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Imported Diseases and Infectious Disease Surveillance. George Turabelidze, MD, PhD Missouri Department of Health and Senior Services. International Tourism. Popularity of international tourism continues to grow Growth of travel to developing countries exceeds travel growth to developed world

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imported diseases and infectious disease surveillance

Imported Diseases and Infectious Disease Surveillance

George Turabelidze, MD, PhD

Missouri Department of Health and Senior Services

international tourism
International Tourism
  • Popularity of international tourism continues to grow
  • Growth of travel to developing countries exceeds travel growth to developed world
  • A list of exotic destinations and extreme travel activities is also growing
  • Exposure to diseases rare in the developed countries is rising
world tourism 2005
World Tourism, 2005
  • International tourist arrivals in 2005 hit all-time record of 800 million
  • The 2005 results represent a 5.5% increase worldwide; higher than the long-term average annual growth rate of 4.1%
  • Tourism to Asia/Pacific, Middle East, and Africa expected to grow at higher rate compared to average worldwide growth rate
  • International arrivals are forecasted to reach 1.6 billion by year 2020

UN World Tourism Organization, 2006

travel increase by region 2005
Africa – 9%

Asia/Pacific – 8%

Middle East – 8%

Americas – 6%

Europe – 4%

Only region without increase in international arrivals in the last 5 years was North America (-.3%)

Travel Increase by Region, 2005

UN World Tourism Organization, 2006

risk of illness in travelers
Risk of Illness in Travelers
  • From 22 to 64% of travelers to the developing world report some kind of health problem(Steffen et al., 2003)
  • Up to 8% of all American travelers to developing world seek medical care; each day of travel carries 3-4% risk of illness(Hill, 2000)
  • About 26%-27% of febrile travelers will needhospitalization(Wilson et al.2007, Bottieau et al., 2006)
risk of illness in travelers8
Risk of Illness in Travelers
  • According to US Department of Commerce, about 12 million US residents, or 4% of total US population, traveled to the developing world in 2006
  • About 220,000 Missourians could have been travelers to the developing world in 2006
  • An estimated 17,000 Missourians would seek medical care after the travel
extreme travel
Extreme Travel
  • Defined as travel to remote destinations or participating in unusual high-risk activities during travel
  • The average age of adventure traveler is 32 years (44 years for the American traveler as a whole)
  • The risk of illness increases with longer duration and more remote travel
surveillance of imported diseases
Surveillance of Imported Diseases
  • Detection of sentinel events in travelers can lead to outbreak detection
  • Travelers serve as surveillance tool for imported diseases
  • Travelers could be a warning sign for disease outbreaks in developing countries
  • Cluster of infections in returning travelers could warn of specific risk to new travelers to that destination(s) and increase their protection
imported diseases surveillance networks
Imported Diseases Surveillance Networks
  • GeoSentinel – clinical surveillance data on travelers from six continents
  • TropNetEurop – clinician-basedEuropean Network on Imported Infectious Disease Surveillance
  • DoD GEIS – syndromic surveillance by US DoD Global Emerging Infections System
  • Quarantine Activity Reporting System (QARS), a web-based secure electronic system
  • Public Health departments surveillance

Quarantine Stations

  • 18 U.S. Quarantine Stations (QS) based at major ports of entry and land border crossings in 2006
  • Foreign Quarantine Regulations (Title 42 CFR Part 71)
    • Required reportable syndromes by conveyance operators entering U.S. ports:
        • Fever ≥ 100°F (37.8°C) > 48 hours
        • Fever + rash
        • Fever + glandular swelling
        • Fever + jaundice
        • Diarrhea (≥ 3 or more loose stools in a 24 hour period)
    • Recommended reportable syndromes by conveyance operators entering U.S.
        • Fever + abnormal bleeding
        • Fever + cough or difficulty breathing
        • Fever + head or neck pain
final diagnoses of deaths and illnesses reported in qars during and after travel 2006
Final Diagnoses of Deaths and Illnesses Reported in QARS During and After Travel, 2006

Kornylo, et al., CDC, CSTE Presentation, 2007

fever after stay in the tropics
Fever After Stay in the Tropics
  • 1743 febrile patients were prospectively followed at the Institute of Tropical Medicine in Antwerp, Belgium (Bottieau et al.,2006)
  • Tropical diseases –39%, cosmopolitan –34%, and unknown –24%
  • Africa – malaria (35%), rickettsiosis (4%) Asia– dengue (12%), malaria (9%), enteric fever – (4%) Latin America– dengue (8%), malaria (4%)
fever in returned travelers
Fever in Returned Travelers
  • 6957febrile travelers (GeoSentinel, 1997-2006 data)
  • 35% with systemic febrile illness, 22% unspecified fever,15% diarrhea, 14% respiratory, and 10% other diagnosis
  • Malaria most common, followed by dengue, enteric fever, rickettsiosis
  • Malaria overwhelmingly more common in visitors to Pacific Islands and sub-Saharan Africa
  • Enteric fever common in south-central Asia travelers, whereas rickettsioses in southern Africa travelers

