How do the contributions of travel and refugee medicine impact infection control currently?

Certain imported infections require specific infection control precautions, whereas many “exotic” tropical infections require only standard precautions.

Infections in recently arrived travelers and immigrants reflect microbe resistance patterns of the visited region, and may not respond to standard empiric treatments. Some of these imported antibiotic resistant bacteria have infection control implications with potential to spread locally.

Finally, travelers may serve as sentinels for emerging infections and resistance genes.

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What elements of travel and refugee medicine need to be adhered to for prevention and control?

The clinician and infection control practitioner need to quickly recognize pathogens associated with common imported infections, as well as less common imported infections associated with person-to-person spread. Common syndromes in the ill returned traveler are presented below. Pathogens with specific infection control implications are presented in more detail.

Fever in the returned traveler

Symptoms, exam findings, and laboratory findings are often non-specific, and vary by region visited. The most common etiologies (and incubation period) include:

Malaria (7 days to 6+ months)

Dengue (typically 4-7 days, range 3-14 days)

Rickettsial disease (7-28 days)

Typhoid and paratyphoid (3-28+ days)*

Chikungunya (3-7 days, up to 12 days)

*Salmonella typhi and paratyphi are transmitted though fecal-oral transmission, and patients and asymptomatic carriers may transmit the disease after return from high prevalence regions (South Asia especially). Healthcare workers, childcare workers, and food handlers should have follow up stool cultures to exclude persistent carriage prior to return to work. Stool carriage may persist for months in a minority of patients, and for over a year in the 1-4% who become chronic carriers.

Other causes of fever in returned travelers include leptospirosis (water exposures), brucellosis (unpasteurized milk products), Q fever (rural travel in farm areas, and unpasteurized milk or cheese), mononucleosis, acute schistosomiasis (fresh water contact, especially in Africa), hepatitis B, and acute HIV (both with sexual contact or blood exposures). In addition to tuberculosis, endemic fungal infections (histoplasmosis), and amoebic liver abscesses may occur in travelers, refugees, and immigrants. Select diseases with infection control implications include:

Meningococcal meningitis may occur in patients returned from the meningitis belt in sub-Saharan Africa and Hajj pilgrims to Mecca. Quinolone resistance has been reported from New Delhi and North Dakota/Western Minnesota, and ciprofloxacin should not be used as post-exposure prophylaxis in imported cases from those regions.

Hepatitis E virus is an emerging worldwide cause of acute hepatitis. Water-borne outbreaks have occurred in multiple geographic regions, and fecal-oral transmission occurs. Severe disease is common in pregnant women, and in persons with liver disease.

Hepatitis A virus is the most common vaccine-preventable disease in travelers, and domestic cases remain associated with recent foreign travel. Post-exposure prophylaxis within 14 days of exposure in contacts under 40 years old may include hepatitis A vaccine rather than immunoglobulin.

Mumps cases have occurred in unimmunized visitors, and have led to large outbreaks in recent years. Many secondary cases had received two vaccine doses. Standard and droplet precautions should be maintained for 5 days after onset of parotiditis.

Measles has been imported from worldwide regions including Europe. Most cases in the U.S. occur in unimmunized individuals. Consider atypical measles in those individuals vaccinated only with inactivated measles vaccine (1963-1967).

Varicella immunity is often lacking in adults from tropical regions (particularly rural regions).

Monkeypox should be considered in travelers with a vesicular rash, fever, and lymphadenopathy after travel to Central Africa. Contact and airborne precautions should be initiated, and public health authorities alerted.

Viral hemorrhagic fever (VHF) is an uncommon cause of fever in travelers, but immediate recognition of patients is necessary since person-to-person transmission may occur. Examples include ebola, Marburg, Rift Valley fever, and Crimean Congo hemorrhagic fever (tick bites). Other hemorrhagic fevers include yellow fever and dengue hemorrhagic fever.

Consider VHF in travelers with fever within 21 days after visits to rural West and Central Africa. Contact precautions are mandatory. Where available, airborne precautions are often used. Some locales use more aggressive infection control precautions.

Respiratory symptoms in the returned traveler, refugee, or immigrant

Respiratory infections are common in travelers. Viruses are the most common pathogens, and routine bacterial pathogens such as Streptococcus pneumoniae, Mycoplasma pneumoniae and Legionella occur. Q fever should be considered in travelers returned from farm regions. Migratory parasitic infections, including Strongyloides, Ascaris, and hookworm can mimic respiratory infection. Immigrants, refugees, and travelers may also be at risk for tuberculosis, histoplasmosis, and paragonimiasis.

