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International Journal of Infectious Diseases 48 (2016) 113–117 Contents lists available at ScienceDirect International Journal of Infectious Diseases journal homepage: www.elsevier.com/locate/ijid Review Management of infections in critically ill returning travellers in the intensive care unit—I: considerations on infection control and transmission of resistance§ Hakan Leblebicioglu g, Alfonso J. Rodriguez-Morales b, Gian Maria Rossolini c,d, Rogelio López-Vélez e, Jean-Ralph Zahar f, Jordi Rello a,* on behalf of ESGCIP and ESGITM a CIBERES, Vall Hebron Research Institute, Universitat Autònoma de Barcelona, Barcelona, Spain b Public Health and Infection Research Group, Faculty of Health Sciences, Universidad Tecnológica de Pereira, Pereira, Risaralda, Colombia c Department of Medical Biotechnologies, University of Siena, Siena, Italy d Department of Experimental and Clinical Medicine, University of Florence, and Clinical Microbiology and Virology Unit, Florence Careggi University Hospital, Florence, Italy e National Referral Unit for Tropical Diseases, Infectious Diseases Department, Ramón y Cajal University Hospital, Madrid, Spain f Infection Control Unit, Université d’Angers, Centre Hospitalier Universitaire d’Angers, Angers, France g Department of Infectious Diseases and Clinical Microbiology, Ondokuz Mayis University Medical School, Samsun, Turkey A R T I C L E I N F O S U M M A R Y Article history: Depending on their destinations and activities, international travellers are at a significant risk of Received 25 January 2016 contracting both communicable and non-communicable diseases. On return to their home countries, Received in revised form 19 April 2016 such travellers may require intensive care. The emergence of severe acute respiratory syndrome Accepted 21 April 2016 coronavirus (SARS-CoV) and Middle East respiratory syndrome coronavirus (MERS-CoV), and more Corresponding Editor: Eskild Petersen, recently Ebola haemorrhagic fever, has highlighted the risks. Other well-known communicable Aarhus, Denmark. pathogens such as methicillin-resistant Staphylococcus aureus and carbapenemase-producing Enter- obacteriaceae have been described previously. However, malaria remains by far the most important Keywords: cause of death. The issues related to imported antibiotic resistance and protection from highly Resistance contagious diseases are reviewed here. Surveillance strategies based on epidemiological data (country Infection control visited, duration of travel, and time elapsed since return) and clinical syndromes, together with Traveller systematic search policies, are usually mandatory to limit the risk of an outbreak. Single-bed hospital ICU rooms and isolation according to symptoms should be the rule while awaiting laboratory test results. Migrant Because person-to-person contact is the main route of transmission, healthcare workers should implement specific prevention strategies. ß 2016 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). 1. Imported antibiotic resistance development of new antibiotics active against MDR pathogens has led to what has been termed the ‘antibiotic resistance crisis’. The Infections caused by multidrug-resistant (MDR) pathogens are situation has been further complicated recently by the emergence typically associated with increases in morbidity, mortality, and and dissemination of strains that remain susceptible to only a few healthcare-associated costs, and represent an increasing public antibiotics (extensively drug-resistant (XDR) strains), which are health challenge of global dimensions.1 The combination of a difficult to treat.2 progressive loss of antibiotic efficacy due to the emergence and The most challenging MDR pathogens include (1) methicillin- dissemination of resistance and the slow rates of discovery and resistant Staphylococcus aureus (MRSA), (2) vancomycin-resistant enterococci (VRE), (3) Enterobacteriaceae producing extended- spectrum beta-lactamases (ESBLs) or carbapenemases (CPE), (4) DOI of original article: http://dx.doi.org/10.1016/j.ijid.2016.04.020 XDR Pseudomonas aeruginosa that remain susceptible only to § ESGCIP is the ESCMID Study Group for Infections in Critically Ill Patients; polymyxins, and (5) carbapenem-resistant Acinetobacter (CRA). ESGITM is the ESCMID Study Group for Infections in Travellers and Migrants. Among these, CPE and CRA are currently the most problematic due * Corresponding author. E-mail address: jrello@crips.es (J. Rello). to their XDR phenotypes, their propensity for epidemic diffusion in http://dx.doi.org/10.1016/j.ijid.2016.04.019 1201-9712/ß 2016 The Authors. