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Abstract

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

Background. The Centers for Disease Control and Prevention's (CDC) Quarantine Activity Reporting System (QARS), which documents reports of morbidity and mortality among travelers, was analyzed to describe the epidemiology of deaths during international travel.

Methods. We analyzed travel-related deaths reported to CDC from July 1, 2005 to June 30, 2008, in which international travelers died (1) on a U.S.-bound conveyance, or (2) within 72 hours after arriving in the United States, or (3) at any time after arriving in the United States from an illness possibly acquired during international travel. We analyzed age, sex, mode of travel (eg, by air, sea, land), date, and cause of death, and estimated rates using generalized linear models.

Results. We identified 213 deaths. The median age of deceased travelers was 66 years (range 1–95); 65% were male. Most deaths (62%) were associated with sea travel; of these, 111 (85%) occurred in cruise ship passengers and 20 (15%) among cargo and cruise ship crew members. Of 81 air travel-associated deaths, 77 occurred in passengers, 3 among air ambulance patients, and 1 in a stowaway. One death was associated with land travel. Deaths were categorized as cardiovascular (70%), infectious disease (12%), cancer (6%), unintentional injury (4%), intentional injury (1%), and other (7%). Of 145 cardiovascular deaths with reported ages, 62% were in persons 65 years of age and older. Nineteen (73%) of 26 persons who died from infectious diseases had chronic medical conditions. There was significant seasonal variation (lowest in July–September) in cardiovascular mortality in cruise ship passengers.

Conclusions. Cardiovascular conditions were the major cause of death for both sexes. Travelers should seek pre-travel medical consultation, including guidance on preventing cardiovascular events, infections, and injuries. Persons with chronic medical conditions and the elderly should promptly seek medical care if they become ill during travel.

International travel has become increasingly common, accessible, and affordable.1,2 In 2010, there were 711 million international outbound trips worldwide, a 7% increase from 2009.3 The number of international visitors to the United States rose to a record 60 million in 2010.4 This growth has provided more opportunities for pathogens to spread beyond geographic and political borders and has increased interest in preventing morbidity and mortality among international travelers.

Previous studies of United States, Canadian, Scottish, and Australian civilians who died abroad have analyzed expatriate death reports at consulates, embassies, and government agencies.5–17 Few studies have addressed passenger mortality during commercial travel on aircraft and cruise ships.18–25 The U.S. Department of State (DOS) Web site lists data on some U.S. citizens who die in a foreign country because of non-natural causes (eg, injuries).26 However, this Web site does not include all deaths of U.S. military or government officials abroad, and DOS may not be notified about deaths of U.S. citizens who reside abroad.

The Centers for Disease Control & Prevention's (CDC) Division of Global Migration and Quarantine (DGMQ) has statutory authority to make and enforce regulations to prevent the introduction or transmission of communicable diseases into the United States.27 The 20 CDC DGMQ quarantine stations have jurisdiction over all U.S. land border ports, seaports, and airports.28 The U.S. Code of Federal Regulations mandates that the pilot or captain of an international aircraft or ship reports illnesses and deaths occurring aboard the vessel to the nearest CDC quarantine station.29 This reporting requirement does not apply to U.S. land borders, private physicians, hospitals, or clinics. U.S. Customs & Border Protection (CBP), domestic health departments, and others voluntarily report illnesses and deaths among international travelers to CDC quarantine stations.27

Our objective was to analyze data on public health investigations of death in international travelers arriving in the United States, and to describe the epidemiology of travelers' deaths reported to CDC quarantine stations.

Methods

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

We examined data from the CDC Quarantine Activity and Reporting System (QARS), a secure online database developed by CDC in 2005 to track illnesses and deaths among inbound international travelers of any citizenship entering the United States and that are reported to CDC quarantine stations. These QARS reports include individual traveler demographic data, clinical summaries, and travel itineraries. For reported deaths, quarantine station staff also collect information on the presumptive cause of death, chronic medical conditions, and when available, the official cause of death. This investigation was approved by CDC with a non-research determination.

