Abstract

Background

In countries with high rates of measles immunization, imported cases of measles represent an important continuing source of measles infection.

Methods

Airlines and state health departments report cases of suspected measles in international travelers to the Centers for Disease Control and Prevention Quarantine Stations. We reviewed these reports, maintained in an electronic database, to determine the demographic and epidemiologic characteristics of international air travelers infected with measles.

Results

We reviewed 35 confirmed cases of measles in air travelers and analyzed their demographic and epidemiologic characteristics. The median age of case travelers was 17 (range: 4 months–50 years). These travelers arrived from all regions of the world, including 10 countries with immunization rates of measles‐containing vaccine below 90% and five others experiencing local outbreaks. Of 17 travelers for whom immunization status was known, 2 had been adequately immunized with at least two doses of a measles‐virus containing vaccine, 9 were inadequately immunized, and an additional 6 infants had not been immunized because of age.

Conclusions

Measles importations continue in the United States. Travelers should be aware of the importance of assuring up‐to‐date immunizations, especially when visiting countries experiencing a local measles outbreak. In addition, parents traveling with infants, and their physicians, should be aware of recommendations regarding the early administration of a dose of measles‐containing vaccine for infants at least 6 months old traveling internationally.

In carrying out responsibilities to prevent the introduction and spread of contagious diseases into the United States, personnel of the Division of Global Migration and Quarantine, US Centers for Disease Control and Prevention (CDC), receive reports of suspected and confirmed cases of measles in international travelers entering US ports as provided for by federal public health law and state agreements through the Council of State and Terrritorial Epidemiologists. These reports, from international vessel or aircraft captains, state and local health officials, US Customs and Border Protection officers, and foreign Ministries of Health, have been collected in an electronic database, the Quarantine Activity Reporting System (QARS), since August 1, 2005.

With the elimination of endemic measles transmission in the United States in 2000, 1 travel‐related and imported cases are the sources of measles exposure for persons living in the United States, 2 in some cases leading to multiple secondary cases and costly outbreak investigations and disease control efforts. 3 More generally, the issue of measles in travelers is also of importance in other countries with highly immune populations. 4

To identify possible improvements in current control strategies for limiting measles importation into the United States, this report reviews the clinical and epidemiologic characteristics of cases occurring in air travelers reported in QARS over a 32‐month period. Current control strategies and secondary cases related to importations have been discussed elsewhere. 5

Methods

The QARS database of all reported illnesses or deaths in international travelers, compiled from daily reports made by 18 CDC Quarantine Stations located at major US international airports and two land border stations, was searched for all records from August 1, 2005 to March 31, 2008, containing the words “measles” or “rubeola.” Reports were then categorized as confirmed or suspected measles cases according to the Council of State and Territorial Epidemiologists' case definitions for measles (Table 1) or were excluded from the analysis. For some cases, results of laboratory testing were obtained from state public health reports to the CDC Division of Viral Diseases or through testing by CDC laboratories. Cases were excluded from analysis if they were not in air travelers, their serologic studies were incompatible with a diagnosis of measles, or a positive diagnosis of an alternative illness was made. Adequacy of immunization to measles was judged by current US standards (Table 2).

Table 1

Current case definitions for measles as adopted by the (US) Council of State and Territorial Epidemiologists 12

Clinical case definition 
An illness characterized by all of the following: 
 • A generalized rash lasting ≥3 days 
 • A temperature ≥101°F (≥38.3°C) 
 • Cough, coryza, or conjunctivitis 
Laboratory criteria for diagnosis 
 • Positive serologic test for measles immunoglobulin M (IgM) antibody, or 
 • Significant (generally a fourfold) rise in measles antibody (IgG) level by any standard serologic assay, or 
 • Isolation of measles virus from a clinical specimen* 
Case classification 
Case classification requires a consideration of the clinical presentation. 
 • Suspected: Any febrile illness accompanied by rash. 
 • Probable: A case that meets the clinical case definition, has noncontributory or no serologic or virologic testing, and is not epidemiologically linked to a confirmed case. 
 • Confirmed: A case that is laboratory confirmed or that meets the clinical case definition and is epidemiologically linked to a confirmed case. A laboratory‐confirmed case does not need to meet the clinical case definition. 
Clinical case definition 
An illness characterized by all of the following: 
 • A generalized rash lasting ≥3 days 
 • A temperature ≥101°F (≥38.3°C) 
 • Cough, coryza, or conjunctivitis 
Laboratory criteria for diagnosis 
 • Positive serologic test for measles immunoglobulin M (IgM) antibody, or 
 • Significant (generally a fourfold) rise in measles antibody (IgG) level by any standard serologic assay, or 
 • Isolation of measles virus from a clinical specimen* 
Case classification 
Case classification requires a consideration of the clinical presentation. 
 • Suspected: Any febrile illness accompanied by rash. 
 • Probable: A case that meets the clinical case definition, has noncontributory or no serologic or virologic testing, and is not epidemiologically linked to a confirmed case. 
 • Confirmed: A case that is laboratory confirmed or that meets the clinical case definition and is epidemiologically linked to a confirmed case. A laboratory‐confirmed case does not need to meet the clinical case definition. 
*

Identification of measles genotype by reverse transcriptase‐polymerase chain reaction (RT‐PCR) and sequencing by WHO reference laboratory [Centers for Disease Control and Prevention (CDC)] from clinical samples confirms infection.

