the future. Consequently, surveillance should be maintained to track the development of MRSA-ST398.
The present study has several limitations. We only looked at residents in NHs and not at the relatives of the residents and healthcare NH workers, who might be a cause of MRSA-ST398 transmission. In addition, extra-nasal colonization was not assessed in our study. The MRSA-TetR carrier group vs the MRSA-TetS carrier group were analyzed, and the results must be interpreted with caution because these groups were too small to allow firm conclusions to be drawn.
In conclusion, the prevalence of MRSA-ST398 colonization in NHs in Osona county is 15.6% of MRSA carriers and 2.5% of the total of residents studied. The prevalence of MRSA in the NHs studied was similar to that found in previous studies. Nursing homes are a well-known reservoir for MRSA, and in the region where this study was conducted, they could also be a reservoir for MRSA-ST398.
ACKNOWLEDGMENTS
CIBER (Centro de Investigación biomédica en Red) de Enfermedades Respiratorias is an initiative of Spain’s health research institute, Instituto de Salud Carlos III. IGTP (Institut de Recerca Germans Trias i Pujol) is included in the CERCA (Centres de Recerca de Catalunya) programme/Genetalitat de Catalunya.
Financial support. No financial support was provided relevant to this article.
Potential conflicts of interest. All authors report no conflicts of interest relevant to this article.
SUPPLEMENTARY MATERIAL
To view supplementary material for this article, please visit https://doi.org/10.1017/ice.2017.244