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 114 H. Leblebicioglu et al. / International Journal of Infectious Diseases 48 (2016) 113–117 healthcare settings, and the high mortality rates associated with promedmail.org), clinicians should consider that (1) for several invasive infections.2 countries (especially low-income settings) epidemiological infor- In principle, any of these pathogens can be encountered, either mation is scarce or lacking, and (2) the epidemiology of MDR/XDR as colonizers or as infecting agents, in travellers returning from pathogens can change rapidly. So this information should be areas of endemicity and in patients repatriated from foreign considered partial and should be updated regularly. healthcare facilities. Acquisition may be the consequence of Exposure to medical practices in facilities from endemic areas, exposure to contaminated food or environments, of close contact either unanticipated or scheduled, is an additional risk factor for with colonized individuals, or of admission to hospitals and carriage/infection by MDR/XDR pathogens.16 exposure to medical practices either for unexpected reasons (e.g., Recommendations for ICUs, based on the current evidence, trauma, acute diseases) or for medical tourism (e.g., specialized include the following: surgery, organ transplantation). As has been clearly documented, the transmission of MRSA has increased with the growth of (1) Carrying out a risk assessment for carriage/infection by MDR/ international travel, resulting in either asymptomatic colonization XDR pathogens for all ICU admissions of patients returning or clinically significant MRSA infections.3,4 Some evidence is also from international travel or transferred from foreign hospitals. available for the international dissemination of VRE via transfer/ (2) Enforcing infection control precautions upon admission for all repatriation of patients from hospitals located in endemic areas.5 patients returning from international travel or transferred from Concerning Gram-negative organisms, the impact of international foreign hospitals with known risk factors for carriage/infection travel has been firmly established in the dissemination of MDR by MDR/XDR pathogens. The infection control precautions Enterobacteriaceae, including high-risk clones producing ESBLs should cover the various types of MDR/XDR pathogens for (especially enzymes of the CTX-M type) and/or carbapenemases of which a risk was assessed, and should be kept in place until various types (e.g., KPC, OXA-48, NDM, VIM).6–8 The risk of the carriage/infection by MDR/XDR pathogens has been ruled out spread of MDR strains of Enterobacteriaceae in this situation by the proactive surveillance and clinical microbiology includes not only Escherichia coli, Klebsiella spp, and Enterobacter diagnostic workup. spp, but also classical enterobacterial pathogens such as Salmonella (3) Carrying out proactive surveillance for MDR/XDR pathogens for enterica and Shigella spp, with evidence of imported cases of which a risk was assessed by culture and/or molecular typhoid fever and shigellosis caused by MDR strains.8,9 The methods. transmission of MDR Acinetobacter has been documented follow- ing the international transfer of patients from intensive care units 2. Protection from highly contagious disease in critically ill (ICUs) in countries with high-level endemicity,10 and the returning travellers in the ICU repatriation of evacuees involved in military operations in endemic areas.11 Less evidence is available for the travel-related dissemi- 2.1. Introduction to potentially life-threatening travel-associated nation of MDR/XDR P. aeruginosa strains, but this is clearly a infectious diseases possibility following the transfer of colonized patients from ICUs where these strains are endemic or are causing outbreaks.12 Depending on their destinations and activities, international The admission to the ICU of patients colonized or infected by travellers are at a significant risk of contracting both communica- MDR/XDR pathogens is a matter of concern, since it may be ble and non-communicable diseases.17 The emergence of severe followed by cross-infections and outbreaks in the ICU setting acute respiratory syndrome coronavirus (SARS-CoV), Middle East unless suitable infection control practices are enforced immedi- respiratory syndrome coronavirus (MERS-CoV), and more recently ately. Moreover, infections caused by MDR/XDR pathogens may Ebola haemorrhagic fever, has highlighted the risks. However, require different antimicrobial treatments from those routinely other well-known communicable pathogens such as MRSA18 and used in the ICU, which are based on the local epidemiology; this CPE19,20 have been described previously. ICU patients, because of may result in inappropriate empiric treatment and thus increased the severity of illness, the workload, and the antibiotic selection morbidity and mortality. pressure, are important potential reservoirs of dangerous micro- Therefore, the possibility of carriage or infection by an MDR/ organisms. The most important challenges for ICU practitioners are XDR pathogen should always be considered for critically ill first to identify admissions with the highest risk of communicable returning travellers admitted to the ICU. A risk assessment should disease, and second to rapidly