Knowledge of different risks for infection will improve control measures.
Countries such as Sweden that have a low prevalence of methicillin-resistant
Global transmission of methicillin-resistant
The primary purpose of our study was to use validated data from the surveillance system in Sweden to analyze the risk for MRSA among Swedish residents traveling abroad, internationally adopted children, and immigrants. A secondary purpose was to determine whether different types of MRSA were acquired in different countries or regions.
The study was reviewed and approved by the Regional Ethics Approval Board in Stockholm (Protocol 2005/4:10). MRSA cases (infections as well as carriage) are notified in parallel to the Swedish Institute for Infectious Disease Control (SMI) by the doctor caring for the patient and by the bacteriological laboratory having isolated the MRSA strain, using a unique personal identification number issued to all Swedish residents and used in all contacts with the health care system. At SMI, a case record is created after the arrival of the first notification. Any subsequent notifications are merged with the initial case record. After completion of the epidemiologic investigation and contact tracing around each MRSA case, the epidemiologic notification form data are validated by SMI with input from MRSA contact persons, who are public health representatives involved in control efforts locally in the respective counties (
For additional analysis, the reported cases of MRSA were divided into the following categories: residents of Sweden traveling abroad for recreational purposes, residents of Sweden traveling abroad because of work or studies, foreign residents traveling to Sweden for a temporary visit, immigrants, internationally adopted children, or Swedish citizens returning home after having lived abroad for >1 year. The risk for MRSA in travelers, immigrants, and adopted children was also evaluated by including and excluding reported cases found through public health-initiated case-finding activities and secondary cases in transmission chains.
Travel data from the commercial Swedish Tourist and Travel Database (TDB) were used as a denominator when analyzing the risk for being reported as having MRSA in travelers from Sweden. The TDB is based on monthly interviews with 2,000 randomly selected residents of Sweden. We used the TDB variables age group, sex, purpose of travel (leisure or work), main destination, and time of travel. TDB for 2000–2003 and interviews of 9,213 persons with a history of travel abroad were used. Information in the TDB was weighted and extrapolated to estimate the total number of travelers from Sweden and to derive a total of 45,855,000 travel episodes (
Denominator data on the yearly number of immigrants to Sweden were obtained from Statistics Sweden (
Isolates from all persons with new cases of MRSA were sent to SMI, where laboratory diagnosis of MRSA was confirmed by using PCR for the
Stata 8.2 software (StataCorp LP, College Station, TX, USA) was used for all statistical analyses, and a 95% level of significance was applied. Sex, age group, purpose of travel, and destination were used as explanatory variables in multivariable analysis of travelers with a diagnosis of MRSA and its reporting as an outcome. Generalized estimating equations with independent correlation and robust standard errors were used to enable clustering of data in the adjusted model that included all travelers <75 years of age.
During 2000–2003, a total of 1,733 cases of MRSA were reported in Sweden, 444 of which were considered to have been acquired abroad. Among these imported cases, 292 (65.8%) were in residents of Sweden who traveled abroad; 31 (7.0%) had traveled for work reasons or studies. Fifty-six (12.6%) of the cases were in newly arrived immigrants to Sweden, 40 (9.0%) in internationally adopted children from non-Nordic countries, 30 (6.8%) in foreign residents visiting Sweden, 20 (4.5%) in citizens of Sweden returning home after having lived abroad for >1 year, and 6 (1.4%) in persons who could not be grouped. Of the imported MRSA cases, 246 (55.4%) were HA and 146 (32.9%) were CA; 190 (42.8%) were in persons with MRSA disease.