Respiratory infections with infection control implications are listed below.

Tuberculosis infection occurs in long-term travelers at a rate of 3.5 per 1000 person-months of travel, and active disease occurs at a rate of 0.6 per person-year in the same population. Foreign-born individuals with reactivation disease will reflect the resistance patterns of their previous region.

Influenza occurs in the southern hemisphere winter and year round in tropical regions.

H5N1 avian influenza has become endemic in domestic poultry and/or wild birds in Asia, the Near East, Europe, and Africa. Sporadic human cases have occurred, though none with the capacity for efficient human-to-human transmission (though limited transmission may have occured rarely).

H7N9 avian influenza emerged in China in 2013, and is associated with poultry exposure. Airborne precautions, eye protection, and contact precautions are recommended. H7N9 should be considered in patients with fever, cough or sore throat and travel to China (or other areas with active disease) within 10 days.

Middle East Respiratory Syndrome (MERS) is caused by a coronavirus that emerged in the Middle East in 2012. Airborne precautions, eye protection, and contact precautions are recommended. It should be considered in patients with fever, cough, signs of pneumonia, and travel to an area with ongoing cases (i.e., The Arabian Peninsula) within 14 days.

Hantavirus is associated with rodent exposures. Person-to-person spread is not common, but has probably occurred with the Andes virus in Argentina.

Melioidosis causes pneumonia (and/or skin infection) in travelers or immigrants from Southeast Asia and Northern Australia. It can present years later; and may occur in the Americas. Notify the microbiology laboratory if diagnosis is considered, both to aid identification and to prevent laboratory worker exposure. Person-to-person spread appears rare.

SARS transmission has not occurred since control of the 2003 outbreak. Unexplained pneumonia in travelers (within 10 days) to China, Hong Kong, or Taiwan, or in healthcare workers exposed to such patients, should prompt notification of the local health department and consideration of testing.

Diphtheria is rare in the U.S., but should be considered in returned travelers with pharyngitis with an adherent membrane, or membrane covered skin ulcers. Seroprotection rates in adults suggest large numbers of at risk persons. Droplet precautions and contact investigations should be initiated for post-exposure antibiotic prophylaxis and monitoring.

Pneumonic plague should be considered in acutely ill patients with travel in the previous week to rural endemic areas in Africa, South and Central Asia, South America, and the Southwestern U.S. Droplet precautions should be undertaken for suspected cases, though this infection is extremely rare in travelers.

Intestinal symptoms in the returned traveler, refugee, or immigrant

The incidence of traveler’s diarrhea is 20-50% in most tropical regions, and most episodes are caused by bacterial pathogens. The most common are enterotoxigenic and enteroaggregative Escherichia coli, Campylobacter jejuni, Salmonella spp., and Shigella spp. A minority of patients develop post-infectious irritable bowel syndrome. Diarrhea developing after travel is most commonly caused by a parasitic infection.

Travelers with diarrhea starting shortly after travel should prompt consideration of the following:

Bacterial pathogens as listed above.

Noroviruses. These are an increasingly recognized cause and/or co-pathogen in traveler’s diarrhea. It has a short incubation (1-2 days), and is transmitted by the fecal-oral route, and aerosolization of vomitus. Environmental cleaning and contract precautions are critical.

Cholera. This is an unusual infection in travelers, but should be considered in patients returning from endemic regions (incubation up to 5 days).

Clostridium difficile. This has occurred in travelers treated with antibiotics for traveler’s diarrhea.

Travelers with diarrhea starting after return should also prompt consideration for parasitic infections.

  • Giardia is the most common cause of diarrhea in returned travelers. Cysts in the stool are infectious.

  • Entamoeba histolytica is the second most common etiology of imported diarrhea-associated parasitic infection. Cysts and trophozoites in stool are infectious.

  • Strongyloides is the third most common parasitic etiology. Immigrants with subsequent immunosuppression (even decades later) may present with hyperinfection syndrome.

  • Campylobacter, Shigella, and Salmonella are the most common bacterial etiologies in returned travelers.

Filariform larvae passed in stool are infectious through human skin.

