Chagas disease: A Latin American health problem becoming a world health problem

Abstract

Political repression and/or economic stagnation stimulated the flow of migration from the 17 Latin American countries endemic for Chagas disease to developed countries. Because of this migration, Chagas disease, an autochthonous disease of the Continental Western Hemisphere is becoming a global health problem. In 2006, 3.8% of the 80,522 immigrants from those 17 countries to Australia were likely infected with Trypanosoma cruzi. In Canada in 2006, 3.5% of the 156,960 immigrants from Latin America whose country of origin was identified were estimated to have been infected. In Japan in 2007, there were 80,912 immigrants from Brazil, 15,281 from Peru, and 19,413 from other South American countries whose country of origin was not identified, a portion of whom may have been also infected. In 15 countries of Europe in 2005, excluding Spain, 2.9% of the 483,074 legal Latin American immigrants were estimated to be infected with T. cruzi. By 2008, Spain had received 1,678,711 immigrants from Latin American endemic countries; of these, 5.2% were potentially infected with T. cruzi and 17,390 may develop Chagas disease. Further, it was estimated that 24-92 newborns delivered by South American T. cruzi infected mothers in Spain may have been congenitally infected with T. cruzi in 2007. In the USA we estimated that 1.9% of approximately 13 million Latin American immigrants in 2000, and 2% of 17 million in 2007, were potentially infected with T. cruzi. Of these, 49,157 and 65,133 in 2000 and 2007 respectively, may have or may develop symptoms and signs of chronic Chagas disease. Governments should implement policies to prevent donations of blood and organs from T. cruzi infected donors. In addition, an infrastructure that assures detection and treatment of acute and chronic cases as well as congenital infection should be developed.

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Please cite this article in press as: Schmunis, G.A., Yadon, Z.E., Chagas disease: A Latin American health problem becoming a world health problem.
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journal homepage: www.elsevier.com/locate/actatropica
Chagas disease: A Latin American health problem becoming a
world health problem
Gabriel A. Schmunis∗, Zaida E. Yadon
Health Surveillance, Disease Prevention and Control, Pan American Health Organization, Regional Office of the World Health Organization,
525 23th Street N.W., Washington, DC 20037, USA
article info
Article history:
Available online xxx
Keywords:
Chagas disease
Immigration
Blood transfusion
Organ transplant
Congenital transmission
abstract
Political repression and/or economic stagnation stimulated the flow of migration from the 17 Latin Amer-
ican countries endemic for Chagas disease to developed countries. Because of this migration, Chagas
disease, an autochthonous disease of the Continental Western Hemisphere is becoming a global health
problem. In 2006, 3.8% of the 80,522 immigrants from those 17 countries to Australia were likely infected
with Trypanosoma cruzi. In Canada in 2006, 3.5% of the 156,960 immigrants from Latin America whose
country of origin was identified were estimated to have been infected. In Japan in 2007, there were
80,912 immigrants from Brazil, 15,281 from Peru, and 19,413 from other South American countries whose
country of origin was not identified, a portion of whom may have been also infected.
In 15 countries of Europe in 2005, excluding Spain, 2.9% of the 483,074 legal Latin American immigrants
were estimated to be infected with T. cruzi. By 2008, Spain had received 1,678,711 immigrants from
Latin American endemic countries; of these, 5.2% were potentially infected with T. cruzi and 17,390 may
develop Chagas disease. Further, it was estimated that 24–92 newborns delivered by South American T.
cruzi infected mothers in Spain may have been congenitally infected with T. cruzi in 2007. In the USA
we estimated that 1.9% of approximately 13 million Latin American immigrants in 2000, and 2% of 17
million in 2007, were potentially infected with T. cruzi. Of these, 49,157 and 65,133 in 2000 and 2007
respectively, may have or may develop symptoms and signs of chronic Chagas disease.
Governments should implement policies to prevent donations of blood and organs from T. cruzi infected
donors. In addition, an infrastructure that assures detection and treatment of acute and chronic cases as
well as congenital infection should be developed.
© 2009 Elsevier B.V. All rights reserved.
1. Introduction
Chagas disease is an autochthonous disease of 22 countries in
the continental Western Hemisphere (WHO, 1991, 2002), caused
by the protozoa Trypanosoma cruzi (T. cruzi). Human infection
is primarily transmitted by domestic and sylvatic insects of the
subfamily Triatominae (Hemiptera, Reduviidae), the kissing bug,
whose habitat in the Americas ranges from the US and Mexico in
the north to Argentina and Chile in the south. T. cruzi infection may
be also transmitted to humans congenitally, by blood transfusion
and organ transplant and by the oral route (WHO, 1991, 2002).