Wilson et al, 2007

travel related hospitalization
Travel-Related Hospitalization
  • Most common diagnoses in 211 travelers hospitalized in 1999-2003 in Israel: malaria (26%), unspecified fever (16%), dengue (13%), diarrhea (11%), leishmaniasis (9%)
  • Most common by destination: Africa - malaria, FUO, diarrhea Asia - dengue, FUO, diarrhea Latin America - leishmaniasis, malaria, FUO

Stienlauf, et al.,2005

imported diseases in relation to traveler s place of exposure
Imported Diseases in Relation to Traveler’s Place of Exposure
  • GeoSentinel’s clinical data (30 sites) on 17,353 ill travelers returning from six developing regions, 1996-2004
  • 67% of all travelers with four syndromes: fever, acute diarrhea, rash, chronic diarrhea
  • Malaria, dengue, mononucleosis, rickettsiosis, typhoid fever most common in fever patients
  • Travel destinations were associated with the probability of certain diseases

Freedman et al., 2006

imported diseases in relation to traveler s place of exposure20
Imported Diseases in Relation to Traveler’s Place of Exposure
  • Fever: sub-Saharan Africa, southeast Asia
  • Acute diarrhea: south central Asia
  • Rash: Caribbean, Central/South America
  • Parasite-induced diarrhea more common than bacterial in all regions except southeast Asia
  • Rickettsiosis more common than typhoid or dengue in sub-Saharan travelers

Freedman et al., 2006

specific diagnoses within selected syndromes
Specific Diagnoses within Selected Syndromes
  • Fever:malaria, dengue, EBV, rickettsiosis, typhoid fever
  • Acute diarrhea: parasitic (giardiasis, amebiasis), bacterial (campylobacter, shigella, salmonella)
  • Rash:insect bite, cutaneous larva migrans, allergic rash, skin abscess, mycosis, leishmaniasis, myiasis, swimmer’s itch, impetigo, scabies

Modified from Freedman et al., 2006

top etiologic diagnoses by region
Top Etiologic Diagnoses by Region
  • Carribean:cutaneous larva migrans, dengue, insect bite, giardiasis, strongyloidosis, amebiasis
  • Central America:insect bite, cutaneous larva migrans, amebiasis, strongyloidosis, giardiasis, malaria, dengue, myasis
  • South America:giardiasis, insect bite, amebiasis, leishmaniasis, dengue, malaria cutaneous larva, strongyloidosis, myasis, campylobacter
top etiologic diagnoses by regions
Top Etiologic Diagnoses by Regions
  • Africa:malaria, insect bite, giardiasis, strongyloidosis, amebiasis, skin abscess
  • South Asia:giardiasis, insect bite, dengue, skin abscess, malaria, enteric fever, amebiasis, campylobacter
  • Southeast Asia: dengue, campylobacter, insect bite, cutaneous larva, malaria, skin abscess, giardiasis
  • Other regions: malaria, insect bite, amebiasis, giardiasis, skin abscess
most common tropical infections by time interval between return date and fever onset
Most Common Tropical Infections by Time Interval Between Return Date and Fever Onset
  • < 1 month:falciparum malaria, rickettsiosis, dengue, non-falciparum malaria, acute schistosomiasis, enteric fever
  • 1-3 months:non-falciparum malaria, falciparum malaria, acute schistosomiasis, helminthic eneteritis
  • 4-12 months:non-falciparum malaria, falciparum malaria, protozoan enteritis
  • Data from 1962 tropical travelers seen in outpatient and inpatient settings in Antwerp, Belgium from 2000 to 2005 (Bottieau et al., 2007)
relative risk for travelers
Relative Risk for Travelers
  • High: viral diarrhea, E.coli enteritis, URI
  • Moderate:malaria (w/o prophylaxis), salmonella, shigella, campylobacter, giardiasis, amebiasis, hepatitis A, dengue, EBV, gonorrhea, chlamydia, herpes simplex
  • Low:malaria (with prophylaxis), leptospirosis, typhoid, cholera, HIV, HBV, syphilis, Lyme, schistosomiasis, TB, helminthosis, ricckettsiosis, borelliosis, measles
  • Very low:anthrax, plague, VHF, tularemia, melioidosis, legionella, yellow fever, rabies, poliomyelitis, diphtheria, trypanosomiasis, trichinosis,, filariasis, toxocariasis, echinococcosis, gnathostomiasis

