Health Articles
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problem is amplified when one considers children living in the rural setting, where the
prevalence of acute malnutrition rises to 6.3 for those under the age of five (Pan American
Health Organization, 2008).
Literature Review
Global Infectious Diseases
"To have, by [2015], halted, and begun to reverse, the spread of HIV/AIDS, the scourge of malaria and other major diseases that afflict humanity." —U.N. Millennium Declaration (U.N., 2000, p. 13, emphasis added).
The U.N. Millennium Declaration (U.N., 2000) provided a structure for the formation of
the Millennium Development Goals (MDGs), eight objectives (see Figure 1) with corresponding
quantitative targets, intended to eliminate "extreme poverty, hunger, and disease by 2015"
(Hotez et al., 2007a, p. 1018) by improving global access to "peace, security, development,
human rights, and fundamental freedoms" (U.N., 2005, Resolution adopted by the General
Figure 1. The eight U.N. Millennium development goals, (U.N., 2000). Images U.N., 2013.
The sixth MDG, posited to "combat HIV/AIDS, malaria, and other diseases," is targeted
at reducing the global burden of morbidity and mortality related to some of the most prevalent
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infectious diseases (U.N., 2005). Both in terms of the initial framing of the sixth goal and the
subsequent coalition and campaign formation to address this goal, there exists an apparent
dichotomy regarding the diseases garnering the highest priority. Emphasis is placed on
HIV/AIDS and malaria, with a clear relegation of other targeted infections into the category "and
other diseases." Tuberculosis is often grouped with malaria and HIV/AIDS in terms of the
conceptualization of international infectious disease, prompting a distinction between "the ‘big
three' (HIV/AIDS, tuberculosis, and malaria)" and "other diseases" (Molyneux, 2008, p. 510).
As a result of the significant morbidity and mortality attributed to tuberculosis,
HIV/AIDS, and malaria over the last three-plus decades, there has been a concerted and largely
well-funded campaign of public and private players, with the aim of averting the loss of millions
of lives, and even more lost quality-adjusted life years (QALYs), by addressing the need for
prevention and control of these diseases (Katz, Komatsu, Low-Beer, & Atun, 2011; Komatsu et
al., 2010; The Global Fund to Fight AIDS Tuberculosis and Malaria, 2010). While the merits of
addressing the vast morbidity and mortality associated with tuberculosis, HIV/AIDS, and malaria
appear quite clear, the narrow focus on these three diseases in the face of hundreds of other
infectious diseases with significant health and societal burdens have led to criticism. As a direct
result of these narrowly focused initiatives, there is little resource or room left to address those
"other diseases," which are "some of the most prevalent diseases and causes of morbidity and
mortality amongst the poorest and most marginalized in society" (Molyneux, 2008).
The tight international focus on a non-majority of infectious diseases is not without
consequence. The burden caused by many viral, bacterial, ectoparasitic, fungal, and helminthic
diseases has remained largely unaddressed on the international stage, and neglected in terms of
public and private funding (Hotez, Ottesen, Fenwick, & Molyneux, 2006; Lammie, Fenwick, &
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Utzinger, 2006; Molyneux, Hotez, & Fenwick, 2005; Utzinger et al., 2009 & 2012). Due to the
shifting dynamics of resource channeling toward a limited number of infectious diseases and
away from a more extensive set of what are largely tropical illnesses, this latter group has been
referred to collectively as neglected tropical diseases (NTDs). Much of the drive for significant
and sustained funding of the "big three" has been derived from the well-defined epidemiology of
malaria, tuberculosis, and HIV/AIDS, specifically in terms of the quantification of morbidity and
mortality outcomes (Hotez et al., 2006; King & Bertino, 2008). This sort of epidemiologic
burden quantification has thus far been lacking for the neglected tropical diseases (Allotey,
Reidpath, & Pokhrel, 2010), which has hampered the effort to seek adequate funding and
intervention for the "other diseases." The neglect of significant, sufficient attention and funding
for this group of infectious diseases is multifaceted and includes economic, epidemiologic,
social, and geographic determinants (Allotey et al., 2010).
Prevalence of the neglected tropical diseases.
What began as a group of 13 infectious diseases (see Table 1)—seven helminthic, three
bacteria, and three protozoal—the neglected tropical diseases now number greater than 40 and
include ectoparasitic, fungal, and viral infectious agents as well (Utzinger et al., 2009).
The 13 Original Neglected Tropical Diseases
Helminths (parasitic intestinal worms)
Bacterial
Protozoan
Nematode (roundworm) Trematode (fluke)
Trachoma (bacterial) Human African trypanosomiasis (protozoan) Hookworm
Leprosy (bacterial)
Chagas disease (protozoan)
Buruli ulcer (bacterial) Leishmaniasis (protozoan)
Ascariasis Filariasis Onchocerciasis Dracunuliasis
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Among the neglected tropical diseases, the intestine-dwelling nematodes rank among the
most common chronic infectious diseases in low-income countries (de Silva et al., 2003).
Globally, three of the most common nematodes—ascaris lumbricoides, trichuris trichiura, and
hookworms—have prevalence estimates ranging from 1.5 billion individuals (Bundy, 1994) to
2.0 billion individuals (Savioli, Engels, & Endo, 2005). This accounts for global prevalence
estimates of 25% for ascaris lumbricoides, 20% for hookworm, and 17.5% for trichuris trichiura
(Crompton, 1999). Regionally, prevalence of infection by this dominant subset of nematodes
varies, reaching 50% in many sectors of India (Mani et al., 2002), with estimated prevalence
ranges among certain regions in Bangladesh of 70–95% for ascaris lumbricoides, 38–79% for
trichuris trichiura, and 2–71% for hookworm (Mascie-Taylor et al., 2003).
With prevalence of infection reaching a maximum at school age (Bundy, 1994), intestinal
nematode infections are one of the most common infectious diseases among children (Watkins,
Cruz, & Pollitt, 1996). An estimated one-third of children worldwide are infected (Awasthi et
al., 2008). As was the case among the general population prevalence estimates, childhood
disease prevalence varies markedly by region. In stool analysis of preschool children in
Uzbekistan, greater than 80% had infection with one or more intestinal parasites (Gungoren,
Latipov, Regallet, & Musabaev, 2007). Similarly, among children in Zanzibar, there was 99.7%
helminth prevalence, with 38% exhibiting infection with two organisms, and 55% with three
organisms (Simeon, Grantham-McGregor, Callender, & Wong, 1995). In terms of the disease
burden on individual causative agents, among Guatemalan school children aged 7–12 years,
Watkins et al. (1996) found a prevalence of 91% for ascaris lumbricoides and 82% for trichuris
trichiura on stool analysis. Similar studies produced regional ascaris prevalence estimates
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among Uzbeki children ranging from 1–24% (Gungoren et al., 2007), and of 33% among
preschool children in northern India (Mani et al., 2002).
Morbidity and mortality of the neglected tropical diseases.
Intestinal parasite infections and their deleterious consequences represent a significant
public health worry globally, specifically among children (Awasthi, Bundy, & Savioli, 2003;
Gungoren et al., 2007). In broader terms, concerted effect of improper sanitation, lack of access
to safe drinking water, and poor hygiene result in approximately 6,000 childhood deaths daily,
with a direct correlation between intestinal parasite infection and crude infant mortality rate
(Esrey, Potash, Roberts, & Shiff, 1991; Gungoren et al., 2007). Indeed, the relation of public
health and sanitation deficits and the resultant infectious disease morbidity and mortality is
multifaceted. Esrey et al. (1991) showed a 26% reduction in mean mortality upon screening for,
treating, and eliminating diarrheal illness. When this approach was taken with the additional step
of treating and eliminating ascaris lumbricoides, however, there was a 55% reduction in mean
The harmful effects of intestinal parasite infection, specifically nematode infection, have
been studied and described largely in relation to the childhood demographic and the impedance
of growth and development. However, concern for effects among adults have been highlighted
in the literature, including enhanced susceptibility to (Nacher et al., 2002; Spiegel, Tall,
Raphenon, Trape, & Druilhe, 2003) and severity of malarial disease (Druilhe, Tall, & Sokhna,
2005), decreased work ability and productivity (Crompton, 2000; O'Lorcain & Holland, 2000;
Stephenson, Latham, & Ottesen, 2000), and iron deficiency (Beasley et al., 1999; Crompton,
2000; Mebrahtu et al., 2004; O'Lorcain & Holland, 2000; Stephenson et al., 2000; Stoltzfus et
al., 1997). Moreover, conjecture has been made as to other potential effects, including more
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rapid advancement of HIV/AIDS (Fincham, Markus, & Adams, 2003), immunodeficiency,
bronchial asthma, appendicitis, and infertility (Moore et al., 2001; van den Biggelaar et al.,
Among children, there has been significant concern regarding the chronic effects of
intestinal parasite infection (Awasthi et al., 2003), largely centered on cognitive and physical
development. In addition to the aforementioned concerns and effects of intestinal parasite
infection, consequences of infection that are a specific worry in children include malnutrition
(Crompton, 1999; Stephenson, Latham, Adams, Kinoti, & Pertet, 1993; Tanumihardjo et al.,
1996); stunted physical growth, development, and fitness (Adams, Stephenson, Latham, &
Kinoti, 1994; Bagi et al., 2004; Crompton, 2000; Egger et al., 1990; O'Lorcain & Holland, 2000;
Raj, Sein, Anuar, & Mustaffa, 1996; Stephenson et al., 1993; Stephenson, Holland, & Cooper,
2000; Thein-Hlaing, Thane-Toe, Than-Saw, Myat-Lay-Kyin, & Myint-Lwin, 1991); and
decreased cognitive function with subsequently impaired educational achievement (Crompton,
1999; Jukes et al., 2006; Nokes, Grantham-McGregor, Sawyer, Cooper, & Bundy, 1992; Nokes
& Bundy, 1994; O'Lorcain & Holland, 2000; Taylor-Robinson, Jones, & Garner, 2009; Watkins
& Pollitt, 1997). Taken in concert, these potential and likely effects of chronic intestinal parasite
in children merit concern. Furthermore, Pelletier, Frongillo, Schroeder, and Habicht, (1994)
assert that there exists a direct correlation between weight and risk of death in preschool
children, some of the most susceptible to intestinal parasites (Bundy, 1994).
In addition to the prevalence estimates for the neglected tropical diseases, it is beneficial
to consider the disease burden in terms of subsequent disability and death, often presented as
disability-adjusted life years (DALYs). There is a relative dearth of data regarding the morbidity
and mortality of the neglected tropical diseases (Allotey et al., 2010), which has been a
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significant cause for the relative inability to garner substantial financial and resource backing of
campaigns targeted at these diseases (Hotez et al., 2006; Molyneux, 2008; Utzinger et al., 2009;
Weiss, 2008). This lack of epidemiologic backing is in stark comparison to the plethora of data
supporting the morbidity and mortality ramifications of the "big three" of HIV/AIDS, malaria,
and tuberculosis. And, while disease and disability burden estimates exist in the literature, it has
been asserted that they represent gross underestimations of the actual disease load caused by the
neglected tropical diseases (Finkelstein, Schleinitz, Carabin, & McGarvey, 2008; Hotez et al.,
2006; Jia et al., 2007).
