The Role of International Travel in the Spread of Methicillin-Resistant Staphylococcus aureus

Authors

  • Yvonne P. Zhou BSc(Hons),

    1. Department of Pharmacy, Singapore General Hospital, Singapore, Singapore
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  • Annelies Wilder-Smith MD, PhD,

    1. Lee Kong Chian School of Medicine, Nanyang Technological University, Singapore, Singapore
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  • Li-Yang Hsu MPH

    Corresponding author
    1. Department of Medicine, Yong Loo Lin School of Medicine, Singapore, Singapore
    • Corresponding Author: Li-Yang Hsu, MPH, Department of Medicine, Yong Loo Lin School of Medicine, 1E Kent Ridge Road, NUHS Tower Block Level 10, Singapore 119228, Singapore. E-mail: liyang_hsu@yahoo.com

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  • Part of this work was presented at the 13th Conference of the International Society of Travel Medicine at Maastricht, the Netherlands, May 19–23, 2013.

Abstract

Background

Increasing international travel has facilitated the transmission of various multidrug-resistant bacteria—including methicillin-resistant Staphylococcus aureus (MRSA)—across continents. Individuals may acquire MRSA from the community, healthcare facilities, or even from animal exposure. Skin contact with colonized individuals, fomites, or animals during an overseas trip may result in either asymptomatic colonization or subsequent clinically significant MRSA disease. MRSA strains that harbor the Panton-Valentine leucocidin toxin are particularly associated with community transmission and may potentially have enhanced virulence resulting in serious skin and soft tissue infections or even necrotizing pneumonia. More importantly, secondary transmission events upon return from traveling have been documented, leading to potentially detrimental outbreaks within the community or the healthcare setting. We sought to review the existing literature relating to the role of various aspects of travel in the spread of MRSA. Risk factors for acquiring MRSA during travel together with the need for targeted screening of high-risk individuals will also be explored.

Methods

Data for this article were identified via PubMed searches using a combination of search terms: “methicillin resistance,” “MRSA,” “livestock-associated MRSA,” “community-associated MRSA,” “travel,” and “outbreak.” The relevant articles were extensively perused to determine secondary sources of data.

Results and Conclusions

Our review of the current literature suggests that international travel plays a significant role in the transmission of MRSA, potentially contributing to the replacement of existing endemic MRSA with fitter and more transmissible strains. Therefore, selective and targeted screening of travelers with risk factors for MRSA colonization may be beneficial. Healthcare professionals and patients should be considered for screening if they were to return from endemic areas, with the former group decolonized before returning to patient care work, in order to reduce the transmission of MRSA to vulnerable patient populations.

Staphylococcus aureus is a common human commensal and opportunistic pathogen, and it is present in the nares of approximately 30% of healthy individuals.[1] Nasal carriage of S. aureus has been associated with subsequent mild to life-threatening infections, including skin and soft tissue infections (SSTIs), pneumonia, endocarditis, septic arthritis, and osteomyelitis.[2, 3] Methicillin-resistant S. aureus (MRSA) was first described in 1961, 2 years after the commercial introduction of methicillin.[4] Over the next few decades, MRSA became established in hospitals throughout America and Europe, and subsequently Asia.[5] The organism was thought to be confined to healthcare settings until the 1990s, when reports of MRSA infections in healthy patients with no recognizable healthcare-associated risk factors appeared. Community-associated MRSA (CA-MRSA) strains that were genetically distinct from their healthcare-associated counterparts (HA-MRSA) were found to be responsible for this increase in community infections.[6]

CA-MRSA is able to infect young healthy individuals, suggesting that it may be more virulent than HA-MRSA. The Panton-Valentine leukocidin (PVL), a pore-forming toxin encoded by two genes lukF-PV and lukS-PV, may contribute to its virulence.[4, 6, 7] PVL is known to cause tissue necrosis and lysis of leucocytes in vitro and is associated with deep-seated skin abscesses and necrotizing pneumonia.[4, 6] On the other hand, PVL has also been shown to possess immunomodulatory properties in a murine model.[8]

