an epidemiological overview on oral outbreaks of chagas ... · student dina vemming oksen umeå...
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Student Dina Vemming Oksen
Umeå International School of Public Health
Epidemiology and Global Health
Autumn 2011
Thesis, 15 ECTS
Degree of Master of Science. Main field of study: Public Health
Specialisation: Epidemiology
60 ECTS
An epidemiological overview on oral outbreaks of Chagas disease in South America
Dina Vemming Oksen
Nr 8/2012
0
An epidemiological overview on
oral outbreaks of Chagas disease in South America
Dina Vemming Oksen
2011
Miguel San Sebastian Chasco, MD, PhD. Department of Public Health and Clinical Medicine/Epidemiology and Global Health, Umeå University, Umeå, Sweden
Pedro Albajar Viñas, MD, PhD. WHO/HTM/NTD, Geneva, Switzerland
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Acknowledgements
I would like to extend a warm thanks to my supervisors Pedro Albajar Viñas from the
Neglected Tropical Disease department at WHO and Miguel San Sebastian Chasco from
the department of Public Health and Clinical Medicine at Umeå University. Without their
help and guidance I would have never been able to write this thesis. I was able to study
oral outbreaks of Chagas disease from the best possible vantage point at the library in
Geneva and the Chagas disease unit at the department of Neglected Tropical Diseases,
and I am very grateful.
I would also like to thank my wonderful family and boyfriend for their great help and
support.
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Index
Abstract ............................................................................................................................... 4 1. Introduction ..................................................................................................................... 5
2. Background ..................................................................................................................... 6 2.1 Chagas disease at a glance ........................................................................................ 6
2.1.1. The Amazon Region ......................................................................................... 7 2.1.2. Triatomines and T.cruzi .................................................................................... 8 2.1.3. Pathological and clinical picture of Chagas disease ......................................... 8
2.1.4. T. cruzi transmission routes .............................................................................. 9
2.2. Oral transmission and oral outbreaks in the scientific literature............................ 10
2.2.1. Severity of oral outbreaks ............................................................................... 10 2.2.2. Oral transmission and oral outbreaks .............................................................. 10 2.2.3. Animal reservoirs of T. cruzi .......................................................................... 11 2.2.4. Food contamination ........................................................................................ 11
2.2.5. Surveillance, control and prevention of oral outbreaks .................................. 13 2.2.6. Travel medicine .............................................................................................. 13
3. Aim ............................................................................................................................... 14 4. Methods......................................................................................................................... 15
4.1. Study design ........................................................................................................... 15
4.2. Data collection methods ......................................................................................... 15 4.2.1. Definitions....................................................................................................... 15
4.2.2. Search words ................................................................................................... 15 4.3. Selection method .................................................................................................... 16
4.3.1. Inclusion criteria ............................................................................................. 17 4.3.2. Exclusion criteria ............................................................................................ 17
4.3.3. ProMED and EMS .......................................................................................... 17 4.4. Limitations ............................................................................................................. 17 4.5. Method of analysis ................................................................................................. 18
5. Results ........................................................................................................................... 20 5.1. Published cases .................................................................................................. 20
5.2. Synthesis of outbreaks extracted from ProMED mail ....................................... 22 5.3. Synthesis of outbreaks extracted from EMS ...................................................... 22
5.4. Mortality, outbreak source and social occasion ................................................. 23
5.5. Map of oral outbreaks ........................................................................................ 25
6. Discussion ..................................................................................................................... 27 6.1. Emerging transmission form? ............................................................................ 27 6.2. Geographical distribution................................................................................... 27 6.3. Surveillance system in the Amazon Region ...................................................... 28 6.4. The social aspect of transmission ...................................................................... 28
7. Recommendations ......................................................................................................... 30 7.1. Food safety prevention measures ........................................................................... 30 7.2. Travel medicine implications of oral outbreaks..................................................... 30 7.3. Prevention target areas ........................................................................................... 31
7.3.1. Primary, secondary and tertiary prevention .................................................... 31
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8. Conclusion .................................................................................................................... 33 9. References ..................................................................................................................... 34
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Abstract Introduction: Chagas disease is one of the world's neglected tropical diseases. The
World Health Organization (WHO) estimates that presently 10 million people worldwide
are infected. Recently the oral transmission of Chagas disease has been given more
attention as a result of more outbreaks being detected in the Amazon region. There are
still many uncertainties regarding oral outbreaks, one being the epidemiological picture,
another whether oral transmission is an emerging transmission mode. Moreover, oral
transmission is possibly more lethal as a form of transmission. Aim/objectives: Main
objective: Perform an epidemiological overview of available literature on the oral
outbreaks of Chagas disease in the countries of the Amazon Region. Specific objectives:
Mapping oral outbreaks of Chagas disease according to available literature, Event
Management System (EMS) and ProMED-mail data. To make a timeline of published
cases and retrieve information on mortality, source and form of social gathering.
Method: Literature review with a research synthesis of known cases of oral outbreaks
and a meta-analysis of the data found. The search was conducted in PubMED/MEDLINE
and LILACS. The limitation of the study was mainly access to South American journals.
Results: Geographically there was a broad outbreak distribution and some clustering.
Oral outbreaks were more extensively described in the Brazilian literature; however,
Venezuela, Colombia and Bolivia had all reported oral outbreaks. Outbreaks occurred in
rural and urban areas. Mortality of oral outbreaks ranged from 0-6 deaths; number of
cases from 3-103. The source of the oral outbreaks was most often hypothesized to be
palm fruit juice and undercooked meals. Social occasions were most often families
sharing meals and drinks. The timeline showed that outbreaks were already mentioned in
1965. From then there was a large interval, and in the last decade the number of oral
outbreaks has risen. Discussion: Oral outbreaks occur in several countries of the Amazon
Region, and in both urban and rural areas. It was not possible to say if outbreaks are
emerging; however, it was clear that there is a current risk of oral transmission for local
people as well as tourists. Oral outbreaks can be large and severe, and rapid treatment
needed. The conclusion from this thesis is that oral outbreaks are not sufficiently
monitored. The strengthening of surveillance systems for oral outbreaks is a priority to
establish further prevention measures.
Keywords: Oral, transmission, outbreak, Chagas disease, Amazon
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1. Introduction
Chagas disease is one of the world's neglected tropical diseases. At present, the World
Health Organization (WHO) estimates that 10 million people worldwide are infected (1).
The largest part of infected cases occurs in the 21 Latin American countries. Chagas
disease was restricted to Latin America for many years. This pattern has changed as cases
in the last decades have occurred in the Region of the Americas, the Western Pacific
Region and the European Region, as well (2, 3). This new pattern is mainly caused by
population movement such as migration, but also through blood transfusion, congenital
transmission and other less frequent routes of transmission (4).
Transmission of Chagas disease can occur in several different ways, including the
contact of any skin break or mucosa with infected faeces of vectors, through transfusional,
congenital transmission or organ transplantation and even laboratory incident. Oral
transmission of Chagas disease has been considered to be a rare transmission form (3, 5).
Recently, oral transmission has been given more attention as a result of more outbreaks
being detected especially in the Amazon region (6-11). As of yet, there are still many
uncertainties regarding oral transmission, one being the epidemiological picture, and also
whether oral transmission is an emerging transmission mode, or if it has in fact been there
all along. It has been estimated that there is an increase of 2.2 new cases per month of
oral transmission in Brazil, and that this figure is underestimated mostly because of the
access limitation of the Amazon region (12).
People in the countries of the Amazon Region have been struggling with Chagas
disease for centuries. Oral transmission is possibly a more lethal form of transmission,
which rise questions on both long term morbidity and mortality (13). One oral outbreak
in Santa Catarina, Brazil in 2005 had a lethality rate of 12,5% (12). Family episodes with
suggested oral transmission have been increasingly discovered, especially in Brazil (14).
Oral transmission has implications not only for the people living in the countries of the
Amazon Basin, but also for travelers to these regions. Cases of acute Chagas disease have
been reported in European citizens returning to Europe from travels in South America (5,
15).
In view of the general lack of knowledge on oral transmission of Chagas disease,
the importance of undertaking an epidemiological overview of this transmission form is
evident from the public health point of view. Furthermore, there is a lack of surveillance
of oral outbreaks in the countries of the Amazon Region, which may cause many cases to
go undetected and untreated. Creating a surveillance system to detect acute cases
efficiently and in a timely fashion may be an overlooked priority for those countries. This
thesis will attempt to provide an overview of oral transmission in South America, looking
at cases reported in the literature throughout history.
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2. Background
2.1 Chagas disease at a glance
In the following, key aspects of Chagas disease will be presented to give a brief general
overview of this neglected tropical disease and its many public health aspects.
The Brazilian scientist and medical doctor Carlos Chagas discovered the disease
that now bears his name in 1909, whilst he was working in a poor rural area of the
Brazilian State of Minais Gerais. Chagas noticed specific clinical symptoms in his
patients and made the connection between the presence of the haematophagous
triatomine bugs and these symptoms. During only a few years Carlos Chagas managed to
map the aetiology of Chagas disease, the entomologic aspects of the disease-bearing
vectors and to demonstrate the necessity to establish care for patients suffering from
Chagas disease (1, 16).
Chagas is caused by the protozoan parasite Trypanosoma Cruzi (T.cruzi) and is
transmitted primarily through insects of the triatomine subfamily. These vectors infect
both humans and a very large number of other mammals and are present all over the
Americas. There is no vaccine for Chagas disease, and the most effective ways of
preventing it is through vector control, improvement of housing and hygiene conditions
and blood screening to avoid infection through blood transfusion and organ
transplantation. Chagas disease has an acute phase lasting about two months after
infection and a chronic phase lasting for the lifetime of the patient without successful
antiparasitic treatment. Chagas disease is curable if it is treated shortly after infection, in
the acute or early chronic phase of the disease. Efficacy of the treatment decreases with
the length of the infection. Specific treatment for cardiac, digestive, neurological or
mixed alterations can also become necessary (4). Most patients are asymptomatic, and
clinical manifestations of the disease and antiparasitic treatment response vary according
to different geographical areas (1). Thus there are various public health aspects of Chagas
disease to take into consideration for surveillance, control and prevention measures.
Since the time of Carlos Chagas there has been little development in
underdiagnosis as well as treatment offer and a large number of people in South America
are estimated to die of Chagas disease untreated and in silence. WHO estimates that over
25 million people are at risk of the disease, and that more than 10 000 people died from it
in 2008 alone. Chagas disease has even spread outside Latin America. It has been
detected in the United States of America, Canada, many European countries and some
Western Pacific countries like Australia and Japan (17). The Amazon region had long
been considered not to be endemic of Chagas disease, however, in recent years there has
been more attention on the area due to an increased number of detected acute cases in the
region (6-11, 14, 18).
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2.1.1. The Amazon Region
The Amazon region is a diverse region in regards to environment, nature and population.
The countries of this Region include Bolivia, Brazil, Colombia, Ecuador, French Guyana,
Guyana, Suriname, Peru and Venezuela. The official languages are Portuguese in Brazil,
French in French Guyana, English in Guyana, Dutch in Suriname and Spanish in the
remaining Amazon countries. The region predominantly exists of tropical humid forest
area, and over 30 million people live there, of which 6 million people alone are in the
Brazilian Amazon. Around 260 000 Indigenous people live in the region, communicating
in 170 different languages. Little is known yet, about the epidemiological status of
endemic infectious diseases in this region, Chagas disease included (19). The Amazon
region has not been considered endemic of Chagas disease until the last decade, however
that has changed. Human encroachment of the natural habitats of the disease bearing
vectors has forced them to adapt to human settings. Human migration, uncontrolled
deforestation, road construction, mining and other commercial activities as well as
keeping large animal pastures have changed the epidemiological pattern of Chagas
disease (7, 19, 20).