The 2004 World Health Report (WHO, 2004) included extensive estimates of global
disease burden, represented as disability-adjusted life years (DALYs). These data, stratified
among various disease etiologies, included global and regional estimates for the burden caused
by the neglected tropical diseases. With some expressing concern that these estimates of
morbidity and mortality for the neglected tropical diseases undersold the true effect, upward
revisions of disability estimates were made for several in this group of infectious diseases (Hotez
et al., 2006). As depicted in Table 2 and Figure 2, upward revisions were made for four of the 13
original NTDs—hookworm, ascariasis, schistosomiasis, and trichuriasis. In these instances, a
DALY range is provided, in which the lower limit of the range represents the original WHO
estimates, and the upper limit represents the revision presented by Hotez et al. (2006).
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The Global Burden of Disease of the 13 Original Neglected Tropical Diseases
Global Disease Burden (DALYs / 1000)
Note: When present, range minimum depicts WHO estimates (2004) and maximum depicts corrected estimates by Hotez et al. (2006). Buruli ulcer and dracunuliasis burdens are insignificantly low.
Figure 2. Graph of the global burden of disease of the 13 original neglected tropical diseases, in disability-adjusted life years (DALYs). Dark gray shows baseline WHO estimates (2004). Light gray shows corrected estimates by Hotez et al., 2006. Vertical axis represents disease burden (in DALYs), while horizontal axis represents the disease.
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By the more conservative estimates, as depicted in Figure 2, the three NTDs accounting
for the largest disease burden, in dark gray, are filariasis, trachoma, and leishmaniasis. The
revised estimates (light gray), however, point to hookworm infection, ascariasis, and trichuriasis
as the most burdensome of the NTDs.
A different profile of disease burden is seen when the NTD are considered solely in the
context of the Americas (Table 3 and Figure 3). As portrayed by the WHO's more conservative
estimates, the three most burdensome NTDs in the Western Hemisphere are Chagas disease,
trachoma, and schistosomiasis. Conversely, upon revision, the most burdensome of the NTDs in
the Americas are trichuriasis, Chagas disease, and ascariasis.
The Burden of Disease of the 13 Original Neglected Tropical Diseases in the Americas
Americas Disease Burden (DALYs / 1000)
Note: When present, range minimum depicts WHO estimates (2004) and maximum depicts corrected estimates by Hotez et al., 2006. Buruli ulcer and dracunuliasis burdens are insignificantly low.
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800 700 600 500 400 300 200 100
Figure 3. Graph of the burden of disease of the 13 original neglected tropical diseases in the Americas, in disability-adjusted life years (DALYs). Dark gray shows baseline WHO estimates (2004). Light gray shows corrected estimates by Hotez et al., 2006. Vertical axis represents disease burden (in DALYs), while horizontal axis represents the disease.
The global burden of disease for the NTDs, per the conservative, initial estimates, is
17,655 DALYs per 1000 (WHO, 2004). Comparatively, the revised estimates of disease burden
represent a greater than three-fold increase, at 56,600 DALYs per 1000 (Hotez et al., 2006). The
disease burden of the NTDs is considered in light of the burden of the most prevalent global
infectious diseases in Table 4 and Figure 4. Given the upward revision of 56,600 DALYs per
1000, the NTDs burden ranks below HIV/AIDS, at 84,458 DALYs per 1000, but above the other
two "big three" diseases, with the burden from malaria at 46,486 DALYs per 1000, and the
burden from tuberculosis at 34,736 DALYs per 1000.
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The Global Burden of Prevalent Infectious Diseases
Disease / Class
Global Disease Burden (DALYs / 1000)
Lower Respiratory Infection
Note: When present, range minimum depicts WHO estimates (2004) and maximum depicts corrected estimates by Hotez et al., 2006.
90000 80000 70000 60000 50000 40000 30000 20000 10000
Figure 4. Graph of the global burden of prevalent infectious diseases, in disability adjusted life years (DALYs). Dark gray shows baseline WHO estimates (2004). Light gray shows corrected estimates by Hotez et al., 2006. Vertical axis represents disease burden (in DALYs), while horizontal axis represents the disease.
In the Americas, the infectious disease subset with the greatest burden of illness is
HIV/AIDS, followed by lower respiratory tract disease, and acute diarrheal illness, as depicted in
Table 5 and Figure 5. Below that of HIV/AIDS, the revised NTD burden ranks above the
estimates for tuberculosis and malaria, the other two "big three" diseases.
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The Burden of Prevalent Infectious Diseases in the Americas
Disease / Class
Americas Disease Burden (DALYs)
Note: When present, range minimum depicts WHO estimates (2004) and maximum depicts corrected estimates by Hotez et al., 2006.
Figure 5. Graph of the burden of prevalent infectious diseases in the Americas, in disability adjusted life years (DALYs). Dark gray shows baseline WHO estimates (2004). Light gray shows corrected estimates by Hotez et al., 2006. Vertical axis represents disease burden (in DALYs), while horizontal axis represents the disease.
Given the significant contribution of NTDs to the burden of infectious diseases, both
worldwide and regionally in some of the most impoverished nations of the Western Hemisphere,
the importance of understanding the characteristics of infection, as well as modes of treatment
and elimination, cannot be overstated. With the global predominance of three nematodes
(ascaris, trichuris, and hookworms) as leading causes of disease burden among the neglected
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tropical diseases, focusing on nematodes in terms of modes of infection and treatment is well
merited. The relevancy of considering the nematodes in the context of Paraguay, a South
American nation, is underscored by the predominant role of two nematode species—ascaris and
trichuris—among the top three NTDs in terms of disease burden.
While the exact burden of ascaris and trichuris in Paraguay are unknown, the WHO has
estimates for the number of school-age children and preschool children requiring "preventive
chemotherapy" with antiparasitic medication for soil-transmitted helminths (STHs) (WHO,
2013). Depicted below, in Table 6, are the counts of preschool and school age children in
Paraguay requiring antiparasitic treatment / prophylaxis for STH infections, from the year 2008
through 2011. While many countries within the WHO's STH database have accompanying data
regarding outcomes and success of treatment campaigns, such data is not available for Paraguay.
When first reported in 2008, 587,561 preschool children and 1,411,519 school children met the
WHO criteria for prophylaxis, which will be discussed in detail. By 2011, however, the number
in at risk groups, necessitating treatment, fell to 271,130 preschool children and 655,081 school
age children (WHO, 2013).
Count of Children at Risk of Soil-Transmitted Helminth Infection
Preschool School Age
Note: Above populations are at risk and indicated for antiparasitic medication. Adapted from World Health Organization data (2013).
These counts of the number of children eligible for prophylactic administration of
antiparasitic medication are tallied for all soil-transmitted helminths, of which the two focal
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organisms in this study – ascaris lumbricoides and trichuris trichiura – are two of the most
prevalent members. It is upon these two organisms, ascaris lumbricoides and trichuris trichiura,
that the remainder of this analysis will focus.
Characteristics of infection.
Ascaris lumbricoides and trichuris trichiura are parasitic intestinal worms with
transmission characterized by fecal-oral ingestion of the organisms' eggs (Bundy & Medley,
1992; Dold & Holland, 2011), often from utensils, food, water, and soil (Bradley & Jackson,
2004; Hagel & Giusti, 2010; Stephenson, Holland, & Cooper, 2000). Largely confined to
tropical and subtropical regions, most infected individuals are asymptomatic or exhibit mild
symptoms (Bradley & Jackson, 2004). In many cases, individuals are infected with both
organisms (Stephenson et al., 2000), with the severity of infection of ascaris lumbricoides highly
correlated with the severity of trichuris trichiura infection, and vice versa (Kightlinger, Seed, &
Kightlinger, 1995; Norhayati et al., 1997).
Ascaris lumbricoides.
Ascaris lumbricoides is the most prevelant gastrointestinal helminth infection, and ranks
among the most detrimental of the neglected tropical diseases worldwide, especially among
children (Hagel & Giusti, 2010), with the greatest intensity of infection occurring between ages 5
and 15 years (Hagel & Giusti, 2010). Infecting 1.2 billion individuals globally, the ascaris
lumbricoides organism is the largest of the nematodes that infect humans (de Silva et al., 2003),
as well as the most abundant egg-laying nematode (Guerra et al., 1991), able to produce greater
than 200,000 eggs daily (Hagel & Giusti, 2010). The eggs of ascaris are capable of surviving for
more than a decade, and, like the eggs of other nematode species, are able to adhere to "utensils,
furniture, money, fruits, vegetables, doors, hands and fingers" (Hagel & Giusti, 2010, p.349).
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The abundant egg production of a single ascaris organism, in combination with the impressive
durability of the infectious eggs, necessitates that efforts at treatment and elimination must, in
addition to providing medication therapy, address the larger environmental and public health
picture in terms of long-term infectivity of eggs secondary to poor sanitation practices (Hotez et
The burden of ascaris is most striking in those of that are impoverished or of lower socio
economic status (Dold & Holland, 2011). Due to the social, economic, and societal
marginalization experienced by such groups, poor housing and the lack of adequate sanitation are
typical characteristics of their living environments (Hagel & Giusti, 2010; Holland et al., 1988),
often resulting in unhygienic means of voiding feces (Haswell-Elkins, Elkins, & Anderson,
1989), which serves to promote the continued infection of the community via the ascaris eggs
that are shed in feces.
Though most individuals infected with ascaris are free of symptoms, approximately 8%
to 15% of those infected will be symptomatic (Albonico, Crompton, & Savioli, 1999). The most
common symptoms of those presenting with ascaris infection include abdominal bloating and
pain, nausea, diarrhea, and loss of appetite (Crompton, 2001; Hadju et al., 1996). The prevalence
and intensity of ascaris infection, and subsequent symptomatology, are factors of individual
human characteristics such as age, immune system, and behavioral influences, as well as such
environmental factors as housing and sanitation conditions (Kightlinger, Seed, & Kightlinger,
Trichuris trichiura.
Similar to ascaris lumbricoides in many ways, the nematode trichuris trichiura is also
most prevalent in tropical and sub-tropical regions. Though not generally as prevalent as ascaris,
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prevalence values for trichuris can reach greater than 90% among certain childhood populations
(Stephenson et al., 2000). Indeed, the highest infection rates are among children, as well as those
without proper sanitation resources and those of low socio-economic status (Guerra et al., 1991;
Kabatereine, Kemijumbi, Kazibwe, & Onapa, 1997).
As with ascaris, minor infections with trichuris often occur without symptomatology.