The vast majority of S. aureus become methicillin-resistant via acquisition of the mobile genetic element staphylococcal chromosomal cassette mec (SCCmec), which carries the mecA gene that encodes for a penicillin-binding protein with low affinity for most beta-lactam antibiotics (PBP 2a).[9] SCCmec can be transferred horizontally from MRSA to methicillin-sensitive S. aureus (MSSA) strains or even from methicillin-resistant coagulase-negative staphylococci to MSSA strains in the presence of antibiotics.[10, 11] Apart from the importation of SCCmec mobile genetic element, clonal spread—where the clones are defined by multilocus sequence types (STs)—is the other main mechanism for the global spread of MRSA.[12] Multilocus sequence typing (MLST) is a technique that assigns different STs to MRSA by comparing the alleles at various loci within housekeeping genes with those from a database, permitting the tracking of MRSA clonal spread across regions.[13]

A review paper that had addressed the pathogenesis of MRSA infection suggested direct skin-to-skin and skin-to-fomite contact with an MRSA-colonized individual or fomite, respectively, as important routes of transmission.[14] Among travelers, it has been speculated that a change in skin colonization could have resulted from reduced hygiene standards and increased sweating during traveling. The distribution of these pathogens from the colonized reservoirs such as nares, throat, axilla, and groins to areas where there is a breach to skin barrier (eg, micro-trauma as a consequence of insect bites, scratching, or minor wounds) in travelers may result in subsequent infections.[15, 16]

Globalization and increasing international travel has facilitated the transmission of various strains of multidrug-resistant bacteria across continents.[5, 17-20] Similarly, the spread of MRSA internationally has resulted in a global concern. The purpose of this paper is to review the spread of MRSA via different aspects of international travel and their significance, including their impact on healthcare-associated infections. Risk factors for acquiring MRSA during travel coupled with the need for targeted screening of high-risk individuals will also be explored.

Methods

We searched PubMed for published English language reports and reviews on MRSA and travel. Combinations of search terms were used to obtain potentially relevant articles: “methicillin resistance,” “MRSA,” “livestock-associated MRSA,” “community-associated MRSA,” “travel,” and “outbreak.” These articles were then reviewed, with their references crosschecked to obtain secondary sources of data.

Results and Discussion

A total of 1 cohort study,[21] 1 case-control study,[22] and 21 case reports and case series[18, 19, 23-42] with 254 individuals affected by imported MRSA were identified in this review. The cases described involved individuals who were either colonized or infected with MRSA and who had acquired it mostly from leisure traveling, medical tourism, medical repatriation, migration, or had recent contact with individuals colonized with MRSA. The imported cases of MRSA from the various endemic countries and the associated ST of MRSA are summarized in Table 1.