Travelers, including immigrants, have been considered a poten-
tial source of introduction of diseases like Chagas disease since the
early ages. This concern was as valid for plague in the XIV century
as it is for Tuberculosis (Jia et al., 2008) and SARS today (Ostroff
et al., 2005). From the late 1800s to the 1930s and 1940s, millions
∗Corresponding author. Present address: 4256 Warren Sreet N.W., Washington,
DC 20016, USA. Tel.: +1 202 966 7662.
E-mail address: Gabriel.schmunis@gmail.com (G.A. Schmunis).
of people, predominantly from Italy, Portugal and Spain, migrated
from Europe to Latin America. In general, about 10 million peo-
ple migrated to Argentina and Brazil alone (Moya J., cited by Padilla
and Peixoto, 2007), leaving behind poverty and political repression,
while taking advantage of favorable immigration policies in the
New World (Padilla and Peixoto, 2007). Between the 1960s and the
1980s, political turmoil and economic stagnation spurred migra-
tion from Latin America to developed countries. While the United
States (US) was the most frequent destination, Latin Americans also
migrated to Australia and Canada.
In the 1990s, the original flow of migration from Europe to Latin
America reversed course, and people from Latin America moved
to Europe. This migration, fueled by periodic economic recession
and opportunities created by the formation of the European Union
(EU), further accelerated after 2000. By 2005, there were more than
2 million people born in Latin America living in Western European
countries that favored immigration of descendants to whom visas
and dual citizenship rights were extended. Most were in the South-
ern European countries, such as Italy, Portugal and Spain (Padilla
and Peixoto, 2007). In the United States, it was estimated that
there were millions of Latin American immigrants (documented or
0001-706X/$ – see front matter © 2009 Elsevier B.V. All rights reserved.
doi:10.1016/j.actatropica.2009.11.003

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undocumented) living in the US (US Census Bureau, 2000; Passel
and Cohn, 2009a).
The potential for Chagas disease (American trypanosomiasis)
cases to be found and/or transmitted in Canada (Schipper et al.,
1980) and the US (Pearlman, 1983; Kirchhoff and Neva, 1985; Theis
et al., 1987; Kirchhoff et al., 1987; Kirchhoff, 1989; Schmunis, 1991;
Hagar and Rahimtoola, 1991; Wendell and Gonzaga, 1993) due
to the presence of immigrants from endemic countries has been
stressed since the 1980s. Therefore, it was not surprising when 2
Chagas cases in Canada and 5 in the US resulted from transfusions
using infected blood that was donated by an immigrant, a native of
a Chagas endemic country (Leiby, 2005). Organ transplants were
another route of transmission of T. cruzi in the US (CDC, 2002;
Mascola et al., 2006).
Blood and organ donation as well as congenital infection are the
primary modes of infection in the destination countries of immi-
grants (Schmunis, 2007a,b).
The possibility that vector transmission may occur in Europe
or in other continents by autochthonous triatominae is considered
remote. More feasible however, is the risk of accidental transport of
domestic Latin American species of triatominae to other regions or
continents (i.e. in the baggage of airline passengers) (Schofield et al.,
2009). In the US, the social conditions in the rural areas are not usu-
ally adequate for the intimate contact between vectors and humans.
Therefore, the probability of vector transmission is low and few
autochthonous Chagas disease cases have been documented in the
US (Dorn et al., 2007).
Until recently, Chagas disease cases described in Europe were
considered a novelty: one case imported from Colombia in France
(Brisseau et al., 1988), one from Brazil in Italy (Sztajzel et al., 1996),
one from Bolivia in Switzerland (Crovato and Rebora, 1997), one
case from Venezuela in Denmark (Enemark et al., 2000), one con-
genital case in Sweden (Pehrson et al., 1981), one infection through
bone marrow transplant in Spain (Villalba et al., 1992), and 2% over-
all prevalence for T. cruzi in Germany among immigrants from Latin
America (Frank et al., 1997). Presently, cases of T. cruzi infection are
no longer rare in countries with Latin American immigrants and a
call for attention was made to have Chagas disease in mind in the
differential diagnosis and possible etiology of cardiomyopathies in
Spain (Florian Sanz et al., 2005). The importance of Chagas disease
in immigrant-receiving countries depends on the potential number
of infected migrants and their infection rate for T. cruzi. Estima-
tion of the burden of Chagas disease in immigrants from endemic
countries is essential to plan preventive measures, as well as to
determine the resources needed for screening and treatment of
acute and chronic cases in destination countries. Chronic Chagas
disease can develop after a latency period of many years in up to
30% of those infected (Prata, 2001).