Moderate infections, however, present most commonly with patient signs and symptoms
including nausea, vomiting, decreased appetite, diarrhea, abdominal pain, protein malnutrition,
and anemia, with the most severe presentations often among children (Stephenson et al., 2000).
Patient perception of infection.
As previously highlighted, the prevalence and intensity of infection with ascaris and
trichuris intestinal parasites is enhanced by poor socio-economic status and underdevelopment,
conditions which often lead to inadequate housing, lack of drinkable water, improper disposal of
human waste, and a lack of health and hygiene education (Cooper, 1991). It is clear, then, that
there exist behavioral, social, and economic determinants of infection prevalence and severity,
just as there exist biological determinants, such as immune status. With this realization, the
importance of considering patient perceptions of behaviorally and socially related transmission
of infection when developing and implementing treatment and elimination strategies is quite
evident (Dold & Holland, 2011).
The causes, implications, and prevention of intestinal parasite infection are often not
appreciated by the community of affected individuals (Kamunvi & Ferguson, 1993). Mascie-
Taylor et al. (2003), in their analysis of intestinal parasite awareness and knowledge among the
people of rural Bangladesh, found that while 43% of those surveyed noted that eliminating
worms from one's body was positive in terms of health, 23% asserted that having intestinal
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worms itself offered positive health benefits. In terms of the acquisition of infection, 70% were
either mistaken about or not aware of the mode of entry of the worms into the body. Similarly,
in terms of behavioral and sanitary practices that increase the risk of infection, 50% of
individuals noted that defecating in their home courtyard was a risk, though only 27% noted that
defecating along a river bank was also a risk. In terms of food consumption that increases the
risk of parasite infection, 93% associated worms with eating sweet foods, while only 6%
associated worms with unwashed vegetables. Regarding prevention, 99% of individuals reported
hand washing following defecation, food preparation, feeding their children, and prior to eating.
When the technique for hand washing was assessed, however, 33% of individuals used only
soap, 18% used mud, 6% used only water, and 3% used ash, all methods known to be less
effective than washing with soap and water in eliminating bacteria, parasites, and other
communicable agents.
Treatment, Eradication, and Prevention of Intestinal Parasite Infection
The importance of an intestinal parasite management approach that incorporates the
multiplicity of determinants that contribute to infection and the subsequent morbidity and
mortality is crucial. As discussed, these determinants are not simply biological. In the same
vein, the solution to the burden of intestinal parasite infection is not purely biomedical. As
emphasized by Hotez et al. (2004) in their analysis of the management of tropical infectious
diseases, the long-term effectiveness of measures aimed at addressing these diseases must
include three components—addressing the need for development aimed at improving sanitation
infrastructure, improved health and hygiene education, and an anti-helminthic medication
program. Additionally, as the soil-transmitted helminthic infections are often endemic, the
directed medical therapy for anthelminthic treatment must target each of the endemic organisms
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(Dold & Holland, 2011). The importance of an approach that integrates control measures aimed
the frequently co-endemic infections is echoed by the World Health Organization (2002), as they
recommend a combined approach to treatment that addresses the regionally prevalent helminth
infections, whether nematode or trematode species. With this in mind, the importance of a
multifaceted approach to reducing the morbidity and mortality associated with ascaris and
trichuris will be considered as treatment and preventive modalities are examined.
Antihelminthic medication.
While the medical treatment of existing egg and organism loads in infected individuals is
not the only effort needed to combat intestinal parasites, it plays a vital role in tandem with
improvements in health education and sanitation. Specifically, while elimination of infection
from a community cannot be accomplished solely by antihelminthic medication—due to the
ever-present possibility for re-infection in conditions with inadequate sanitation practices—
medical treatment of individuals leads acutely to a significant reduction in infectious loads, as
well as a reduced morbidity secondary to infection (World Health Organization, 2002).
The medical treatment of soil-transmitted helminthiasis (STH), such as ascariasis and
trichuriasis, is based largely upon benzimidazoles, a class of medications first discovered in 1961
(Bennett & Guyatt, 2000). While the WHO endorses four single-dose medications as options for
the treatment of STH, including ascariasis, trichuriasis, and hookworm, the two preferred
medications, albendazole and mebendazole, are both benzimidazoles (World Health
Organization, 1995; World Health Organization, 2006). The favorability of albendazole and
mebendazole over the other two compounds—levamisole and pyrantel pamoate—is related to
their broad coverage of other co-endemic infections, ease of dosing and administration,
effectiveness, low cost, and low rate of side effects (Bennett & Guyatt, 2000; Hotez, Raff,
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Fenwick, Richards, & Molyneux, 2007b; Hotez et al., 2006; Molyneux et al., 2005; World
Health Organization, 1995). The ease of dosing and administering albendazole and mebendazole
are of great advantage. Albendazole and mebendazole are administered by mouth. Albendazole
is administered as a one-time 400 mg dose for individuals greater than or equal to two years of
age (World Health Organization, 2006). For those between 12 and 24 months of age, the World
Health Organization (2006) recommends a halved dose of 200 mg. Mebendazole, however, is
typically administered as 500 mg total spread over 3-5 days. These two benzimidazoles target a
plethora of pathogenic agents, highlighted below in Table 7. Of note is the characteristic that
both compounds are effective against ascaris, trichuris, and hookworm – two of which, ascaris
and trichuris, are prevalent in Paraguay.
Organisms Treated by Albendazole and Mebendazole
Albendazole
ascariasis
trichuriasis
lymphatic filariasis
cutaneous larva migrans microsporidiosis cysticercosis
visceral larva migrans
eosinophilic enterocolitis
Mebendazole
ascariasis
trichuriasis
trichostrongyliasis
eosinophilic enterocolitis
visceral larva migrans
Note: Soil-transmitted helminths (STHs) are italicized. Adapted from Table 208-1: Overview of Agents Used for the Treatment of Parasitic Infections in Moore (2012).
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Antihelminthic drug efficacy.
The efficacy of antiparasitic treatment varies, dependent upon the targeted pathogen and
the chosen compound. Measurements of antiparasitic medications are typically presented as
reported cure rate and/or reduction in egg count. As reported by Bennett and Guyatt (2000) in
their review of the efficacy of albendazole and mebendazole treatment, the cure rate for ascaris
after single-dose albendazole is greater than 80%. Comparatively, with the mebendazole
regimen of 500 mg over 3-5 days, the median reported cure rate is greater than 90%. In terms of
reduction in egg count, both albendazole and mebendazole resulted in nearly undetectable egg
counts after treatment (Bennett & Guyatt, 2000).
The efficacy of albendazole and mebendazole against trichuris is much more variable
than that of ascaris. The mebendazole regimen over 3-5 days has a media reported cure rate of
approximately 80%, though the 95% confidence interval ranges from 40% to 100% (Bennett &
Guyatt, 2000). Even more varied, Bennett and Guyatt (2000) found that the median cure rate for
trichuris using albendazole was 38%, with the 95% confidence interval stretching from 4.9% to
99.3%. The variance of efficacy in the treatment of trichuris continues when considering
reduction in egg count, with a median reduction of approximately 90% when using mebendazole
(95% CI of 55% - 100%), and 80% when using albendazole (95% CI of 5% - 100%) (Bennett &
While the heterogeneity of treatment efficacy for trichuris is quite stark, literature has
pointed to significant regional variance in terms of reported cure rates and reduction in egg
count. Bennett and Guyatt (2000) note that the global median reported cure rate of 38% is
skewed secondary to the observation that albendazole treatments is less effective in Asia than it
is in other regions. Of note, when the markedly lower reported cure rate for the treatment of
PARASITES IN PARAGUAY
trichuris with albendazole in Asia (33.3%) are excluded from analysis, the global mean cure rate
climbs from 38% to 61% (Bennett & Guyatt, 2000).
Indications for antihelminthic drug administration.
The World Health Organization's recommended prophylactic medication approach for
soil transmitted helminth (STH) infections, including ascaris and trichuris, is based upon risk
stratification of the targeted community (WHO, 2006). Based upon the prevalence of infection
among school children, the schema for medication administration differentiates between high-
risk and low-risk populations. High-risk populations are those with a school-age prevalence of
greater than or equal to 50%, while low-risk populations are those with a prevalence of greater
than or equal to 20% and less than 50%.
Just as the risk stratification of a community is defined in regard to the childhood
population, so too are the treatment efforts, with a focus on the treatment of school age children.
The World Health Organization recommends prophylaxis of all school-age children twice
annually in high-risk populations, with annual treatment of school-age children in low-risk
communities. For both risk-stratified populations, additional groups recommended for
medication administration include women of childbearing age, lactating women, second and
third trimester pregnant women, and preschool children (WHO, 2006). For populations with
STH prevalence less than 20%, the World Health Organization (2006) recommends against
broad antiparasitic treatment programs, largely due to the lack of benefit in the face of potential
risk associated with large-scale, repeated medication administration within a population.
However, in these non-endemic circumstances, disease specific treatment of diagnosed intestinal
parasite cases is merited.
PARASITES IN PARAGUAY
Side effects and risks of treatment.
The potential risks of treatment can be conceptualized in terms of immediate side effects
experienced by the patient and more global, ecologic effects resulting from the repeated blanket
treatment of targeted populations. The most common side effects experienced by patients after
ingestion of either albendazole or mebendazole, depicted below in Table 8, are gastrointestinal in
nature, with at a rate of 1% (Urbani & Albonico, 2003). In addition to short-term gastrointestinal
disturbances, patients given albendazole may have intermittent, reversible hair loss and
asymptomatic, transient elevations in liver enzymes. More rare side effects of albendazole
ingestion include an acute decrease in white blood cell count and skin rash (Moore, 2012).
Side Effects of Albendazole and Mebendazole Treatment
Albendazole
Occasional
decreased white blood cell count
abdominal pain headache reversible hairloss elevated liver function tests
Mebendazole
Occasional
severe decrease in white blood cells
decreased blood platelets
elevated liver function tests hairloss
Note: Adapted from Table 208-1: Overview of Agents Used for the Treatment of Parasitic Infections in Moore (2012).
Beyond the gastrointestinal upset typical of the benzimidazoles class of drugs, use of
mebendazole, like albendazole, can lead to a transient, asymptomatic elevation of liver enzymes.
PARASITES IN PARAGUAY
More rare effects of mebendazole ingestion include an acute, more severe decrease in white
blood cells, decreased blood platelet counts, and short-term hair loss (Moore, 2012).
While there has been a dearth of human studies assessing the fetal risk of albendazole or
mebendazole administration to pregnant women, models in pregnant rats given mebendazole
have indicated teratogenic effects (Bethony et al., 2006). However, due to the balance of risk
and benefit, the practical recommendation is the avoidance of albendazole and mebendazole
during the first trimester of pregnancy (Albonico et al., 2003).