We defined a case as a travel-related death for which a QARS report was entered from July 1, 2005 through June 30, 2008, in which the international traveler died (1) on a U.S.-bound conveyance (aircraft, ship, or vehicle), or (2) within 72 hours after arriving in the United States, or (3) at any time after arriving in the United States from an illness possibly acquired during international travel. We extracted the following data from QARS reports: demographics (age and sex), mode of transportation (aircraft, ship, land vehicle, or pedestrian), location of death, travel dates, traveler type (ie, passenger or crew member), citizenship, presence of chronic medical conditions, and cause of death. When data were missing from QARS death reports, we contacted CDC quarantine stations, medical examiners' offices, and hospitals to complete case reports. Data were entered into a Microsoft Excel® database. Causes of death were categorized as cancer, cardiovascular, infectious disease, unintentional injury, intentional injury, and other (Table 1).

Table 1.  Cause of death categories and definitions
Cause of death categoryDefinition
CardiovascularAny cardiovascular condition, including atherosclerotic heart disease, stroke, myocardial infarction, hypertensive heart disease, pulmonary embolism, congestive heart failure, cardiac arrhythmia, coronary artery disease, ischemic heart disease, aortic stenosis, aortic aneurysm, cardiomyopathy, myocardial fibrosis, and others
Infectious diseaseAny illness resulting from a communicable pathogen, such as bacteria (including mycobacteria), viruses, and fungi
CancerAny malignant neoplasm, including adenocarcinoma, carcinoid tumor, liver cancer, lung cancer, lymphoma, melanoma, and thyroid cancer
Unintentional injuryAny unintended damage to the body caused by an outside agent or force, such as occupational injury (crush injury, methanol intoxication, and strangulation), or drug overdose, hypoxic encephalopathy, and recreational injury
Intentional injuryAny intended damage to the body caused by an outside agent or force, including suicide (alcohol and narcotic overdose, hanging)
OtherAny causes of death that could not be grouped into the above categories, including asthma, chronic obstructive pulmonary disease, cirrhosis, neurodegenerative condition, and undetermined causes of death

Death rates for passengers on international commercial conveyances were calculated for each year, by conveyance type. To present full, continuous yearly data (ie, four quarters) and to adjust for seasonality, we defined year 1 as July 1, 2005 to June 30, 2006; year 2 as July 1, 2006 to June 30, 2007; and year 3 as July 1, 2007 to June 30, 2008. We defined quarter 1 as January to March, quarter 2 as April to June, quarter 3 as July to September, and quarter 4 as October to December. To calculate mortality rates for cruise ship passengers, we divided the total number of reported cruise ship passenger deaths that met the case definition by the number of cruise passenger-nights traveled. We calculated the denominator by using data from the U.S. Maritime Administration (MARAD) for cruises with an international itinerary and a port of arrival in the United States during years 1, 2, and 3.30

To determine mortality rates for commercial aircraft passengers, we divided the total number of reported commercial aircraft passenger deaths that met the case definition by the number of airline passengers arriving in the United States from foreign ports. Denominator data were obtained from the U.S. Bureau of Transportation Statistics (BTS).31 Since MARAD and BTS do not collect data for crew members from cruise lines or airlines, respectively, we were unable to calculate crew mortality rates.

We conducted bivariate analysis by using likelihood ratio chi-square tests, both asymptotic and exact, to evaluate associations between sex and cause of death. We analyzed monthly, quarterly, and yearly death rates among commercial aircraft and cruise ship passengers from July 2005 through June 2008 by using a general linear regression model in SAS (SAS 9.2, SAS Institute, Inc., Cary, NC, USA) to assess seasonality and trends in death rates over time.