implement preventive measures in be performed, considering the area of provenance, the history of order to avoid nosocomial transmission. the patient, and the presence of additional risk factors for carriage Surveillance strategies for the early detection of unusual or infection by similar resistant pathogens.2,12 infectious disease events should be the rule. Syndromic surveil- The epidemiology of MDR/XDR pathogens may vary according lance can help to reduce the identification time. All patients to geographical area. The proportion of MRSA among S. aureus transferred from hospitals in high-risk countries (Table 1) should isolates remains very high in some European countries, the USA, be considered as potential carriers of MDR or highly drug-resistant Latin America, and the Far East, but is considerably lower in other microorganisms. All of these patients should be screened for rectal European countries such as the Netherlands and the Scandinavian carriage at admission and a few days after any antibiotic therapy.21 countries.13 ESBL-producing Enterobacteriaceae are now dissemi- While awaiting screening results, the patient should be hospital- nated worldwide, with very high rates detected among ICU ized in a single-bed room. Contact and body fluid precautions patients in Latin America, the Asia-Pacific region, and the Middle should be added. All patients with fever and clinical or East.14 For their part, CPE have achieved a notable level of radiographic evidence of pneumonia or acute respiratory distress endemicity in some areas of Europe (e.g., Greece and Italy), the syndrome, and with a history of travel from countries in or near the Middle East (e.g., Turkey, Israel), South America (e.g., Colombia), Arabian Peninsula (Bahrain, Iraq, Iran, Israel, the West Bank and and China.15 Travellers/patients from areas of high endemicity for Gaza, Jordan, Kuwait, Lebanon, Oman, Qatar, Saudi Arabia, Syria, MDR/XDR pathogens have a higher risk of exposure to these the United Arab Emirates, and Yemen) within 14 days before pathogens, and the possibility of being infected or colonized by symptom onset, or close contact with a symptomatic traveller who these agents at the time of repatriation should always be developed fever and acute respiratory illness within 14 days after considered. When consulting sources of information regarding travelling from countries in the region, should be considered as resistance and endemicity (such as ProMED-mail, http://www. potentially infected by MERS-CoV.22 Viral haemorrhagic fever H. Leblebicioglu et al. / International Journal of Infectious Diseases 48 (2016) 113–117 115 Table 1 Distribution of the most common organisms by region and reservoir Infectious agents Geographical origin Reservoir Main type of transmission Main type of protection Viruses MERS-CoV Middle East Dromedary camels Droplet contact Droplet precautions SARS-CoV South China Chinese horseshoe bats Droplet contact, airborne Droplet precautions H7N9 Eastern China, Hong Kong, Taiwan, Malaysia Poultry, wild birds Droplet? Droplet precautions Influenza virus Droplet Droplet precautions Haemorrhagic fever Droplet, contact Droplet precautions Ebola Africa, Guinea, Sierra Leone Bats Droplet, contact Bacteria Carbapenemase-producing Southern Asia, India, Middle Eastern Countries; Human Contact Contact precautions Enterobacteriaceae Maghreb countries, Israel, Romania, Italy, Turkey, Greece XDR-TB and MDR-TB Russia, eastern Europe, southern Africa Human Airborne Airborne precautions Meningococci Human Droplet Droplet precautions MERS-CoV, Middle East respiratory syndrome coronavirus; SARS-CoV, severe acute respiratory syndrome coronavirus; XDR-TB, extensively drug-resistant tuberculosis; MDR-TB, multidrug-resistant tuberculosis. should be suspected in selected patients coming from Sub-Saharan disease and they should be prepared for this eventuality (a heavy Africa with fever and bleeding disorders, depending on the price was paid during the SARS outbreak). In an endemic area, geographical origin and local epidemiological situation. A general MERS-CoV infection is more likely to be acquired in healthcare syndromic approach to tropical infections in the ICU is described in facilities than in the community: in the 2014 outbreak in Jeddah, Table 2.23 Saudi Arabia, more than four out of five exposures were at Although many imported infectious diseases may require ICU healthcare facilities, mainly due to poor and insufficient isolation admission, the most frequent ones are relatively few in number. In measures at admission.25 a descriptive analysis of acute and potentially life-threatening Patients with suspected highly contagious tropical infectious tropical diseases among 82 825 ill Western travellers reported to diseases should be placed directly in an emergency department GeoSentinel from 1996 to 2011, 3655 patients (4.4%) with isolation room (if available) and should be examined and assessed 13 diseases were identified; falciparum malaria (76.9%), enteric as soon as