Decreasing antihelminthic drug efficacy in certain regions has led to the concern for the
development of resistance among soil-transmitted helminths that infect human populations
(Brun, Schumacher, Schmid, Kunz, & Burri, 2001; Osei-Atweneboana, Eng, Boakye, Gyapong,
& Prichard, 2007; Sundar et al., 2000). Specifically, repeated multi-drug treatment campaigns
raise alarm for the emergence and dissemination of rug-resistant intestinal parasites (Smits,
While the concern for resistance among human intestinal parasites is of relatively recent
onset, the veterinary and livestock fields have been aware of this trend in animal models for at
least two decades, with prevalent resistance arising secondary to regular large-scale treatment
programs (Geerts, Coles, & Gryseels, 1997). While the deleterious effects of such resistance
among animal and livestock populations has been described in terms of economic loss, the
effects of prevalent resistance among human intestinal parasites would result in a even more
marked increase of morbidity among some of the world's poorest.
As a result of the concern for emerging antiparasitic resistance, there has been a call for
more in-depth safety and efficacy investigations of antiparasitic medications (Reddy et al.,
2007), as well as the importance of implementing schemas for detecting drug resistance early in
PARASITES IN PARAGUAY
the course via monitoring of treatment efficacy (Scherrer, Sjöberg, Allangba, Traor, & Utzinger,
2009). Measures to monitor for the emergence of resistance to antiparasitic medications, such as
parasitic egg hatching assays, have been in place for greater than two decades (Coles et al.,
1992). However, such laboratory technique and application has yet to become prevalent in the
care of human patients. Than being said, there has been an adaptation of such veterinary
monitoring and resistance detection tools for the human population, targeting resistance to
human hookworm infections (Albonico et al., 2005).
This retrospective study is a chart review of de-identified clinic records from consecutive
patients presenting to three temporary primary care clinics in the Capital District of Paraguay,
South America, between June 20 and June 24, 2011. The clinics, functioning as the medical arm
of a short-term medical mission, were conducted at three different sites—Village 1 from June
20–21, Village 2 on June 22, and Village 3 from June 23–24.
Each of the villages, rather impoverished barrios outside of the capital city of Asunción,
varied in terms of the predominant language spoken. While nearly every patient presenting to
clinic in Village 1 and Village 3 spoke Spanish, this was not the case at Village 2. In Village 2, a
large majority of patients spoke only the indigenous language, Guarani. This necessitated an
extra interpreter in many instances—often from English to Spanish, then Spanish to Guarani, and
the reverse. Additionally, as may be deduced from the predominance of patients whose primary
language was Guarani, a large proportion of patients seen in Village 2 were more traditionally
indigenous compared to the populations attended to in Village 1 and Village 3.
PARASITES IN PARAGUAY
Data Collection
The clinic records that formed the basis of this analysis were history and physical forms
that were completed as the individual patient was seen in clinic (see Appendix A). The patient
flow typically began with patients presenting to an intake table staffed with Paraguayan nursing
students for the recording of demographic information, vital signs, and presenting concerns and
symptoms on the clinic form. Patients would then be directed to the appropriate available
services, including vision clinic, dental clinic, or medical clinic, depending on the presenting
While attended to in medical clinic by one of four volunteer providers from North
America (one physician, two nurse practitioners, and one medical student), the provider
completed clinic records for the individual patient. These volunteer healthcare providers staffed
the primary care medical clinic, which was conducted alongside a dental and vision clinic staffed
by other foreign volunteers. Only those patients attended to by one of the four North American
primary care clinic providers are included in this analysis; those only presenting to the dental or
vision clinic are not included in the analysis.
Following the provider encounter, patients prescribed treatments were directed to the
pharmacy, staffed by other members of the mission trip, and the patient's prescriptions were
filled. Each portion of the patient's visit consisted of completion of a given portion of the clinic
Analysis
Descriptive analysis of patient demographics and presenting problems, as well as the
diagnostic and treatment decisions of the providers, formed the basis of this study. The original
clinic records were hard copy sheets completed by hand. This hard copy was de-identified by
PARASITES IN PARAGUAY
project staff and entered into a Microsoft Excel spreadsheet. De-identification consisted of the
removal of patient names, location identifiers more specific than state or district, patient-specific
dates, health record numbers, and all other patient-identifying numbers, in accordance with the
Safe Harbor Method for the de-identification of protected health information (U.S. Department
of Health & Human Services, 2013).
As the data upon which this analysis was based are previously collected medical records
with proper de-identification of protected health information, an Exempt Research Proposal was
submitted to the Institutional Review Board of Wright State University, Office of Research and
Sponsored Programs, in July 2012 (see Appendix B). Institutional Review Board approval was
received in August 2012.
All patient chief complaints, physician diagnoses, and physician treatment options were
treated as dichotomous variables and were binomially coded in Microsoft Excel. Counts of chief
complaints, diagnoses, and treatments were calculated by summing binomially coded columns,
and stratified based on age (under 18 years of age or over 18 years of age), gender (female or
male), location (Village 1, Village 2, or Village 3), and provider (Provider 1, Provider 2,
Provider 3, or Provider 4).
Prevalence values for chief complaints, diagnoses, and treatments were calculated in
Microsoft Excel as the count of positive values divided by the total population or stratified sub
population, and were presented as percentages. Additionally, via IBM's SPSS Statistics software
Version 20.0.0, t-test and ANOVA values were calculated to ascertain the statistical significance
of demographic differences and variance in prevalence across the sub-stratified categories (i.e.
"parasites" as a presenting concern at Village 1 versus Village 3, etc.). An alpha value of 0.05
was used to mark significance in this analysis, with marginal significance as alpha of 0.10. For
PARASITES IN PARAGUAY
the continuous variable age, across all stratified categories, standard deviations and 95%
confidence intervals were calculated using Microsoft Excel.
All core variables, both dependent and independent, are depicted in Table 9. Relevant
dependent variables for analysis of parasitism and management of parasitism were: the
prevalence of patients presenting with the concern of "parasites," the prevalence of a diagnosis
of "parasites," and the prevalence of prescription of antiparasitic medication (albendazole 400
mg by mouth once, or mebendazole 100 mg by mouth daily for three days).
Variables for Analysis
Variable
Variable Type
"Parasites" as a Presenting Concern
Continuous (frequency)
Depedent
"Parasites" as a Diagnosis
Continuous (frequency)
Variables
Anti‐parasitic Medication Prescription
Continuous (frequency)
Continuous (years)
Independent Patient Age Category
Categorical (U18 or 18+)
Variables
Categorical (Village 1 or 2 or 3)
Categorical (Male or Female)
The dependent variable was considered to be a function of the independent variables,
including age category (under 18 years (-18) or 18 years and above (18+), clinic location, and
Counts of patients seen are depicted in Table 10. In sum, 505 patients were seen by
medical providers in clinic and included in analysis. During the two-day clinic in Village 1, 197
patients were seen. During the one-day clinic in Village 2, 76 patients were attended to. Finally,
over the course of the two-day clinic in Village 3, 232 patients were seen.
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Count of Patients Seen in Clinic by Location, Gender, and Age Group
Village 1
Village 2
Village 3
Female patients outnumbered male patients overall, with 327 females seen, compared to
178 male patients. This was the case at each of the three clinic locations. Additionally, in terms
of age category, children (under age 18 years) outnumbered adults (age 18 years or older); the
number of children attended to amounted to 310, compared to 195 adults overall. This was not
consistent between the 3 clinic locations, however: in Village 2, more adults (43) were seen than
Descriptive Results
Patient age.
The age distribution across the entire population of patients seen is depicted in Figure 6,
as are the age distributions by gender. The median patient age for all clinic attendees, as
depicted in Table 11, was 10 years, with a significant difference (p < 0.0001) between median
ages for females (17 years) and males (5 years). Subdivided by village, the median age was
significantly different (p < 0.0001) between females and males for Village 1 (F = 23 years, M =
6 years) and Village 3 (F = 12 years, M = 5 years). The median age by gender for Village 2 (F =
PARASITES IN PARAGUAY
24.5 years, M = 18.5 years) was not significantly different than those of Village 1 or Village 3 (p
Age Histogram of All Patients Seen
Age (years)
Age Histogram of Female Patients Seen
Age (years)
Age Histogram of Male Patients Seen
Age (years)
Figure 6. Histograms depicting the cumulative age distribution and distribution by gender.
PARASITES IN PARAGUAY
Median Age of Patients Seen in Clinic by Location and Gender
Median Age in Years (Lower Quartile, Upper Quartile)
Village 1
Village 2
Village 3
Female 23 (8, 37.8) b
24.5 (5, 46.8) c
18.5 (5.3, 53.3) c
a Median age by gender significantly different overall (Female = 17, Male = 5, p < 0.0001).
b Median age by gender significantly different for Village 1 (Female = 23, Male = 6, p < 0.0001).
c Median age by gender not significantly different for Village 2 (Female = 24.5, Male = 18.5, p = 0.3036).
d Median age by gender significantly different for Village 3 (Female = 12, Male = 5, p = 0.0067).
e Median age by location significantly different between Village 1 and Village 2 (V1 = 10, V2 = 24.5, p < 0.0001).
f Median age by location not significantly different between Village 1 and Village 3 (V1 = 10, V3 = 8, p = 0.2875).
g Median age by location significantly different between Village 2 and Village 3 (V2 = 24.5, V3 = 8, p < 0.0001).
The median patient age by clinic location, as depicted in Table 11, was significantly
different (p < 0.0001) between Village 1 (10 years) and Village 2 (24.5 years), and between
Village 2 (24.5 years) and Village 3 (8 years), with p < 0.0001. The difference in median age
between Village 1 (10 years) and Village 3 (8 years) was not statistically significant (p =
Patient presenting concerns.
The presenting concerns for patients are illustrated in Table 12. The most prevalent
presenting concerns for the population as a whole, across all three clinic locations, age
categories, and genders, were cough (43%), headache (32%), parasites (30%), and runny nose
(30%). These four complaints were the most common for both children and adults. Presenting
concerns and the frequency of concerns among children included cough (41%), headache (33%),
runny nose (29%), and parasites (27%). Similarly, among adults, the most prevalent presenting
concerns and frequencies were cough (47%), parasites (34%), headache (32%), and runny nose
PARASITES IN PARAGUAY
The most common presenting concerns at the clinic in Village 1 were cough (44%),
parasites (32%), headache (31%), and runny nose (28%). Comparatively, the most frequent
concerns presented in Village 2 were cough (47%), headache (34%), runny nose (33%), and sore
throat (30%). Finally, in Village 3, the most abundant concerns were cough (42%), headache
(32%), runny nose (30%), and parasites (29%).
Prevalence of Gastrointestinal and Constitutional Patient Presenting Concerns
Prevalence by Clinic Location
Presenting Concern Total Prevalence Age Category Village 1 Village 2 Village 3 Total by Age
Combined
Vomiting
Combined
Parasites
Combined
Headache
Combined
Diarrhea
Combined
Combined
Diagnoses made in clinic.