Results

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

From July 1, 2005, through June 30, 2008, 4,525 case reports of illnesses and deaths among travelers were entered into QARS. The number of reports increased from 1,467 in year 1 to 1,730 in year 3. During years 1 to 3, 242 reported deaths were entered into QARS; of these, 213 (88%) met our case definition. The median age of deceased travelers was 66 years (range 1–95). Demographic characteristics of deceased travelers were stratified by timing of death relative to travel (Table 2). Although all cases were symptomatic on a conveyance, 190 (89%) persons died onboard a conveyance, 18 (8%) at a hospital, 4 (2%) at an airport, and 1 (<1%) at a residence. Most deaths, 131 (62%), were associated with maritime travel. Autopsies were obtained in only 36 (17%) of 213 deaths.

Table 2.  Demographics of deceased travelers reported in QARS stratified by place and time of death relative to travel, July 1, 2005 to June 30, 2008 (N = 213)
DemographicTotalPlace and time of death
Aboard US-bound conveyance≤72 Hours after arrival in United States>72 Hours after arrival in United States
NPercentNPercentNPercentNPercent
  1. QARS = Quarantine Activity Reporting System.

  2. *Includes Barbados (1), Belarus (1), Brazil (2), China (2), Egypt (1), Germany (2), Haiti (1), Honduras (1), Iran (1), Japan (1), Latvia (1), Malaysia (1), Myanmar (1), Pakistan (1), Peru (1), Portugal (1), South Korea (1), Sudan (2), The Netherlands (1), Ukraine (1), Venezuela (1).

Total deaths213100.0190100.020100.03100.0
Sex
 Male13965.312565.81260.0266.7
 Female7334.36433.7840.0133.3
 Not reported10.510.500.000.0
Age (y)
 Median (range)66 (1–95)68 (1–95)57 (3–86)53 (47–64)
 Not reported31.431.600.000.0
Race
 White10046.98946.81050.0133.3
 Black3315.573.715.000.0
 Asian83.82915.3420.000.0
 Not reported7233.86534.2525.0266.7
Ethnicity
 Non-Hispanic14467.613269.51155.0133.3
 Hispanic157.0115.8420.000.0
 Not reported5425.44724.7525.0266.7
Traveler type
 Air passenger8037.66534.21470.0133.3
 Air stowaway10.510.500.000.0
 Maritime passenger11152.110655.8315.0266.7
 Maritime crew209.4189.5210.000.0
 Land border crosser10.500.015.000.0
Passport country
 United States8539.97841.1525.0266.7
 Canada52.352.600.000.0
 India52.331.6210.000.0
 Mexico41.921.1210.000.0
 Philippines41.942.100.000.0
 United Kingdom31.431.600.000.0
 Other*2511.72111.1420.000.0
 Not reported8238.57438.9735.0133.3

Causes of death were reported as cardiovascular 149 (70%), infectious disease 26 (12%), cancer 13 (6%), unintentional injury 9 (4%), intentional injury 2 (1%), and other 14 (7%) (Figure 1). Pneumonia was the most common infectious etiology, causing, contributing, or associated with 14 (53%) infectious disease deaths. Of 26 infectious disease deaths, 14 (54%) were attributed to specific infections (Table 3), and 19 (73%) were associated with one or more chronic medical conditions (Table 4).

image

Figure 1. Causes of death by category reported to QARS, July 1, 2005 to June 30, 2008 (N = 213). QARS = Quarantine Activity Reporting System.

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Table 3.  Infections identified in deaths from infectious disease reported in QARS, July 1, 2005 to June 30, 2008 (N = 26)
InfectionTotal
NPercent
  1. QARS = Quarantine Activity Reporting System.

HIV/AIDS27.7
Neisseria meningitidis27.7
Burkholderia pseudomallei13.8
Hepatitis C (chronic)13.8
Haemophilus spp. bacteremia13.8
HIV and Streptococcus pneumoniae13.8
Klebsiella pneumoniae13.8
Leptospira spp. and cytomegalovirus13.8
Neisseria gonorrhoeae (disseminated) and hepatitis C (chronic)13.8
Rabies13.8
Streptococcus spp. (non-pneumococcal)13.8
Viral hepatitis (unspecified)13.8
Unknown1246.2
Total26100.0
Table 4.  Chronic medical conditions present in infectious disease deaths reported to QARS, July 1, 2005 to June 30, 2008 (N = 26)
Medical conditionTotal
NPercent
  1. QARS = Quarantine Activity Reporting System.