This paper reviews the available information on the number
of immigrants from 17 Latin American endemic countries for T.
cruzi, and reports updated estimates of T. cruzi infected individuals
and how many of them may need medical attention in Australia,
Canada, Japan, the European Union (EU) and non-EU European
countries, and the United States. We also report estimates of the
expected number of congenital infections among newborn from
immigrant Latin American women living in Spain.
2. Materials and methods
2.1. Source of data
The number of Latin American immigrants in Australia and
Canada in 2006 was obtained from the Australian Bureau of
Statistics (2007) and Statistics Canada (2006). Data for immigrants
to Japan were obtained for Brazilians and Peruvians only (General
Immigration Directorate, Ministry of Justice, Japan, 2008). The
number of Latin American legal immigrants in European coun-
tries other than Spain in 2005 was obtained from Padilla and
Peixoto (2007). When no breakdown of the country of origin of the
immigrants was available in the destination country, the average
prevalence rate of T. cruzi infection for the 17 endemic countries
of 2.9%, was used for the calculations. The total number of human
T. cruzi infections in the 17 endemic countries divided by the total
population of those countries as reported by Schofield and Dias
(1996). The source for the number of immigrants from the 17
endemic countries in Spain, 2008, was the Instituto Nacional de
Estadistica (INE) (2009), Spain. Estimates of the expected number
of newborns with congenital T. cruzi infection were calculated as
the total number of live newborns to Latin American women (INE,
2007), multiplied by the probability of a woman being infected with
T. cruzi (the T. cruzi infection rate in the country of origin), and the
probability of transmitting T. cruzi to the live newborn (Gurtler et
al., 2003). We used two different rates of T. cruzi transmission from
the infected mother to the live newborn: 1.3% and 5%, as reported
in the literature (Carlier and Torrico, 2003; Yadon and Schmunis,
2009). Estimates of congenital infections were not done for Costa
Rica, El Salvador, Guatemala, Nicaragua and Panama, because the
basic data needed to calculate the number of live newborns of
immigrant mothers from those countries were not available.
Data on Latin American immigrants in the USA were obtained
from the US Census Bureau (2000) an agency that enumerates
the characteristics of the entire resident population, regardless of
national origin or immigration status. Data on immigrants from
2007 were obtained from the Pew Hispanic Center (2009) and is
based on the US Census Bureau American Community Survey (ACS)
for that year.
2.2. Assumptions
For the calculations, it was assumed that the nation wide infec-
tion rate of the immigrant population in the destination country
was the same as prevalence of the infection in the country of ori-
gin of the immigrant population in 1990: Argentina, 8.2%; Chile,
2.8%; Colombia, 3.9%, Costa Rica, 4.3%; Ecuador, 1.2%; El Salvador,
6.1%; Honduras, 5.8%; Guatemala, 7.9%; Mexico, 0.7%; Nicaragua,
1.7%; Panama, 9.0%; Paraguay, 9.3%; Peru, 3.0%; Uruguay, 1.2%;
and Venezuela, 4.0% (Schofield and Dias, 1996). To estimate the
nation wide infection rate in Bolivia (15.4%), the Bolivian popula-
tion reported by Schofield and Dias (1996), was used along with the
nation wide number of cases of 1,130,000 as reported by Valencia
(1990). Similarly, the infection rate for Brazil (1.3%) was estimated
using 1,961,000 as the number of human infections reported for
1995 (Akavan, 2000). We thought that this rate represents bet-
ter the decrease in the number of infections that occurred since
the 1970s in Brazil (Akavan, 2000). The year 1990 was selected
for the prevalence in the different countries (except for Brazil, as
mentioned above) because it was only in the late 1990s that some
Latin American endemic countries began to expand their control
activities and thus decreased their infection rates. In fact, most
adult immigrants become infected during childhood, before vec-
tor control programs from most countries started (Perez de Ayala
et al., 2009). Therefore, the year 1990 represents better the real
prevalence of the immigrants born before the 1980s, who are the
majority.
In order to estimate the burden that Chagas disease may consti-
tute for the health services, it was assumed that the number of Latin
American immigrants that would need medical attention because
of Chagas disease pathology would be 20% of those infected. This
is a conservative number, considering that it is expected that up
to 30% of those infected may develop symptoms and/or signs of
cardiac or gastrointestinal Chagas disease (Prata, 2001). The data

Please cite this article in press as: Schmunis, G.A., Yadon, Z.E., Chagas disease: A Latin American health problem becoming a world health problem.
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Table 1
Latin American immigrants in Australia and Canada by country of origin and expected number infected with T. cruzi.