The diagnoses made in clinic by the volunteer providers, as well as the corresponding
frequencies, are depicted in Table 13. The most prevalent diagnoses made across all patients
seen in the three clinic locations were parasites (46%), upper respiratory infection (29%)
PARASITES IN PARAGUAY
headache (9%), and hypertension (5%). Among the childhood population, the most frequent
diagnoses made were parasites (43%), upper respiratory infection (27%), headache (10%), and
allergic rhinitis (5%). Comparatively, among adults, the most abundant diagnoses were parasites
(50%), upper respiratory infection (32%), hypertension (8%), and headache (7%).
The most prevalent diagnoses varied by clinic location. In Village 1, the most frequently
diagnosed entities were parasites (45%), upper respiratory infection (28%), hypertension (8%),
and headache (8%). Comparatively, in Village 2, the most common diagnoses were parasites
(49%), upper respiratory infection (34%), hypertension (8%), acute otitis media (7%), and
headache (7%). Finally, in Village 3, the most abundant diagnoses were parasites (45%), upper
respiratory infection (28%), headache (11%), and allergic rhinitis (4%).
Prevalence of Gastrointestinal Diagnoses Made in Clinic
Prevalence by Clinic Location
Diagnosis
Total Prevalence Age Category Village 1 Village 2 Village 3 Total by Age
Acute Gastroenteritis
Combined
Gastroesophageal Reflux
Combined
Parasites
Combined
At Risk / Malnutrition
Combined
Treatments Prescribed in Clinic.
The treatments prescribed in clinic by the volunteer providers, as well as their
corresponding frequencies, are depicted in Table 14. The most prevalent treatments prescribed
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over all patients seen were antiparasitic medication (51%), vitamins (37%), analgesics (29%),
and antibiotics (15%). Among children, the four most frequently prescribed treatments were the
same as those for the total population, and included antiparasitic medication (49%), vitamins
(35%), analgesics (31%), and antibiotics (15%). Comparatively, among the adult population, the
most frequently prescribed treatments consisted of the same four medications as the entire
population, and included antiparasitic medication (53%), vitamins (39%), analgesics (27%), and
antibiotics (15%).
The most prevalent treatments prescribed varied by clinic location. In Village 1, the most
frequently prescribed treatments were antiparasitic medication (51%), vitamins (32%),
analgesics (28%), and topical ointments (12%). Comparatively, in Village 2, the most
commonly prescribed treatments were antiparasitic medication (58%), vitamins (47%),
analgesics (34%), and antibiotics (18%). Finally, in Village 3, the most abundantly prescribed
treatments were antiparasitic medication (47%), vitamins (38%), analgesics (28%), and
antibiotics (18%).
Prevalence of Treatments Prescribed in Clinic
Prevalence by Clinic Location
Treatment
Total Prevalence Age Category Village 1 Village 2 Village 3 Total by Age
Antibiotics
Combined
Antiparasitic Medication
Combined
Analgesic
Combined
Vitamins
Combined
PARASITES IN PARAGUAY
Analytic Results
Prevalence of "parasites" as a presenting concern by patients.
The frequencies of the presenting concern "parasites" are depicted in Table 15 and Figure
7, stratified by age category, gender, and clinic location. Among the entire population of patients
seen in clinic, the frequency of the presenting concern "parasites" was 30%. When considered
by age category, there existed a marginally significant difference (p = 0.073) between the
frequencies of this presenting concern, with increased prevalence among adults (35%) compared
to children (27%). When grouped by gender, the presenting concern of "parasites" was more
common among females (33%) than males (25%). This difference was of marginal significance
Frequency of Parasite Presenting Concern, Diagnosis, and Treatment
Village 1
Village 2
Village 3
Gender Totals
Parasite
Presenting
Age Total
Parasite
Diagnosis
Age Total
Treatment
Prescribed
Age Total
a Difference in prevalence by patient age category is marginally significant (Child = 0.27, Adult = 0.35, p = 0.073)
b Difference in prevalence by patient gender is marginally significant (Female = 0.33, Male = 0.25, p = 0.052)
c Difference in prevalence by clinic location is not significant (Village 1 = 0.32, Village 2 = 0.26, Village 3 = 0.29, p = 0.573, ANOVA model)
d Overall ANOVA corrected model by village not significant with p = 0.335, R Squared = 0.025, and adjusted R Squared = 0.003.
e Difference in prevalence by patient age category is not significant (Child = 0.43, Adult = 0.50, p = 0.11)
f Difference in prevalence by patient gender is not significant (Female = 0.48, Male = 0.42, p = 0.187)
g Difference in prevalence by clinic location is not significant (Village 1 = 0.45, Village 2 = 0.49, Village 3 = 0.45, p = 0.836, ANOVA model)
h Overall ANOVA corrected model by village not significant with p = 0.672, R Squared = 0.017, and adjusted R Squared = -0.005.
i Difference in prevalence by patient age category is not significant (Child = 0.49, Adult = 0.53, p = 0.359)
j Difference in prevalence by patient gender is marginally significant (Female = 0.54, Male = 0.45, p = 0.066)
k Difference in prevalence by clinic location is not significant (Village 1 = 0.51, Village 2 = 0.58, Village 3 = 0.47, p = 0.275, ANOVA model)
l Overall ANOVA corrected model by village not significant with p = 0.655, R Squared = 0.017, adjusted R Squared = -0.005.
PARASITES IN PARAGUAY
When grouped by clinic location, there was no statistically significant difference (p = 0.573) in
prevalence of the presenting concern "parasites" across Village 1 (32%), Village 2 (26%), and
Village 3 (29%). Indeed, the composite ANOVA model of clinic location in relation to the
presenting concern of "parasites" explained less than 1% of the variance in frequency across
villages (adjusted R-squared = 0.003).
Figure 7. Graph of the frequency of "parasites" as a presenting concern among patients presenting to clinic by clinic location, patient age, and patient gender. Vertical axis represents frequency.
Prevalence of "parasites" diagnosis.
The frequencies of the diagnosis of "parasites" made in clinic are depicted in Table 15
and Figure 8, stratified by age category, gender, and clinic location. The differences in
frequency were not statistically significant across age category (p = 0.1100), gender (p =
0.1870), or clinic location (p = 0.8360). Among the entire population of patients seen in clinic,
the frequency of the diagnosis of "parasites" was 46%. When considered by age category, the
PARASITES IN PARAGUAY
prevalence among adults was 50%, compared to 43% among children. Grouped by gender, the
prevalence of the presenting concern "parasites" was 48% among females and 42% among
males. When grouped by clinic location, there was no statistically significant difference (p =
0.836) in prevalence of the diagnosis of "parasites" among Village 1 (45%), Village 2 (49%),
and Village 3 (45%). The composite ANOVA model of clinic location in relation to the
diagnosis of "parasites" explained less than 1% of the variance in frequency across villages
(adjusted R-squared value of - 0.005).
Figure 8. Graph of the frequency of "parasites" as a diagnoses made in the clinic by clinic location, patient age, and patient gender. Vertical axis represents frequency.
Prevalence of antiparasitic treatment prescription.
The frequencies of the prescription of antiparasitic treatment are depicted in Table 15 and
Figure 9, stratified by age category, gender, and clinic location. Among the entire population of
patients seen in clinic, the frequency of the prescription of antiparasitic treatment was 51%.
PARASITES IN PARAGUAY
When considered by age category, the difference in antiparasitic prescription rates between
children (49%) and adults (53%) was not statistically significant (p = 0.359). When grouped by
gender, the prescription of antiparasitic medication was more common among females (54%)
than males (45%). This difference between females and males was marginally significant (p =
Figure 9. Graph of the frequency of antiparasitic treatments prescription made in the clinic by clinic location, patient age, and patient gender. Vertical axis represents frequency.
When grouped by clinic location, there was no statistically significant difference (p =
0.2750) in prevalence of antiparasitic treatment prescription across Village 1 (51%), Village 2
(58%), and Village 3 (45%). The ANOVA model evaluating clinic location in relation to
antiparasitic treatment prescription explained less than 1% of the variance in frequency across
villages (adjusted R-squared value = - 0.005).
PARASITES IN PARAGUAY
Discussion
Two foci are central to this analysis of data collected from a short-term medical mission
in Paraguay—a general description of the patient population seen in clinic and a more in-depth
analysis of the management of intestinal parasites within this patient population. The
management of parasitic disease is considered with respect to the rates of "parasite" as a
presenting concern, "parasite" as a diagnosis, and antiparasitic treatment prescription.
Additionally, the prescription of antiparasitic treatment is examined in light of World Health
Organization (2006) recommendations for antiparasitic prophylaxis against soil-transmitted
Patient Population
As depicted in Figure 6, the age distribution of the entire population of patients seen (505
individuals) was skewed toward childhood, most markedly under the age of 13 years. Several
prominent peaks in the age histogram occur at approximately age 5 years, as well as adults aged
20, 30, and 50 years. As each of the clinics for Villages 1–3 were conducted in out of session
schools, it may be of little surprise that children were the most prevalent patient population.
The most marked variance in patient population occurred along lines of patient gender
and patient age. The distribution of age in terms of gender points to a male population largely
skewed toward childhood ages (median age = 5 years), and a female population less skewed in
this direction (median age = 17 years), as shown in Figure 7. This distribution of ages for males
indicates a male patient population largely comprising children under the age of 11 years.
Comparatively, the distribution of female patients, while still skewed toward younger ages, had
substantially more adults, clustered in the 20s, 30s, and 50s. In contrast, there was a dearth of
male adults, with only 33 visiting clinics the entire week. Synthesizing this data with anecdotal
PARASITES IN PARAGUAY
experience from the Paraguay STMM, a likely cause for this distribution of ages by gender is the
caregiver – child relationship. Though not analyzed in this study, adult caregivers, typically
female, accompanied the large majority of school-age children. It was rare that a male caregiver
would accompany the children to the clinic. While it seemed that most of the adult males
presented alone, the large majority of adult females presented alongside their children—often in
family groups of up to 8 family members.
These data suggest that the household dynamics in Paraguay are such that the female
caregiver may be responsible for caring for the children to a much greater extent than the male
caregiver, at least during the daytime, when each of the five days of clinic were held.
Additionally, due to the peaks in adult female ages in the 20s, 30s, and 50s, it seems likely that
the female caregivers included both mothers and grandmothers. This distribution of patient age
with a skew toward childhood was evident for Villages 1 and 3, and for the aggregate population.
The fact that the distribution of ages was not as skewed for Village 2 may be due to the small
sample size (n = 76) compared to Village 1 (n = 197) and Village 3 (n = 232).