The Amazon region consists largely of a rural and poor population. This has
implications in the sense that Chagas disease and poverty have been closely linked
throughout history. For centuries poor housing conditions in rural settings and more
recently slum dwellings of larger cities have been a risk factor of transmission by
domesticated and peri-domesticated insects (21, 22). Additionally to poor hygiene
conditions, poor dwellings, like thatched straw huts, enable the domestication of vectors.
Furthermore, living in close proximity with pets and animals facilitate peri-domestication
of the vectors, and the risk of human infection increases. By encroaching on the natural
life cycle of the vectors in the Amazon region, humans have become part of the feeding
cycle of the vectors, as well as a part of the life cycle of the parasite T.cruzi (7).
Mainly south of Amazon Basin there have been significant achievements with
control programs, which have included vector control and blood screening approaches.
At the same time, an improvement of housing conditions has occurred, especially for the
rural population. Since the 1990s there have been considerable advances in parasite and
vector control in South America, largely due to initiatives like the Southern Cone, Central
American, Andean Pact and the Amazonian Intergovernmental Initiative in cooperation
with the Pan American Health Organisation (PAHO) (4). Transmission by domiciliated
vectors has been considerably reduced in many South American countries, and also
transmission by blood transfusion has been reduced through these multinational
initiatives (1). Brazil, Chile, Uruguay and Venezuela, for instance, have reduced the
incidence of Chagas disease considerably through programs, but also due to a decrease in
population and improved housing conditions in rural areas. Nevertheless, in Bolivia,
Paraguay and southern parts of Peru, Chagas disease is still highly prevalent and control
measures, including detection and treatment are insufficient. Despite advances in
Colombia, Ecuador, Central America and Mexico the situation is quite similar, especially
considering patient care (4, 22).
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2.1.2. Triatomines and T.cruzi
To understand the epidemiology of Chagas disease one needs to look at the transmission
vector and its particular habits. The T.cruzi parasite is transmitted to humans by vectors
of the Reduviidae family and the subfamily of Triatomines. These insects feed on
mammals by sucking blood, and T.cruzi is most often transferred via their faeces,
deposited on the skin of the host after feeding. The parasites are able to penetrate through
mucous membranes as well as skin injuries, when the host scratches the skin after being
bitten (20). There are many popular names for the vector. In Brazil for instance a
common name for the vector is Barbeiro- "the barber". In Argentina, Bolivia, Chile,
Paraguay and Uruguay they are called Vinchucas. In Colombia, Peru and Venezuela they
are called Chipos and in Central America, Mexico and Panama they are known as
Chinches. The English name is the kissing bug (22). The quantity of local names suggests
that humans have known the insects for a long time. Around 100 different triatomine
species are susceptible to infection with the T.cruzi parasite. In Argentina, Bolivia, Brazil,
Chile, Paraguay and Peru the principal vector species has been Triatoma Infestans. In
Brazil, the species Panstrongylus megistus and Triatoma sordida are also prevalent. In
Venezuela Rhodnius prolixus is present and in Central America Triatoma dimidiatea.
Apart from the triatomine insects, T.cruzi is known to infect eight different mammalian
orders. In the Amazon region T.cruzi is commonly found in animals (22). The
geographical diversity of the parasite bearing vectors is evident. Since vectors are more
or less prone to domestication, and because they carry different T.cruzi strains it is
necessary to take vectors species into consideration for prevention as well as control
strategies.
2.1.3. Pathological and clinical picture of Chagas disease
The parasite T.cruzi produces pathological processes in mammals that can occur in
various organs and tissues. When T.cruzi is transmitted it invades the victim’s
bloodstream and the lymphatic system. Hereafter it nestles in the muscle and cardiac
tissue, which causes inflammation and immune system responses (23). Chagas disease
has an acute as well as a chronic phase. Morbidity and mortality are higher in the acute
phase for children under five, immune-suppressed people or people with high parasitemia
as in patients from outbreaks of food-borne Chagas disease (5, 23).
The acute phase can occur at any age in disease endemic areas, however, the
highest frequency is before the age of 15, typically starting in the age group 1-5 years.
The acute phase of Chagas disease usually lasts 6-8 weeks, and most frequently is oligo-
or asymptomatic. After the acute phase most patients appear to be healthy. The infection
by T.cruzi can then only be detected serologically or through parasitological tests (3, 24).
In the acute phase, if the transmission is vectorial, visible port of entry can be identified,
such as the chagoma, a skin lesion in exposed areas of the body, or the Romaña's sign, a
purplish oedema on the lids of one eye. The sign occurs only in about 10% of infected
persons, and can easily be misdiagnosed with conjunctivitis, for example, which is
common in rural areas. Other clinical features of the acute phase, especially prevalent in
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infected children, are fever, persistent fast heartbeat, swollen lymph nodes, oedema and
liver and spleen enlargement. Generic and unspecific symptoms include; diarrhoea,
vomiting, headache, muscle pain, loss of appetite and extreme fatigue (22, 25). These
symptoms are not very specific, and can easily be confused with other disease aetiologies.
When the patient enters the chronic phase of Chagas disease it will last for the
lifetime of the individual without successful antiparasitic treatment. The phase starts
when parasitemia falls to a level where it is undetectable with direct parasitological tests,
and when symptoms and clinical manifestations typically disappear. Depending on the
geographical area, 10 - 40% of patients in the chronic phase will develop lesions in target
organs according to the T.cruzi strain they are infected with and the host immune
response, among others (3). The most common manifestations of chronic Chagas disease
are mainly cardiomyopathy and also intestinal mega syndrome. Cardiomyopathy is found
everywhere, from North to South America. Mega syndrome occur more often south of
the Amazon Region (20). These differences are explained, among others by the presence
of different strains of the parasite T.cruzi in different regions. Up to 30-50% of infected
people, however, remain in an indeterminate form for their whole life, showing no
symptoms (1, 22).
Chagas disease can be challenging to diagnose. There are several diagnostic tools
including, direct parasitological tests, serological tests, molecular tests, hemaculture and
xenodiagnosis (9, 26). Parasitemia is generally high in the acute phase (25). After this
phase the parasitemea level most often stabilized because of the immune reaction of the
patient. The parasite then nestles in specific target tissues of the body, preferably heart or
muscle of the digestive system, thus making it difficult to isolate the parasite in the
patient’s blood stream. Oral transmission in particular is often characterized by very high
parasitemia in the bloodstream, probably due to higher inoculum of infection (13, 25).
2.1.4. T. cruzi transmission routes
The list of possible infection routes of Chagas disease includes vectorial, transfusional
(through T.cruzi infected blood), congenital, through organ transplantation, oral
transmission and accidental, through laboratory accidents (22). Vectorial transmission
happens when the bug feeds on humans and defecates, and the human then smears faeces
into the punctured skin, and become infected with T.cruzi. Vectorial transmission is
considered the main transmission form in Latin America, whereas outside of Latin
America the main transmission forms are transfusional, congenital and accidental due to
the absence of the vector (5). In 2006 WHO certified Brazil as being free of transmission
through Triatoma infestans, the main intradomicilliary vector of Chagas disease (12).
However, with the new reports of oral transmission in the Amazon region, this victory
was only partial (6-11). Brazil and other countries of the Amazon region now have to
face the challenge of the sustainability of the vectorial achievements through
entomological surveillance and the problem of an incipient knowledge of oral
transmission and oral outbreaks.
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2.2. Oral transmission and oral outbreaks in the scientific literature
Oral transmission is a transmission route that, like Chagas disease itself, has not received
much attention in previous literature on Chagas disease. The following provides an
overview of how oral transmission has appeared and reappeared in the scientific literature,
since this mode of transmission was first hypothesized. The terminology and perception
on the transmission mode’s technical features, its feasibility and the actual prevalence of
it has changed throughout time.
2.2.1. Severity of oral outbreaks
Oral transmission of Chagas disease may or may not present more severe outcomes for
the patient in the chronic phase. The inoculum or amount of T.cruzi at the initial infection
is possibly important for how Chagas disease develops in the patient. A Brazilian study
showed that patients with a known severe acute form had the most severe chronic forms
(23). A very high quantity of parasites in the patient is the most plausible hypothesis of
severe acute phase that often characterizes oral transmission of Chagas disease. This
means that the chronic phase can have higher morbidity for victims that have been
infected with Chagas disease orally. Moreover, the mortality of oral transmission is high
and the risk is higher for younger children and immune-suppressed people more
vulnerable to high parasitemia.
2.2.2. Oral transmission and oral outbreaks
Oral transmission of Chagas disease has been hypothesized to derive from several
different types of food contamination. The most commonly mentioned hypothesis is
transmission through ingestion of food contaminated by infected insects or their faeces.
Oral transmission has also been mentioned to happen through ingestion of food
contaminated with the urine or anal gland secretion from the opossum (Didelphis
marsupialis). Transmission to infants through mother’s milk is also technically oral
transmission (22, 27). Even ingestion of infected undercooked or raw meat is a possible
oral transmission route that is relevant particularly in relation to certain Indian initiation
practices in Colombia (22, 28, 29).
It is important to make the distinction between oral outbreaks and oral
transmission. Oral transmission is a term describing the way the T.cruzi parasite is
transferred to the host. Oral outbreaks however, are related to food contamination and
when two or more people are infected at the same time and place. Dias (28) describes
outbreaks as occurring most often in secluded, defined geographical spaces in a specific
moment with different types of food involved, such as sugar cane or açai juice, or other
palm fruit juices, soup, under-cooked meat, milk and others. Outbreaks in the Amazon
Region characteristically occur in small groups of people, like families, that share a
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common meal (7, 30). This thesis will focus on oral outbreaks described in the scientific
literature; however the technical features of oral transmission will also be described in
some detail because of the rather complex nature of the transmission form.
2.2.3. Animal reservoirs of T. cruzi
In general, oral transmission has been mentioned sporadically in the scientific literature
throughout history. The hypothesis of oral transmission was initially mentioned in
connection with carnivorous transmission of Chagas disease, where carnivorous animals
fed on other animals infected with T.cruzi and T.cruzi was transferred orally. As early as
1921, Nattan-Larrier experimented on oral infection of mice via blood infected with
T.cruzi (31). Several people experimented on oral transmission of Chagas disease in
animals in the early 30ies (32-35). In 1939 Mazza et al. experimented on T.cruzi infection
by giving milk with infected insects to dogs (27). Diaz-Ungria (1968) macerated flies
from a highly vector infested area in Venezuela and fed a dog with contaminated milk.
The dog then presented symptoms of acute Chagas disease (36). Ribeiro, Garcia and
Bonomo (1987) showed that omnivorous animals, especially the opossum, feeding on
infected animals and triatomines gives high infection indices in same animals (37). This
also highlights the importance of opossums as reservoirs due to the migratory habits of
this animal. In the 2002 WHO report on Chagas disease, oral transmission is mentioned
in connection with the sylvatic cycle in which mammals eat triatomines and other
reservoir hosts and become infected, or when domestic pets eats infected rodents or bugs
(3). In 2009 Roellig and his colleagues investigated scavenging behaviour of raccoons as
a possible oral transmission route of T.cruzi in the sylvatic cycle (38).
These experiments on animals were performed both to investigate and
demonstrate the sylvatic cycle of the T.cruzi parasite in nature, which is important in
relation to vector control measures and to find possible hosts of the parasite that can
come into contact with humans, such as the opossum, or domestic animals such as dogs
or cats. However, the experiments also demonstrated the possibility of oral transmission.
Oral transmission of T.cruzi to humans has not been experimented on directly;
nevertheless the possible oral transmission routes to humans have been investigated,
namely contaminated food.
2.2.4. Food contamination
Food contaminated with T.cruzi is often hypothesized to be the source of oral outbreaks
of Chagas disease (25). There are several aspects of food contamination, among others
the viability of the parasite surviving in the food, the way that the food has been
contaminated and the actual infectivity of ingested contaminated food. Unfortunately it
has never been possible to locate and test the source after an outbreak, because the
symptoms appear some time after the infection occurred (39). This means that any
contaminated food will have been thrown out by the time the outbreak is discovered.