Table 2

Acceptable presumptive evidence of immunity to MMR (US standards) 12

 Routine International travelers 
(1) Documentation of adequate vaccination* : preschool‐ aged children and adults not at high risk: one dose, school‐aged children (grades K‐12): two doses, or Documented administration of two doses of live measles‐virus vaccine,* or 
(2) Laboratory evidence of immunity, or Laboratory evidence of immunity, or 
(3) Born before 1957, or Born before 1957, or 
(4) Documentation of physician‐diagnosed measles Documentation of physician‐diagnosed measles 
 Routine International travelers 
(1) Documentation of adequate vaccination* : preschool‐ aged children and adults not at high risk: one dose, school‐aged children (grades K‐12): two doses, or Documented administration of two doses of live measles‐virus vaccine,* or 
(2) Laboratory evidence of immunity, or Laboratory evidence of immunity, or 
(3) Born before 1957, or Born before 1957, or 
(4) Documentation of physician‐diagnosed measles Documentation of physician‐diagnosed measles 

MMR = measles, mumps, and rubella.

*

The first dose should be administered on or after the first birthday; the second dose of measles‐containing vaccine should be administered no earlier than 1 month (ie minimum of 28 d) after the first dose. Combined MMR vaccine generally should be used whenever any of its component vaccines is indicated.

Children aged 6–11 months should receive a dose of monovalent measles vaccine (or MMR, if monovalent vaccine is not available) before departure. Children who receive a dose of measles‐containing vaccine before their first birthdays should be revaccinated with two doses of MMR vaccine, the first of which should be administered when the child is aged 12–15 months (12 mo if the child remains in a high‐risk area) and the second at least 28 days later.

This investigation was determined not to be human subject research by CDC.

Results

A total of 52 reports were recovered of which 4 cases occurred on ships, 2 were identified in land travelers, and 46 reports of illness were identified in air travelers (36 were confirmed as measles, and 10 were excluded); however, 1 confirmed air travel case was the result of domestic exposure to an imported case. This report will focus on the 35 reports of confirmed measles in air travelers consistent with apparent acquisition of infection overseas.

Among the 35 confirmed measles cases, 30 were laboratory‐confirmed (29 confirmed by anti‐measles immunoglobulin M antibody and 1 positive for measles virus‐specific nucleic acid by polymerase chain reaction assay). The remaining five were epidemiologically linked to confirmed cases. No traveler gave a history of recent receipt of a measles‐virus containing vaccine.

Demographics

Nineteen case travelers (54%) were male. The median age of cases was 17 years, with a range from 4 months to 50 years. The 35 travelers with confirmed measles had arrived from or recently visited 18 different countries (Table 3) in five world regions: Asia/Pacific (14), Europe (13), Eastern Mediterranean (4), Americas (3), and Africa (1). Twenty (57%) were US passport holders. At least two of the travelers were members of the same family.

Table 3

Sources of reported measles cases in air travelers and national coverage for at least one dose of a measles‐containing vaccine (source: UNICEF/WHO IMMUNIZATION SUMMARY. A statistical reference containing data through 2007)

Arriving from Number of cases reported National MCV coverage rate (2007) (%) 
Australia 94 
Bangladesh 88 
Belgium 92 
China 94 
Egypt 97 
France 87 
Germany 94 
Hong Kong 81* 
India 67 
Israel 97 
Italy 87 
Japan 98 
Nigeria 62 
Poland 98 
Switzerland 86 
Thailand 96 
United Kingdom 86 
Venezuela 55 
Yemen 74 
Arriving from Number of cases reported National MCV coverage rate (2007) (%) 
Australia 94 
Bangladesh 88 
Belgium 92 
China 94 
Egypt 97 
France 87 
Germany 94 
Hong Kong 81* 
India 67 
Israel 97 
Italy 87 
Japan 98 
Nigeria 62 
Poland 98 
Switzerland 86 
Thailand 96 
United Kingdom 86 
Venezuela 55 
Yemen 74 

[Note that results from the 2009 National Immunization Survey showed that among United States children ages 19–35 mo, 90% had received at least one dose of measles‐containing vaccine (MMWR 2010;59:1171–1177).]

MCV = measles‐containing vaccine.

Timing of Travel

Twenty‐one travelers flew up to 4 days before rash onset; 3 flew on the day of rash onset and 11 flew 1–3 days after the rash appeared.

Duration of Travel

Travelers were in transit from 5–24 hours from origin to final destination.

Immunization Status of Travelers

Information on immunization status was available for 17 travelers (49%) (Table 4). Of these, four had not received any doses of measles‐containing vaccine, five had received one dose, one had two doses, one had three doses, and six were infants not vaccinated because of age. No traveler was born before 1957.

