CUBAN MEDICAL LITERATURE

Malaria Surveillance of International Travelers
Living in Havana City, 2000-2001

Carmen Julia Suárez Miranda(1); Antonio Pérez(2); Alina Pérez Carreras(3); Omar Fuentes González(4)

ABSTRACT: A prevalence study was made of Cuban international travelers and foreigners living in Havana, who arrived in Cuba either by air or sea between January 1st, 2000 and December 31st, 2001, as well as of students in the Latin American School of Medicine ( ELAM) in the 1999-2000 and 2000-2001 school years.

Malaria prevalence calculations were made by continent and country of origin. General (by continent), and specific (by country), rates were calculated. The same procedure was used for ELAM students. The main source of malaria was found among Cuban passengers coming from the African continent in the period 2000-2001, with the highest rates of incidence and risk of introduction in the passengers coming from Nigeria and Cameroon.

In Latin America, malaria prevalence was higher in travelers arriving from Nicaragua. In the 2000-2001 school year, the highest rates of infected individuals came from Africa, mainly from Nigeria. ELAM students were found to be a high-risk group in malaria prevalence in the present study.

Keywords: MALARIA, EPIDEMIOLOGICAL SURVEILLANCE, INTERNATIONAL TRAVELERS, HAVANA CITY.

INTRODUCTION

It is estimated that malaria represents 2.3% of the global disease burden, 9% in Africa. According to the World Health Organization, in 1998 more than two billion people - 40% of the world population - live in malaria-risk areas.[1-6] Between 1.5 and 2.7 million people die as a result of this disease every year, while between 300 and 500 million suffer from it.[5-8]

Historically, communicable diseases have spread from one continent to another and from one country to another by land, sea, and air.

International travel has thus increased the risk of arrival of people who suffer from or carry disease, and intermediate vectors or hosts who find in our ecosystem a favorable habitat in which to develop (Ministry of Public Health, International Sanitary Control Program, Havana City: MINSAP, 1998).[9]

The situation gets worse as travel to endemic areas increases. As endemic areas grow, so does the parasite’s resistance to prophylactic regimes, thus causing a significant increase in imported malaria (Valdés García L, Carbonell García I, Delgado Bustillo J, Santin Peña M. Paludismo: Enfermedades emergentes y reemergentes. Ciudad de La Habana: MINSAP; 1998). As a result, the disease has appeared in countries like the United States, where autochthonous outbreaks occurred at the end of the 1980s.[6-9] Imported malaria has also been reported in other First World countries like France, the United Kingdom, Germany, Switzerland, Australia and Italy.[10-12]

In Latin America, malaria has been reported in about twenty countries including Mexico, Costa Rica, El Salvador, Guatemala, Honduras, Nicaragua, Panama, Guyana, Colombia, Brazil and Venezuela.[8-13]

In the last few decades Cuba has increased its international relations, which is why 40 years ago the Surveillance and International Sanitary Control Program was implemented [a component of the UATS system, eds.]. This program aims at identifying and preventing the introduction of exotic diseases such as malaria into Cuba. Malaria introduction has been the greatest risk in recent years, so special measures were required.

This study aims at presenting the results and experiences of international surveillance of passengers who arrive in Havana and the group of students in the Latin American School of Medicine ( ELAM) who come from abroad.

METHOD

Type of Study

A prevalence study of malaria was carried out.

UNIVERSE

The total number of Cuban international travelers and foreigners living in Havana City who arrived in Cuba between January 1st, 2000 and December 31st, 2001, either by air or sea, and all students at ELAM during the 1999-2000 and 2000-2001 school years.

Sources of Information

Records from the International Sanitary Control Program at the Epidemiology Department of the Provincial Health and Epidemiology Center of Havana City.

Traveler records of the International Sanitary Control Program at José Martí International Airport.

PROCEDURE

Sources of potential malaria were identified by measuring malaria prevalence in international travelers living in Havana City who arrived in Cuba in the period under study. Upon arriving in Cuba, these passengers are assisted by the International Sanitary Control staff in arrival terminals (airport or port). They declare what country they are arriving from and whether they are sick. They receive a warning card and are instructed to contact the health authorities in the area where they live.

If a passenger arrives sick, he is immediately isolated for diagnosis and treatment at the Pedro Kourí Institute of Tropical Medicine (IPK), which is the institution in charge of exotic diseases in Cuba. IPK informs the provincial health authorities, which in turn advise municipal authorities of the case.

If the passenger is asymptomatic upon arrival, the port or the airport will inform the Provincial Health and Epidemiology Centers by telex, email or telephone. These institutions in turn contact each Municipal Health and Epidemiology Unit, which informs the specific health areas regarding the travelers’ situation and will start epidemiological surveillance through the family doctor and nurse, who apply a thick blood smear test. If the blood sample is positive, the traveler is immediately isolated at IPK. The time frame between the traveler’s arrival in Cuba and his or her visit to their doctor should not exceed 72 hours.

The analysis of this procedure made it possible to determine the total number of passengers, as well as the number of infected travelers, in the period under study. Calculations were made of general (by continent) and specific (by country) rates of travelers infected with malaria by continent and endemic countries of origin.