Of the 292 residents of Sweden who traveled abroad, 267 met the age criteria and were included in this analysis. Most persons with MRSA had traveled to Thailand (n = 33), the United Kingdom (n = 24), Greece (n = 22), the former Yugoslavia (n = 20), Lebanon (n = 16), the United States (n = 14), Cyprus (n = 12), Spain (n = 12), Turkey (n = 9), and Syria (n = 8). The overall risk for being reported as having MRSA was 5.8 cases/1,000,000 travelers (95% confidence interval [CI] 5.2–6.6). The crude risk for travelers to specific regions ranged from 0.1 (95% CI 0.01–0. 4) per 1,000,000 travelers to Nordic countries to 59.4 (95% CI 44.5–79.3) per 1,000,000 travelers to North Africa and the Middle East (
| Variable | Estimated no. travelers | No. with MRSA infection (no. with MRSA disease) | Crude risk/1 million travelers (95% CI) | % Community-acquired cases | Adjusted OR (95% CI) |
|---|---|---|---|---|---|
| Sex | |||||
| F | 25,219,000 | 109 (62) | 4.3 (3.6–5.2) | 42.2 | Reference |
| M | 20,634,000 | 158 (71) | 7.7 (6.6–8.9) | 27.2 | 1.5 (1.2–2.0) |
| Age group, y | |||||
| 0–14 | 6,497,000 | 30 (24) | 4.6 (3.2–6.6) | 83.3 | Reference |
| 15–29 | 8,657,000 | 72 (36) | 8.3 (6.6–10) | 31.9 | 1.0 (0.6–1.5) |
| 30–44 | 13,234,000 | 49 (26) | 3.7 (2.8–4.9) | 44.9 | 0.8 (0.5–1.3) |
| 45–59 | 12,342,000 | 62 (29) | 5.0 (3.9–6.4) | 22.6 | 0.8 (0.5–1.2) |
| 60–74 | 5,127,000 | 54 (18) | 11 (8.1–13.8) | 9.3 | 1.2 (0.7–1.9) |
| Purpose of travel | |||||
| Leisure | 36,323,000 | 237 (123) | 6.5 (5.7–7.4) | 34.2 | Reference |
| Work | 9,532,000 | 30 (10) | 3.1 (2.2–4.5) | 26.7 | 2.4 (1.5–3.8) |
| Region of origin† | |||||
| Nordic | 15,962,000 | 1 (0) | 0.1 (0.01–0.4) | 0.0 | 0.1 (0.01–0.6) |
| Western Europe | 7,614,000 | 7 (3) | 0.9 (0.4–1.9) | 14.3 | Reference |
| Southern Europe | 7,601,000 | 18 (5) | 2.4 (1.5–3.8) | 0.0 | 2.4 (1.0–5.8) |
| Central and Eastern Europe | 2,885,000 | 7 (5) | 2.4 (1.2–5.1) | 28.6 | 2.8 (1.0–8.1) |
| UK and Ireland | 2,815,000 | 26 (11) | 9.2 (6.3–13.6) | 7.7 | 10.3 (4.4–24..0) |
| North America | 1,627,000 | 17 (4) | 10.4 (6.5–16.8) | 35.3 | 10.6 (4.2–26.7) |
| Northeastern Mediterranean | 4,317,000 | 63 (30) | 14.6 (11.4–18.7) | 38.1 | 15.8 (7.0–35.6) |
| South America | 152,000 | 6 (5) | 39.5 (17.7–87.9) | 33.3 | 31.2 (10.0–97.6) |
| East Asia | 1,622,000 | 54 (27) | 33.3 (25.5–43.5) | 27.8 | 36.5 (16.2–82.0) |
| Oceania and Pacific Islands | 250,000 | 11 (5) | 44.0 (24.4–79.5) | 36.4 | 43.0 (15.5–119.4) |
| Sub-Saharan Africa | 232,000 | 11 (7) | 47.4 (26.3–85.6) | 54.5 | 46.3 (17.3–123.6) |
| North Africa and Middle East | 774,000 | 46 (31) | 59.4 (44.5–79.3) | 58.7 | 59.0 (25.1–138.9) |
| Total | 45,855,000 | 267 (133) | 5.8 (5.2–6.6) | 33.3 |
*MRSA, methicillin-resistant
The adjusted OR for having MRSA was 1.5× higher among male participants (95% CI 1.2–2.0) than female participants (
Percentages of CA-MRSA for the respective regions, correlated linearly with adjusted ORs (r = 0.81, p = 0.001). Among age groups, the proportion of cases of CA-MRSA was highest in persons 0–14 years of age (83.3%), lowest in persons 60–74 years of age (9.3%), and intermediate for other age groups.