Country of origin Australia, 2006 Canada, 2006
Number of
immigrants
Estimated number of
infected immigrants
Number of
immigrants
Estimated number of
infected immigrants
Argentina 11,369 932 11,805 968
Bolivia 690 106 1,235 190
Brazil 7,491 97 12,500 163
Chile 23,305 653 10,595 297
Colombia 5,706 223 33,160 1,293
Costa Rica 310 13 2,295 99
Ecuador 1,508 18 5,650 68
El Salvador 9,400 573 14,975 913
Guatemala 313 25 5,085 402
Honduras 201 12 1,920 111
Mexico 1,802 13 33,045 231
Nicaragua 672 11 2,145 36
Panama 180 16 Not reported
Paraguay 341 32 1,550 144
Peru 6,322 190 10,435 313
Uruguay 9,376 113 3,480 42
Venezuela 1,536 61 7,085 283
Total 80,522 3,088 (3.8%) 156,960 5,553 (3.5%)
() Estimates of percentage of infected immigrants.
were rounded to the nearest hundredth of a unit using conventional
methods.
3. Results
Table 1 summarizes the number of T. cruzi infection estimated in
Australia and Canada in 2006. For Australia, it was estimated that
3.8% (3088) of 80,522 immigrants from endemic countries were
infected with T. cruzi and 618 of them, would need medical follow
up related to the infection. In Canada, according to the 2006 census,
there were 130,455 immigrants from Mexico and Central America
and 250,710 from South America, but the number of immigrants by
country of origin was only available for 156,960 persons, of which
3.5% (5553) were estimated to be infected (Table 1). Of these, 1111
may eventually need a related medical follow up. In 2005, 483,074
legal Latin American immigrants from the endemic countries were
living in 15 European countries, excluding Spain. It was estimated
that 2.9% (14,010) of the persons in this group may be infected
with T. cruzi, and 2803 would need a related medical attention. The
countries with the highest estimated number of T. cruzi infected
immigrants were Italy with 5185, Germany with 2225, Portugal
with 1617 and the United Kingdom with 1373 (Table 2). These data
may underestimate or overestimate the number of infected immi-
grants and of those needing medical attention. In the first case, the
number of infected immigrants may be underestimated because
undocumented immigrants were not accounted for. In the second
case, while in Italy and Portugal immigrants were from endemic
countries only, those from the other countries may include immi-
grants from the Spanish speaking Caribbean countries (Cuba and
the Dominican Republic) where Chagas disease is not endemic.
The number of immigrants to Spain from Latin American coun-
tries was 1,808,771 in 2008; 1,678,711 were from the 17 countries
endemic for T. cruzi.Table 3 shows the number of immigrants from
each originating country, and estimates that 5.2% (86,948) may har-
bor T. cruzi in 2008. The Latin American countries with the highest
number of immigrants to Spain were Ecuador, Colombia, Bolivia,
and Argentina. However, Bolivians, Argentineans, Colombians and
Paraguayans were the immigrant groups with the highest number
Table 2
Latin American legal immigrants in selected European countries: expected number of T. cruzi infection among immigrants, and number of subjects that would need medical
attention due to Chagas disease.
Countries Number of immigrants Total Estimated of immigrants
infected with T.cruzi, 2.9%
Expected number of immigrants infected with T.
cruzi that have or would have Chagas disease
South America Central America and Mexico
Austria 4,174 759 4,933 143 29
Belgium (a) 7,972 1,102 9,074 263 53
Denmark 3,095 613 3,708 108 22
Finland 971 277 1248 36 7
France (e) 25,357 3,950 29,307 850 170
Germany 66,459 10,270 76,729 2,225 445
Greece (b) 494 75 569 17 3
Italy (f) 167,197 11,599 178,796 5,185 1,037
Luxembourg (c) 601 45 646 19 4
Netherlands 19,714 1,638 21,352 619 124
Norway 4,450 535 4,985 145 29
Portugal (d) 55,366 386 55,752 1,617 323
Sweden 15,778 1,815 17,593 510 102
Switzerland 28,239 2,792 31,031 900 180
United Kingdom (b) 42,204 5,147 47,351 1,373 275
Total 442,071 41,003 483,074 14,010 2,803
Data from 2005 obtained from Padilla & Peixoto, 2007, except calculations on estimates of immigrants infected with T. cruzi and those that would need medical attention.
Exceptions to 2005 data were (a) data were for 2004; (b) for 2003; (c) for 2001;and (d) for 1999;(e) residence allowed up to 2004; and (f) residence allowed up to 2005.

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Table 3
Estimates on the number of Latin American immigrants in Spain by country of origin, expected number of immigrants with T.cruzi infection, and these that would need
medical attention, 2008.