Other common gastrointestinal parasites

  • Ascaris eggs are not immediately infectious, as they require 18 plus days to embryonate.

  • Taenia solium. The ingestion of eggs passed in gravid proglottids in stool can lead to neurocysticercosis. Eggs can survive weeks in the environment.

Neurologic symptoms in the returned traveler, refugee, or immigrant

Neurologic symptoms are uncommon in returned travelers. Acute symptoms should prompt investigation for meningitis, cerebral malaria, arthropod-borne encephalitis, angiostrongyliasis, African trypanosomiasis (with travel to sub-Saharan Africa), Japanese encephalitis, West Nile, tick borne encephalitis, and rabies.

Chronic symptoms after return should prompt consideration for TB, brucellosis, HTLV-1, African trypanosomiasis, and neurocysticercosis. Neurologic symptoms that start after diarrhea should prompt consideration of ciguatera and marine toxins associated with shellfish ingestion.

  • Rabies should be considered in all returned travelers with altered mental status. Contact precautions with droplet precautions for invasive procedures should be implemented. Organ donation from deceased patients should not be used unless rabies is excluded from potential cases.

  • Meningococcal meningitis caused by quinolone resistant Neisseria has been reported in cases acquired in New Delhi India, North Dakota, and Western Minnesota. Contacts should receive alternative prophylaxis (rifampin, or ceftriaxone). Droplet precautions should be used.

  • Polio remains endemic in Pakistan, Afghanistan, and Nigeria, with some cases from Chad, Angola, Somalia, Camaroon, andn Kenya. Contacts of rare imported cases should undergo assessment for stool testing for virus, and receive a booster IPV. Fecal oral transmission demands contact precautionss.

  • Herpes virus B causes encephalitis after monkey bites or scratches. Patients with vesicular skin lesions may transmit disease.

Neurologic syndromes in immigrants

  • Leprosy is most likely primarily spread by respiratory droplets. Treated patients quickly become non-infectious.

  • Patients with neurocysticercosis are not infectious to others. If the patient or family members are also infected with intestinal Taenia solium, the passed T. solium eggs may persist in the environment and inadvertent ingestion of eggs may lead to neurocysticercosis

Imported antibiotic resistance: travelers are at risk for infection with antibiotic resistant gram-negative Enterobacteriaceae

  • Travel is a risk factor for infection and carriage with ESBL-producing Enterobacteriaceae.

  • Travelers (particularly those with healthcare exposures in South Asia) are at risk for infection with NDM-1 carbapenemase producing Enterobacteriaceae.

  • The role of active surveillance for NDM-1 and ESBL producers in travelers is not well defined.

Immigrant and refugee health

Immigrants and refugees to the U.S. undergo a mandatory medical evaluation prior to arrival. Non-immigrants and travelers do not undergo routine resting.

Immigrants are screened for tuberculosis (chest x-ray), syphilis, leprosy, and STDs.

HIV testing is no longer required.

Refugees and non-immigrant travelers to the U.S. are not required to show proof of vaccinations unless they later apply for permanent residency status. Immigrant visa applicants are required to undergo routine vaccinations, but are only required to receive the first dose by arrival.

  • Refugees from sub-Saharan Africa receive empiric malaria treatment (refugees from other regions are tested if they have symptoms).

  • Refugees receive albendazole and ivermectin (except African refugees from Loa Loa endemic regions, who receive albendazole and praziquantel)

The most common infections in immigrants living in Spain (mostly West African and Latin American origin) were:

  • Filariasis (Onchocerca, Mansonella, Loa Loa): most cases were in sub-Saharan Africans.

  • Intestinal parasites: the most common were Ascaris lumbricoides and Giardia intestinalis.

  • Malaria: mean time 2 months.

  • Chagas.

  • Tuberculosis: latent and active.

  • Chronic hepatitis: particularly Hepatitis B.

  • STDs.

What are the key conclusions from available clinical trials or meta-analyses related to travel and refugee medicine that guide infection control practice and policies?

There is very little data to guide proper infection control practice in returned travelers. Instead, the pathogenesis of various infections is used to predict pathogens at risk for spread.

There is data on the efficacy of protective measures for the individual traveler. For example:

  • Malaria prophylaxis is greater than 95% effective (doxycycline, mefloquine, and atovaquone-proguanil).

  • Vaccine seroprotection and/or efficacy studies are summarized in Table I.