A total of 56 persons who had recently arrived in Sweden as immigrants had cases of MRSA (
| Country of origin | No. immigrants† | No. with MRSA acquisition (no. with MRSA disease) | Risk/100,000 immigrants (95% CI) |
|---|---|---|---|
| Malta | 21 | 1 (0) | 4,761.9 (120.5–23,816.0) |
| Kazakhstan | 933 | 4 (2) | 428.7 (116.9–1,094.0) |
| South Africa | 556 | 2 (1) | 359.7 (43.6–1,293.3) |
| Sudan | 360 | 1 (1) | 277.8 (7.0–1,537.9) |
| Italy | 1,382 | 2 (1) | 144.7 (17.5–521.8) |
| Ecuador | 995 | 1 (1) | 100.5 (2.5–558.6) |
| Lebanon | 2,100 | 2 (0) | 95.2 (11.5–343.6) |
| Mongolia | 1,055 | 1 (1) | 94.8 (2.4–527.0) |
| Japan | 1,274 | 1 (0) | 78.5 (2.0–436.6) |
| The Philippines | 1,335 | 1 (1) | 74.9 (1.9–416.6) |
| Afghanistan | 6,166 | 4 (3) | 64.9 (17.7–166.0) |
| United States | 4,094 | 2 (0) | 48.9 (5.9–176.4) |
| Former Yugoslavia | 45,587 | 20 (10) | 43.8 (26.8–67.8) |
| Germany | 6,564 | 2 (0) | 30.5 (3.7–110.0) |
| Poland | 3,658 | 1 (0) | 27.3 (0.7–152.2) |
| Iran | 7,856 | 2 (1) | 25.5 (3.1–91.9) |
| Thailand | 4,883 | 1 (0) | 20.5 (0.5–114.0) |
| United Kingdom | 5,306 | 1 (0) | 18.9 (0.47.7–105.0) |
| Turkey | 5,568 | 1 (1) | 18.0 (0.5–100.0) |
| Russia | 8,254 | 1 (0) | 12.1 (0.3–67.5) |
| Somalia | 8,546 | 1 (1) | 11.7 (0.3–65.2) |
| Iraq | 43,730 | 4 (3) | 9.1 (2.5–23.4) |
| Other countries | 191,302 | 0 | – |
| Total | 351,525 | 56 (27) | 15.9 (12.0–20.7) |
*MRSA, methicillin-resistant
In 2000–2003, a total of 4,169 children were adopted from non-Nordic countries. Forty adopted children from 12 countries were reported as having cases of MRSA shortly after their arrival in Sweden, i.e., 9.6 (95% CI 6.9–13.0) cases per 1,000 adoptions (
| Country | No. adoptions | No. with MRSA acquisition (no. with MRSA disease) | Risk/1,000 adoptions (95% CI) |
|---|---|---|---|
| The Philippines | 27 | 2 (0) | 74.1 (9.1–242.8) |
| South Korea | 467 | 14 (0) | 30.0 (16.5–49.8) |
| Bulgaria | 91 | 2 (1) | 22.0 (2.7–77.1) |
| Belarus | 174 | 3 (1) | 17.2 (3.6–49.6) |
| Russia | 263 | 4 (0) | 15.2 (4.2–38.5) |
| Ethiopia | 71 | 1 (1) | 14.1 (0.4–76.0) |
| Ukraine | 74 | 1 (0) | 13.5 (0.3–73.0) |
| People’s Republic of China | 1,074 | 7 (3) | 6.5 (2.6–13.4) |
| Colombia | 460 | 3 (0) | 6.5 (1.3–18.9) |
| South Africa | 154 | 1 (0) | 6.5 (0.16–35.6) |
| India | 243 | 1 (0) | 4.1 (0.1–22.7) |
| Vietnam | 328 | 1 (0) | 3.0 (0.1–16.8) |
| Other countries | 743 | 0 | – |
| Total | 4,169 | 40 (6) | 9.6 (6.9–13.0) |
*MRSA, methicillin-resistant
STs inferred from PFGE results and region of acquisition for 414 MRSA cases (excluding secondary cases and cases with STs seen in <5 cases) are shown in the
We have estimated risks for MRSA among travelers returning from specific geographic regions. Other studies have reported individual cases of MRSA diagnosed in connection with travel (
The overall prevalence and transmission rate of MRSA within a country or region is just one of several factors that can influence the risk for MRSA acquisition by travelers to that country or region. This risk will also depend on type of exposure and duration of stay. For example, risk for MRSA acquisition will vary, depending on whether the person had received healthcare or had only community contacts, whether he or she stayed in a hotel at a holiday resort for a week, stayed with relatives for 3 months, or just stayed overnight on a business trip. In Europe, we observed a relatively high risk for MRSA acquisition in travelers to the United Kingdom, Ireland, and southern Europe, which is consistent with the high prevalence of MRSA reported for these regions (
The risk for immigrants and adopted children of acquiring MRSA may not be representative of the overall risk in the general population in their respective countries of origin. These 2 populations may have spent time in institutional settings (e.g., orphanages, refugee camps, or hospitals) in which the risk for MRSA exposure may be different from that in the community in general. In addition, analysis of MRSA risk among newly adopted children and immigrants was based on small numbers of persons, which resulted in wide CIs of the estimated risks. Despite this uncertainty, agreement was seen between the estimated risk for MRSA acquisition among returning travelers, immigrants, and adopted children. Eight of 12 countries from which the adopted children with MRSA originated and 14 of the 22 countries from which immigrant cases originated belonged to the 6 regions with highest risk for MRSA among travelers (northeastern Mediterranean, South America, East Asia, Oceania and Pacific islands, sub-Saharan Africa, and North Africa and the Middle East).