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Even if the food had been saved, the actual survival of the parasites in the food for longer
periods is questionable.
Lainson, Shaw and Naiff (1980) looked at the survival rate of T.cruzi in different
contaminated foods (40). Survival of the parasite was seen for up to three hours in as
diverse foods as milk, beans, beef and rice. Cardoso et al. (2006) investigated the survival
of T.cruzi in sugar cane used to prepare juice and found that T.cruzi was found in the
juice up to four hours after contamination (41). Soarez, Dias, Marsden and Garcia-Zapata
(1987) investigated the survival of trypomastigotes in sugar cane juice and found a 24-
hour survival rate (42). Thus, juice, other beverages and food would be intermediary
transmission vessels of T.cruzi, and therefore difficult to obtain samples from. In Brazil
açai juice has long been suspected as a possible source of outbreaks of acute Chagas
disease (43).
Hervé Rogez from the Technical Institute of Amazônia investigated the possible
ways that T.cruzi could enter into the production of açai juice in Brazil. He found that the
disease-bearing insect prefers palm trees, and in particular the açai palm species. The açai
fruits are collected most often in the morning, and processed directly at a market with
little hygienic procedures; thus, contaminated fruits could easily be processed into the
açai juice (44). Others have also hypothesized on juice production in the Amazon and
oral transmission of Chagas disease, Brazil especially, where juice is often prepared
outdoors during the evening under a strong light that attracts infected vectors, and then
left to cool during night (7, 14). Household contamination of foods is also an issue for
oral transmission. Lainson, Shaw and Naiff (40) speculated that kitchen foods can
become contaminated with T.cruzi from vector faeces or if the entire insect falls into the
food and disintegrate. Much food in the Amazon region is eaten cold, even if it is well
cooked before. Leftovers from the day before will be kept at room temperature and
contamination by the vectors can take place (40). In relation to household contamination
there have also been speculations on transmission by the opossum, because this animal
often enters human dwellings to scavenge for food. Opossums have been shown to
secrete T.cruzi through the anal glands. If the animal secretes on food or kitchen utensils
these would be contaminated with T.cruzi (29). Valente et al. (14) suggests that the
presence of T.cruzi in the anal gland secretions of the opossum, which has both wild and
peri-urban habits, is an important element of oral transmission that should not be
overlooked. In short, research clearly shows the viability of T.cruzi in food and different
possibilities for food contamination have been discussed.
Another issue in regards to food contamination is the infectivity of the parasite
when it is actually ingested as opposed to entering through the skin. Some studies have
suggested that the oral transmission route holds higher infectivity, because T.cruzi can
penetrate the mucous membrane of the esophagus before reaching the gastric cavity (45,
46). Camandaroba, Lima and Andrade (45) experimented on the influence of the parasitic
strain in relation to oral transmission, and found that some strains held higher infectivity
through the oral route. Strains more adapted to the sylvatic cycle have been shown to be
involved in family outbreaks in the Amazon Region (14). Also the higher infectivity may
be connected to the high mortality detected in oral outbreaks (12). A further question is
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whether or not the high parasitemia in the acute phase of an oral transmission case causes
higher morbidity and mortality than other transmission forms in the chronic phase due to
the degree of damage done to the tissue (12, 47).
2.2.5. Surveillance, control and prevention of oral outbreaks
On a global scale, oral outbreaks have only recently been recognized as a target area for
prevention and attention. Current control and prevention recommendations from WHO
include good hygiene practices in food preparation as well as for transportation, storage
and consumption (4). In 2005 a scientific working group initiated by The Special
Program for Research and Training in Tropical Diseases (TDR) coordinated by WHO
and the Pan American Health Organization (PAHO), published a report on Chagas
disease. This report looks at the objectives and recommendations for the future of Chagas
disease. There is no mention of oral transmission, except in relation to mammals eating
infected insects. In 2009, however, PAHO published the guide “Surveillance, prevention,
control and clinical handling of Chagas disease transmitted through food.” This Spanish
guide provides the most extensive information on oral transmission to date for health
practitioners and health workers. There have been several Intergovernmental Initiative of
Surveillance and Prevention of Chagas Disease (AMCHA) meetings in South America
where oral outbreaks have been discussed (48). AMCHA is organized by the individual
countries and WHO. Thus it can be said that there is growing attention on oral outbreaks
globally as well as in the Amazon Basin countries. Prevention and surveillance of oral
transmission, however, is still not present in all countries.
Oral outbreaks are a form of transmission of Chagas disease that needs
surveillance and rapid control and treatment measures. Rapid detection and action is a
necessity to ensure recovery of patients. Oral outbreaks have a different social aspect than
vectorial transmission, as it has been happening in different social settings such as
schools, health facilities and parties (30, 43, 49). Because oral outbreaks are connected
with food handling hygiene and food safety measures, it is necessary to take these aspects
into consideration for prevention and surveillance measures (25).
2.2.6. Travel medicine
As previously mentioned, the production of acai juice in Brazil is an issue for oral
outbreaks as described by Hervé Rogez (44). The juice is sold at markets, and if it is
contaminated there is the possibility of infection of a large number of otherwise socially
unconnected people. The fact that juice and other food products are sold to tourists as
well could have implications for travel medicine, because tourists could become infected
by drinking contaminated juice when visiting such markets in Brazil, or drinking un-
pasteurized juice from similar places. This raises the question on whether oral
transmission should be included in differential diagnosis for travellers and tourists to
these regions.
14
In Europe there is some focus on the immigration aspect of Chagas disease, which
implicates blood transfusions and organ donation, however oral transmission has not
received enough attention (5). Brazil has one reported case of an Italian tourist infected
orally with Chagas disease. This case was discovered in Italy, after the tourist had
returned from Brazil, and later discovered to be connected with an oral outbreak in Santa
Catarina (50). Tourist statistics for Brazil shows that the largest number of travellers and
tourists are from Italy and the United States of America (51). However, Italy currently
has no travel recommendations concerning the risk of Chagas disease (5).
Surveillance could be necessary to establish in the Amazon region to discover the
real number of oral outbreaks, as well as enable treatment. If, the number of oral
outbreaks are indeed higher than estimated this would mean that a lot of people in the
Amazon Region are suffering as well as dying silently from oral outbreaks. This thesis
will attempt to look at the epidemiological distribution of oral outbreaks and try to
determine the need for surveillance in the countries of the Amazon Region.
3. Aim
Main objective:
To perform an epidemiological overview of available literature on the oral outbreaks of
Chagas disease in the countries of the Amazon basin: Brazil, Venezuela, Colombia,
Bolivia, Ecuador, Peru, Guyana, Suriname, and French Guyana.
Specific objectives:
- To map oral outbreaks of Chagas disease in the Amazon Basin according to available
literature and the surveillance systems; Event Management System of WHO and
ProMED- mail from the International Society for Infectious Diseases.
- To make a timeline of published cases and retrieve information on mortality of
outbreaks, source of outbreaks and the form of social gatherings of outbreaks.
15
4. Methods
4.1. Study design
This thesis is a literature review study. It includes a research synthesis on known cases of
oral outbreaks as well as a meta-analysis of the data found (52).
4.2. Data collection methods
The search was conducted in the databases: PubMED/MEDLINE and LILACS. LILACS
is a Latin American and Caribbean health science database. It is a unique source of
information because it contains articles published in local languages such as Portuguese,
Spanish, French as well as English. With regards to time specification there was none,
because the aim included a chronological overview of all oral outbreaks.
4.2.1. Definitions
It was important to define oral transmission and oral outbreaks for the process of data
collection and to define inclusion and exclusion criteria. The following definitions were
formulated and used:
Oral transmission can occur when infected vector faeces come into contact with the
mouth, either through food or simply by touching a contaminated surface and then
putting the fingers in the mouth.
Oral outbreaks happen when a number of people ingest food contaminated with infected
faeces from the vector or the vector itself. An oral outbreak is when two or more
autochthonous cases appear at the same time.
4.2.2. Search words
The search words were chosen to concentrate the search on oral outbreaks of Chagas
disease. Articles on acute cases were initially included because of the possibility of acute
cases not being recognized as oral outbreaks in early literature. English key words were
translated into four different languages for the LILACS search, so as to broaden the
search, and include non - English articles. Seeing that the languages most spoken in the
Amazon Region are Spanish and Portuguese, the translation of search words in these
languages was included. A French translation and search for key words was included
because of French Guyana. Dutch, which is spoken in Suriname and Guyana, was
excluded, as it is not an indexed language in LILACS. The key words and combinations
16
used for the search were very broad so as to include as many articles as possible. The fact
that Chagas disease is a neglected tropical disease necessitated as well as enabled this
search approach. Using Mesh terms was neither feasible nor practical because of the
specificity of the search words themselves (Table 1).
Table 1. Search words English Spanish Portuguese French
Chagas Chagas Chagas Chagas
trypanosomiasis tripanosomiasis tripanossomíase trypanosomiase
Acute cases casos agudos casos agudos Aiguë, cas aigus
oral oral oral orale
outbreaks brotes surtos épidémie
transmission transmissión transmissão transmission
The search was made in PubMed for English results and LILACS for Spanish,
Portuguese and French. LILACS also included translation of the search word to the
indexed languages in each search, which broadened the search. The search words were
combined in the following way:
Chagas/trypanosomiasis + (AND/OR) acute cases/oral/outbreaks/transmission
This gave eight combinations that were used for the English search in PubMED and the
combinations were repeated for Spanish, Portuguese and French in LILACS. All in all
that gave 36 combinations of search words in the four different languages. The search
resulted in 66 articles. After this first search, a second search was conducted manually.
Reference lists of the 66 articles were read and experts at WHO were consulted to
discover any articles that might be missing from the resulting list of articles. These
procedures resulted in 95 articles. All articles were then sorted in EndNote Web ®.
4.3. Selection method
For the overview on oral outbreaks studies with a quantitative disposition was included
with empirical character. After the 95 articles had been entered into EndNote Web ®, full
text and/or abstracts of articles were reviewed and the articles were classified according
to inclusion and exclusion criteria. If inclusion criteria were fulfilled the article was
included. This selection process resulted in a total number of 43 articles. After this a
second selection took place, where the articles were read thoroughly according to a set of
pre-defined information retrieval categories for the analysis. The articles had to contain
information on country, area of case origin and number of cases. This more thorough
selection resulted in 25 articles for the meta-analysis.
Figure 1 displays the search and selection process in the form of a flowchart.
17
4.3.1. Inclusion criteria
Studies where the definition of an oral outbreak was compatible with the description of
the cases in the studies were included. Thus, studies with only one acute case were not
included, or several cases reported in different points of time or different geographical
locations. The study cases had to constitute an outbreak according to the definition of oral
outbreaks provided for this thesis. Geographical restrictions were the countries of the
Amazon Basin: Brazil, Venezuela, Colombia, Bolivia, Ecuador, Peru, Guyana, Suriname,
and French Guyana. Only studies pertaining to these countries were included. This was
done because of the aim to provide an overview of this particular region.
4.3.2. Exclusion criteria
If the case description did not fit the definition of an oral outbreak they were excluded.
Assessment of the quality of the study took place in the sense that the case information
validity or credibility was assessed for all sources. Only published cases were included,
thus government reports and other reports were excluded. In some cases, where older
publications of acute Chagas disease where hypothesized to derive from oral transmission,
the study cases had to constitute an outbreak according to the definition of oral outbreaks
of this thesis. The fact that oral outbreaks have been reported to such a limited degree,
made it necessary to include as much information as possible.
4.3.3. ProMED-mail and EMS
To supplement the scarce material on oral outbreaks, outbreak information was included
from ProMED-mail and the Event Management System of WHO (EMS) according to the
same inclusion criteria as the literature search. EMS and ProMED-mail are international
surveillance systems of infectious diseases. EMS is an internal information system of
WHO and a disease surveillance tool. Chagas disease was included in this surveillance
system from 2005, however it has not been updated regularly and the reports are sporadic.