    Seroprotection of travel vaccines

    Disease Product Seroprotection Comment
    Hepatitis A Havrix 99-100% 90% + efficacy after one dose, possibly lower in over 40 year olds.
    VAQTA 99-100% 97% 4 weeks after 1st dose.
    Hepatitis B Engerix-B 96% 88% in over 40 years old.
    Hepatitis A/B Twinrix 99.9% Hep A98.5% Hep B Accelerated series (1, 7, 21-30 day) provides 63% Hep B and 98.5% Hep A seroprotection.
    Typhoid TY21a (oral) Efficacy 60-80% in endemic regions.
    Vi (IM) 88-96% seroconversion in US population; Efficacy in endemic regions 50-74%.
    Yellow fever YF-VAX 95%
    Measles MMR 95% first dose, 99+% two doses Atypical measles in adults immunized before 1968 when have not received live vaccines.
    Mumps MMR 96% first dose Large numbers of mumps cases in the 2005 Iowa outbreak had received two doses of MMR.
    Varicella Seroconversion 99% 2 dose regimen 80% efficacy.
    Meningococcus Menactra and Menveo 97-100% seroconversion Menveo non-inferior with higher titers.
    Menomune 97-99%
    Japanese encephalitis virus Ixiaro 96.4% In a booster study, seroprotection was 69.2% 15 months after primary series.
    JE-VAX 90+%

  • Antibiotic treatment for traveler’s diarrhea is effective in shortening the course of disease.

What are the consequences of ignoring key concepts related to travel and refugee medicine?

Most travel-associated infections do not put other patients and staff at risk. However, failure to recognize infections with potential person-to-person spread may introduce travel associated disease to other patients, staff, and the community.

Travelers may import antibiotic resistant genes and bacteria, with subsequent spread within hospital populations and communities.

Travelers may introduce vector borne diseases if an efficient local vector exists (such as Aedes mosquitoes for Chikungunya, or Anopheles mosquitoes for malaria).

What other information supports the key conclusions of studies of or advice from travel and refugee medicine?

Most conclusions are built on expert opinion and observation. Transmission risk is often estimated based on experience in endemic regions, while risk of transmission of imported disease may vary in hospitals with appropriate infection control precautions.

Summary of current controversies.

There is minimal controversy in the recognition and treatment of ill returned travelers and infection control. The need for routine screening of travelers returned from abroad for carbapenemase and ESBL gene carriage has yet to be determined.

What is the role or impact of travel and refugee medicine relative to the rules or impact of other aspects of infection control?

Routine infection control standards apply to returned travelers who are ill. Most imported infections require standard precautions alone, including hand hygiene compliance. Recognition of syndromes which require contract, droplet, or airborne precautions for imported pathogens reduces subsequent disease transmission risk.

Travelers themselves may practice “infection control” by limiting pathogen exposure though pre-travel vaccination, safe dietary choices, insect avoidance, hand hygiene, and safe sex practices. An effective pre-travel consultation will educate travelers on these issues.

Overview of important clinical trials, meta-analyses, case control studies, case series, and individual case reports related to infection control and travel and refugee medicine.

See Table I.

What national and international guidelines exist related to travel and refugee medicine?

National and international guidelines on the management of travelers, immigrants, and refugees are particularly useful for pre-travel assessments, as well as reviewing prevalent diseases the ill traveler may have been exposed to. Select examples include:

  • The CDC publishes standard recommendations for pre-travel care in the Yellow Book and on the CDC website at www.cdc.gov/travel.

  • The Public Health Agency of Canada publishes recommendations for travel medicine at http://origin.phac-aspc.gc.ca/tmp-pmv/prof-eng.php.

  • The CDC also publishes standards for immigrant and refugee health at www.cdc.gov/immigrantrefugeehealth.

  • The WHO publishes recommendations on travel health at www.who.int/ith.

What other consensus group statements exist and what do key leaders advise?

Additional useful guidelines include:

The IDSA Guidelines for the Practice of Travel Medicine. The IDSA’s guidelines primarily focus on appropriate pre-travel care.

The British National Travel Health Network and Centre provides travel recommendations at http://www.nathnac.org/. Pre-travel care, outbreaks, and helpful lists of frequently asked questions are available.

References

“PROMed mail is a moderated outbreak-reporting source and is maintained by the International Society of Infectious Diseases (www.promedmail.org)”.