Table 4

Age and country of origin of travelers over 1 year of age whose vaccination status was reported

Age (years) Country of origin Doses of measles vaccine 
United Kingdom 
NR* 
NR* 
15 India 
25 United States 
34 NR* 
35 Venezuela 
36 NR* 
38 United States 
39 NR* 
50 United States 
Age (years) Country of origin Doses of measles vaccine 
United Kingdom 
NR* 
NR* 
15 India 
25 United States 
34 NR* 
35 Venezuela 
36 NR* 
38 United States 
39 NR* 
50 United States 
*

NR = not reported.

Discussion

Over the 32‐month period analyzed, 35 confirmed cases of measles in international air travelers arriving in the United States were reported to CDC Quarantine Stations, about 1 case per month. These numbers likely underestimate the number of importations of measles into the United States. Quarantine Stations are located at airports receiving only 85% of all international arrivals. In addition, persons who become ill after travel may not be reported to quarantine stations. In comparison, the CDC's Divison of Viral Diseases received 78 reports of measles importations from state authorities during the period this report covers. However, unlike the data received by the Divison of Viral Diseases, QARS reports included only travelers who were presumably infectious at the time of travel, ie, within 4 days of rash onset. 6 In addition, the 35 cases discussed here do not include maritime or land border cases, which, while few, might have more significant epidemiologic impact than air travel cases because of prolonged shipboard exposures or exposures in buses or trains.

Although international flights to the United States typically last 5 or more hours, we assess all flights, regardless of duration, for the need for contact investigation, based upon the timing of illness in relation to travel in the index case, and the length of time which has elapsed between the flight and notification to the CDC.

Contact investigations were carried out if cases traveled within 4 days of their rash onset and were reported within 21 days of travel, according to standard CDC protocols. While details of these investigations have been reported elsewhere, it should be noted that between January 1 and April 25, 2008, five cluster outbreaks of measles (defined as at least three cases occurring as an epidemiologically linked cluster) occurred in the United States of which four were associated with imported infections. 5 The index cases for two of these outbreaks arrived from countries with reported rates of measles immunization over 90% experiencing measles outbreaks at the time they traveled. Each of these index cases is included in this report (Figure 1).

Figure 1

Dates of arrival of travelers with measles on international flights.

Figure 1

Dates of arrival of travelers with measles on international flights.

The results of this investigation offer several opportunities to improve our approach to the control of measles. The substantial predominance of adults among cases may reflect the characteristics of the traveling public, as well as relative rates of immunity in different age cohorts. The fact that over half of all cases occurred in US passport holders emphasizes the importance of further improving high levels of measles immunity in this country, particularly in persons traveling abroad. Travelers need to be aware that measles can be acquired not only where endemic measles continues to be an ongoing public health problem but also in nonendemic countries where local outbreaks of measles are reported, including, during the time this report covers, the United Kingdom, Israel, Switzerland, and Belgium. More specifically, two travelers arrived from the United Kingdom during the outbreak there from April 2007 to May 2008, 7 and one traveler each came from Israel during the outbreak from August 2007 to January 2008, 8 from Switzerland during the outbreak from November 2006 to July 2009, 9 and from Belgium during the outbreak period August 2007 to November 2007. 10 Indeed, cases from Europe were the second most numerous among world regions. While this undoubtedly reflects the large number of trips between Europe and the United States, our results suggest the need for travelers to be more alert to local disease activity in countries not routinely considered to pose a high risk for measles exposure.

Six cases occurred in infants who were younger than 1 year of age, the age at which measles‐containing vaccine is typically administered in the United States. Five of these children were over 6 months old at the time they began their trips and could have been immunized according to the immunization recommendation that children aged 6–11 months leaving the United States should receive a dose of monovalent measles vaccine or measles, mumps, and rubella (MMR) vaccine, if monovalent vaccine is not available. 11 This finding suggests that medical practitioners and parents may not always be familiar with this recommendation. Some of these infants may have been in family groups traveling to visit relatives abroad, suggesting that efforts to publicize the need for measles immunization in families with kin overseas may be especially valuable.

It is of concern that 14 travelers with measles flew from 0 to 3 days after rash onset, making it likely that most, if not all, of these travelers flew while they had rash. 12 More attention to the careful observation of boarding travelers might reduce the risk these persons present to fellow travelers as well as to their contacts upon arrival. Travelers should also be educated about the hazards they may pose to others when traveling with rash illnesses and the need to delay their trips until their illness has been professionally evaluated and any risk of transmission has been resolved.

Acknowledgments

We acknowledge the diligent work of our colleagues in the CDC Quarantine and Border Health Services Branch who received and transmitted these reports and collected the associated data in QARS used in this analysis. We also acknowledge the generous assistance of Susan Redd with data recorded by the CDC Division of Viral Diseases.

Declaration of Interests

The authors state they have no conflicts of interest to declare.

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