WHO representatives in the Amazon region as well as other parts of South America can
use the EMS as a tool, however not all have chosen to do so. This means that the
information from the EMS is not complete, however the reports might show a trend, and
were therefore included in this thesis. The same accounts for ProMED-mail that is an
open and online information system where newspaper reports, government reports and
physicians reports outbreak information from affected countries are registered.
4.4. Limitations
The objective was not to give a perfect image of the oral outbreak history. The scarcity of
information reduced the possibility of obtaining such an image. What was feasible to do
was to give an overview of the information available, however imperfect. The main
18
limitations of this study were the access to journals pertaining from South America. The
literature search took place at WHO library in Geneva, which can be considered to have
one of the most well assorted European collections of journals and articles from
development countries, South America included. Nevertheless, there were some articles
that were inaccessible, and that would only be accessible in the individual South
American countries. This was especially the case for supplement editions of certain South
American Journals. Efforts were made to procure the articles through contacts in the
countries concerned, however not all were retrievable.
4.5. Method of analysis
The following information was extracted from the 25 articles found in the literature
search; country, area of case origin, number of cases and mortality of outbreak. Moreover,
suspected transmission source and form of social gathering were included as categories to
look at geographical variation or homogeneity of the cases described. The age and sex of
the patients were not included as predefined information retrieval categories because oral
outbreaks have not been shown to differentiate for age and sex. The following data
analysis was performed on the collected data:
- A map of the reported outbreaks was produced to graphically show the dispersion of
outbreaks in the Amazon Region.
- A timeline of the reported outbreaks was produced to look at whether outbreak reports
have increased and to which degree.
- Number of cases and mortality was compared to see the range as well as the size of the
outbreaks.
- Suspected transmission and form of social gathering was compared country wise to see
geographical variation or homogeneity.
19
Figure 1. Flowchart for article search and selection
1st. search
2nd search
1st. selection
2nd selection
Deeper analysis
Total no. of articles, n
=66
Total no. of articles, n
=95
Total no. of articles,
n =43
Articles for result,
n =25
Articlesfor result, n =
- English key word search in PubMed - Spanish, Portuguese, French search in LILACS
-Manual search: reading reference lists and consultation of experts
- Reviewed the full text of articles and classified according to:
Inclusion criteria Exclusion criteria
- Thorough reading of articles following a set of pre-defined information retrieval categories for the meta-analysis
20
5. Results The 25 articles that the literature search resulted in were written mainly in English and
Portuguese. One article was written in Spanish and no articles were found in French. The
main part of the literature found came from Brazil. Moreover, ten reports were found in
EMS and ten reports from ProMED-mail. The articles were sorted in table 2 and 3
according to what year the outbreaks had occurred. The reports from EMS and ProMED-
mail were sorted in table 4 and 5 according to the time of the reports.
5.1. Published cases
Table 2 presents the data of published cases in Brazil that was found in the literature
search. In table 3 the published cases of Venezuela and Colombia are presented. Brazil,
Venezuela and Colombia were the only countries beside brazil that had published cases
that lived up to the inclusion criteria.
Table 2. Published cases in Brazil
Article Year Area Cases Deaths Source of
transmission
Social occasion
da Silva et al., 1968
(53); Nery-
Guimarães et al.,
1968 (54)
1965 Teutônia,
Estrela, Rio
Grande do Sul
State
17 6 Infected opossum
found, contaminated
food from this
animal reservoir
was suspected
Attended local
agricultural
college, all ate there
Shaw et al., 1969 (55) 1969 Belém. Pará
State
4 - - Family
Shikanai-Yasuda et
al., 1991 (39); Pereira
et al., 2009 (25);
Umezawa et al., 1996
(56)
1986 Paríba, Catolé
do Rocha
State
26 2 Sugar can juice,
infected opossum
found, infected
utensils by faeces
suspected
Meeting on farm
Valente et al., 2009
(30) , Valente, 1999
(14)
1996 Rio Bispo,
Mazagão,
Amapá
State
17 0 Consumption of
açai juice
Geographical isolation,
involved families
Pinto et al., 2001 (57) 1998 Abaetetuba,
Pará State
13 - Shared meal Family outbreak
Pinto, Valente &
Valente, 2004 (58);
Pinto et al., 2009 (59)
2000 Cametá, Pará
State
3 2 No hypothesis of
source
-
Pinto et al., 2009
(59)
2000 Belém,
Pedreira
district, Pará
State
11 0 Unprocessed
beverage suspected
No common gatherings
Pinto et al., 2003 (60) 2002 Igarapé-Miri,
Pará State
12 2 Food
contamination- poor
hygiene
Family outbreak
Barbosa-ferreira et
al.,2010 (61);
Medeiros, Guerra &
Lacerda 2008 (62),
Monteiro et al., 2010
(63)
2004 Tefé,
Amazônia
State
9 - açai wine -
21
Ianni & Mady, 2005
(64)
2005 Navegantes,
Santa
Catarina State
25 5 Sugar cane juice Road side food court
Ianni & Mady, 2005
(64)
2005 Bacia do
Igarapé da
Fortaleza –
Macapá,
Amapá State
26 - açai juice -
Dias et al., 2008 (65);
Bastos, 2010 (66)
2006 Macaúbas,
Chapada
Diamantina,
Bahia State
7 2 Improperly stored
water possibly
infected by faeces
from T. Sordida
Single household, two
parties
Nóbrega et al., 2009
(43)
2006 Barcarena,
Pará State
11 0 açai juice Staff members og
health post attending
meeting
Bastos et al., 2010
(66)
2006 Ibipitanga,
Bahia State
6 0 sugar cane juice Family
Cavalcanti, 2009 2006 Aratuba
municipality,
Ceará State
8 0 stew with liquid
coriander and
scallion from
orchard
Family together on
vacation
Barbosa-ferreira et
al., 2010 (61)
2007 Coari,
Amazônia
State
25 ? açai juice -
Barros et al., 2009
(30)
2007 Breves, Pará
State
12 0 meal Members of an
extended family who
had shared a common
meal
Barros et al., 2009
(30)
2007 Bagre, Pará
State
13 0 meal Members of an
extended family who
had shared a common
meal
Table 3. Published cases in Venezuela and Colombia
Article Country Year Area Cases Deaths Source Social
gathering
Alarcón de
Noya et al.,
(2010) (67)
Venezuela 2007 Caracas 103 1 Fresh guava
juice
School
Hernandéz
L.M.L. et al.
(2009) (68)
Colombia 1999 Guamal,
Magdalena
13 5 Palm wine -
Hernandéz
L.M.L. et al.
(2009) (68)
Colombia 1999 Tibú,
Santander
14 - - Members of the
military forces
Hernandéz
L.M.L. et al.
(2009) (68)
Colombia 2003 Bucamaranga, Santander 3 - -
Hernandéz
L.M.L. et al.
(2009) (68)
Colombia 2008 Lebrija,
Santander
10 2 Orange
juice
Party, everyone
drank orange
juice
Ríos J.F. et al.
(2011) (69)
Colombia 2009 Turbo,
Antioquia
3 1 Meal Common source
of food/ate at
the same
occasion in the
same house
22
Comparing table 2 and 3 it shows that oral outbreaks were most extensively described
and investigated in the Brazilian literature. The areas were the outbreaks occurred were
most often in the Amazon Region in rural and poor localities, however, outbreaks like
Santa Catarina was in an urban setting. In the Santa Catarina case the source was traced
to a juice producer in the nearby slum area (49). It is remarkable that only Venezuela and
Colombia had published oral outbreak cases.
5.2. Synthesis of outbreaks extracted from ProMED-mail
In table 4 the oral outbreaks of ProMED-mail are presented. Data was extracted from the
system in the same manner as for the published cases, so as to make them more
compatible. Shortly, there were three outbreaks in Brazil; three in Venezuela; two in
Colombia; one in Bolivia. In total ten oral outbreaks were reported from 2005 to 2011.
Table 4. Oral outbreak reports extracted from ProMED-mail (70)
No of
reports Country Cases Deaths Time of
report Transmission
mode Area
1 Brazil 19 4 23-mar-05 Sugar cane juice Santa Catarina
2 Brazil 20 - 28-jul-06 Bacaba wine Santarem, Para State
3 Venezuela 128 1 19-dec-07 Juice Caracas, (School)
4 Colombia 9 2 10-dec-08 Food
Contamination Bucaramanga, (Santander)
5 Venezuela 80 4 03-apr-09 Guyaba juice,
(chipo) Vargas, (school)-(Chichiviri
de la costa)
6 Brazil 13 - 12-jan-10 Acai Juice Santa Isabel do Rio Negro
(Amazonas)
7 Venezuela 58 - 08-may-10 Food
Contamination,
(chipo)
Caracas
8 Colombia 7 - 03-jun-10 Food
contamination Cesar
9 Venezuela 6 1 08-nov-10 Food
contamination Táchira
10 Bolivia 14 - 25-nov-10 Food
contamination Beni
5.3. Synthesis of outbreaks extracted from EMS
The EMS system revealed some reports of oral outbreaks. In table 5 the oral outbreaks
that have been reported to the system by WHO employees is presented. There were six
outbreaks reported in Colombia, two outbreaks in Venezuela, one outbreak in Bolivia and
one outbreak in Brazil. A total of ten outbreaks were reported from 2005 to 2011.
23
Table 5. Oral outbreak reports extracted from EMS (WHO)
No of
reports
Country Cases Deaths Time of
report
Transmission mode Area
1 Brazil - - 06-Apr-05 Infectious label in EMS Santa Catarina
2 Venezuela - - 14-Dec-07 Infectious label in EMS Caracas
3 Colombia - - 10-Dec-08 Infectious label in EMS Santander
4 Colombia 5 1 18-Jan-09 Food Safety label in EMS Santander
5 Colombia - - 24-may-09 Food Safety label in EMS Santander
6 Colombia 8 - 05-Feb-10 Eating at the same restaurant Antioquia
7 Venezuela 16 - 06-may-10 Suspected consumption of
contaminated products
Caracas
8 Colombia 5 - 28-may-10 Not mentioned Santander
9 Colombia 10 - 13-Jun-10 Oral transmission suspected
(Family party)
Cesar
10 Bolivia 14 0 26-oct-10 Consumption of Mayo fruit
juice
Guyaramerin
Comparing the outbreak information from EMS and ProMED there are overlaps
where the surveillance systems describe the same outbreaks such as the outbreaks in
Santa Catarina, Brazil; Caracas, Venezuela; Santander, Colombia; Cesar, Colombia and
Beni, Bolivia. Moreover, some outbreaks have already been described in the published
literature; Santa Catarina, Brazil; Caracas, Venezuela; Bucaramanga, Colombia. The
systems do not just describe the same outbreaks however. The outbreak information from
these surveillance systems appears sporadic and the cases reported are those that have
been given attention in the Medias mainly. Nevertheless, the information from the
systems clearly shows an upward trend in number of reports as well as a geographical
diversity of outbreaks.
Moreover both systems register outbreaks from 2005 where the Santa Catarina
outbreak in Brazil took place, and thereafter reports sporadically occurred until 2010
where both systems have a large increase in number of reports (see tables 4 And 5). This
development mirrors the development for the publication of outbreaks in the scientific
literature.
5.4. Mortality, outbreak source and social occasion
Looking at the data from both published outbreaks and outbreaks from the surveillance
systems, the mortality of oral outbreaks in Brazil and other countries together ranged
from 0-6 deaths. Number of infected cases ranged from 3-103. The ProMED-mail report
citing 128 cases (see table 4.) in Caracas, Venezuela was not included in this range
because the scientific publication on the same outbreak citing 103 cases has more validity
and credibility.
24
In figure 2 the mortality is plotted according to number of cases, year and deaths.
From the graph displayed in figure 2 the number of deaths from oral outbreaks does not
seem to follow any particular pattern. The mortality differs in size as is shown in Figure 4.