Table 1. Global spread of MRSA via international travel
ReferenceClinical presentationNo. of individualsCountry where the study was carried outCountry where MRSA was imported fromMLSTReport of occurrence at the travel destination/country of origin for immigrants
  1. MLST = Multilocus sequence typing; SSTIs = skin and soft tissue infections; MRSA = methicillin-resistant Staphylococcus aureus.
Denis and colleagues (2005)[23]Mostly SSTIs2BelgiumNorth AfricaST80ST80 has been reported in the Middle East[6, 21, 89] and North Africa, including Algeria[90]
1BelgiumEcuadorST8ST8 is prevalent in Latin America[47, 91]
Josseaume and colleagues (2013)[18]Colonization, infected prosthesis, bronchoalveolar lavage5FranceAlgeria, Spain, Morocco, Portugal, Thailand
Haenii and colleagues (2011)[24]Limb infection (a traveler transmitted the MRSA to a dog in France upon returning)1 (dog)FranceUnited StatesST8ST8 MRSA (USA300) is the dominant CA-MRSA strain in the United States[44-46]
Maier and colleagues (2005)[25]Cutaneous abscesses, necrotizing pneumonia, infected joint infections, and colonization12GermanyMiddle East, Pakistan, Greece, Italy, TurkeyST80ST80 has been reported in the Middle East,[6, 21, 89] and also among European countries, including Sweden,[21] Belgium,[23] Denmark,[85] and Greece[92]
5GermanyEngland, TurkeyST22ST22 has dominated the United Kingdom since the 1990s[93]
1GermanyThe PhilippinesST30ST30 is a common isolate in the Philippines[21, 53]
1GermanyUnited StatesST8ST8 MRSA (USA300) is the dominant CA-MRSA strain in the United States[44-46]
Zanger and colleagues (2012)[22]SSTIs (abscesses, furuncles, folliculitis, impetigo, ulcerative lesions, and cellulitis)2GermanyAustraliaST30ST30 is prevalent in the Oceania[4, 6, 21, 43, 50]
1GermanyIsrael, JordanST80ST80 has been reported in the Middle East[6, 21, 89]
1GermanyEcuadorST8ST8 is prevalent in Latin America[47, 91]
1GermanyIndiaST772ST772 has been reported in both the community and hospitals within India[55]
1GermanySamoaST931
Tappe and colleagues (2010)[26]Skin abscesses3GermanyPakistan, Costa Rica, Thailand
Brennan and colleagues (2012)[27]Colonization (transmitted by a recently traveled nurse to nine others)10IrelandIndiaST772ST772 has been reported in both the community and hospitals within India[55]
SSTIs (mostly)4IrelandIndia
Rossney and colleagues (2007)[28]SSTI (majority), pneumonia, bloodstream infections, colonization4IrelandAfricaST5, ST8, ST30ST5, ST8, and ST30 strains have been reported in Africa[94]
3IrelandAsiaST30, ST80, ST154ST30 has been reported in Asia[21, 53]; ST154 was previously reported in Mongolia[95]
1IrelandUSAST8ST8 MRSA (USA300) is the dominant CA-MRSA strain in the United States[44-46]
1IrelandMiddle EastST80ST80 has been reported in the Middle East[6, 21, 89]
Stenhem and colleagues (2010)[21]Both MRSA carriers and individuals with clinical disease (no mention on site of infection)26SwedenUnited Kingdom, IrelandST22, ST36ST22 and ST36 have dominated the United Kingdom since the 1990s[93]
Stenhem and colleagues (2010)[21]Both MRSA carriers and individuals with clinical disease (no mention on site of infection)41SwedenEast AsiaST239, ST30, ST72ST239 has been reported in Taiwan, China, and Mongolia[95-97]; ST30 has been reported in Hong Kong and Japan[54, 98]
5SwedenOceania, Pacific Islands, HawaiiST30ST30 is prevalent in Oceania[4, 6, 21, 43, 50]
39SwedenNorth Africa, Middle East, MediterraneanST80ST80 has been reported in the Middle East[6, 21, 89] and North Africa, including Algeria[90]
Bochet and colleagues (2008)[29]Cutaneous abscesses4SwitzerlandThe PhilippinesST30ST30 is a common isolate in the Philippines[21, 53]
Liassine and colleagues (2004)[30]Impetigo3SwitzerlandSenegal, Algeria, Angola, Netherlands
Tietz and colleagues (2005)[31]Colonization1SwitzerlandUnited StatesST8ST8 MRSA (USA300) is the dominant CA-MRSA strain in the United States[44-46]
Ellington and colleagues (2010)[32]SSTIs (majority), colonization17United KingdomBengal Bay area or the Indian subcontinentST772ST772 has been reported in both the community and hospitals within India[55]
Ali and colleagues (2011)[33]Cutaneous pustules and colonization (transmitted by a recently traveled nurse to five others)6United KingdomThe PhilippinesST30ST30 is a common isolate in the Philippines[21, 53]
Ellington and colleagues (2010)[34]SSTIs (majority), necrotizing pneumonia4United KingdomAustraliaST93Queensland (QLD) ST93 is the second most common CA-MRSA strain in Australia and had surfaced since 2000[99]
Helgason and colleagues (2007)[35]Multiple cutaneous abscess, cellulitis, and folliculitis2United KingdomJamaicaST8
Cutaneous abscess, folliculitis, bursitis2United KingdomSpainST80ST80 has been reported among European countries, including Sweden,[21] Belgium,[23] Denmark,[100] and Greece[92]
Kaiser and colleagues (2004)[19]Colonization31The NetherlandsMiddle, west, southern, southeastern Europe, South Africa, South East Asia, China, Egypt
Yabe and colleagues (2010)[36]SSTIs, osteomyelitis (MRSA transmitted by relatives who had visited the United States)8JapanUnited States, HawaiiST8 (USA300)ST8 MRSA (USA300) is the dominant CA-MRSA strain in the United States[44-46]
Shibuya and colleagues (2008)[37]Subcutaneous abscess in the cervical region1JapanUnited StatesST8ST8 MRSA (USA300) is the dominant CA-MRSA strain in the United States[44-46]
Neela and colleagues (2008)[38]No mention if it is collected from an asymptomatic colonizer or from an infected site1MalaysiaBangladeshST772ST772 has been reported in both the community and hospitals within India[55]
Hsu and colleagues (2005)[39]Cutaneous abscess1SingaporeTaiwanST59ST59 MRSA has been reported in Taiwan and Hong Kong[54, 96, 101]
Ko and colleagues (2013)[40]Buttock carbuncle1South KoreaThe PhilippinesST30ST30 is a common isolate in the Philippines[21, 53]
Park and colleagues (2007)[41, 42]Perianal abscess1South KoreaUnited States, HawaiiST8 (USA300)ST8 MRSA (USA300) is the dominant CA-MRSA strain in the United States[44-46]