Countries Number of immigrants Estimated T.cruzi infected
immigrants
Estimated number of immigrants that
would need medical attention
Argentina 196,447 16,109 3,222
Bolivia 236,023 36,348 7,270
Brazil 119,209 1,550 310
Chile 48,939 1,370 274
Colombia 284,043 11,078 2,216
Costa Rica 1,651 71 14
Ecuador 415,535 4,986 997
El Salvador 5,029 307 61
Guatemala 3,424 270 54
Honduras 21,520 1,248 250
Mexico 23,673 166 33
Nicaragua 8,391 143 29
Panama 2,228 201 40
Paraguay 66,950 6,226 1,245
Peru 123,173 3,695 739
Uruguay 61,407 737 147
Venezuela 61,069 2,443 489
Total 1,678,711 86,948 (5.2%) 17,390
(). Estimates of percentage of infected immigrants.
of individuals infected with T. cruzi. It was estimated that 16,909
infected immigrants from South America, and 481 from Central
America and Mexico residing in Spain, would eventually require
medical attention because of Chagas disease (Table 3).
Female Latin American immigrants from 12 endemic coun-
tries delivered 32,948 newborns in Spain in 2007. Of them, 1849
were estimated to have been born from mothers infected with T.
cruzi. Considering that 1.3% or 5%, of newborns delivered by an
infected mother whose country of origin was 1 of the 12 coun-
tries listed in Table 4 may be infected with T. cruzi, the number
of congenital cases in Spain is estimated to be between 24 and
92 in 2007 (Table 4). It is most likely that T. cruzi infected immi-
grants in Japan would have originated from those Latin American
countries with a large ethnic Japanese population. According to the
General Immigration Directorate, Ministry of Justice, Japan (2008),
there were in Japan 80,912 immigrants from Brazil and 15,281
from Peru in 2007 (there were also 19,143 immigrants whose
country of origin was not identified), yielding an estimated num-
ber of 1052 and 458 of T. cruzi infections respectively. However,
the higher socioeconomic status of this group at their country
of origin makes this possibility unlikely. Even if unlikely, Cha-
gas disease may occur. A case of Chagasic chronic heart disease
has been diagnosed in a Japanese-Brazilian traveler (Takeno et al.,
1999).
According to the 2000 census, 14,006,502 foreign-born Hispan-
ics live in the United States; 12,858,180 of them were born in the 17
Latin American countries endemic for T. cruzi. It was estimated that
1.9% (245,787 individuals) in 2000 were infected with T. cruzi and
that 20% (49,157 individuals) of those infected have or will have
symptoms and signs of Chagas disease (Table 5). In 2007, the num-
ber of foreign-born Hispanics increased to 18,049,838. Of them,
16,689,172 were from T. cruzi endemic countries; 2% (325,671) are
estimated to be infected and 20% (65,133) may require medical
attention because of Chagas disease. Fig. 1 shows estimates of the
number of Latin American immigrants; the number infected with
T. cruzi; and the potential number with Chagas disease in receiving
countries.
4. Discussion
Despite the difficulties and limitations of using secondary data
for policy decisions, our results provide estimates of T. cruzi infec-
tion and disease cases among immigrant from disease endemic
countries. These estimates depend on several assumptions. For our
estimates we considered that the overall prevalence rate of T. cruzi
is stable and constant by age, geographic area and socioeconomic
status. This approximation may not be completely valid since there
is some evidence that the prevalence of Chagas disease was differ-
ent across decades in many of the endemic countries. Most of the
immigrant population recorded in the US in 2000 and 2007 and
in Spain in 2007–2008, were born in the 1970s or before. In those
years, this group may have been exposed to higher rates of T. cruzi
infection through vector transmission or blood transfusion than the
rate we are using in our estimates. Therefore, we may have under-
Table 4
Estimates of expected number of newborns with congenital Chagas disease depending of the mother’s country of origin, Spain, 2007.
Country of origin of the
mothers 15–44 years old
Number of live
newborns
Number of live newborns from
T.cruzi infected women
Number of expected
congenital cases (t= 1.3%)
Number of expected
congenital cases (t= 5%)
Argentina 2,542 208 3 10
Bolivia 6,442 992 13 50
Brazil 2,625 34 0 2
Chile 621 19 0 1
Colombia 5,088 198 3 10
Ecuador 9,300 112 1 6
Honduras 424 25 0 1
México 483 3 0 0
Paraguay 1,533 143 2 7
Peru 2,052 62 1 3
Uruguay 749 9 0 0
Venezuela 1,089 44 1 2
Total 32,948 1,849 24 92

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Table 5
Number of Latin American immigrants in the USA by country of origin and estimates of the expected number of immigrants infected with T.cruzi, and immigrants that would
need medical attention, 2000 and 2007.