It is high in some cases like the Santa Catarina outbreak, the Guamal outbreak and the
Teutônia outbreak, and low in others. The Caracas outbreak for example had a very low
mortality. This particular outbreak happened at a school and the deceased was a child
with very high parasitemia (67).
Figure 2. Mortality of oral outbreaks from the scientific literature
Note: For figure 2 only outbreaks with information on deaths were included.
The source of the oral outbreaks was hypothesized to be açai juice, sugar cane
juice, water, palm wine and meals that were undercooked or contaminated in some way.
The most commonly suspected source was açai juice and it was the most common source
suspected in Brazil. Otherwise there was little geographic variation and the scarcity of
data on the source made it difficult to say if there was any geographical variation or
indeed homogeneity. Poor hygiene in handling food or drinks was hypothesized, as well
as the contamination of food via the opossum. Nevertheless, no sources had been directly
investigated in any published cases or surveillance system case reports.
The social occasions related to the outbreaks were most often families sharing
meals and drinks. Other social occasions included eating at the same roadside food court,
eating a common meal at a school or workplace and attending parties. It was difficult to
see if there was any geographical variation, again due to the scarcity of the data.
17
26
17
13
3
11
12
25
7
11 6 8 12 13
103
10
3
-1
0
1
2
3
4
5
6
7
1950 1960 1970 1980 1990 2000 2010 2020
De
ath
s
Year
Chagas disease cases
Cases
25
5.5. Map of oral outbreaks
Figure 3. Map showing the distribution of oral outbreaks in the Amazon basin
Background map © Google
To display the spread of oral outbreaks, a map was produced from the information
retrieved from the scientific articles, ProMED-mail reports and EMS reports. Figure 3
displays the distribution of oral outbreaks in the Amazon region. That is, in the countries
of Brazil, Colombia, Venezuela and Bolivia. Red dots marked on the map means that the
outbreaks were described in the literature, and orange dots are the outbreaks that were
found in the surveillance systems EMS and ProMED-mail. The map shows a broad
distribution and some clustering of oral outbreaks, especially in Brazil in the state of
Pará. The size of the dots in Venezuela indicates very large outbreaks in that particular
region and country. Furthermore, it seems the largest outbreaks were in Venezuela, and
the largest quantity reported from Brazil.
26
Figure 4. Timeline of published oral outbreaks and EMS and ProMED-mail reports on
oral outbreaks
Note: The size of the dots of the Figure 4 denotes the outbreak size
Figure 4 shows a large gap in outbreak reports from the first outbreaks in 1965 and
1969 to the next in 1986. Then there is another gap lasting around ten years till the next
case in 1996 and two years after in 1998. The number of outbreaks rises rapidly from
then on til now. The size of the dots shows the size of the outbreak and it seems like the
size of outbreaks varies significantly. However large outbreaks seems to have been
registrered from the beginning.
1950 1960 1970 1980 1990 2000 2010 2020
Year
Chagas disease cases
Cases
27
6. Discussion
The severity of oral outbreaks was clearly shown in the previous results (see Figure 2). It
is certain that oral outbreaks can have a very high mortality rate. Mortality risk will
depend on the condition and age of the patient. Oral transmission of Chagas disease could
possibly be more severe to young children, older people and immune-suppressed people.
The range of cases for oral outbreaks was shown to vary from 3 to 103. This is a large
case range and an indication of the diverse nature of oral transmission and oral outbreaks.
An oral outbreak of 100 cases at the same point in time will require a coordinated and
rapid effort from health authorities. The social aspect of oral outbreaks is important also
for prevention measures as it is to be a common factor for oral outbreaks.
6.1. Emerging transmission form?
The trend for reports of oral outbreaks in the Amazon region is that the number of reports
has been rising rapidly in the latest couple of years. The timeline in Figure 4 displays the
fact that the scientific community has been aware of oral outbreaks since 1965.
Furthermore, scientists have been aware of the possibility of oral outbreaks since the
30ies when scientists began experimenting on oral transmission of Chagas disease (32). It
is clear that oral transmission is not a new event; however it is possible that oral
outbreaks are increasing as well. The results of this thesis did not reveal whether or not
Chagas disease is emerging or if the problem has been there all along. Looking at the
timeline though it seems very evident that oral outbreaks have been happening for a very
long time and also that outbreaks can have passed by unnoticed. Silent suffering and
death of thousands of people have been the rule rather than the exception for Chagas
disease in general. The silence surrounding oral outbreaks is not an exception. The fact
that encroachment on the vectors natural habitat, the rain forest, is increasing could also
be an explanatory factor to the increase in cases that has been detected recently.
However one looks at it, oral outbreaks are a real risk for all inhabitants of the countries
of the Amazon region. The distribution of cases was very wide geographically speaking,
and not only limited to the Amazon forest region.
6.2. Geographical distribution
The mapping of cases showed clearly that oral outbreaks are occurring all over the
Amazon Region countries and there are several implications to this (see Figure 3). Increasing surveillance in the Amazon region could possibly reveal a significantly larger
number of outbreaks than described in this thesis. In any case the results show that oral
outbreaks are a common occurrence in Brazil, however the occurrence of oral outbreaks
in Venezuela, Bolivia and Colombia show that oral outbreaks are not limited to Brazil.
Moreover, the outbreaks were not only restricted to regions with Amazon forest, but
28
appeared also in urban areas and areas far from the Amazon, like the outbreak in Caracas,
Venezuela, and the outbreak in Santa Catarina, brazil which is near Argentina. Although
not included in the results because of the inclusion criteria, French Guyana has suspected
outbreaks as well due to several acute cases (71). They have even started informing the
public about the risk of oral transmission (72).
Brazil is one of the countries that have been very active in elimination and control
of Chagas disease, and one of the first countries of the Southern Cone initiative to be
declared free of transmission by the main domiciliated vector (Triatoma infestans). Brazil
is in this light well equipped for the discovery of Chagas disease cases, as the country has
experts as well as knowledge on Chagas disease in general. Also the encroachment of
humans on the Amazon forest in Brazil has increased in recent years, which increases the
risk of infection (7). The country has perhaps been more vigilant in discovering cases,
which can explain that most oral outbreaks have been reported from Brazil. The sheer
size of the country Brazil compared to the other countries may also be a factor. Yet
looking at the geographical distribution of oral outbreaks clearly shows that there is a real
risk of oral outbreaks in all countries of the Amazon Region.
6.3. Surveillance system in the Amazon Region
The scientific literature that was included in this literature review serves to show the need
for increased surveillance of oral outbreaks. EMS and ProMED-mail have similar
timelines of outbreak registration, however the reports appear to be random and should
not be taken as to reflect the real number of outbreaks. It should be mentioned also that
EMS is a complimentary working tool and as such not a highly vigilant surveillance
system unit in the WHO. ProMED-mail also cannot be taken to be highly accurate and all
encompassing as a surveillance system, since it is based on voluntary reports. Thus, none
of these systems are really meant to monitor oral outbreaks on a systematic basis. The
question is then what is being done otherwise to monitor outbreaks in the Amazon
Region.
Local surveillance efforts pertain to governments of the Amazon countries, most
notably Brazil where the focus on oral transmission transpires as the strongest in the
Amazon basin. This is evident from the number of publications from Brazil. However,
the AMCHA meetings has recently had increased focus on oral outbreaks as an emerging
problem in the Amazon basin (48). Thus, the need for prevention and surveillance are
being acknowledged to some extent.
6.4. The social aspect of transmission
The conclusion from the case information listed in tables 2 to 5 is that oral outbreaks
occur at social occasions including different sources of food and drinks. The social
occasion varied from schools to eating at the same road side food court or family dinners
and parties. Sources listed ranged from hypotheses on juice, wine, water and other
29
beverages or undercooked meat. For prevention measures there are several implications
of this. In Brazil for example the most commonly suspected source açai juice is a very
common beverage often sold under unhygienic conditions in market places. This means
that food hygiene and safety measures are of importance for Brazil and that particular
attention should be given to the production, sale distribution and ingestion of açai juice.
Possibly export of açai juice can be an issue of prevention for Brazil, as the parasite has
been shown to be able to survive up to 24 hours in unpasteurized juice (42).
Furthermore, there is the problem of hygiene during cooking, and undercooked
meals, as well as food storage practices. These are also issues for prevention measures
and related to family practices and poverty issues. Hygienic practices in poor rural and
urban settings are important when people live in close proximity with either palm trees
were infected vectors reside or with animals such as the opossum (14, 29). Both vectors
and mammals have easy access to kitchen spaces in thatched huts with poor possibilities
of adequate food storage. Nevertheless, the diversity of the social occasions shows that
oral outbreaks happen indiscriminately of social layers. The Caracas school outbreak in
Brazil showed a high number of cases and low number of deaths, which could be related
to the fact that the outbreak happened in a urban area with easy access to health care and
prevention measures (67). Outbreaks happening in rural settings do not have the same
opportunities for rapid detection and care. The obstacles for reporting and detecting
outbreaks in regions that are very hard to access are thus issues needing to be addressed.
30
7. Recommendations
7.1. Food safety prevention measures
Knowledge on oral transmission and the necessity of food hygiene practices should be
promoted in all countries. There are two levels of society that should be taken into
consideration for food safety practice guidelines. First of all governments should provide
regulation and recommendations for food production for producers and manufacturers,
and second of all recommendations and awareness should be spread at population level.
The contamination of high risk foods that have been presented here in this thesis, such as
açai juice, sugar cane juice and undercooked meals are target areas of food protection
measures. However, all sources of food or drinks can be contaminated in an area where
T.cruzi is present in wild animals, vectors or domestic animals. If unsafe food handling
practices take place at some point in the food production chain there is a risk of
contamination.
WHO recommendations for effective control of food borne diseases are that it
should always be based on updated disease information and incidence of the disease in
question (73). The conclusion from this thesis is that oral outbreaks are not sufficiently
monitored in the Amazon region, and thus the basis for an effective control of food
contamination is not present. The strengthening of surveillance systems for oral outbreaks
in the countries of the Amazon region is therefore a priority to establish food safety
measures.
7.2. Travel medicine implications of oral outbreaks
The oral transmission case of the Italian tourist in Brazil is important because it shows
that oral transmission is a risk for anyone at present (15, 50). Tourists as well as other
travelers could be in danger of contracting Chagas disease orally. Common food safety
precautions when traveling to the Amazon region should be sufficient. Nevertheless,
travel clinics and physicians have to be aware of the risk, as well as raise awareness of
the risk of contracting Chagas disease orally in the countries of the Amazon Region.
Some European countries like Belgium, Spain and the Netherlands have included
counseling about Chagas disease for travelers to South America, as well as included
Chagas disease as a differential diagnosis after such trips in travels clinics (5). Oral
outbreaks of Chagas disease can also have implications for travel medicine in the sense
that the level of parasitemia may produce more severe symptoms and outcomes.
Travelers to the Amazon Region should be forewarned of the risk of ingesting food that
has not been properly handled and in places where hygiene is lacking.
31
7.3. Prevention target areas
Preventing oral outbreaks is a definite public health recommendation from the results
above. The severity and risk for the people if the countries of the Amazon Region are
clear from the epidemiological overview given in this thesis. Public health scientists
usually refer to three types of prevention. Primary prevention is about creating awareness
of a particular public health problem. Secondary prevention is to create a system for
detection and rapid response to a disease and tertiary prevention is treatment of the
disease. For oral outbreaks of Chagas disease the prevention recommendations would
thus be:
-Primary prevention: Information campaigns on oral transmission and oral outbreaks.
-Secondary prevention: Information systems, surveillance systems, outbreak alert info.
-Tertiary prevention: Rapid treatment of acute Chagas disease.