Global Spread of MRSA via International Travel

The concept of continent-specific PVL-positive CA-MRSA clones as categorized by MLST was first put forward by Vandenesch and colleagues in 2003.[43] ST80 and ST30 (South West Pacific clone) were the predominant CA-MRSA clones in Europe and Oceania, respectively, whereas ST1 (USA400), ST8 (USA300), and ST59 (USA1000) were the most prevalent clones in the United States.[6, 43] USA300, a dominant CA-MRSA clone that had previously caused several outbreaks among sports teams, prison inmates, military personnel, and day care centers in the United States, is now endemic in several hospitals as well, resulting in serious hospital-acquired infections.[44-46] Its remarkable virulence, enhanced environmental survival and transmissibility have also resulted in its global spread, and it has now become the dominant CA-MRSA strain in several countries, including Canada, Venezuela, Colombia and Ecuador.[47] It has also been sporadically reported in Europe, Iraq, Australia, and Japan where its isolation was often associated with travelers from the United States, or recent travel to the United States.[6, 36, 48, 49]

Tristan and colleagues had subsequently described the intercontinental spread of several PVL-positive CA-MRSA clones where five major routes of intercontinental exchange of clones were observed. First, the ST8 (USA300) clone was found to have spread from the United States to Europe; second, the ST1 (USA400) clone spread from the United States to Europe and Asia; third, the ST59 (USA1000) clone from the United States spread to Asia; fourth, the ST80 clone spread from Europe to Asia; finally, the ST30 clone spread from Oceania to Europe.[50]

Another epidemiologic study examining the global spread of MRSA via international travel was carried out in Sweden by Stenhem and colleagues between 2000 and 2003. A total of 444 imported cases of MRSA were reported in individuals who had traveled abroad or who were internationally adopted children or immigrants. Imported cases were mostly healthcare-acquired (55.4%) but community acquisition of MRSA correlated with regions that had a high risk of MRSA, and 42.8% of the travelers in this study had clinical MRSA disease. The overall risk of acquiring MRSA was 5.8 cases per 1,000,000 travelers, with risk being lowest at 0.1 per 1,000,000 travelers to Nordic countries and highest at 59.4 per 1,000,000 travelers to North Africa and the Middle East.[21] Another Swedish study by Larsson and colleagues described the MRSA epidemiology over time, method, and country of acquisition. They noted an almost 10-fold increase in MRSA cases between 2000 and 2010. Only 24% of the MRSA cases were of Swedish origin, indicating that more than three fourths of cases had contracted MRSA outside of Sweden. An association between spa type (a single locus-based typing method) and certain regions of acquisition/origin was also observed in this study.[51]