Country 2000 2007
Number of
Immigrants
Estimates of T.cruzi
infected immigrants
Estimates of immigrants that
would need medical attention
Number of
Immigrants
Estimates of T.cruzi
infected immigrants
Estimates of immigrants that
would need medical attention
Argentina 125,220 10,268 2,054 170,306 13,965 2,793
Bolivia 53,280 8,205 1,641 66,368 10,221 2,044
Brazil 212,430 2,762 552 344,929 4,484 897
Chile 80,805 2,263 453 88,271 2,472 494
Colombia 509,870 19,885 3,977 603,653 23,542 4,708
Costa Rica 71,870 3,090 618 87,220 3,750 750
Ecuador 298,625 3,584 717 402,294 4,828 966
El Salvador 817,335 49,857 9,971 1,108,289 67,606 13,521
Guatemala 480,665 37,973 7,595 683,807 54,021 10,804
Honduras 282,850 16,405 3,281 422,674 24,515 4,903
Mexico 9,177,485 64,242 12,848 11,739,560 82,177 16,435
Nicaragua 220,335 3,746 749 233,808 3,975 795
Panama 105,175 9,466 1,893 103,314 9,298 1,860
Paraguay 11,980 1,114 223 17,212 1,601 320
Peru 278,185 8,346 1,669 414,120 12,424 2,485
Uruguay 25,040 300 60 47,934 575 115
Venezuela 107,030 4,281 856 155,413 6,217 1,243
Total 12,858,180 245,787 (1.9%) 49,157 16,689,172 325,671 (2%) 65,133
(). Estimates of percentage of infected immigrants.
Fig. 1. Migration flows of immigrants from endemic countries for Trypanosoma cruzi, estimates of infected individuals, and the potential number of individuals that may
have or may develop Chagas disease in the destination countries.
estimated the expected number of infected individuals (Yadon and
Schmunis, 2009). On the other hand, we also applied the prevalence
rates of 1990 to the smaller portion of the population recorded in
the US census 2000 or 2007 and in Spain 2008 that were born in
the late 1990s, and thus would have been exposed to a lower risk.
This may have led to the overestimation of the expected number
of infected immigrants. However, this overestimation is unlikely
because in the 1990s, vector transmission was only interrupted in
2 countries; Uruguay in 1997 and Chile in 1999.
Thus, the number of the immigrant population that could have
benefited from the decrease in infection rate in their country of
origin after 1990 was small. In 2007, the median age of the Mexi-
cans immigrants was 35 years; the Central American immigrants,
36 years, and for the South American immigrants, 40 years (Pew
Hispanic Center, 2009). These data suggest that most immigrants
were born before 1980. Another potential source of error is the
assumption that the population emigrating from a Latin Ameri-
can country has been exposed to the same risks as those that did
not emigrate. In fact, T. cruzi infection is not evenly distributed
in the endemic countries. Not taking into account the geograph-
ical variability (rural vs. urban) and socioeconomic variables of the
immigrants could bias the results in two ways. If a high propor-
tion of the population that emigrates comes from a poor rural area,
with a high prevalence rate of T. cruzi infection, the use of the
overall prevalence in the country of origin would underestimate
the proportion of infected immigrants. In contrast, if most of the

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emigrating population is coming from a non-endemic urban area
of their country, the opposite bias will occur, and the number of
infected individuals will be overestimated (Yadon and Schmunis,
2009). Unfortunately, available data on immigrant population did
not include information of the geographic area (endemic or not for
T. cruzi) or the social status in the country of origin.
The international movements of the Latin American popula-
tion have undergone notable changes in recent decades, especially
in countries outside the traditional T. cruzi endemic region.
These transformations bring attention to the importance of hav-
ing adequate information for health policy-making in destination
countries of immigrants from endemic countries, where Chagas
diseases cases would need to be prevented or detected, and treated.
This is especially the case in Australia, Canada, European countries,
Japan and the US, although it would also be true for any country
receiving immigrants from Latin American countries.
Although there is now ample evidence that there are high num-
bers of immigrants from Latin America living abroad that may
harbor T. cruzi, it takes time to implement specific measures to
prevent infection though blood donation, organ transplants, or to
implement secondary prevention of congenital Chagas disease.
In Canada, a survey on immigrants and refugees, that showed a
1% seroprevalence for T. cruzi (Steele et al., 2007) and a recent case
of a possible transmission of T. cruzi by an infected needle, spurred
new interest in this disease (Kirkey, 2007). Blood and organ donors
are required to fill a questionnaire that include questions related to
Chagas disease, and individuals known to have the disease are not
allowed as donors (Lennox et al., 2007).