Measuring the risk for MRSA in travelers, adopted children, and immigrants involved analyzing 3 different groups related to specified countries and regions. Because of the large degree of agreement between the 3 groups, results obtained may reflect not only risks for MRSA in these 3 populations, but also an overall comparatively higher risk for MRSA in some regions than in others.
The study was based on persons (carriers and those with clinical disease) with reported cases of MRSA in Sweden during 2000–2003. Only minor changes, which did not affect our primary findings, were seen when carrier cases were excluded from the travel analysis. Approximately 50% of MRSA cases among immigrants, but only 15% (6/40) of adopted children, had MRSA disease. Twelve of the 13 countries from which immigrants originated belonged to the 6 regions with highest risk for MRSA among travelers. For adopted children, the numbers of countries involved and cases decreased when carriers were excluded. However, 2 of 4 countries (4 of 6 cases) still belonged to the same 6 regions. Results for these 3 populations with acquired MRSA are consistent even when carriers were excluded from the analysis.
One strength of our study is that all regions/countries were investigated by using the same surveillance system, thus avoiding problems that might arise when data for different countries are compiled from different sources. Because the travel analysis was based on residents of Sweden who traveled to other countries and results were adjusted for sex and age, the main conclusions should also be valid for other western countries. Possible biases related to MRSA cases reported in Sweden during 2000–2003 and use of the TDB have been evaluated (
Most persons infected with MRSA had HA-MRSA; only 33% had CA-MRSA. However, CA-MRSA showed a strong correlation with regions with a high risk for MRSA among travelers. This finding might be caused by a higher propensity among clinicians to sample patients with a history of activity (e.g., backpacking) under less than optimal sanitary conditions or travel to exotic regions. The 5 regions with the highest OR of acquiring MRSA in adjusted analysis were outside Europe.
Geographic distribution of MRSA STs was consistent with that in studies of other regions. ST22 and ST36 are well documented in the healthcare system in the United Kingdom (
In addition to showing an association between specific STs and regions, we also identified the transmission setting (healthcare or community) in which the isolate was acquired. We observed that most STs among imported cases of MRSA were associated with either HA-MRSA or CA-MRSA. ST30 and ST80 were strongly associated with CA-MRSA. ST72 was identified only among 8 adopted children from South Korea. However, information for the orphanages was not available. Thus, the possibility that 8 children could have been part of the same local transmission chain could not be ruled out. However, ST72 has recently been reported from several areas of South Korea among children and as a community-associated sequence type (
Several limitations of our study involve factors relevant to MRSA acquisition (length of stay abroad, contacts with institutions with a higher probability of MRSA transmission such as healthcare settings, orphanages, or refugee camps) that were not measured. In addition, there may have been inconsistencies in how MRSA cases were selected in the surveillance system. In some counties in Sweden, MRSA screening of adopted children is conducted; in other counties, it is not practiced. Thus, underdiagnosis of MRSA carriage among adopted children was likely. No similar screening recommendations are known for newly arrived refugees or immigrants.
In countries with a low prevalence of MRSA, a larger proportion of cases are imported than in countries with a high prevalence of MRSA. The risk for additional domestic transmission indicates a greater need to focus public health measures toward these imported cases. We observed differences in risk for MRSA among travelers returning from different regions, adopted children, and immigrants. Risk estimates for MRSA measured in these 3 groups showed a consistent pattern; some regions showed a higher risk for acquiring MRSA. Although most imported cases of MRSA were HA-MRSA, community acquisition showed a correlation with regions that have a high risk for MRSA among travelers. Knowledge of these differences in risk for MRSA will improve control measures and decrease domestic transmission.
Cross-tabulation of region of acquisition and sequence type for cases of methicillin-resistant Staphylococcus aureus acquired abroad and reported in Sweden, 2000-2003*
We thank Ann Lindmark and Maj Ringman for excellent laboratory work and Sharon Kühlmann-Berenzen for valuable statistical advice.
This study was supported by the Swedish Institute for Infectious Disease Control.
Dr Stenhem is a clinical specialist in infectious diseases in the Department of Epidemiology, Swedish Institute for Infectious Disease Control in Solna, Sweden. His research interest is infectious disease epidemiology, particularly disease surveillance and MRSA epidemiology.