“The CDC online Traveler's Health website reports major outbreaks, and is a definitive source for standard pre-travel recommendations (www.cdc.gov/travel)”.

“Country-specific outbreaks can be searched through The British National Travel Health Network and Centre website at http://www.nathnac.org/”.

“The package inserts of FDA approved vaccines are available at: http://www.fda.gov/BiologicsBloodVaccines/Vaccines/ These typically include data on vaccine efficacy and/or seroprotection”.

Mandal, BK, Mukherjee, PP, Murphy, C, Mukherjee, R, Naik, T. “Adult susceptibility to varicella in the tropics is a rural phenomenon due to the lack of previous exposure”. J Infect Dis. vol. 178. 1998. pp. S52-4. (PUBMED:9852974 Varicella immunity in South Asia inhabitants from rural areas is significantly lower than those from urban areas. Presumably, the same would be true of immigrants.)

Marin, M, Quinlisk, P, Shimabukuro, T, Sawhney, C, Brown, C, Lebaron, CW. “Mumps vaccination coverage and vaccine effectiveness in a large outbreak among college students–Iowa, 2006”. Vaccine. vol. 26. 2008. pp. 3601-7. (Many college students infected by a mumps outbreak in 2005 in Iowa had received two doses. Most had received the vaccinations more than 10 years previous. PUBMED:18539365.)

McQuillan, GM, Kruszon-Moran, D, Deforest, A, Chu, SY, Wharton, M. “Serologic immunity to diphtheria and tetanus in the United States”. Ann Intern Med. vol. 136. 2002. pp. 660-6. (Seroprevalence of tetanus and diphtheria antibodies was lacking in a substantial minority of the U.S. population. PUBMED:11992301.)

Parker Fiebelkorn, A, Redd, SB, Gallagher, K. “Measles in the United States during the postelimination era”. J Infect Dis. vol. 202. 2010. pp. 1520-8. (Measles cases in the USA from 2001-2008 are summarized. Imported cases came from diverse worldwide regions. Most, but not all, measles cases were in unvaccinated individuals. PUBMED:20929352.)

Schaffzin, JK, Pollock, L, Schulte, C. “Effectiveness of previous mumps vaccination during a summer camp outbreak”. Pediatrics. vol. 120. 2007. pp. e862-8. (Mumps attack rates during a summer camp outbreak in New York state ranged from 3.6% among those who had previously received two doses of vaccine to 42.9% among the unvaccinated.The index case was an unvaccinated UK resident. PUBMED:1790874.)

Carnie, JA, Lester, R, Moran, R. “Public health response to imported case of poliomyelitis, Australia, 2007”. Emerg Infect Dis. vol. 15. 2009. pp. 1733-7. (The public health response to a case of imported polio is described, including isolatation, post-exposure IPV booster dose, and timing of stool testing for contact groups and patients. PUBMED:19891859.)

“(CDC) CfDCaP. Updated recommendations for isolation of persons with mumps”. MMWR Morb Mortal Wkly Rep. vol. 57. 2008. pp. 1103-5. (Mumps droplet and contact isolation has been shortened from 9 days to 5 days after onset of parotiditis. PUBMED:1884603.)

Crowcroft, N, Brown, D, Gopal, R, Morgan, D. “Current management of patients with viral haemorrhagic fevers in the United Kingdom”. Euro Surveill. vol. 7. 2002. pp. 44-8. (The United Kingdom's approach to infection control for patients with possible or definite viral hemorrhagic fever is presented. PUBMED:12631945.)

Freedman, DO, Weld, LH, Kozarsky, PE. “Spectrum of disease and relation to place of exposure among ill returned travelers”. N Engl J Med. vol. 354. 2006. pp. 119-30. (The Geosentinal Surveillance Network reports the most common diagnoses in travelers presenting for post-travel care to select specialty clinics. PUBMED:16407507.)

Grais, RF, Ellis, JH, Glass, GE. “Assessing the impact of airline travel on the geographic spread of pandemic influenza”. Eur J Epidemiol. vol. 18. 2003. pp. 1065-72. (The influence of modern air travel patterns of disease spread is modeled, highlighting the influence of transportation patterns on pathogen spread. PUBMED:14620941.)

Soumahoro, MK, Fontenille, D, Turbelin, C. “Imported chikungunya virus infection”. Emerg Infect Dis. vol. 16. 2010. pp. 162-3. (The geographic areas of Chikungunya and widespread at-risk areas are presented. PUBMED:20031074.)