In most European Countries, attempts to prevent transmission
of T. cruzi are limited, and there are few efforts to carry out surveys
on the prevalence of T. cruzi in blood donors or other popula-
tion groups. In France however, a survey demonstrated less than
0.7‰prevalence for T. cruzi among 1570 army recruits mainly from
French Guyana (Kerleguer et al., 2007).
Recently, an acute case acquired in French Guiana as well as 8
chronic cases were also reported in France (Lescure et al., 2008).
The French Government has a preventive policy regarding Chagas
disease. Donors born in an endemic area or from a mother coming
from an endemic area are screened. Donors traveling in endemic
areas, when returned from those areas, regardless of the length of
stay, are deferred from blood donation for four months. In addition,
blood collection in the overseas territory of French Guyana was
halted, and the blood supply comes directly from France (Assal and
Aznar, 2007). In Italy, positive serology for T. cruzi was found in 1%
of 99 Latin American pregnant women; 23% of 99 Bolivian residing
in an Italian city; 4% of 99 adopted children; 0.6% (an acute case
acquired in Brazil) of 155 expatriates/travelers; and 6.7% of 268
patients (Anselmi et al., 2009).
Serology was positive in 12.8% of 1012 mostly undocumented
Latin American women living in Switzerland. The highest preva-
lence, 26.2%, was found among 127 immigrants from Bolivia
(Jackson et al., 2009a).
Since the early 1990s, Spain was the destination of choice for
thousands of Latin American immigrants. In 2008, the majority of
the 86,947 individuals estimated to be infected with T. cruzi in Spain
were born in South America. The seroprevalence rate in Barcelona
for 1770 blood donors at risk (those from endemic countries or
that have resided there), 1524 of whom were born in the endemic
areas, was 0.62%, but increased to 10% among 59 Bolivian immi-
grants (Piron et al., 2008). Serology was also positive in 4.2% of 98
samples from women of child bearing age (Soriano et al., 2007). In
Madrid, serology was positive in 18% of 230 pregnant women from
Bolivia, and one case of vertical transmission was detected during
the follow up (Gonzalez-Granado et al., 2009). In Valencia, 10% of
626 Latin American pregnant women, and 1.24% of 3625 donors at
risk were positive for T. cruzi (Parada et al., 2008). Cases of trans-
fusional transmission have been reported in Spain (Flores-Chaves
et al., 2008a; Perez de Pedro et al., 2008). T. cruzi antibodies were
also found in 3 out of 98 cord blood donors and all positive donors
were from Bolivia (Solves et al., 2009).
From the above, it is obvious that the country of origin of the
immigrants is a risk factor. Thus, it is important that the number of
immigrants from some of these countries in Spain may be higher.
It has been estimated that the number of Bolivian immigrants is
between 350,000 (Sack, 2009) and 400,000 (Perrogon, 2007), and
of the Argentineans, 262,000 (Schmunis, 2007b). If these reports
are correct, the number of infected immigrants in Spain would be
much higher than the numbers presented here.
In Spain, blood donor screening is mandatory under Royal
Regulation # 1088 on blood donation, which automatically and
permanently defers donors with positive serology for T. cruzi (Real
Decreto, 2005). If tests for screening are not available, individu-
als born in endemic areas, newborn from mothers coming from
endemic areas, and those who received transfusions in endemic
areas, need to be excluded from donating blood labile components.
These individuals may donate blood only when having a negative
serological test for T. cruzi.
In the USA, our estimates indicate that overall, 1.9% in 2000,
and 2% in 2007, of the immigrants from the 17 countries endemic
for T. cruzi may be infected, and 49,157 and 65,133 respectively,
may need medical attention. Skolnick (1989) estimated 100,000
T. cruzi infected persons in the US among immigrants from Latin
America. Milei et al. (1992), calculated 370,000 infected individu-
als, with 74,000/75,000 of them having a Chagasic cardiomyopathy.
The majority of these individuals either were undiagnosed or misdi-
agnosed. Recently, using immigrant data and prevalence rates from
2005, it was estimated that 300,167 individuals were infected by T.
cruzi in the US, and 30,000–45,000 of them had a cardiomyopathy
(Bern and Montgomery, 2009). However, their results and ours are
not comparable because data and assumptions used were differ-
ent. Another recent report, estimated that the number of infected
individuals are up to 1 million (Simon and McKay, 2009). As our
estimates on the number of immigrants are for the years 2000
and 2007, they will underestimate the inflow of the documented
or undocumented immigrants from the 17 endemic countries that
arrived in the US after 2007. In 2008, it was estimated that there
were 11.9 million unauthorized immigrants in the US; of which 59%
(7,000,000) come from Mexico (Passel and Cohn, 2009a). Only from
those undocumented Mexican immigrants, one might expect to
find 49,000 T. cruzi infected individuals, of whom 9800 will require
medical services.