possible. Standard precautions and cough and fever (18.1%), and leptospirosis (2.4%) were the most frequent. respiratory etiquette should be applied systematically. During Ninety-one percent of patients had fever. The median time from admission, these patients should avoid any contact with other travel to presentation was 16 days. Thirteen (0.4%) patients died: patients, and unprotected healthcare workers should avoid contact 10 with falciparum malaria, two with melioidosis, and one with with them. If possible, point-of-care bedside laboratory tests severe dengue. Falciparum malaria was mainly acquired in West should be used for sampling, or all analyses should be done in a Africa, enteric fever on the Indian subcontinent, and leptospirosis, biosafety level 3/4 laboratory. Samples should be inactivated (with scrub typhus, and murine typhus in Southeast Asia.24 formalin) before testing in a routine laboratory. Transfer to the ICU or to a high-level isolation unit must be carried out in a secure 2.2. Transmission risks of highly contagious tropical infectious manner. diseases associated with healthcare settings Many organisms are present in the ICU, but only a few are involved in person-to-person transmission. An overview of the Emergency departments at general hospitals are the first units precautions recommended for selected tropical infections and to deal with an unknown highly contagious tropical infectious conditions is shown in Table 3. Table 2 Syndromic approach to tropical infections in the ICU Syndrome Diseases Fever and toxic appearance Dengue fever, malaria, typhoid fever, early shigellosis, leptospirosis, and anicteric hepatitis. The presence of a Fever and rash haemorrhagic rash may indicate arboviral, rickettsial, and meningococcal aetiologies. Aetiologies of VHF that have been known to cause person-to-person transmission are Lassa virus, Ebola virus, Marburg virus, and Crimean-Congo haemorrhagic fever virus Fever and thrombocytopenia Malaria, dengue, leptospirosis, rickettsiosis Fever with eosinophilia Schistosomiasis (Katayama fever or acute neurological sequelae of myelitis or encephalitis), visceral larva migrans, tropical pulmonary eosinophilia, acute fascioliasis, acute trichinosis Severe pneumonia or ARDS Streptococcus pneumoniae, Legionella pneumophila, bacterial sepsis with other pathogens, tuberculosis, Burkholderia pseudomallei (melioidosis), plague, histoplasmosis, malaria, typhoid fever, leptospirosis, scrub typhus, hantaviruses, coronaviruses, highly pathogenic avian influenza A (H5N1) Pulmonary renal syndrome Falciparum malaria, leptospirosis, hantavirus infection, scrub typhus, severe pneumonia Hepatorenal dysfunction Falciparum malaria, leptospirosis, scrub typhus, hepatitis E or A with fulminant hepatic failure and the hepatorenal syndrome, yellow fever virus Acute abdomen Appendicitis, cholecystitis, diverticulitis, perforated peptic ulcer, enteric fever, amoebic liver abscess Dysentery and severe gastrointestinal Amoebic (Entamoeba histolytica) and bacillary (Shigella spp, especially S. dysenteriae and S. flexneri, fluid losses Campylobacter jejuni, non-typhoidal Salmonella spp, Yersinia enterocolitica, enteroinvasive Escherichia coli, and enterohaemorrhagic E. coli (EHEC)) Altered sensorium Cerebral malaria, meningitis, typhoid fever, viral encephalitis (Japanese encephalitis virus, Rift Valley fever virus, Murray Valley encephalitis virus, West Nile virus, St. Louis encephalitis virus, rabies virus, Nipah virus). Eosinophilic meningoencephalitis (Angiostrongylus cantonensis, Gnathostoma spinigerum, migrating ascarids, and schistosomiasis) ICU, intensive care unit; VHF, viral haemorrhagic fever; ARDS, acute respiratory distress syndrome. 116 H. Leblebicioglu et al. / International Journal of Infectious Diseases 48 (2016) 113–117 Table 3 Precautions recommended for selected tropical infections and conditions Infection/condition Precautionsa Comments Amoebiasis Standard Person-to-person transmission is rare (care when handling diapered infants and mentally challenged persons) Chagas disease (Trypansoma cruzi) Standard Not transmitted from person to person (only vertical transmission and organ/ blood donation) Coronavirus: SARS-CoV, MERS-CoV Airborne Aerosol-generating procedures and ‘super-shedders’ present highest risk for High-level transmission isolation unit Dengue virus Standard Not transmitted from person to person Chikungunya virus Install screens in windows and doors in endemic areas; use DEET-containing mosquito repellents and clothing to cover extremities Echinococcosis (hydatidosis) Standard Not transmitted from person to person Encephalitis, arthropod-borne viral Standard Not transmitted from person to person, except rarely by transfusion and for Japanese encephalitis West Nile virus by organ transplant, breast milk, or transplacentally Central European tick-borne Install screens in windows and doors in endemic areas; use DEET-containing Venezuelan equine mosquito repellents and clothing to cover extremities