Adapted from Spira, 2003

approaching public health report of traveler with illness
Approaching Public Health Report of Traveler with Illness
  • Person (demographics, vaccinations, chemoprophylaxis)
  • Place (travel region, exposures)
  • Time (travel dates, exposure dates, incubation period)
immunizations for travelers
Immunizations for Travelers
  • Routine vaccinations
  • Required:Yellow fever, meningococcal (Saudi Arabia)
  • Recommended:Hepatitis A and B, japanese encephalitis, meningococcal, rabies, tick-borne, encephalitis, typhoid, varicella
chemoprophylaxis for travelers
Chemoprophylaxis for Travelers
  • Malaria (doxycycline, mefloquine, cloroquine, primaquine, etc.)
  • Traveler’s diarrhea (rifaximin, ciprofloxacin, azithromycin)
  • Leptospirosis (doxycycline)
  • Rickettsiosis (doxycycline)
exposure based risk factors ingestion
Exposure-based Risk Factors,Ingestion
  • Untreated water – hepatitis A/E, salmonella, shigella, giardia, poliomyelitis, amoebiasis, cryptosporidium, cyclospora, dracunculiasis, cholera, typhoid fever
  • Unpasteurized dairy – brucellosis, salmonellosis, Q fever, shigella, listeriosis
  • Undercooked food – salmonellosis, shigella, E.coli, campylobacter, trichinosis, helminthosis, amoebiasis, toxoplasma
exposure based risk factors insect exposure
Exposure-based Risk Factors,Insect Exposure
  • Mosquitoes – malaria, dengue, yellow fever, encephalitis, filariasis
  • Lice – epidemic typhus, relapsing fever, trench fever
  • Fleas – plague, murine typhus
  • Ticks – Lyme disease, babesiosis, ehrlichiosis, rickettsiosis, encephalitis, Q fever, tularemia, Crimean-Congo hemorrhagic fever
  • Mites – scrub typhus, scabies
  • Sandflies – leishmaniasis, bartonellosis, filariasis
  • Flies, tsetse – trypanosomiasis, onchocerciasis
exposure based risk factors animal contact
Exposure-based Risk Factors,Animal Contact
  • Animal mammal contact – anthrax, rabies, Q fever, typhus, tularemia, brucellosis, leptospirosis, echinococcosis
  • Contact with/aerosolization of rodent urine – Lassa fever, hantavirus, leptospirosis
  • Exposure to birthing products – Q fever, brucellosis
  • Exposure to animal hides - anthrax
exposure based risk factors recreation
Exposure-based Risk Factors, Recreation
  • Freshwater exposure –leptospirosis, schistosomiasis, melioidosis, acanthamoeba, naegleria
  • Soil exposure or ingestion – anthrax, helminthosis, cutaneous larva migrans, melioidosis
  • Sexual contact – HIV, hepatitis B/C, syphilis, gonorrhea, herpes
  • Airborne – influenza, measles, tuberculosis
  • IDU/Transfusions – HIV, hepatitis B and C, malaria, toxoplasmosis, babesiosis
  • Ill contacts– TB, EBV, meningitis, Lassa, pneumonia
extreme traveler s risk by exposure
Extreme Traveler’s Risk by Exposure
  • Salt water exposure: skin infection with M.marinum, Aeromonas, V.vulnificus
  • Freshwater exposure (including white water rafting): leptospirosis, schistosomiasis
  • Remote trekking: traveler’s diarrhea, rickettsiosis, rabies
  • Spelunking (caving): histoplasmosis, rabies
  • Cycling: rabies
incubation periods of travel associated infectious diseases short 10 days
Arboviral infections



Enteric bacterial

Enteric viral

Fungal respiratory








Q fever




Viral hemorrhagic fever

Incubation Periods of Travel –Associated Infectious Diseases, Short (< 10 days)
incubation periods of travel associated infectious diseases medium 10 21 days
Acute HIV

American trypanosomiasis



Enteric protozoa

Q fever


Lyme disease




Typhoid fever

Viral hemorrhagic fever

Incubation Periods of Travel –Associated Infectious Diseases, Medium (10-21 days)
incubation periods of travel associated infectious diseases long 21 days
African trypanosomiasis



Hepatitis A, B, and E


Enteric protozoa





Typhoid fever


Incubation Periods of Travel –Associated Infectious Diseases, Long (>21 days)
incubation periods of travel associated infectious diseases variable weeks years