The same procedure was followed with the special group of ELAM students. Specific rates of sick students were calculated.

RESULTS

A total of 10,527 Cuban international travelers and foreigners living in Havana arrived in Cuba either by air or sea, coming from 65 countries on four continents: Latin America and the Caribbean, Africa, Asia and Europe. Of the total, 9,276 passengers arrived from 32 countries in Latin America and the Caribbean; 935 travelers from 20 African countries; 244 passengers from nine Asian countries; and 72 travelers from four European countries. In 2000, the highest percentage of travelers arrived from Latin America and the Caribbean. In 2001, the same airport and port received 7,077 travelers, coming from 75 countries on the same four continents: 5,896 passengers from 30 Latin American and Caribbean countries; 797 from 28 African countries; 341 from 16 Asian countries; and 44 from one European country. In both years the highest number of passengers arrived from Latin America and the Caribbean.

The number of passengers coming from endemic regions for the identification of potential malaria sources (Table 1) showed a total of 8,521 travelers (80.9%) coming from 46 endemic countries in Latin America and the Caribbean, Africa and Asia. Of these, 7,363 passengers (79.3%) came from 19 endemic countries in Latin America and the Caribbean; 925 (98.9%) from 19 African countries; and 233 (95.4%) from eight Asian countries. In 2000, 70% of the countries from which Cuban and foreign passengers living in Havana arrived were malaria endemic.

TABLE 1: Continental distribution of number and percentage of travelers coming from malaria endemic zones in 2000 and 2001 

Source: Epidemiology Department, Provincial Health and Epidemiology Center, Havana City

In 2001, potential malaria sources were related to the arrival of 6,409 travelers from endemic areas (90.5%), coming from the same continents as the year before, and from 60 malaria endemic countries. Of the total, 5,322 passengers arrived (90.2%) from 19 countries in Latin America and the Caribbean; 773 passengers (96.6%) from 26 African countries; and 314 travelers (92.0%) from 15 Asian countries.

It is notable that in 2000 the number of travelers arriving from malaria endemic zones was higher, while in 2001 the number of passengers coming from these zones diminished and the number of endemic countries increased, especially in Africa and Asia.

In the distribution of travelers from endemic countries in 2000, the highest percentages were found in Mexico (14.2%), Venezuela (12.3%) and Brazil (11.3%) within Latin America and the Caribbean; South Africa (34.8%), Ghana (14.5%) and Angola (8.6%) in Africa; and China (41.6%), Vietnam (28.3%), and India and Iraq (7.7% each) in Asia.

The distribution in 2001 showed the same countries in top positions for Latin America and the Caribbean, and South Africa and Angola in Africa, with Guinea Bissau now ranked third with 9.3%. China and Vietnam topped the list in Asia again, plus Turkey with 6.6%.

Screening of the total number of passengers from malaria endemic areas (Table 2) identified 38 positive cases of Plasmodium, 24 of which were found in 2000 with a general rate for continents of 23.5/10,000 travelers, and a specific rate for endemic countries of 28.9/10,000 passengers. Nineteen infected passengers came from Africa, for a general rate of 203.2/10,000 travelers, and a specific rate for endemic countries of 205.4/10,000 travelers. Five cases were detected in passengers coming from Latin America and the Caribbean, for a general rate of 5.3/10,000 travelers and a specific rate of 6.7/10,000 travelers. Fourteen cases were detected in 2001 (a general rate of 20.9/10,000 travelers and a specific rate of 22.9/10,000 travelers); with Africa maintaining the highest rates. No infection was identified in passengers arriving from endemic areas in Asia during the period under study.

TABLE 2: Number of sick travelers and malaria prevalence rate per 10,000 travelers from endemic continents

Source: Epidemiology Department, IPK

The distribution of malaria cases by country in Africa (Table 3) included 19 sick travelers from seven countries in 2000 (general rate of 695.9/10,000 travelers), with Cameroon (10,000/10,000 travelers) and Nigeria (5333.3/10,000 travelers) being the countries with the highest rates.

TABLE 3: Malaria cases, number of passengers and prevalence rate per 10,000 travelers from African countries

Source: Epidemiology Department, IPK

In 2001, the highest rates of passengers who contracted malaria in the African continent were found coming from Ivory Coast (3,333.3/10,000 travelers) and Equatorial Guinea (2,000/10,000 travelers). In 2000, Nigeria contributed the highest number of cases, while Cameroon showed the highest rate.

The distribution of infected travelers from Latin America and the Caribbean (Table 4) during 2000 totaled five, including Nicaragua with the highest rate (135.1/10,000 travelers). The total number of cases dropped to 3 in 2001. The rate from Haiti was 86.9/10,000 travelers, from Nicaragua 79.3/10,000 travelers and from Colombia 34.6/10,000 travelers. In the two years considered for the study, Nicaragua showed the highest number of cases and the highest rate for this continent.