  2. *Some persons had >1 underlying condition.

  3. No weight or height data were reported to QARS.

Any chronic medical condition*1973.1
Chronic cardiac disease519.2
Chronic lung disease415.4
Diabetes mellitus519.2
HIV/AIDS311.5
Autoimmune disease27.7
Chronic liver disease311.5
Immune-suppressing medication13.8
Hypertension623.1
Thymic dysplasia13.8
Solid organ transplantation27.7
Malnutrition13.8
Obesity13.8
Morbid obesity27.7
Alcohol abuse27.7
Chronic disease—other or unspecified726.9

When comparing the two most common causes of death, cardiovascular and infectious disease, we found that travelers who died of infectious disease were significantly younger than those who died from cardiovascular conditions (median age of 49 vs. 67 y, p = 0.002). Sixty-two percent of cardiovascular deaths occurred in persons ≥65 years of age. Five deceased travelers were younger than 18 years of age; they died from pneumonia, rabies, sepsis, cardiac arrhythmia, and a neurodegenerative condition.

The nine unintentional injury deaths included three occupation-related deaths in cargo ship crew members, four drug overdoses (three in passengers and one in a crew member), one recreational injury (in a cruise ship passenger), and one hypoxic encephalopathy (in an aircraft stowaway). Both intentional injury deaths were suicides. Maritime crew members were significantly more likely to die from unintentional injury than were maritime passengers (4 of 20 vs. 4 of 131, respectively; relative risk = 6.29; 95% CI 1.74–22.82; p < 0.05), with no difference in risk for crew members on cruise or cargo ships.

Of the 81 air travel-associated deaths, 77 were airline passengers, 3 were patients undergoing air medical evacuation to the United States, and 1 was an aircraft stowaway; none were crew members. Only one death was associated with land travel, and this person died of rabies.

We calculated an airline passenger death rate of 0.33 deaths per 1 million passengers during years 1 to 3. There was no seasonality or change in airline passenger death rates by year. After the data were controlled for seasonality of deaths, the annual airline passenger death rate remained steady at 0.32 to 0.34 per million passengers per year during the 3-year period.

The overall cruise ship passenger death rate from July 1, 2005 through June 30, 2008 was 0.60 deaths per million cruise passenger-nights. The cruise ship passenger death rates declined significantly during each year's third quarter (p = 0.0025; Figure 2). However, the cruise ship passenger death rates increased significantly, from 0.37 to 0.82 deaths per million passenger-nights from year 1 to year 3 (p = 0.0094).

image

Figure 2. Quarterly death rates in cruise ship passengers per million passenger-nights, reported to QARS, July 1, 2005 to June 30, 2008. QARS = Quarantine Activity Reporting System. Quarter 1: January-March; Quarter 2: April-June; Quarter 3: July-September; Quarter 4: October-December.

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The rate of cardiovascular deaths among cruise ship passengers increased significantly from 0.27 to 0.66 per million passenger-nights over the 3-year period (p = 0.0088) and decreased every third quarter (significant seasonality) (p = 0.0055). In contrast, the rate of non-cardiovascular deaths among cruise ship passengers did not differ significantly by year for years 1 to 3 (range 0.1–0.18 per million passenger-nights).

Discussion

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

This analysis represents the first comprehensive investigation of causes of death among international travelers arriving in the United States on conveyances. Our investigation showed that cardiovascular conditions were the major cause of death for travelers of both sexes. This finding is consistent with an earlier report that the most common cause of death for U.S. travelers abroad in 1975 and 1984 was cardiovascular disease.9 From 2005 to 2007, approximately one third of deaths in the U.S. population were attributed to cardiovascular disease (including stroke).32–34 In contrast, 70% of the deaths in our investigation were attributed to cardiovascular conditions, which is more than twice the proportion of cardiovascular deaths for the U.S. population.