Although data in the US suggest that 1 in 25,000 blood donors
may be infected with T. cruzi, seropositive rates in Los Angeles and
Miami are higher; 1 per 7500 donors and 1 per 9000 respectively.
Among directed donors in Los Angeles the seropositivity rate was
higher, one in 2400 (Leiby, 2005). In a trial with 148,969 sam-
ples, one in 4655 samples was confirmed positive in 2006–2007
(Stramer et al., 2007). The US Food and Drug Administration (2006)
recommended testing of blood donors with an approved EIA assay.
Although testing is not yet mandatory, it is estimated that about 65%
of the blood supply is being screened. The AABB (formerly known as
the American Association of Blood Banks) recommends that blood
donations that have repeatedly tested reactive by ELISA should
be quarantined and removed from distribution, and the donor be
deferred from making donations (CDC, 2007). Recipients of blood
components from donors that tested positive should be identified
and tested for T. cruzi infection. Those that tested positive for T.
cruzi, their at-risk family members, children from infected mothers
and potentially infected recipients, should receive a comprehensive
clinical assessment (CDC, 2007).
Either because of accidental diagnosis of T. cruzi infection or
because subjects present symptoms, those individuals will need

Please cite this article in press as: Schmunis, G.A., Yadon, Z.E., Chagas disease: A Latin American health problem becoming a world health problem.
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G.A. Schmunis, Z.E. Yadon / Acta Tropica xxx (2009) xxx–xxx 7
expert medical supervision. It is a welcome development that train-
ing of medical personnel on Chagas disease became available in
Spain in recent years, and clinics with enough expertise to treat
Chagas disease have been established in several cities (Florian Sanz
et al., 2005; Gazcon, 2005; Gazcon et al., 2008; Manzardo et al.,
2008; Mu˜
noz et al., 2009; Perez de Ayala et al., 2009). In the US, the
first clinic specifically focused in treating Chagas disease opened in
California in 2007.
Congenital Chagas disease has been diagnosed in Sweden
(Pehrson et al., 1981), Switzerland (Jackson et al., 2009a,b), and
Spain (Riera et al., 2006; Guarro et al., 2007; Mu˜
noz et al., 2007;
Flores-Chávez et al., 2008b). Our estimates in Spain, suggest that
there are at least 24–92 cases of congenital Chagas disease per year
that remains undiagnosed.
In Houston, TX, in the US, among 2107 Hispanic and 1658 non-
Hispanic pregnant women, 0.3–0.6%, depending on the test, was
positive for T. cruzi (Di Pentima et al., 1999). Up to now there are
only 3 potential cases of vertical transmission described in the US,
2 of them not from immigrant women (Leiby et al., 1999; Buekens
et al., 2008). It is estimated that 63–315 (Bern and Montgomery,
2009) and 83–635 congenital cases (Yadon and Schmunis, 2009)
may have been be undiagnosed yearly in the US.
As only secondary prevention is possible for congenital Chagas
disease, early detection is a must. The experience in Latin America
shows that when cases are being looked for, they are readily found.
Despite current economic uncertainties, remittances to Mexico
reached $25 billions, Brazil $7.2, Colombia $4.8, Guatemala $4.3,
El Salvador $3.8, Peru $2.9, Ecuador $2.8, and Bolivia $1.0 billion,
in 2008 (Jordan, 2009). These remittances are important sources
of income for the countries of origin of the expatriates. In spite of
the above, the flow of new immigrants arriving from Mexico, the
bulk of the immigrants in the US, has declined sharply since mid-
decade. On the other hand, the Mexican immigrants that are already
in the US are remaining (Passel and Cohn, 2009b). In any case, the
percentage of immigrants infected with T. cruzi will decrease in the
long term as the control program in their country of origin becomes
successful.
Despite that estimates presented here are an approximation to
the problem, they show that globalization of Chagas disease has
become a wide spread public health and medical problem. These
figures might be used by policy makers as a base line to develop
a plan for prevention and treatment of acute and chronic Chagas
disease in the receiving countries. Answering the challenges that
this infectious disease represents, will require collaboration from
all stakeholders, from health authorities and health personnel to
the Hispanic community. Once all of them are aware of the problem,
it would be easier to implement prevention and control measures.
Acknowledgments
The authors thanks Ms. Carmen Chand for assistance in collect-
ing the references; Mr. Jiro Nakamura for finding and translating
the number of immigrants from South America to Japan in 2007;
Dr. Stephen Ault for reviewing the manuscript; and Dr. Sondra
Schlesinger, and Ms. Katherine Darling for assistance in editing the
manuscript.
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