Incubation Periods of Travel –Associated Infectious Diseases, Variable (weeks-years)
  • Malaria is among top three causes of fever in travelers to every region in the developing world
  • Incidence in the United States is about 1200 cases per year; 63 episodes of introduced malaria were detected from 1957 to 2003
  • In most severe cases presentation could be similar to hemorrhagic fever illness, such as caused by Ebola virus
  • Diagnosis of malaria is ruled out only after sequential blood smear testing!
  • Caused by flavivirus transmitted by urban mosquito
  • 329 confirmed cases in US travelers in 1996-2005
  • Four serotypes of virus; immunity to one serotype is not cross-protective
  • Infection ranges from subclinical form to influenza-like to severe with bleeding and shock
  • Previous dengue infection increases risk of dengue hemorrhagic fever with subsequent infection
  • Anti-dengue antibodies cross-react with anti-WNV,-yellow fever, -JE, -other flavivirus antibodies
rickettsioses in travelers
Rickettsioses in Travelers
  • Tick-borne rickettsiosis should be suspected in febrile travelers, especially if rash is present
  • Vast majority of travelers with rickettsiosis have African tick bite fever (R.africae) or Mediterranean spotted fever (R.conorii)
  • In 530 German travelers with fever who traveled to southern Africa, 11% had serological evidence of recent rickettsial infection(Jelinek T, Loscher T, 2001)
  • In Swedish travelers to southern Africa, risk of rickettsiosis was 4 to 5 times higher than risk of malaria(Raeber PA, et al., 2003)

Western blot of pooled mouse antisera to R.africae – human isolate (lane 1),

R.africae – tick isolate (lanes 2–4), R.conorii – Kenyan strain (lane 5),

R.conorii – Moroccan strain (lane 6) and Israeli SFG rickettsia (lane 7).

report of febrile illness
Report of Febrile Illness

A 29 year old man from Columbia, MO was admitted to a local hospital with a one-day history of fever 104°F, headache, nausea, and vomiting. Two days prior to admission he flew from New York City to St. Louis on commercial airline. According to the patient, one of the passengers who was sitting a few rows behind him was “coughing a lot,” and the patient was convinced that he became infected on the plane. The patient also suspected that the “coughing passenger” was traveling from abroad and that he was probably “spreading unusual disease”. The patient and his family requested a public health investigation and wanted to pursue legal action against the airline for letting an “infectious passenger” on board of the aircraft.

cabin airflow patterns
Cabin Airflow Patterns
  • Sterile air entering
  • Heating/cooling
  • HEPA filters
  • High airflow rates
  • Laminar airflow
  • Frequent exchanges

World Health Organization, 2006

infections transmitted on commercial airlines number of reports
Food-borne Cholera – 3 Salmonellosis – 15 Staphylococcal – 8 Shigellosis – 3 Viral enteritis – 1

Vector-borne Malaria – 7 Dengue – 1

Airborne/fomitesInfluenza – 2 Measles – 3 Meningococcal – 0 SARS – 4 Smallpox – 1

Tuberculosis - 2

Infections Transmitted on Commercial Airlines (number of reports)
cabin air quality
Cabin Air Quality
  • No scientific evidence currently exists that links cabin air quality to heightened health risks compared with other modes of transport or with office buildings
  • Existing data suggests that risk of transmission for airborne infections on the aircraft is associated with sitting within two rows of a contagious passenger for a flight time of more than 8 hours


Travel Destinations








South Central




Other Developing Countries

  • Diarrhea, Acute
  • Rash
  • Diarrhea, Chron
  • Fever, Systemic
  • Rash
  • Diarrhea, Acute
  • Fever, Systemic
  • Diarrhea, Chron
  • Rash
  • Diarrhea, Acute
  • Fever, Systemic
  • Diarrhea, Chron
  • Fever, Systemic
  • Diarrhea, Acute
  • Rash
  • Diarrhea, Acute
  • Diarrhea, Chron
  • Fever
  • Rash/GI Illness
  • Fever, Systemic
  • Rash/Diarrhea
  • Acute
  • Diarrhea, Chron
  • Diarrhea, Acute
  • Fever, Systemic
  • Rash/Diarrhea,
  • Chronic



Ingestion – Animal – Recreational - Insects



Incubation Period



(<10 days)


(10 – 21 days)


(>21 days)


(weeks, years)

Laboratory and other tests


report of febrile illness56
Report of Febrile Illness
  • About 3 months prior to admission to the hospital patient traveled to Venezuela to see Angel Falls
  • Exposures: freshwater, mosquitoes
  • He received yellow fever vaccination
  • He took malaria chemoprophylaxis
  • You suspect malaria, but patient is not tested because he was given malaria chemoprophylaxis
  • You insist on malaria test, and…. you are correct! Plasmodium vivax detected!