Infectious disease caused 12% of the deaths in our investigation, but only one of these deaths, which occurred in an HIV-positive person with pneumococcal pneumonia, may have been preventable by vaccination.35 The other three persons who died from vaccine-preventable diseases (two meningococcal meningitis and one rabies) did not meet the vaccination criteria of the Advisory Committee on Immunization Practices and CDC's Health Information for International Travel (Yellow Book) and were unlikely to have received these vaccinations before travel.36–40

The male predominance of deceased travelers reported to CDC is consistent with previous published reports.5,9–11,14–15,20 An analysis of GeoSentinel data from 1997 to 2007 showed that male travelers had a higher risk of acute hepatitis A, chronic viral hepatitis, and sexually transmitted infections (STI).41 Of the males who died from infectious disease in our investigation, one died of disseminated Neisseria gonorrhoeae, one from viral hepatitis, one from chronic hepatitis C, and three from HIV/AIDS complications; no deaths of females were attributed to STIs, hepatitides, or HIV/AIDS. However, male travelers were not more likely to die of infectious disease than female travelers.

Sixty-two percent of deaths in our investigation were associated with maritime travel; of these, 85% were associated with cruise ships. This is not surprising, given that the longer voyage duration of cruise ship travel compared to air travel allows more time for a death to occur and for deaths to be reported to CDC. Also, it has been reported that some ill persons chose to embark on cruises with the intention of dying at sea.19 Finally, deaths aboard airlines are underreported because national or local laws often prohibit pronouncing a traveler dead on an aircraft.21

Although reporting to CDC quarantine stations is passive, and not all deaths in arriving international travelers are reported to QARS, the results of our investigation and others indicated that vaccine-preventable and tropical diseases are not major causes of death in international travelers.5,6 ,8–11,13–15 This finding may reflect advancements in global public health, improved adherence of travelers to appropriate pre-travel guidance, the presence of pre-existing immunity, or a low risk of exposure to infectious pathogens by travelers, especially cruise ship passengers.

It is unclear how many of the 26 fatal infections were acquired before rather than during travel. It is unknown whether the deaths in our investigation, excluding those related to injury, could be attributed to or were coincidental to international travel, or if medical care available at U.S. hospitals, but unavailable on cruise ships, could have averted some of these deaths.

Using Peake et al.'s23 data, we calculated a mortality rate for North American cruise ship passengers of 9.8 deaths per million passenger-nights among four ships in one cruiseline. In contrast, our investigation found a much lower mortality rate for cruise ship passengers (0.6 deaths per million passenger-nights). Differences in passenger populations and methodology (Peake's active case finding vs. CDC's passive surveillance) may explain some of this discrepancy. The significant increase in death rates in cruise ship passengers from years 1 to 3 in our investigation may represent improved reporting to CDC by airlines, cruise lines, and CBP due to increased CDC training to encourage reporting. It has been suggested that increasing numbers of travelers may have chronic or terminal illnesses, but there are no data to confirm this hypothesis.

Mortality rates in cruise ship passengers were lowest during the third quarter in all 3 years, predominantly due to decreases in cardiovascular mortality. This third-quarter reduction could reflect the known seasonality of myocardial infarctions, which peaks in the winter and drops in the summer.42 Also, there may be a seasonal variation in cruise ship passenger demographics or activities which affect cardiovascular mortality. We were unable to obtain demographic data from the cruise industry to confirm any variation.