7.3.1. Primary, secondary and tertiary prevention
Primary prevention would be information campaigns. French Guyana has already made
efforts to warn people of oral transmission. Information posters on food hygiene, vectors
and protection exist already. In their information poster campaign the government of
French Guyana urges people to cover food, to sleep under a bed net, to cover all openings
of the house and to avoid sources of light directly over the food. They also provide
pictures of the vectors that can transmit T.cruzi to people (72). This is an example of an
information campaign that focuses on oral transmission and to prevent oral outbreaks. In
Brazil, the Health Ministry and the Ministry of Agriculture have jointly set down
regulations for the manufacturing and processing of açai. In addition they published
Technical Regulation on health and hygiene procedures for food handling and drinks
made with açai product (74). Primary prevention efforts should also include the
establishment of travel recommendations and advice for tourists travelling to the Amazon
Region.
Secondary prevention efforts include creating or improving surveillance systems.
There are several difficulties in developing a surveillance system in the Amazon region.
As mentioned earlier, large areas of the Amazon Region are very hard to access, because
there is no developed infrastructure and some villages are only accessible by the Amazon
River. This means that even if local physicians and health professionals are vigilant, they
may not be able to discover all oral outbreaks. Moreover, the sheer size of the area
presents a major challenge for developing a surveillance system, as well as a rapid
response system for outbreaks. From a public health and health economic perspective,
investing in prevention efforts, however, will save both Disability Adjusted Life Years
(DALY´s) and treatment costs in the long run. There are thus great advantages for the
countries of the Amazon Region to invest or reallocate money to prevention efforts.
32
To implement the other prevention levels, a sound surveillance system is the basis
to be able to evaluate the prevention needs. Health policy making relies on the ability to
evaluate need and efforts (73). Secondary prevention also includes the direct work of
preventing the actual contamination of foods- food safety measures. Existing procedures
to implement contamination control are for example Standard Operational Procedures,
Pest Control, Good Manufacturing Practices and Hazard Analysis and Critical Control
Points, as suggested by Pereira et al. (2009) (25). Standard Operational Procedures and
Good Manufacturing Practices refers to a set of standards for among other things;
manufacturing, storage and distribution of foods. Hazard analysis and critical control
points refer to a systematic preventive approach to ensuring food safety and includes
physical as well as chemical and biological contamination hazards. These methods are
implementation tools for food safety policy programs and for prevention of oral
outbreaks they may be useful (25).
Rapid treatment is the third aspect of prevention and includes treatment of acute
Chagas disease. It is necessary to discover and treat patients of an oral outbreak quickly.
This is linked with surveillance efforts. Even though diagnosis is made more difficult due
to unspecific symptoms, Chagas disease should be suspected in endemic areas or areas
where the vector has been detected to be prevalent. Including Chagas disease as a
differential diagnosis for tourists returning from the Amazon Region is necessary at the
tertiary prevention level. Another issue is the availability of medicine to treat acute
patients. The two medications produced to treat Chagas disease are Benznidazole® and
Nifurtimox®. These drugs are effective, but with many side-effects (1). Optimally they
should be made available to all countries of the Amazon Region to treat acute patients
rapidly.
Conclusively, prevention of oral outbreaks includes intervention on several levels
of society and presents a future challenge to the countries of the Amazon Region; a
challenge that possibly could save the lives of a great deal of people.
33
8. Conclusion
The conclusions that can be made from this thesis are that oral outbreaks of Chagas
disease are happening all over the Amazon Region. Oral outbreaks can be severe and
affect a great deal of people. It is clear that there is a distinct need of increasing both
awareness and surveillance of this problem on several levels of society in the countries of
the Amazon region. Detection and rapid treatment are priorities for oral outbreaks and
oral transmission. Surveillance data is required for health policy making, implementation
and evaluation.
It is not possible to say whether or not oral outbreaks are an emerging disease or if
it has been prevalent in the Amazon region all along. However, an epidemiological
overview of oral outbreaks in the Amazon was given. Even though the information may
be incomplete due to the lack of surveillance systems and published cases, the indication
is that oral outbreaks are a real threat in the countries of the Amazon Region as well as to
tourists traveling to these countries. Europe and other countries with large tourist flux to
the Amazon Region should develop guidelines for oral transmission of Chagas disease as
a differential diagnosis to physicians and travel clinics.
If oral outbreaks are actually happening on a much larger scale than is known,
people are dying and suffering in silence. It is clear from this thesis that oral outbreaks
deserve more attention than it is getting. In general the silence surrounding Chagas
disease needs to be broken to stop the suffering of millions.
34
9. References
1. WHO. Chagas disease (American trypanosomiasis). 2010. Accessed 20th
November 2011, from: http://www.who.int/mediacentre/factsheets/fs340/en/index.html.
2. Lescure F.X., Canestri A., Melliez H., Jauréguiberry S., Develoux M., Dorent R.,
Guiard-Schmid J. B., Bonnard P., Ajana F., Rolla V., Carlier Y., Gay F., Elghouzzi M.H.,
Danis M. & Pialoux G. Chagas disease, France. Emerg Infect Dis. 2008;14(4):644-6.
3. WHO Expert Committee. Control of chagas disease- Second report of the WHO
Expert Comittee. Geneva: WHO, 2002.
4. WHO. Working to overcome the global impact of neglected tropical diseases-
First WHO report on neglected tropical diseases. Geneva: WHO, 2010. Available from:
http://www.who.int/neglected_diseases/en/
5. WHO. Control and prevention of Chagas disease in Europe. Geneva, Switzerland:
WHO, 2009.
6. Aguilar V.H.M. Abad-Franch F., Racines V.J. & Paucar C.A. Epidemiology of
Chagas disease in Ecuador. A brief review. Mem Inst Oswaldo Cruz. 1999;94 Suppl
1:387-93.
7. Coura J.R., Junqueira A.C., Fernandes O., Valente S.A. and Miles M.A.
Emerging Chagas disease in Amazonian Brazil. Trends Parasitol. 2002;18(4):171-6.
8. Coura J.R. [Transmission of chagasic infection by oral route in the natural history
of Chagas disease]. Rev Soc Bras Med Trop. 2006;39 Suppl 3:113-7.
9. Pinto A.Y. Valente S.A., Valente V.A.C., Ferreira Junior A.G. & Coura J.R.
[Acute phase of Chagas disease in the Brazilian Amazon region: study of 233 cases from
Pará, Amapá and Maranhão observed between 1988 and 2005]. Rev Soc Bras Med Trop.
2008;41(6):602-14.
10. Marcili A., Valente V.C., Valente S.A., Junqueira A.C., da Silva F.M., Pinto
A.Y., Naiff R.D., Campaner M., Coura J.R., Camargo E.P., Miles M.A. & Teixeira M.M.
Trypanosoma cruzi in Brazilian Amazonia: Lineages TCI and TCIIa in wild primates,
Rhodnius spp. and in humans with Chagas disease associated with oral transmission. Int J
Parasitol. 2009;39(5):615-23.
11. Yoshida N. Molecular mechanisms of Trypanosoma cruzi infection by oral route.
Mem Inst Oswaldo Cruz. 2009;104 Suppl 1:101-7.
12. Benchimol-Barbosa P.R. Predictors of mortality in Chagas' disease: the impact of
atrial fibrillation and oral transmission on infected population. Int J Cardiol.
2008;133(2):275-7.
13. Benchimol Barbosa P.R. The oral transmission of Chagas' disease: an acute form
of infection responsible for regional outbreaks. Int J Cardiol. 2006;112(1):132-3.
14. Valente S.A.S Valente V.C. & Neto H.F. Considerations on the epidemiology and
transmission of Chagas disease in the Brazilian Amazon. Mem Inst Oswaldo Cruz.
1999;94(Suppl. 1):395-8.
15. Angheben A., Anselmi M., Gobbi F., Marocco S., Monteiro G., Buonfrate D.,
Tais S., Talamo M., Zavarise G., Strohmeyer M., Bartalesi F., Mantella A., Di Tommaso
M., Aiello K.H., Veneruso G., Graziani G., Ferrari M.M., Spreafico I., Gaiera G.,
Lanzafame M., Mascarello M., Cancrini G., Albajar-Vinas P., Bisoffi Z. & Bartolini A.
35
Chagas disease in Italy: breaking an epidemiological silence. Euro Surveillance
2011;16(37).
16. Junqueira C., Caetano B., Bartholomeu D.C., Melo M.B., Ropert C., Rodrigues
M.M. & Gazzinelli R.T. The endless race between Trypanosoma cruzi and host immunity:
lessons for and beyond Chagas disease. Expert Rev Mol Med. 2010;12:e29.
17. Schmunis G.A. and Yadon Z.E. Chagas disease: a Latin American health problem
becoming a world health problem. Acta Trop. 2010;115(1-2):14-21.
18. Dias J.C., Prata A. & Schofield C.J. [Chagas' disease in the Amazon: an overview
of the current situation and perspectives for prevention]. Rev Soc Bras Med Trop.
2002;35(6):669-78.
19. Aguilar H.M., Abad-Franch F., Dias J.C., Junqueira A.C. & Coura J.R. Chagas
disease in the Amazon region. Mem Inst Oswaldo Cruz. 2007;102 Suppl 1:47-56.
20. Perleth M. Historical aspects of American Trypanosomiasis (Chagas' disease).
Frankfurt: Peter Lang; 1997.
21. Grupo de trabajo científico sobre la enfermedad de Chagas. Reporte sobre la
enfermedad de Chagas. Editors: Guhl F. and Lazdins-Helds J.K. 17 a 20 abril de 2005,
Buenos Aires, Argentina. Buenos Aires: WHO/TDR/GTC/09, 2007.
22. Pinto Dias J.C. & de Oliveira Macedo V. Doença de Chagas. In: Coura J.R.,
editor. Dinâmica das doenças Infecciosas e Parasitárias. Rio de Janeiro: Guanabara
Koogan; 2005.
23. Coura J.R. Chagas disease: what is known and what is needed-a background
article. Mem Inst Oswaldo Cruz. 2007;102 Suppl 1:113-22.
24. Pinto Dias J.C. Epidemiologia. In: Brener Z., Andrade Z.A. & Barral-Netto M.,
editors. Trypanosma cruzi e Doença de Chagas. 2 ed. Rio de Janeiro: Guanabara Koogan
S.A.; 2000.
25. Pereira K.S., Schmidt F.L., Guaraldo A.M., Franco R.M., Dias V.L. & Passos L.A.
Chagas' disease as a foodborne illness. J Food Prot. 2009;72(2):441-6.
26. Añez N., Carrasco H., Parada H., Crisante G., Rojas A., Gonzalez N., Ramirez
J.L., Guevara P., Rivero C., Borges R. & Scorza J.V. Acute Chagas' disease in western
Venezuela: a clinical, seroparasitologic, and epidemiologic study. Am J Trop Med Hyg.
1999;60(2):215-22.
27. Mazza S., Montaña A., Benitez C. & Janzi E.Z. Transmissión del Schizotripanum
cruzi al niño por leche de la madre com enfermedad de chagas Mis Est Patol Reg.
1936;28:41-6.
28. Dias J.C. [Notes about of Trypanosoma cruzi and yours bio-ecology
characteristics with agents of the transmission by meals]. Rev Soc Bras Med Trop.
2006;39(4):370-5.
29. PAHO. Enfermedad de Chagas- Guía para vigilancia, prevención, control y
manejo clínico de la enfermedad de Chagas aguda transmitida por alimentos. Ramos Jr.
A.N., Marques D.O.R., Carmo G.M., Pinto Dias J.C., Valente S.A., Santos S.O. &
Gutirrez A.P. editors. Rio de Janeiro: PANASOFTA-VP/OPAS/OMS; 2009.
30. Barros H., Beltrão M., Cerroni M.P., Roberto D., Freitas C., Pinto A.Y.N.,
Valente V.C., Valente S.A., Costa E.G. & Sobel J. Investigation of two outbreaks of
suspected oral transmission of acute Chagas disease in the Amazon region, Pará State,
Brazil, in 2007. Tropical Doctor. 2009;39:231-2.