Murray Valley encephalitis Airborne precautions for Hendra and Hendra-like virus, as human-to-human St. Louis encephalitis spread is unknown West Nile virus Nipah virus Hendra virus Gastroenteritis Standard Use contact precautions for diapered or incontinent persons Cholera Enteropathogenic O157:H7 and other shiga toxin-producing strains Salmonella species (including Salmonella Typhi) Shigella species (bacillary dysentery) Hantavirus pulmonary syndrome Droplet Rarely transmitted from person to person Haemorrhagic fever with renal syndrome, and other Puumala, Seoul, and Sin Nombre viruses Histoplasmosis Standard Not transmitted from person to person Influenza, avian (H5N1, H7, H9 strains) Droplet Leptospirosis Standard Not transmitted from person to person Malaria Standard Not transmitted from person to person except through transfusion rarely and through a failure to follow standard precautions during patient care Install screens in windows and doors in endemic areas; use DEET-containing mosquito repellents and clothing to cover extremities Melioidosis Standard Not transmitted from person to person Meningitis: meningococcal disease Droplet Post-exposure chemoprophylaxis for household contacts and healthcare workers exposed to respiratory secretions Eosinophilic meningitis (Angiostrongylus cantonensis, Gnathostoma spinigerum, migrating ascarids, and schistosomiasis) is not transmitted from person to person Rabies Standard Person-to-person transmission is rare (has been reported in corneal, tissue, and organ transplants). If the patient has bitten another individual or saliva has contaminated an open wound or mucous membrane, wash the exposed area thoroughly and administer post-exposure prophylaxis Relapsing fever Standard Not transmitted from person to person Rickettsial fevers, tick-borne (boutonneuse Standard Not transmitted from person to person fever, Rocky Mountain spotted fever, tick-borne typhus fever, scrub typhus) Schistosomiasis (bilharziasis) Standard Not transmitted from person to person Strongyloidiasis Standard Could hypothetically be transmitted by skin contact with secretions of patients with hyperinfestation syndrome Viral haemorrhagic fevers Standard Not transmitted from person to person Yellow fever Rift Valley fever virus Viral haemorrhagic fevers (2) High-level Crimean-Congo haemorrhagic fever virus, Ebola virus, Marburg virus, Lassa Kyasanur Forest disease virus isolation unit fever virus, Guanarito virus, and Machupo virus can be transmitted from person Omsk haemorrhagic fever virus to person. Unknown for Kyasanur Forest virus, Omsk virus, Junin virus, and Crimean-Congo haemorrhagic fever virus Sabiá virus Ebola virus Emphasize: (1) use of sharp safety devices and safe work practices; (2) hand Marburg virus hygiene; (3) barrier protection against blood and body fluids upon entry into Lassa fever virus room (single gloves and fluid-resistant or impermeable gown, face/eye Junin virus (Argentine haemorrhagic fever) protection with masks, goggles, or face shields); and (4) appropriate waste Guanarito virus (Venezuelan haemorrhagic fever) handling. Use N95 or higher respirators when performing aerosol-generating Machupo virus (Bolivian haemorrhagic fever) procedures. Largest viral load in final stages of illness when haemorrhage may Sabiá virus (Brazilian haemorrhagic fever) occur; additional PPE, including double gloves, leg and shoe coverings may be used, especially in resource-limited settings where options for cleaning and laundry are limited SARS-CoV, severe acute respiratory syndrome coronavirus; MERS-CoV, Middle East respiratory syndrome coronavirus; DEET, N,N-diethyl-meta-toluamide; PPE, personal protective equipment. a Standard precautions include hand hygiene, use of PPE, prevention of needlestick injuries, environment cleaning, and the appropriate handling of waste. Droplet precautions include standard precautions and the use of a single room, surgical masks for healthcare workers when working within 1–2 m of the patient, and a surgical mask on the patient if transport is necessary. Airborne precautions include standard precautions and a single monitored negative-pressure room, closed door, special high-filtration particulate respirators (N95 or FFP2 mask) for healthcare workers, and movement of the patient, wearing a surgical mask, only when essential. H. Leblebicioglu et al. / International Journal of Infectious Diseases 48 (2016) 113–117 117 2.3. Infection prevention and control recommendations for multicentre cohort study looking at epidemiology, microbiology and risk factors. BMC Infect Dis 2014;14:528. hospitalized patients with a suspected highly contagious tropical 7. Ostholm-Balkhed A, Tarnberg M, Nilsson M, Nilsson LE, Hanberger H, Hallgren infectious disease in the ICU A. Travel-associated faecal colonization with ESBL-producing Enterobacteria- ceae: incidence and risk factors. J Antimicrob Chemother 2013;68:2144–53. 8. van der Bij AK, Pitout JD. 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