Apart from Sweden, other European countries including Germany, the United Kingdom, Ireland, and Switzerland have also reported cases of MRSA importations from countries other than America and Oceania.[18, 19, 22-35] On the other hand, exportation of MRSA out of Europe to other countries, including the Caribbean countries, has also been reported; ST8 and ST5 MRSA strains from France into the French West Indies (Guadeloupe and Martinique) were reported as a result of increased traveling and migration.[52]

In Asia, the ST30 MRSA strain that was predominantly found in Oceania was reported as the predominant CA-MRSA in the Philippines, Taiwan, Singapore, and Hong Kong.[53] In addition, a high diversity of MRSA strains including ST8, ST30, ST59, and ST80 have been reported in Asian countries with high international traffic such as Hong Kong and Singapore.[39, 54] Several other case reports of Asian travelers importing PVL-positive MRSA clones from other continents have also been described (Table 1).[36-42]

MRSA Transmission via Medical Tourism, Medical Repatriation and Its Impact on Healthcare-Associated Infections

Repatriation of patients from foreign hospitals or returning of patients who traveled for medical tourism has further fostered the emergence and spread of multidrug-resistant bacteria, including MRSA, from countries where multidrug-resistant organisms are endemic.[17-20, 51, 53] In a recent French study on repatriated patients, MRSA together with multidrug-resistant Acinetobacter baumannii was found to be the most frequently isolated bacteria.[18] The Dutch had also reported an overall MRSA carriage rate of 2.7% in repatriates from foreign hospitals, a rate which was higher than that among Dutch hospitals.[19] In addition, transfer of patients from France and Turkey (endemic for MRSA) to the Netherlands has caused outbreaks of MRSA within the Dutch hospitals previously.[20] Long duration of stay in foreign hospitals, artificial ventilation, and previous antimicrobial use were implicated as risk factors for MRSA acquisition abroad.[18, 19]

Consequence of Traveling on MRSA Transmission by Healthcare Workers

On the other hand, while returning patients may be carriers of HA-MRSA acquired overseas, healthcare workers who are colonized with CA-MRSA during their leisure travel may also serve as a vector for transmitting such organisms to other vulnerable patients in the healthcare setting, leading to outbreaks that could potentially result in devastating outcomes. Ali and colleagues reported an outbreak of PVL-positive ST30 MRSA (South West Pacific clone) in a neonatal intensive care unit in the United Kingdom.[33] A nurse who had traveled to the Philippines a few months prior to the outbreak was implicated as the likely source of the MRSA outbreak, resulting in three neonates and one other staff developing skin pustules.[33] Similarly, another outbreak due to PVL-positive ST772 MRSA occurred in an Irish neonatal intensive care unit with seven neonates found to be asymptomatically colonized.[27] This CA-MRSA strain has been reported in India and has infiltrated into many Indian hospitals.[55] In this particular outbreak, a nurse who was recently hospitalized in India was implicated as the index person.[27]

MRSA Transmission via Water-Related Events

A case report of two Swiss scuba divers who developed cutaneous abscesses secondary to ST30 CA-MRSA infection acquired from their trip to the Philippines had been described previously.[29] Of note, sharing of scuba diving equipment had been demonstrated to be independently associated with CA-MRSA carriage by a study in the Netherlands.[56] A study investigating the survival dynamics of MRSA strains in various types of water in Ireland concluded that both CA-MRSA and HA-MRSA survived in both marine and fresh river water for at least 14 days.[57] However, whether the contaminated seawater, presence of skin abrasions among divers, or the failure to decontaminate diving suites and other related-diving materials after use could be the source of MRSA transmission remains to be elucidated.[56, 57]