Timen, A, Koopmans, MP, Vossen, AC. “Response to imported case of Marburg hemorrhagic fever, the Netherland”. Emerg Infect Dis. vol. 15. 2009. pp. 1171-5. (A case of imported Marburg fever is discussed, along with the subsequent high risk/low risk contact investigation. No secondary cases were identified. PUBMED:19751577.)

Wilson, ME, Weld, LH, Boggild, A. “Fever in returned travelers: results from the GeoSentinel Surveillance Network”. Clin Infect Dis. vol. 44. 2007. pp. 1560-8. (The Geosentinel Surveillance Network reports on common causes of fever in returned travelers, segregrated by geographic region and time since return. Malaria is the most common diagnosis among those returning from sub-Saharan Africa and the Oceania/Pacific Islands region. PUBMED:17516399.)

Koo, HL, Ajami, NJ, Jiang, ZD. “Noroviruses as a cause of diarrhea in travelers to Guatemala, India, and Mexico”. J Clin Microbiol. vol. 48. 2010. pp. 1673-6. (Noroviruses may be an underrecognized cause of traveler's diarrhea, as reported in this study from India, Mexico, and Guatamala. PUBMED:20305012.)

Swaminathan, A, Torresi, J, Schlagenhauf, P. “A global study of pathogens and host risk factors associated with infectious gastrointestinal disease in returned international travellers”. J Infect. vol. 59. 2009. pp. 19-27. (Parasitic infection is the most common etiology in returned travelers with intestinal symptoms who presented to GeoSentinel clinics. Giardia is the most common individual etiology, and other etiologies are reported. PUBMED:19552961.)

Common diseases in immigrants

Monge-Maillo, B, Jiménez, BC, Pérez-Molina, JA. “Imported infectious diseases in mobile populations, Spain”. Emerg Infect Dis. vol. 15. 2009. pp. 1745-52. (The most common diseases in immigrants in Spain are discussed. The immigrant population seeking care includes substantial numbers from Africa, reflected in the high numbers of filarial infection. PUBMED:19891861.)

Antibiotic Resistance

Feodoroff, FB, Lauhio, AR, Sarna, SJ, Hänninen, ML, Rautelin, HI. “Severe diarrhoea caused by highly ciprofloxacin-susceptible Campylobacter isolates”. Clin Microbiol Infect. vol. 15. 2009. pp. 188-92. (Patients infected by quinolone-resistant Campylobacter had frequently traveled outside of Finland. PUBMED:19154485.)

Kumarasamy, KK, Toleman, MA, Walsh, TR. “Emergence of a new antibiotic resistance mechanism in India, Pakistan, and the UK: a molecular, biological, and epidemiological study”. Lancet Infect Dis. vol. 10. 2010. pp. 597-602. (Infection in UK residents by NDM-1 producing Enterobacteriaceae is associated with recent travel and/or medical care in India and Pakistan. PUBMED:20705517.)

Kuster, SP, Hasse, B, Huebner, V. “Risks factors for infections with extended-spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae at a tertiary care university hospital in Switzerland”. Infection. vol. 38. 2010. pp. 33-40. (This is a case control study which identifies recent foreign travel as a risk factor for infection with ESBL-producing Enterobacteriaceae, relative to infection with non-ESBL producing strains. Nine of the 10 patients whose infections started abroad were infected by an ESBL-producer. PUBMED:20108162.)

Lapadula, G, Viganò, F, Fortuna, P. “Imported ciprofloxacin-resistant Neisseria meningitidis”. Emerg Infect Dis. vol. 15. 2009. pp. 1852-4. (Ciprofloxacin resistance was noted in a case of meningitis likely acquired in India. Post exposure prophylaxis from regions with potential quinolone resistance should not use quinolones. PUBMED:19891885.)

Tängdén, T, Cars, O, Melhus, A, Löwdin, E. “Foreign travel is a major risk factor for colonization with Escherichia coli producing CTX-M-type extended-spectrum beta-lactamases: a prospective study with Swedish volunteers”. Antimicrob Agents Chemother. vol. 54. 2010. pp. 3564-8. (Frequent colonization with ESBL-producing Enterobacteriaceae was noted during international travel. PUBMED:20547788.)

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