36
31. Nattan-Larrier L. Infections á Trypanosomes et voies de penetration des virus.
Bull Soc Path Exot. 1921;14:537-42.
32. Brumpt E. Precis de Parasitologie. Paris, Masson, Tome I. 1931.
33. Kofoid C.A. & Donat F. Experimental infection with Trypanosoma cruzi from the
intestine of a conenose bug: Triatoma Pretracta. Proc Soc Exp Biol. 1933;30:489-91.
34. Cardoso F.A. Sur le mecanisme de la transmission de la maladie de Chagas. Ann
Parasit hum Comp. 1933;16:341-9.
35. Dias E. Estudos sobre o Schizotrypanum cruzi. . Rio de Janeiro, 1933.
36. Diaz Ungria C. Estudio experimental del Trypanosoma cruzi en peroos infectados
por la vía bucal: nuevos estudios. Kasmera (Venzuela). 1968;3:73-88.
37. Ribeiro R.D., Rissato e Garcia T.A. & Bonomo W.C. [Mechanisms of
transmission of the etiological agent of Chagas' disease]. Rev Saude Publica.
1987;21(1):51-4.
38. Roellig D.M., Ellis A.E. & Yabsley M.J. Oral transmission of Trypanosoma cruzi
with opposing evidence for the theory of carnivory. J Parasitol. 2009;95(2):360-4.
39. Shikanai-Yasuda M.A., Marcondes C.B., Guedes L.A., Siqueira G.S., Barone
A.A., Dias J.C., Amato Neto V., Tolezano J.E., Peres B.A. & Arruda Júnior E.R. Possible
oral transmission of acute Chagas' disease in Brazil. Rev Inst Med Trop Sao Paulo.
1991;33(5):351-7.
40. Lainson R., Shaw J.J. & Naiff R.D. Chagas' disease in the Amazon basin:
speculations on transmission per os. Rev Inst Med Trop Sao Paulo. 1980;22(6):294-7.
41. Cardoso A.V., Lescano S.A., Amato Neto V., Gakiya E. & Santos S.V. Survival
of Trypanosoma cruzi in sugar cane used to prepare juice. Rev Inst Med Trop Sao Paulo.
2006;48(5):287-9.
42. Soarez V.A., Dias J.C.P., Marsden P.D. & Garcia-Zapata M.T. Sobreviviência do
T. Cruzi em caldo de cana. Resultados preliminares. Rev Soc Bras Med Trop.
1987;20((Suppl. 2):38).
43. Nóbrega A.A., Garcia M.H., Tatto E., Obara M.T., Costa E., Sobel J. & Araujo
W.N. Oral transmission of Chagas disease by consumption of açaí palm fruit, Brazil.
Emerg Infect Dis. 2009;15(4):653-5.
44. Rogez H. O açai (Euterpe oleracea) um alimento funcional mas apresentando alta
contaminação. In: Viñas PA, editor. 2007.
45. Camandaroba E.L., Pinheiro Lima C.M. & Andrade S.G. Oral transmission of
Chagas disease: importance of Trypanosoma cruzi biodeme in the intragastric
experimental infection. Rev Inst Med Trop Sao Paulo. 2002;44(2):97-103.
46. Yoshida N. Trypanosoma cruzi infection by oral route: how the interplay between
parasite and host components modulates infectivity. Parasitol Int. 2008;57(2):105-9.
47. Gus I., Molon M.E. & Bueno A.P. [Chagas disease-review of 8 simultaneous
cases of acute Chagas myocarditis: 25 years later]. Arq Bras Cardiol. 1993;60(2):99-101.
48. AMCHA. 2nd Meeting Intergovernamental Initiative of Chagas Disease
Surveillance and Prevention in the Amazônia, 2005. Technical report. 2006;39(3).
49. Ianni B.M. & Mady C. Como Era Gostoso o Meu Caldo de Cana. Arquivos
Brasileiros de Cardiologica. 2005;85(6):379-81.
50. Sabbatini F., Coccho S., Mongiardo N., D'Andrea L., Bedini A., Borghi V., Prati
F., Mussini C. & Esposito R. Una diagnosi globalizzata- Ovvero un caso di malattia di
Chagas acuta a Modena. Giornale Italiano di Medicina Tropicale. 2005;10(3-4):111.
37
51. Ministéro do Turismo. Anuário Estatístico de Turismo-2011. E-publication:
Government of Brazil, 2011. Available from:
http://www.dadosefatos.turismo.gov.br/export/sites/default/dadosefatos/anuario/downloa
ds_anuario/Anuxrio_Estatxstico_2011_-_Ano_base_2010_-_24-05-2011.pdf
52. Backman J. Rapporter och uppsatser. 2:1 ed. Denmark: Studentlitteratur; 2008.
53. da Silva N.N., Clausell D.T., Nólibos H., de Mello A.L., Ossanai J., Rapone T. &
Snell T. [Epidemic outbreak of Chagas disease probably due to oral contamination]. Rev
Inst Med Trop Sao Paulo. 1968;10(5):265-76.
54. Nery-Guimarães F., da Silva N.N., Clausell D.T., de Mello A.L., Rapone T. &
Snell T. Um Surto epidêmico de doença de Chagas de provável transmissão digestiva,
occorido em Teutonia (Estrêla- Rio Grande do Sul). O Hospital. 1968;73(6):73-110.
55. Shaw J., Lainson R. & Fraiha H. [Epidemiology of the first autochthonous cases
of Chagas' disease recorded in Belém, Pará, Brazil]. Rev Saude Publica. 1969;3(2):153-7.
56. Umezawa E.S., Shikanai-Yasuda M.A., Gruber A., Pereira-Chioccola V.L. &
Zingales B. Trypanosoma cruzi defined antigens in the serological evaluation of an
outbreak of acute Chagas disease in Brazil (Catolé do Rocha, Paraíba). Mem Inst
Oswaldo Cruz. 1996;91(1):87-93.
57. Pinto A.Y.N., Harada G.S., Valente V., Abud J.E., Gomes F., Souza G.C. &
Valente S.A. [Cardiac attacks in patients with acute Chagas disease in a family micro-
outbreak, in Abaetetuba, Brazilian Amazon]. Rev Soc Bras Med Trop. 2001;34(5):413-9.
58. Pinto A.Y.N., Valente S.A., Valente V.A.C. Emerging acute Chagas disease in
Amazonian Brazil: case reports with serious cardiac involvement. Braz J Infect Dis.
2004;8(6):454-60.
59. Pinto A.Y.N., Ferreira A.G., Valente V.A.C., Harada G.S. & Valente S.A. Urban
outbreak of acute Chagas disease in Amazon region of Brazil: four-year follow-up after
treatment with benznidazole. Rev Panam Salud Publica. 2009;25(1):77-83.
60. Pinto A.Y.N Valente S.A.S. LR, Silva O., Castro T.B. & Valente V.C. Ocorrência
de tripanossomíase aguda familiar no município de Igarapé- Miri, Pará: gravidade de
apresentação clínica em idosos. Rev Soc Bras Med Trop. 2003;36((Suppl. 1)):381.
61. Barbosa-Ferreira J.M., Guerra J.A., Santana Filho F.S., Magalhães B.M., Coelho
L.I. & Barbosa M.G. [Cardiac involvement in Acute Chagas' Disease cases in the
Amazon region]. Arq Bras Cardiol. 2010;94(6):147-9.
62. Medeiros M.B., Guerra J.A. & Lacerda M.V. Meningoencephalitis in a patient
with acute Chagas disease in the Brazilian Amazon. Rev Soc Bras Med Trop.
2008;41(5):520-1.
63. Monteiro W.M., Barbosa M.G., Toledo M.J., Fé F.A. & Fé N.F. [Series of acute
Chagas' disease cases attended at a tertiary-level clinic in Manaus, State of Amazonas,
from 1980 to 2006]. Rev Soc Bras Med Trop. 2010;43(2):207-10.
64. Ianni B.M. & Mady C. Como Era Gostoso o Meu Caldo de Cana. Arquivos
Brasileiros de Cardiologica. 2005;85(6):379-81.
65. Dias J.P., Bastos C., Araújo E., Mascarenhas A.V., Martins Netto E., Grassi F.,
Silva M., Tatto E., Mendonça J., Araújo R.F., Shikanai-Yasuda M.A. & Aras R. Acute
Chagas disease outbreak associated with oral transmission. Rev Soc Bras Med Trop.
2008;41(3):296-300.
66. Bastos C.J., Aras R., Mota G., Reis F., Dias J.P., de Jesus R.S., Freire M.S., de
Araújo E.G., Prazeres J. & Grassi M.F. Clinical outcomes of thirteen patients with acute
38
chagas disease acquired through oral transmission from two urban outbreaks in
northeastern Brazil. PLoS Negl Trop Dis. 2010;4(6):e711.
67. Alarcón de Noya B., Díaz-Bello Z., Colmenares C., Ruiz-Guevara R., Mauriello
L., Zavala-Jaspe R., Suarez J.A., Abate T., Naranjo L., Paiva M., Rivas L., Castro J.,
Márques J., Mendoza I., Acquatella H., Torres J. & Noya O. Large urban outbreak of
orally acquired acute Chagas disease at a school in Caracas, Venezuela. J Infect Dis.
2010;201(9):1308-15.
68. Hernandéz L.M.L., Cano A.N.R., Cucunubá Z. & Zambrano P. Brote de Chagas
Agudo en Lebrija, Santander. Revista Del Observatorio de Salud Pública de Santander
(OSPS). 2009;4(1):28-36.
69. Ríos J.F., Arboleda M., Montoya A.N., Alarcón E.P. & Parra-Henao G.J.
Probable brote de transmisíon oral de enfermedad de Chagas en Turbo, Antioquia.
Biomédica. 2011;31(2).
70. ProMED-mail. About ProMED-mail2001, 2009 5 April 2011. Available from:
http://www.promedmail.org/pls/apex/f?p=2400:1950:797228924213635::NO:::.
71. Carme B., Aune I., Nguyen G., Aznar C. & Beaudet B. Four cases of acute
chagasic myocarditis in French Guiana. Am J Trop Med Hyg. 2001;64(3-4):162-3.
72. UFR de Médecine. La Maladie de Chagas en Guyane française. CHC, Direction
de la Santé de Développement Social de Guyane, UFR de medécine. French Guyana.