MRSA Transmission via Sporting Events

Outbreaks of CA-MRSA causing mainly SSTIs among athletes who were involved in sports with repeated close physical contact (eg, football, wrestling, and rugby) or have shared common equipment (eg, unlaundered towels, soap bars, and razor) are well documented in the literature.[58-64]

A case report from the United Kingdom described a MRSA outbreak involving five rugby players who presented with large abscesses at various body sites.[62] They were found to have competed with a touring team from the South Pacific 10 days prior to the manifestation of symptoms. The MRSA strain implicated did not belong to the endemic strains of the United Kingdom and hence possible MRSA transmission from the foreign players was postulated. Although there have been no established reports of international transmission of MRSA via sporting events, it is important for healthcare professionals to consider athletes who had recently visited countries endemic for CA-MRSA or had contact with athletes from endemic countries as potential risk factors for colonization of CA-MRSA. This may potentially impact the choice of empiric antibiotics used in these athletes who present with community-acquired infections.

Livestock-Associated MRSA

S. aureus is one of the three major pathogenic staphylococci in animals besides Staphylococcus hyicus and Staphylococcus intermedius group. S aureus has been reported to cause intramammary infections in ruminants, chicken, and horses.[65, 66] From 2000 onwards, reports of livestock-associated MRSA (LA-MRSA) in animals were increasingly being described across Europe (ST398 MRSA) and Asia (ST9 MRSA).[65, 67-69] The routine use of antimicrobials such as tetracycline in pig and cattle farms appears to be a possible cause of emerging MRSA carriage.[65, 70] Individuals including veterinarians and farmers who have been exposed to LA-MRSA-colonized livestock are at higher risk for LA-MRSA carriage and infection.[65, 71-75] Although LA-MRSA transmission via international travel has yet to be established in the literature, it is pertinent for ill-returning travelers who had recent animal contact at endemic areas to be considered at risk for LA-MRSA colonization or infection.

ST398-MRSA, commonly found among livestock in Europe, has been reported to cause serious infections including diabetic foot infections, skin abscesses, and endocarditis among humans.[76-78] Furthermore, ventilator-associated pneumonia caused by ST398 had been reported, suggesting that LA-MRSA may have the capability to transmit within the healthcare setting.[79] An outbreak with ST398 MRSA in a Dutch hospital reported in 2007 had resulted in serious diabetic foot wound infections, and one healthcare worker who stayed near a pig farm was implicated as the likely source.[76]

Implications on Empiric Treatment Options for Infections in Travelers

In several case reports, returned travelers who present to healthcare professionals with SSTIs were initially prescribed oral beta-lactam antibiotics, the most common first-line antibiotics for the treatment of community-acquired SSTI. However, the infections were found to have worsened before further investigations were carried out to reveal that the SSTI was caused by MRSA.[21, 37, 40] Although such cases are undoubtedly rare at present, obtaining pertinent information on previous travel history, contact history, recent involvement in contact sports, nationality, and occupation of the patients who present with SSTIs remains important as there is a need to consider any possibility of acquiring CA-MRSA or LA-MRSA during travel in order to provide adequate empiric antimicrobial treatment for patients with severe infections or at least to obtain appropriate bacterial cultures.

Possible oral agents that may cover possible CA-MRSA causing SSTIs in travelers include clindamycin, co-trimoxazole, or long-acting tetracyclines (eg, doxycycline or minocycline). Clindamycin and co-trimoxazole have been shown to be active in vitro against >90% of CA-MRSA isolates and may also be active against Streptococcus spp. that also commonly causes SSTIs.[80, 81] In LA-MRSA caused by the ST398 strains, high-level resistance to tetracycline has been reported in view of high usage of tetracycline in pig husbandry. Approximately 80% of LA-MRSA remains susceptible to clindamycin and erythromycin, whereas resistance to co-trimoxazole is uncommon.[70] In view of the fact that antimicrobial susceptibility profiles may vary by region, more detailed studies on antibiotic susceptibility patterns in imported MRSA are required to inform detailed recommendations on the presumptive treatment of S. aureus-associated SSTIs in ill-returning travelers.