Intestinal Parasite Presentation and Diagnosis
The frequency of patients presenting with a concern for parasites, as well as the
frequency of clinical diagnosis of intestinal parasitism by the volunteer health care providers, are
considered here as proxy measurements of actual disease prevalence within the community. The
complaint of "parasites" was consistently within the top four presenting concerns across the core
sub-groups examined in this study—divided along lines of age, gender, and clinic location—with
30% of all patients presenting to clinic with this as a concern. From the perspective of clinical
diagnosis by the volunteer providers, "parasites" was the most common diagnosis made, with
45.5% of all patients receiving this diagnosis. Taken together, and allowing for these measures
PARASITES IN PARAGUAY
to act as proxy values of the actual prevalence of intestinal parasite disease in the entire sample
population, the frequency of "parasites" as a presenting concern and as a diagnosis indicates a
possible prevalence between 30% and 46%. These estimates may grossly underestimate the
actual prevalence of intestinal parasite disease in the sample population, considering that only
15% of those infected are symptomatic (Albonico et al., 1999).
Although attempting to estimate the prevalence of intestinal parasite disease using such
markers as a patient's concern of having the disease and a health care provider's clinical
suspicion of a disease is far from ideal, these estimates are the best that can be produced from the
available data and methods used in chart review. The gold standard for intestinal parasite
diagnosis, stool analysis, would offer the most thorough and precise means of estimating the
disease prevalence within a given population. No method for estimating the presence and load of
intestinal parasites is flawless, however, as the sensitivity of even stool collection and analysis is
dependent on the timing of the test in regard to the laying of eggs by the female parasites while
in the host, leading to potential false negatives when there is a paucity of egg-laying activity
(Cho & Kang, 1975; Yang, Kim, Jung, Huh, & Lee, 1997).
Relative to the global prevalence of ascaris lumbricoides (25%) and trichuris trichiura
(18%), the estimated combined prevalence of intestinal parasite disease in the patient population
examined herein—30% to 46%—may indicate a higher-than-average prevalence of intestinal
parasites relative to the aggregate world population. Prevalence estimates more regionally
specific for Latin America are sparse, with most of the existing literature reporting on the
childhood population. Compared to a prevalence of 91% for ascaris and 82% for trichuris
among Guatemalan school children (Watkins et al., 1996), the composite prevalence range found
in this study (30% to 46%) is markedly lower. The values derived in this study specific for the
PARASITES IN PARAGUAY
childhood population—27 % to 43%—less than half the prevalence reported by Watkins et al.
(1996) among Guatemalan school children.
Age category.
Subdivided by age category (child of less than 18 years versus adult of 18 years or more),
the marginally significant (p = 0.0730) difference in the prevalence of a "parasite" presenting
concern (35% for adults versus 27% for children) is not what might be expected when the
highest prevalence of intestinal parasites by age in the literature is found among school age
children (Awasthi et al., 2008; Bundy, 1994; Watkins et al., 1996). In contrast, when examining
the frequency of the diagnosis of intestinal parasitism made by the clinic providers, there was not
a statistically significant difference between child and adult populations. As the prevalence of
intestinal parasitism is expected to peak in childhood, this is not the expected outcome.
As the prevalence of the presenting concern "parasites" and the diagnosis of "parasites"
by the volunteer providers in clinic serve merely as proxy estimations of the actual prevalence
within this patient sample, any statistically significant difference seen in the groups may be due
to factors other than the main independent variables examined—age, gender, and clinic location.
Possible confounding factors that could cause the observed prevalence outcomes with respect to
age to be different than what would be expected based upon the literature may include hidden
cases among the childhood age category, or the difficulty of parsing a child's presenting
concerns compared to those of an adult. In many clinical encounters, the caregiver acted as the
presenter of the child's concerns, which may have hampered an accurate presentation of the
actual biological or pathological experience of the child from being presented in full.
PARASITES IN PARAGUAY
Females more frequently presented with the concern of parasitism than males, a
difference that was statistically significant. In contrast, the difference in the rate of parasite
diagnosis between males and females was not significant. Taken as a marker or proxy
estimation of the actual parasite prevalence in the patient sample, the greater prevalence of
presenting with "parasites" among females versus males may be due to the gender roles within
the home and the relation of adults to children in the caregiver setting. The prevalence and
intensity of intestinal parasite infection is highest among school age children (Bundy, 1994) and
that the environmental, hygiene, and sanitation structure in the immediate vicinity of a home has
a strong relationship to the risk of infection (Hagel & Giusti, 2010; Haswell-Elkins et al., 1989;
Holland et al., 1988; Hotez et al., 2004). The increased concern for parasite infection among
female versus male patients may be attributed to female caregivers being traditionally involved
in childcare and domestic work close to home, with increased exposure to infectious parasitic
eggs via their children as hosts and in communities lacking proper sanitation infrastructure. In
the population of patients seen during this STMM, it seemed apparent that females spent more
time with the children and around the home, and, hence, may be more likely to be infected due to
these environmental and sociological factors.
Clinic location.
There was no statistically significant difference in the frequency of presenting concern of
parasites or the clinical diagnosis of parasites across the three clinic locations. The finding of
similar frequencies of presentation and diagnosis among the three villages may be expected, as
all three are located within the Capital District are less than 20 miles apart, and are of low socio
economic standing, therefore representing a relatively homogenous patient sample. While
PARASITES IN PARAGUAY
Village 2 stood out, anecdotally, as rather different from Village 1 and Village 3 due to cultural,
language, and economic differences, there were no statistically significant differences in
intestinal parasite prevalence by location. There may be a veiled difference among the
population in Village 2 that is not statistically clear due to the relatively small sample size (n=76)
compared to Village 1 (n=197) and Village 3 (n=232).
Prescription of Antiparasitic Treatment
The central question in this analysis, regarding antiparasitic treatment, was whether the
prevalence of intestinal parasite disease among the Paraguayan patient population seen in clinic
during the STMM falls within a risk group that merits medical prophylaxis as defined by the
World Health Organization (2006). Secondarily, given this risk-stratified recommendation
regarding medical treatment and prophylaxis against intestinal parasites, it is of interest to
consider the frequency of antiparasitic medication prescription in clinic and whether the
approach to prescription matched the standards of the recommendations for prophylaxis from the
World Health Organization (2006).
The World Health Organization's (2006) risk stratification is based upon intestinal
parasite prevalence thresholds of 20% (low-risk group) and 50% (high-risk group)—both of
which merit administration of antiparasitic medication, albeit at different frequencies. High-risk
communities (those with a prevalence of greater than 50%) merit twice-yearly administration of
antiparasitic medication to school age children, while low-risk communities, those with a
prevalence between 20% and 50%, merit once-yearly treatment. Additionally, preschool
children, women of childbearing age, lactating women, and pregnant women in the second or
third trimester who live in low-risk or high-risk communities should be treated. Broad
PARASITES IN PARAGUAY
antiparasitic medication campaigns are not recommended for communities outside of these risk-
stratification recommendations (communities with a prevalence less than 20%) WHO, 2006).
Antiparasitic administration as prophylaxis.
If the clinical and public health approach taken by the Paraguay STMM matched the
threshold of recommended antiparasitic prophylaxis, despite being prescribed based on newly
diagnosed instances of parasitic disease, all children seen in clinic over the age of one year, as
well as all women of childbearing age, excluding those in the first trimester of pregnancy, were
indicated for administration of antiparasitic medication, in light of the recommendations from the
World Health Organization (2006) and the post facto intestinal parasite prevalence estimations of
30% to 46%. This group of individuals indicated for antiparasitic prophylaxis accounts for 78%
of the entire population seen in the five days of clinic, as depicted in Table 16. Of those
individuals indicated for prophylaxis, only 48% were actually given medication. Conversely,
22% of all individuals seen fell outside of the recommendation criteria for prophylaxis, largely
due to being adult males, women outside of childbearing age, or pregnant females. While the
World Health Organization recommendation (2006) is that pregnant women in the first trimester
not receive antiparasitic medication, all pregnant women were excluded from receiving
medication during this STMM, regardless of trimester. For the overall population of those not
indicated for prophylactic medication, 60% received treatment regardless—a higher proportion
than those that were actually indicated for prophylactic administration (60% versus 48%).
PARASITES IN PARAGUAY
Prophylaxis or Treatment – Percent of Patients Seen Indicated for and Receiving Antiparasitic Medication
To Receive
To Not Receive
To Receive
To Not Receive
Medication
Medication
Medication
Medication
If Medication
Prophylaxis a
Combined
If Medication
Treatment b
Composite
Medication as
Prophylaxis or
Treatment c
a If medication administration viewed as a broad prophylactic campaign and not treatment of existing disease diagnosis. Recommendation criteria for prophylaxis based on World Health Organization (2006) protocol.
b If medication administration viewed as treatment of existing disease diagnosis and not a broad prophylactic campaign. Recommendation criteria for treatment based on positive clinical diagnosis of intestinal parasitism.
c If medication administration viewed as either a broad prophylactic campaign or treatment of existing disease
diagnosis, a composite of a and b.
Antiparasitic administration as treatment of newly diagnosed parasitism.
The cause of such discordance with respect to the application of the prophylactic
recommendations—leaving more than half of those indicated for prophylaxis untreated—while
potentially due to improper application of the recommendations, is most likely due to a different
set of clinical drivers influencing prescribing behavior among the providers. This second
prescribing ideology, depicted in the second row of data in Table 16, is based upon the clinical
diagnosis of intestinal parasite disease and the prescription of antiparasitic medication as a means
of treatment, not prophylaxis—hence the discordance between those indicated to receive
PARASITES IN PARAGUAY
medication per the World Health Organization (2006) prophylaxis guidelines and the percent that
was actually given the medication.
This difference is apparent when considering the indication for the administration of
antiparasitic medication as a diagnosis of parasitism, as opposed to falling within a risk category
for prophylactic administration. Nearly 46% of all individuals seen in clinic were diagnosed
with intestinal parasites, with 88% actually receiving treatment—a more appropriate coverage
rate of those indicated for treatment compared to the 48% that were properly given medication if
the goal for administration were prophylaxis. Consideration of the prescription of antiparasitic
medication during the Paraguay STMM in light of these two approaches—prophylactic
administration of medication to at-risk populations versus treating only those with diagnosed
disease—it seems apparent that the volunteer providers favored administration of medication
based on diagnosed disease, not upon a broader, public health-oriented treatment campaign.
It is worthwhile to consider these antiparasitic administration approaches in composite,
examining the population that merits administration for either prophylaxis or treatment—i.e. all
of those patients seen that were indicated for antiparasitic medication, regardless of approach
(prophylaxis or treatment). Of all patients seen, 90% were indicated to receive antiparasitic
medication, either because they fell within the World Health Organization recommendations for
prophylaxis, or because they were diagnosed with intestinal parasitism in clinic. However, of
this composite group indicated for medication administration, only 53% received albendazole or
Consideration of the prescription of antiparasitic medication during the Paraguay STMM
in light of these two approaches—prophylactic administration of medication to at-risk
populations versus treating only those with diagnosed disease—it seems apparent that the
PARASITES IN PARAGUAY
volunteer providers favored administration of medication based on diagnosed disease, not upon a
broader, public health oriented treatment campaign. While more analysis of this finding is
merited, both to confirm statistical relevance and to examine provider decision making in a more
in-depth, thorough manner, it is worth highlighting possible reasons that the administration of
antiparasitic medication during the Paraguay STMM was employed in a disease-treating manner
as opposed to a public health minded, prophylactic and preventive manner to address a broader
portion of the population.