TABLE 4: Malaria cases, number of travelers and prevalence rate per 10,000 travelers from Latin America and the Caribbean  

Source: Epidemiology Department, IPK

It is notable that the regional distribution of cases per year for the special group at ELAM (Table 5) shows that in the 1999-2000 school year, all of the infected students came from Latin America and the Caribbean, with a rate of 34.3/10,000 inhabitants. In the 2000-2001 school year, eight cases were reported (general rate of 23.6/10,000 inhabitants), with Africa showing the highest rate (283.1/10,000 inhabitants), and Latin America and the Caribbean with a noticeably lower rate in relation to the previous school year.

TABLE 5: Distribution of malaria cases and prevalence rates by continent per 10,000 inhabitants: ELAM, 1999-2000 and 2000-2001 school years

Source: Epidemiology Department, ELAM

The specific distribution of sick students by country within the ELAM special group (Table 6) shows that malaria cases were reported from three countries in the 1999-2000 school year. The highest rate was found in Nicaragua (173.2/10,000 inhabitants). In the 2000-2001 school year, Nigeria showed the highest rate (500/10,000 inhabitants). In the two school years included in the study, the highest rates were found in these two countries.

TABLE 6: Distribution of malaria cases and prevalence rates per 10,000 inhabitants by country: ELAM, 1999-2000 and 2000-2001 school years

Source: Epidemiology Department, ELAM

DISCUSSION 

With regards to Latin America and the Caribbean, we believe that the problem can be approached from another perspective, so that the exact province or town from which the traveler arrived can be traced. It is precisely with this goal in mind that it becomes necessary to specify where the passenger came from, in order to identify the true risk the traveler was exposed to. This can be done in the Health Area to which the traveler should report within 72 hours after his/her arrival. The family doctor can obtain this kind of information, making it possible to expand epidemiological surveillance beyond risk macro-identification by continent and country, to identify specific regions in each where malaria or other diseases are present.

In order to clearly illustrate our criterion, we will refer to facts we found through our research. In Latin America and the Caribbean, Mexico, Brazil and Venezuela - countries where malaria is endemic - showed a significant percentage in terms of number of travelers, but not in number of infected travelers. This is logical if we consider that a traveler may have been in Brasilia and did not visit another city or province. This same analysis may be applied to other travelers who may have been in Honduras’ Mosquitia region, for example. In this sense, surveillance can be made applied more clearly and accurately.

Despite Asia’s considerable number of endemic areas, no infection was detected among travelers coming from this continent. This allows us to suggest that, as for Latin America and the Caribbean, it is worthwhile to identify the exact place where the traveler is arriving from in Asia, to be able to assess the actual risk he/she was exposed to, and to take suitable action in epidemiological surveillance with a more rational use of material resources.

The results of the research carried out by Sabatinelli et al[14] were similar to ours, as they found Africa to be the continent from which more Italian travelers arrived in 1997 and 1998. Likewise, Romi at al[15] found similar results in Italian travelers in 1999 and 2000.[16]

Results similar to ours were also obtained by Muentener et al,[17] who argued that French, German, Italian and British tourists came from a larger number of malaria endemic zones in Africa than any other continent.

Couser et al[18] obtained similar results. They argued that U.S. travelers go to, and come from, more malaria endemic zones in Africa than in America, Asia and Oceania.

Like us, these authors did not identify the exact location or territory from which the travelers came, so the risk of exposure was thus very generally expressed in their results. This is the reason why we insist that our health system be equipped with the proper procedures to obtain traveler information and orient disease surveillance to be more geographic-specific.

The malaria endemic countries which rendered the highest infection rates in Africa were Nigeria and Cameroon, while Nicaragua showed the highest rates in Latin America and the Caribbean. This allowed us to conclude that these are high-risk countries to take into account for future surveillance action. It would still be necessary to locate the exact zones of origin in Nicaragua, as was pointed out before.

Sabatinelli et al[14] concurred with us when they found Nigeria a high-risk country for their travelers, as well as Ghana, Senegal and Kenya.

We found results that were similar to those obtained by Couser et al,[18] for whom the highest number of malaria-infected travelers in the United States in 2000 and 2001 came from Nigeria. They also referred to the significant percentage of infected travelers who had visited Latin American and Caribbean countries like El Salvador and Mexico. This information did not match our results, as no cases were reported in our study of travelers coming from these countries.

Conclusions

• The main source of malaria among Cuban travelers in 2000 and 2001 was found in those who came from Africa. Nigeria and Cameroon were the countries with the highest rates in the African continent and thus posed the highest risk of this disease.
• In Latin America and the Caribbean, the highest malaria prevalence was found in travelers arriving from Nicaragua.
• ELAM was a high-risk group in malaria prevalence identified by malaria surveillance of international travelers in the period under study.

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This article first appeared in Revista Cubana Salud Pública 2004;30(3)

THE AUTHORS

1. MD, MSc, National Surveillance and Anti-Vector Unit
2. PhD, Pedro Kourí Institute of Tropical Medicine
3. BS, National Surveillance and Anti-Vector Unit
4. BS, Pedro Kourí Institute of Tropical Medicine