Screening and Decolonization

With the increase in international travel and migration, screening and decolonization of healthy travelers or immigrants arriving from endemic areas may reduce the transmission of MRSA and hence potential outbreaks and infections.[82] In addition, screening allows close monitoring of circulating MRSA genotypes and corresponding antimicrobial susceptibility, which in turn influences treatment options in MRSA infections.[83] However, screening of all returned travelers, new immigrants, and foreigners is impractical in view of the cost and logistic difficulties.

Several reports of successful containment of outbreaks in the community with active screening and subsequent decolonization have been described.[84-87] Robicsek and colleagues performed the first large-scale, universal-admission MRSA surveillance program in the United States across three different hospitals with decolonization of positive cases. This has yielded encouraging results; prevalence of MRSA infections was significantly reduced by 69.6% with universal surveillance from baseline. However, this study screened only patients but not healthcare workers. [87] The Danish had also demonstrated an effective “search and destroy” policy where patients and their family members who were infected or colonized with PVL-positive ST30 CA-MRSA underwent treatment or decolonization, respectively. With the commencement of this new policy, transmission due to ST30 MRSA, primarily imported from the Philippines, was kept to the minimum by free treatment of MRSA carriers and close follow-up visits.[84]

A consensus meeting between the European Society of Clinical Microbiology and Infectious Diseases and the International Society of Chemotherapy in 2010 had suggested selective targeted screening as an alternative to individuals with higher relative risk for both HA-MRSA and CA-MRSA colonization upon hospital admission, including individuals who had traveled recently to endemic countries and also had recent exposure to livestock or animals.[83] At present, there is no recommendation for routine screening for MRSA in returned travelers or immigrants from endemic areas. Nevertheless, we propose that selective targeted screening of individuals with specific criteria suggested in Table 2, who have traveled recently to endemic areas, may be beneficial in curbing the spread of MRSA and hence subsequent potential infections.

Table 2. Criteria for MRSA screening in individuals who had recently traveled to areas with high risk for MRSA acquisition
  1. MRSA = methicillin-resistant Staphylococcus aureus.
1. International or inter-hospital transfers
2. Previous hospitalization or had recent healthcare contact
3. Healthcare workers
4. Caregivers (non-healthcare workers) of vulnerable population (eg, immunocompromised patients and individuals of extreme ages)
5. Individuals who present to healthcare institutions with recent travel or were in contact with individuals from endemic areas
6. Individuals who present to healthcare institutions with recent contact with livestock or animals (including farmers and veterinarians)

Conclusion

Transmission of MRSA, including CA-MRSA, HA-MRSA, and potentially LA-MRSA, is possible with international travel. However, current evidence is largely restricted to case series and case reports, while systematic research on imported MRSA and, most importantly, on the effectiveness of potential interventions for its containment is scarce. Individuals may acquire the MRSA via leisure traveling or overseas healthcare exposure, resulting in either asymptomatic colonization or clinically significant MRSA disease. Newly imported MRSA strains may potentially replace the native strain of MRSA as the dominant strain, resulting in potential outbreaks within the community or healthcare setting.

Hence, it is essential to ensure that a well-established surveillance network of imported S. aureus, similar to that of the European network established by Zanger and colleagues, is present in various regions to monitor the emergence of virulent and antibiotic-resistant strains.[22, 88]

This would in turn greatly aid in establishing recommendations on the presumptive treatment of MRSA-associated infections in ill-returning travelers. Selective targeted screening of patients with risk factors for MRSA colonization may be beneficial in curbing the spread of MRSA, guiding antimicrobial therapy in cases of infection, requiring contact precaution and also decolonization. Healthcare professionals may also be considered for screening if they were to return from endemic areas and decolonized before returning to patient care work.

In response to the worldwide spread of antimicrobial resistance and its link to travel, globalization of medical care, and increasing antibiotic use, the travel medicine community is a critical link in the overall attempt to reduce the global spread of antimicrobial resistance including MRSA.

Declaration of Interests

The authors declared no conflicts of interest.

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