As there is a dearth of prevalence data for neglected tropical diseases in Paraguay, and
Latin America in general, one may consider it difficult to plan a broad-based campaign to
administer antiparasitic prophylaxis aligned with the World Health Organizations
recommendations without availability of the relevant disease prevalences needed for risk
stratification prior to a STMM. While such estimates have been derived in this analysis, this is a
post facto examination of patient presenting concerns and clinical management seen on the
ground, and nothing of this sort was conducted prior to the STMM in Paraguay to assess the rates
of disease and resultant need for management, largely due to the logistic and monetary
impracticality of such an additional endeavor. This fact, as well as potential supply constraints
regarding the availability of antiparasitic medication in the STMM may be causes for parasitic
management that is more disease-treatment oriented than preventive or prophylactic.
Conclusion
The patient population attended to over the five days of the Paraguay STMM clinic was
skewed toward school age children of both genders, as well as females of childbearing age,
likely representing caregivers of the children visiting clinic. There was a dearth of adult males
presenting to clinic, both individually and as caregivers of children. These descriptive findings
PARASITES IN PARAGUAY
are exemplified by the median patient age by gender—17 years for females and 5 years for
Patients most commonly noted health concerns of headache, fevers, cold symptoms, and
parasite infection, leading to common diagnoses by the volunteer healthcare providers of parasite
infection, viral illness (common cold) and migraine headaches. Individuals seen in clinic were
most commonly prescribed antiparasitic medication, vitamins, analgesics (i.e. acetaminophen,
ibuprofen), and antibiotics.
Nearly one-third of all patients seen in clinic presented with a concern for intestinal
parasite infection, with significantly higher prevalences for adults versus children and females
versus males, with no notable difference by clinic location. The higher prevalence of parasitism
as a presenting concern among adults versus children is opposite to what is expected when
considered in light of the literature, which indicates higher reported parasite prevalence among
children. This difference is possibly due to the inability of children to voice their concerns or
ailments compared to the ability of the adult population. The increased concern for parasite
infection among female versus male patients may be attributed to female caregivers being
traditionally involved in childcare and domestic work close to home, with increased exposure to
infectious parasitic eggs via their children as hosts and in communities lacking proper sanitation
Of note, there was no significant difference in the frequency of the diagnoses of
"parasites" by gender, age category, or clinic location, with nearly half of all patients diagnosed
with parasites in clinic.
The administration of antiparasitic medication—albendazole or mebendazole—was more
frequent among female versus male patients, though this difference was not significant among
PARASITES IN PARAGUAY
stratification by age category or by clinic location. This may reflect a preference by the
providers toward treating women before men, due to a limited supply of antiparasitic medication.
While there are many possible reasons for this preference, it may be that the children and women
were viewed as more marginalized and had less resources than male members of the population.
Central to this analysis of intestinal parasite management is the question of how one
prioritizes and administers a limited supply of antiparasitic medication. There have been two
general approached discussed—one based upon broad, mass, prophylactic administration to
nearly all individuals within a community, the other a case-based administration to only those
currently infected. The observation that, of those eligible for prophylactic treatment, only half
received the antiparasitic medication indicates that the providers may have been approaching the
matter of intestinal parasitism from a case-based, clinical standpoint, as opposed to a broader,
public-health-oriented approach of prophylactic management. This case-based, clinical approach
to administering the antiparasitic medication is highlighted by the finding that nearly 90% of
those diagnosed with intestinal parasites received treatment, a stark difference compared to the
48% of those indicated for prophylaxis that received treatment. This variance merits further
evaluation and examination of significance, as it likely points toward key differences of approach
between a clinical, shortsighted approach to patient care and a more longitudinal, public-health
oriented, prophylactic approach to disease management.
As the long-term effectiveness of a campaign against ascaris lumbricoides and trichuris
trichiura, and indeed most of the neglected tropical diseases, is dependent upon a multifaceted
approach to prevention, treatment, and eradication, continued efforts to address these diseases
and reduce the subsequent morbidity must consist of multidisciplinary action. This multifaceted
approach must be aimed at the development of improved sanitation and water infrastructure,
PARASITES IN PARAGUAY
improved education to enhance the understanding of disease-causing behavior, and correct
application of broad-based antiparasitic treatment protocols aimed at the proper and most
vulnerable subpopulations.
Aiming for the future improvement of the prevention, treatment, and eradication of these
neglected diseases necessitates a long-term approach to engaging those affected, as well as the
current healthcare infrastructure in those nations. This requisite approach to success may negate
any possibility for success or progress from a STMM that visits a new nation every year,
providing one round of antiparasitic treatment to populations that likely require multiple rounds
of treatment yearly, as well as drastic changes in water and sanitation structure for any
improvement in long-term health outcomes.
Potential improvements to the model used when the data for this analysis was collected
include the addition of a multi-year cycle of trips and commitment to a given locale, as opposed
to a one-year cycle with a new location each trip. This format of engaging the community may
allow for a more intentional, long-term approach to community health. This multi-year cycle
may consist of new stage each year, including: 1) assessment and consultation alongside local,
native health workers, 2) implementation of community-targeted interventions consisting of
medical attention, public health education, and health infrastructure foci, and 3) outcomes
evaluation and improvement of interventions. With this longitudinal, community-minded
approach to engaging a cross-cultural setting as an outsider and guest, one may have the
opportunity to apply clinical and community health skills in a directed and intentional manner,
with the aim of improving health outcomes related to intestinal parasitism, and global infectious
disease in general.
PARASITES IN PARAGUAY
References
Adams, E., Stephenson, L., Latham, M., & Kinoti, S. N. (1994). Physical activity and growth of
Kenyan school children with hookworm, trichuris trichiura and ascaris lumbricoides
infections are improved after treatment with albendazole. Journal of Nutrition, 124(8),
Albonico, M., Bickle, Q., Ramsan, M., Montresor, A., Savioli, L., & Taylor, M. (2003). Efficacy
of mebendazole and levamisole alone or in combination against intestinal nematode
infections after repeated targeted mebendazole treatment in Zanzibar. Bulletin of the World
Health Organization, 81(5), 343-352.
Albonico, M., Crompton, D., & Savioli, L. (1999). Control strategies for human intestinal
nematode infections. Advances in Parasitology, 42, 277-341.
Albonico, M., Wright, V., Ramsan, M., Haji, H., Taylor, M., Savioli, L., & Bickle, Q. (2005).
Development of the egg hatch assay for detection of anthelminthic resistance in human
hookworms. International Journal for Parasitology, 35(7), 803-811.
Allotey, P., Reidpath, D., & Pokhrel, S. (2010). Social sciences research in neglected tropical
diseases 1: The ongoing neglect in the neglected tropical diseases. Health Research Policy
and Systems, 8, 32.
Awasthi, S., Bundy, D., & Savioli, L. (2003). Helminthic infections. British Medical Journal,
327(7412), 431-433.
Awasthi, S., Peto, R., Pande, V., Fletcher, R., Read, S., & Bundy, D. (2008). Effects of
deworming on malnourished preschool children in India: An open-labelled, cluster-
randomized trial. PLoS Neglected Tropical Diseases, 2(4), e223.
PARASITES IN PARAGUAY
Bagi, A. E., Sammak, B., Mohamed, A., Al Karawi, M., Al Shahed, M., & Al Thagafi, M.
(2004). Gastrointestinal parasite infestation. European Radiology, 14(Suppl 3), E116-131.
Beasley, N., Tomkins, A., Hall, A., Kihamia, C., Lorri, W., Nduma, B., & Bundy, D. (1999).
The impact of population level deworming on the haemoglobin levels of schoolchildren in
Tanga, Tanzania. Tropical Medicine, 4(11), 744-750.
Bennett, A., & Guyatt, H. (2000). Reducing intestinal nematode infection: Efficacy of
albendazole and mebendazole. Parasitology Today, 16(2), 71-74.
Bethony, J., Brooker, S., Albonico, M., Geiger, S., Loukas, A., Diemert, D., & Hotez, P. (2006).
Soil-transmitted helminth infections: Ascariasis, trichuriasis, and hookworm. The Lancet,
367(9521), 1521-1532.
Bradley, J., & Jackson, J. A. (2004). Immunity, immunoregulation and the ecology of trichuriasis
and ascariasis. Parasite Immunology, 26(11-12), 429-441.
Brun, R., Schumacher, R., Schmid, C., Kunz, C., & Burri, C. (2001). The phenomenon of
treatment failures in human African trypanosomiasis. Tropical Medicine, 6(11), 906-914.
Bundy, D. A. (1994). Immunoepidemiology of intestinal helminthic infections. 1. The global
burden of intestinal nematode disease. Transactions of the Royal Society of Tropical
Medicine and Hygiene, 88(3), 259-261.
Bundy, D. A., & Medley, G. F. (1992). Immuno-epidemiology of human geohelminthiasis:
Ecological and immunological determinants of worm burden. Parasitology, 104, S105
Cho, S., & Kang, S. Y. (1975). Significance of scotch-tape anal swab technique in diagnosis of
enterobius vermicularis infection. Kisaengchunghak Chapchi, 13(2), 102-114.
PARASITES IN PARAGUAY
Coles, G., Bauer, C., Borgsteede, F., Geerts, S., Klei, T., Taylor, M., & Waller, P. (1992). World
association for the advancement of veterinary parasitology (W.A.A.V.P.) methods for the
detection of anthelmintic resistance in nematodes of veterinary importance. Veterinary
Parasitology, 44(1–2), 35-44.
Cooper, E. (1991). Intestinal parasitoses and the modern description of diseases of poverty.
Transactions of the Royal Society of Tropical Medicine and Hygiene, 85(2), 168-170.
Crompton, D. W. (1999). How much human helminthiasis is there in the world? Journal of
Parasitology, 85(3), 397-403.
Crompton, D. W. (2000). The public health importance of hookworm disease. Parasitology, 121,
Crompton, D. W. (2001). Ascaris and ascariasis. Advances in Parasitology, 48, 285–375.
de Silva, N., Brooker, S., Hotez, P., Montresor, A., Engels, D., & Savioli, L. (2003). Soil-
transmitted helminth infections: Updating the global picture. Trends in Parasitology,
19(12), 547-551.