An in-flight death rate of 0.31 deaths per million air passengers was calculated from 1977 to 1984 data reported by International Air Transport Association (IATA) members, which is consistent with our results.20 Other in-flight death rates have been reported to be 0.8 deaths per million passengers from October 1985 to March 1986 and 0.1 deaths per million passengers from July 1, 1999 to June 30, 2000.18,43 Since each investigation used different methodologies, it is difficult to compare them to determine overall trends in the mortality of international passengers on commercial flights into the United States. Only one death was reported in a land border traveler, which likely is a consequence of the U.S. Code of Federal Regulations exclusion of land border carriers from reporting requirements.29

Our investigation had several limitations. Historically, cardiovascular diseases have been overdiagnosed in death certificates.44 There may be a misclassification bias in determining causes of death on conveyances which may result in overreporting of cardiovascular deaths. Causes of death were determined by different health-care professionals with varying degrees of medical expertise and different methods of assigning the cause of death and completing the death certificate. For most deaths, we did not have access to death certificates and relied on data reported to quarantine stations. The cause of death reported by a cruise ship physician will likely be less accurate than that certified by a medical examiner. The ship's personnel may have limited or no information on the deceased's history of present illness and past medical history, and ships have limited diagnostic testing capability. Autopsies were conducted for only 17% of deaths in our investigation. Additionally, the wide range of thoroughness in the reporting of chronic medical conditions limited our ability to generalize our findings. This lack of reporting standards has been noted in previous traveler mortality investigations.15,18,20 Finally, QARS does not collect data on deaths on outbound international aircraft, deaths on cruises that begin and end at foreign ports, or deaths abroad.

Travelers are strongly advised to seek pre-travel medical consultation to reduce the risk of travel-associated illness, injury, and death. The pre-travel consultation should be tailored to the traveler's itinerary and underlying medical conditions. Persons with chronic medical conditions and the elderly should discuss their fitness for a proposed travel itinerary with their health-care providers before booking travel and should develop contingency plans if illness develops during travel.25,45–47

Travelers with chronic medical conditions should obtain information on medical facilities available during travel and on the cruise ship, and should discuss this information with their providers to determine if these facilities will be adequate for their needs. Some travel medical experts recommend that cruise passengers with serious medical conditions should select cruises with “short distances between modern ports.”19 Chronic medical conditions including cardiovascular conditions should be stabilized and their management optimized before travel. If chronic conditions cannot be stabilized, then travel should be postponed or cancelled.48 During the 2009 H1N1 influenza pandemic, it was noted that “comorbidity may contribute to mortality.”49 Since 73% of infectious disease deaths in our analysis were reported to have chronic conditions, and half of infectious disease deaths were associated with pneumonia, this suggests that some travelers may benefit from influenza and pneumococcal vaccination before travel.50–52

Travelers should consider their current health status and chronic medical conditions when assessing their risks of developing a severe illness or injury during travel. Pre-existing conditions may be exacerbated by travel-associated stress, dietary indiscretions, increased alcohol intake, increased physical exertion, and medication noncompliance.25 An analysis of Dutch travelers who required aeromedical repatriation determined that 82% of 65 travelers with chronic disease conditions were repatriated when the condition worsened.53 Occasionally, cruise ships may not have the option of timely medical evacuation. Medical repatriation may be significantly delayed during travel in a remote location or during inclement weather.54

Elderly travelers and those with chronic medical conditions should purchase travel insurance that includes emergency evacuation, and should carry a list of medications, a medical summary prepared by their physicians, and emergency contact information for their physicians.45 Anecdotal information provided on some QARS reports indicates that some symptomatic travelers on cruise ships refused medical attention or delayed seeking medical attention until moribund. Therefore, travelers with chronic medical conditions and the elderly should be counseled to seek medical care promptly if they become ill during travel.

We recommend that death certificates and autopsy results should be used whenever possible to assess causes of deaths in travelers and that future analyses of death during travel use the International Classification of Disease (ICD) to code the underlying and immediate causes of death. Further studies are needed to better assess mortality trends and to develop better prevention strategies for illness and death during international travel.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

The authors gratefully acknowledge the assistance of CDC quarantine stations and the medical examiners' offices and hospitals that provided critical information for this investigation. We thank Andre Berro of the CDC Division of Global Migration and Quarantine, who was instrumental in collecting international passenger denominator data. The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention.

Declaration of Interests

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References

The authors state they have no conflicts of interest.

References

  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Acknowledgments
  7. Declaration of Interests
  8. References