73. WHO. Food safety issues. Geneva: WHO, 2002. ISBN: 92 4 1545747.
74. Agencia Nacional de Vigilancia Sanitária. Regulamento Técnico de
Procedimentos Higienico-Sanitários para Manipulacao de Alimentos e bebidos
Preparados com Vegetais. Agencia Nacional de Vigilancia Sanitária. 2005. Available
from:
http://www.biblioteca.sebrae.com.br/bds/BDS.nsf/2E87266883AF949B832576250048E
C48/NT00041F36.pdf
A list of master theses from previous years, 1996-2007, is available at: www.phmed.umu.se/english/divisions/epidemiology/research/publications
Centre for Public Health Report Series (ISSN 1651-341X)
2009
2009:1 Anne Neumann. Assessing the cost-effectiveness of the Saxon Diabetes Type 2 Prevention Program Using a Markov Model. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:2 Yien Ling Hii. Climate variability and increase in intensity and magnitude of dengue incidence in Singapore. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:3 Agnes Mbabaali Nanyonjo. Knowledge, attitude and practices of young people, regarding HIV positive prevention - a mixed method study of the Infectious Diseases Institute Kampala Uganda. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:4 Raman Preet. Tobacco control and prevention: Need for commitment from oral health professionals. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:5 Erika Viklund. A struggle for health against all odds. Women`s experiences from a refugee camp in Ghana. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:6 Veneranda Masatu Bwana. Pulmonary tuberculosis among human immunodeficiency virus (HIV) infected patients in the era of highly active antiretroviral therapy (Haart) in Dar Es Salaam municipal, Tanzania. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:7 Kwabena Titi Ofei. Nutrient intakes and vitamin supplements in early pregnancy in relation to maternal age and body mass index in Umeå, Sweden. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:8 Bege Dauda. Antimalarial drug prescriptions and doctors perception on malaria in hospitals of Kaduna State, Nigeria. A pilot study. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:9 Nurul Kodriati. Economic modelling of the impact of work site cardiovascular screening in Indonesia. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:10 Trisasi Lestari. Burden of childhood TB in hospitals in Java Island: Challenge for DOTS program. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:11 Ziaul Islam Chowdhury. The effect of antenatal care on infant malnutrition in Bangladesh: Secondary analysis of Demographic and Health Survey data. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:12 Mojgan Padyab. Factor structure of the Iranian version of Ways of Coping questionnaire. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:13 Hana Kolac. Studying abroad: Changes in sexual behaviour and access to sexual health services. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:14 Xueyan Bai. Cost-effectiveness analysis on the use of Peripheral Intravenous Catheter (PIV) and Peripherally Inserted Central Catheter (PICC) in hospitalized old tumor patients in China. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:15 Andinet Worku. Pattern and determinants of survival in adult HIV patients on antiretroviral therapy, Ethiopia. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:16 Ailiana Santosa. Sexual dysfunction and quality of life among older people in Purworejo district, Indonesia. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:17 Cynthia Anticona Huaynate. Heavy metal levels and nutritional status in two indigenous communities of the Corrientes river- Loreto- Peru. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:18 Arash Safaverdi. Oral health in Iran. A comparison between Tehran and Pardis. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:19 Angelica Lahid Barragan Romero. Forgotten people in the programs of sexual and reproductive health. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:20 Anna Stecksén. Physical activity habits, Body Mass Index, general health, screen-time and education in families within the SALUT Child Health Promoting Intervention Programme in Västerbotten – results from a pilot study. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:21 Yared Woldemariam Habtewold. Preference for health care financing options and willingness to pay for compulsory health insurance among government employees in Ethiopia. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:22 Irina V. Pecheykina. Comprehensive social and psycho-pedagogical assistance to singe-parent families in Russia. A study protocol for cost-effectiveness analysis. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:23 Irina Popova. Teenage boys and girls with asthma in the Arkhangelsk city, Russia: Self-reported health and coping strategies. A study protocol. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:24 Ulla-Greta Rönnqvist. The face of a woman. A study of the roles of socio-cultural norms and values in the planning of sexual and reproductive health, gender, HIV and AIDS strategies in Mozambique. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:25 Yihuai Liang. Parental corporal punishment and emotional maltreatment (PCPEM) in childhood, mental health and risk behaviors among youth students in Beijing and Hebei, China. Master thesis
in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:26 Bahar Aghaie Nia. Causes and consequences of fleeing from home. An elaborative effort to present the lived-experience of young women living in welfare shelters in Tehran, Iran. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:27 Dao Dinh Sang. Injecting drug users: Their processes of being addicted and their lives in a rural area in Vietnam. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:28 Dang The Hung. Health effects related to second hand smoke in children. Preliminary study in Vietnam. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:29 Hideyuki Kobayashi. Well-being and freedom of patients. Comparison of nursing service between Sweden and Japan. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:30 Asiya Abuliekemu. A literature review of cost-effectiveness analysis on rotavirus vaccine. Umeå Master thesis in public health. International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:31 Nighat Farooqi. Can dietary advice improve the energy intake and physical performance in patients with Chronic Obstructive Pulmonary Disease. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:32 Phan Minh Trang. Chronic respiratory function and symptoms among workers in rubber industry at Ho Chi Minh City. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:33 Xiaohong Gu. Insulin resistance: an important risk marker for the development of silent cerebral infarction in Chinese middle-age patient with hypertension. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:34 Anneli Thylin. Utdelning av läkemedel inom missbruksvård till misshandlade kvinnor – en journalstudie vid Renforsens behandlingshem. Master thesis in public health. Umeå International School of Public Health, Epidemiologi och folkhälsovetenskap, Institutionen för folkhälsa och klinisk medicin, Umeå Universitet, 2009.
2009:35 Zohreh Sadeghkhani. Depression and unequal rights among women and men. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2009:36 Michaela Zenek. Organic Farming- Beneficial to the 3rd world farmer? Bridging sustainable farming and healthier communities in Sub Saharan Africa. Master thesis in public health. Umeå International School of Public Health, Epidemiology and Public Health Sciences, dept of Public Health and Clinical Medicine, Umeå University, 2009.
2010
2010:1 Osama Ahmed Hassan Ahmed. Rift Valley Fever. A Resurgent Threat. Case Studies from Sudan and the Kingdom of Saudi Arabia. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:2 Oziegbe Paul Akhigbe. Motorcycle related maxillofacial injuries in a semi-urban town in Nigeria. A four year review of cases in Irrua Specialist Teaching Hospital. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:3 Eyerusalem Dagne. Role of socio-demographic factors on utilization of maternal health care services in Ethiopia. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:4 Yalem Tsegay Assfaw. Determinants of Antenatal Care, Institutional Delivery and Skilled Birth Attendant Utilization in Samre Saharti District, Tigray, Ethiopia. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:5 Stefanie Butz. Bangladeshi girl: “My parent’s didn´t allow me to learn to swim, so I drowned”. A gender theoretical perspective on environmental migration by applying Connells hegemonic masculinity theory in the field of Public Health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:6 Huo Jinhai. The economic burden of occupational asthma in Europe. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:7 Ernest Njoh Malange. The Cholera Epidemic and Barriers to Healthy Hygiene and Sanitation in Cameroon. A Protocol Study. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:8 Shabnam Salimi. Association of severe periodontitis with microalbuminuria and chronic kidney disease. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:9 Tewodros Bizuwork. Risk factors and causes of mortality among HIV/AIDS patients receiving antiretroviral therapy; Zomba central hospital; Zomba, Malawi. A study protocol. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:10 Michael Tesfamariam. Salutogenic perspective and it´s contribution to improve the care of orphans in Eritrea. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:11 Agegnehu Tesfaye Abdeberhan. Risk factors for (predictors of) loss to antiretroviral therapy in Oromia, Ethiopia. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:12 Masoud Waazghasemi. Overweight and lifestyle characteristics among Swedish adolescents. A study in four pilot areas of Västerbotten. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:13 Julia Schröders. Are we running with the wrong fuel? A study protocol quantitatively and qualitatively assessing short-term effects of a paleolithic diet on healthy German men and women. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:14 Ediri Brume. Obesity in low income African American adults. A New York City Literature Review. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:15 Bruno Guerreiro Semedo. A Review of the State of Chronic Obstructive Pulmonary Disease in Portugal. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:16 Janna Maria Brouwer. Cheap doesn’t always mean better. Anaesthesia in cataract extractions in the normal eye in the Netherlands; a deterministic cost utility analysis using a Markov Model. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:17 Manuel Krone. Is it efficient to vaccinate girls against HPV? A cost-utility analysis of HPV-vaccination in Germany using a Markov-Model. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:18 Ali Mohammed Abbas. Western Moist Snuff and Oropharyngeal Cancer. A Systematic Review. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:19 Marwan Shehda Salama Mosleh. Awarness of anaemia among pregnant women at UNRWA clinics in Gaza strip. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2010:20 Tariq Feroz Memon. The potential risk factors of stroke and their frequencies among stroke patients admitted in Liaquat University Hospital, Hyderanad, Pakistan Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2010.
2011
2011:1 Therese Kardakis, Linda Sundberg, Monica E. Nyström, Rickard Garvare, Lars Weinehall. Utveckling och implementering av kliniska riktlinjer för hälso- och sjukvården – En litteraturöversikt. Epidemiologi och global hälsa, Umeå universitet, 2011.
2011:2 Rathi Ramji. Assessing the Relationship between Occupational Stress and Periodontitis in Industrial Workers. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:3 Waseem Akhtar Choudhary. Barriers to voluntary counselling and testing (VCT) among HIV/AIDS patients. A Study Protocol for the Punjab Province of Pakistan. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:4 Joseph S. Bukalasa. Indoor Air Pollution, Social Inequality and Acute Respiratory Diseases in Children in Tanzania. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:5 Shijun Wang. Health systems in rural areas: A comparative analysis in financing mechanisms and payment structures between China and India. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:6 Nguyen Thi Minh Thoa. Health care utilization and economic growth of households in Ba Vi, Vietnam. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:7 Nazgul Mussanova. Efficiency Analysis of the Health Centres in Karaganda oblast, Kazakhstan. Data envelopment and Malmquist index analysis. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:8 Medet Ospanov. Cost effectiveness analysis of lifestyle intervention in primary health care. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:9 Haleema Masud. Health Policy: What does it mean in Pakistan? Policy Actors’ Perspectives. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:10 George Downward. Diabetes among the Sami population of Sweden. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:11 Fauhn C Minvielle. Women’s right to health in the Anglo-Caribbean. Intimate partner violence, abortion and the State. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:12 Andrea Linander. Explicit Health Care Priority Setting in Practice. -Clinical managers’ views of performing vertical prioritization in Västerbotten County Council. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:13 Petronella Sevelius. Breastfeeding in rural Eritrea: a qualitative study of factors influencing women’s decision to exclusive or non exclusive breastfeeding. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:14 Yehualashet Tadesse. Cervical cancer: Analysis of diagnostic and therapeutic facility in public health institutions in Addis Ababa, Ethiopia. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:15 Muhammad Talha Khan. Diabetes mellitus and sugar consumption; an ecological study. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:16 Hina Khuram. Effect of aerobic physical training on stroke survivors. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:17 Batholomew Chireh. Knowledge, attitude and practices (KAP) concerning Hepatitis B among adolescents in the upper West Region of Ghana. The rural-urban gradient. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:18 Tom Nick Adie. Cost-effectiveness of community-based HIV/AIDS Management program: Implications for Kenya. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:19 Henrietta Opoku. Self-reported vision health status among older people in the Kassena-Nankana District, Ghana. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:20 Arnold Nyiegwen Muweh. Modernity in traditional medicine. Women’s experiences and perceptions in the Kumba health district, SW region Cameroon. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:21 Nazib Uz Zaman Khan. Husbands perceptions about their wives’ long term maternal morbidity: findings from interviews in rural Bangladesh. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2011:22 Abraham Tsegay. Knowledge, attitude and practice of public health practitioners towards safe abortion care services in Tigray regional state, Ethiopia. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2012:1 Md. Muradul Islam. Married men’s views on gender rights and sexuality in a northwest Bangladesh village. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2011.
2012:2 Sundip Gurung. Silent sufferers. Street children, drugs, and sexual abuse in Kathmandu, Nepal. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2012.
2012:3 Parshin Yousefi. Overweight/obesity and lifestyle. Characteristics among Iranian pre-school children. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2012.
2012:4 Nguyen Van Hiep. Sexual risk behaviors among male sex workers in Ho Chi Minh City, Vietnam- Implications for HIV prevention. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2012.
2012:5 Shufen Cao. The home-based elderly care system analysis: An illustration from Hangzhou, China. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2012.
2012:6 Mona Mohamed Ali. Food-and sun habits with a specific focus on vitamin D among pregnant Somali women living in Sweden. A study protocol. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2012.
2012:7 Zafarullah Khan Qamar. Depression among stroke patients and relation with demographic and stroke characteristics. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2012.
2012:8 Dina Vemming Oksen. An epidemiological overview on oral outbreaks of Chagas disease in South America. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2012.
2012:9 Bong Ngeasham Collins. Assessing the outcome of tuberculosis treatment in the Cameroon Baptist convention health board tuberculosis treatment centers. Master thesis in public health. Umeå International School of Public Health, Epidemiology Global Health, Department of Public Health and Clinical Medicine, Umeå University, 2012.
Umeå International School of Public Health
Epidemiology and Global Health
SE-901 85 Umeå, Sweden
Phone +46 90 785 27 29
www.phmed.umu.se/english/divisions/epidemiology
ISSN 1651-341X