Dold, C., & Holland, C. V. (2011). Ascaris and ascariasis. Microbes and Infection, 13(7), 632
Druilhe, P., Tall, A., & Sokhna, C. (2005). Worms can worsen malaria: Towards a new means to
roll back malaria? Trends in Parasitology, 21(8), 359-362.
Easterly, W. (2006). The white man's burden: Why the west's efforts to aid the rest have done so
much ill and so little good. New York, NY: Oxford.
Egger, R., Hofhuis, E., Bloem, M., Chusilp, K., Wedel, M., Intarakhao, C., . . & Schreurs, W.
(1990). Association between intestinal parasitoses and nutritional status in 3–8-year-old
children in northeast Thailand. Tropical & Geographical Medicine, 42(4), 312-323.
PARASITES IN PARAGUAY
Esrey, S., Potash, J., Roberts, L., & Shiff, C. (1991). Effects of improved water supply and
sanitation on ascariasis, diarrhoea, dracunculiasis, hookworm infection, schistosomiasis, and
trachoma. Bulletin of the World Health Organization, 69(5), 609-621.
Fincham, J., Markus, M., & Adams, V. J. (2003). Could control of soil-transmitted helminthic
infection influence the HIV/AIDS pandemic? Acta Tropica, 86(2–3), 315-333.
Finkelstein, J., Schleinitz, M., Carabin, H., & McGarvey, S. T. (2008). Decision-model
estimation of the age-specific disability weight for schistosomiasis japonica: A systematic
review of the literature. PLoS Neglected Tropical Diseases, 2(3), e158.
Geerts, S., Coles, G., & Gryseels, B. (1997). Anthelmintic resistance in human helminths:
Learning from the problems with worm control in livestock. Parasitology Today, 13(4),
Guerra, E., Vaz, A., de Toledo, L., Ianoni, S., Quadros, C., Dias, R., & Barretto, O. (1991).
Helminth and protozoan intestinal infections in pregnant women in their first consultation at
health centers of the state in the Butantã Subdistrict, São Paulo City. Revista do Instituto De
Medicina Tropical De Sao Paulo, 33(4), 303-308.
Gungoren, B., Latipov, R., Regallet, G., & Musabaev, E. (2007). Effect of hygiene promotion on
the risk of reinfection rate of intestinal parasites in children in rural Uzbekistan.
Transactions of the Royal Society of Tropical Medicine and Hygiene, 101(6), 564-569.
Hadju, V., Stephenson, L., Abadi, K., Mohammed, H., Bowman, D., & Parker, R. (1996).
Improvements in appetite and growth in helminth-infected schoolboys three and seven
weeks after a single dose of pyrantel pamoate. Parasitology, 113(Pt 5), 497-504.
Hagel, I., & Giusti, T. (2010). Ascaris lumbricoides: An overview of therapeutic targets.
Infectious Disorders - Drug Targets, 10(5), 349-367.
PARASITES IN PARAGUAY
Haswell-Elkins, M., Elkins, D., & Anderson, R. M. (1989). The influence of individual, social
group and household factors on the distribution of ascaris lumbricoides within a community
and implications for control strategies. Parasitology, 98(Pt 1), 125-134.
Holland, C., Taren, D., Crompton, D., Nesheim, M., Sanjur, D., Barbeau, I., . . & Rivera, G.
(1988). Intestinal helminthiases in relation to the socioeconomic environment of
Panamanian children. Social Science and Medicine, 26(2), 209-213.
Hotez, P., Ottesen, E., Fenwick, A., & Molyneux, D. (2006). The neglected tropical diseases:
The ancient afflictions of stigma and poverty and the prospects for their control and
elimination. Advances in Experimental Medicine, 582, 23-33.
Hotez, P., Molyneux, D., Fenwick, A., Kumaresan, J., Sachs, S., Sachs, J., & Savioli, L. (2007a).
Control of neglected tropical diseases. New England Journal of Medicine, 357(10), 1018
Hotez, P., Raff, S., Fenwick, A., Richards, F., Jr, & Molyneux, D. (2007b). Recent progress in
integrated neglected tropical disease control. Trends in Parasitology, 23(11), 511-514.
Hotez, P., Molyneux, D., Fenwick, A., Ottesen, E., Ehrlich Sachs, S., & Sachs, J. (2006).
Incorporating a rapid-impact package for neglected tropical diseases with programs for
HIV/AIDS, tuberculosis, and malaria. PLoS Medicine, 3(5), e102.
Hotez, P., Remme, J., Buss, P., Alleyne, G., Morel, C., & Breman, J. (2004). Combating tropical
infectious diseases: Report of the disease control priorities in developing countries project.
Clinical Infectious Diseases, 38(6), 871-878.
Internal Revenue Service (2012, December). Exemption Requirements: 501(c)(3) Organizations.
Retrieved Feb. 17, 2013 from
PARASITES IN PARAGUAY
Jia, T., Zhou, X., Wang, X., Utzinger, J., Steinmann, P., & Wu, X. (2007). Assessment of the
age-specific disability weight of chronic schistosomiasis japonica. Bulletin of the World
Health Organization, 85(6), 458-465.
Jukes, M., Pinder, M., Grigorenko, E., Smith, H., Walraven, G., Bariau, E., . . & Bundy, D.
(2006). Long-term impact of malaria chemoprophylaxis on cognitive abilities and
educational attainment: Follow-up of a controlled trial. PLoS Clinical Trials, 1(4), e19.
Kabatereine, N., Kemijumbi, J., Kazibwe, F., & Onapa, A. W. (1997). Human intestinal parasites
in primary school children in Kampala, Uganda. East African Medical Journal, 74(5), 311
Kamunvi, F., & Ferguson, A. G. (1993). Knowledge, attitudes and practices (KAP) of human
intestinal helminths (worms) in two rural communities in Nyanza Province, western Kenya.
East African Medical Journal, 70(8), 482-490.
Katz, I., Komatsu, R., Low-Beer, D., & Atun, R. (2011). Scaling up towards international targets
for AIDS, tuberculosis, and malaria: Contribution of global fund-supported programs in
2011–2015. PLoS One, 6(2), e17166.
Kightlinger, L., Seed, J., & Kightlinger, M. B. (1995). The epidemiology of ascaris lumbricoides,
trichuris trichiura, and hookworm in children in the Ranomafana rainforest, Madagascar.
Journal of Parasitology, 81(2), 159-169.
Kightlinger, L., Seed, J., & Kightlinger, M. B. (1998). Ascaris lumbricoides intensity in relation
to environmental, socioeconomic, and behavioral determinants of exposure to infection in
children from southeast Madagascar. Journal of Parasitology, 84(3), 480-484.
PARASITES IN PARAGUAY
King, C., & Bertino, A. M. (2008). Asymmetries of poverty: Why global burden of disease
valuations underestimate the burden of neglected tropical diseases. PLoS Neglected Tropical
Diseases, 2(3), e209.
Komatsu, R., Korenromp, E., Low-Beer, D., Watt, C., Dye, C., Steketee, R., … &
Schwartländer, B. (2010). Estimation approach and results between 2003 and end-2007.
BMC Infectious Diseases, 10, 109.
Lammie, P., Fenwick, A., & Utzinger, J. (2006). A blueprint for success: Integration of neglected
tropical disease control programmes. Trends in Parasitology, 22(7), 313-321.
Maki, J., Qualls, M., White, B., Kleefield, S., & Crone, R. (2008). Health impact assessment and
short-term medical missions: A methods study to evaluate quality of care. BMC Health
Services Research, 8, 121.
Mani, T., Rajendran, R., Munirathinam, A., Sunish, I., Md Abdullah, S., Augustin, D., &
Satyanarayana, K. (2002). Efficacy of co-administration of albendazole and
diethylcarbamazine against geohelminthiases: A study from south India. Tropical Medicine,
7(6), 541-548.
Mascie-Taylor, C., Karim, R., Karim, E., Akhtar, S., Ahmed, T., & Montanari, R. (2003). The
cost-effectiveness of health education in improving knowledge and awareness about
intestinal parasites in rural Bangladesh. Economics, 1(3), 321-330.
Mebrahtu, T., Stoltzfus, R., Chwaya, H., Jape, J., Savioli, L., Montresor, A., . . & Tielsch, J.
(2004). Low-dose daily iron supplementation for 12 months does not increase the
prevalence of malarial infection or density of parasites in young Zanzibari children. Journal
of Nutrition, 134(11), 3037-3041.
PARASITES IN PARAGUAY
Molyneux, D. H. (2008). Combating the "other diseases" of MDG 6: Changing the paradigm to
achieve equity and poverty reduction? Transactions of the Royal Society of Tropical
Medicine and Hygiene, 102(6), 509-519.
Molyneux, D., Hotez, P., & Fenwick, A. (2005). "Rapid-impact interventions": How a policy of
integrated control for Africa's neglected tropical diseases could benefit the poor. PLoS
Medicine, 2(11), e336.
Moore T. A. (2012). Chapter 208: Agents used to treat parasitic infections. In D. L. Longo, A. S.
Fauci, D. L. Kasper, S. L. Hauser, J. L. Jameson, J. Loscalzo (Ed.), Harrison's Principles of
Internal Medicine (18th ed.) Retrieved March 3, 2013, from
Moore, S., Lima, A., Conaway, M., Schorling, J., Soares, A., & Guerrant, R. (2001). Early
childhood diarrhoea and helminthiases associate with long-term linear growth faltering.
International Journal of Epidemiology, 30(6), 1457-1464.
Nacher, M., Singhasivanon, P., Yimsamran, S., Manibunyong, W., Thanyavanich, N., Wuthisen,
R., & Looareesuwan, S. (2002). Intestinal helminth infections are associated with increased
incidence of plasmodium falciparum malaria in Thailand. Journal of Parasitology, 88(1),
Nokes, C., & Bundy, D. A. (1994). Does helminth infection affect mental processing and
educational achievement? Parasitology Today, 10(1), 14-18.
Nokes, C., Grantham-McGregor, S., Sawyer, A., Cooper, E., & Bundy, D. (1992). Parasitic
helminth infection and cognitive function in school children. Proceedings of the Royal
Society B: Biological Sciences, 247(1319), 77-81.
PARASITES IN PARAGUAY
Norhayati, M., Zainudin, B., Mohammod, C., Oothuman, P., Azizi, O., & Fatmah, M. (1997).
The prevalence of trichuris, ascaris and hookworm infection in Orang Asli children. The
Southeast Asian Journal of Tropical Medicine and Public Health, 28(1), 161-168.
O'Lorcain, P., & Holland, C. V. (2000). The public health importance of ascaris lumbricoides.
Parasitology, 121, S51–71.
Osei-Atweneboana, M., Eng, J., Boakye, D., Gyapong, J., & Prichard, R. (2007). Prevalence and
intensity of onchocerca volvulus infection and efficacy of ivermectin in endemic
communities in Ghana: A two-phase epidemiological study. The Lancet, 369(9578), 2021
Pan American Health Organization. (2008). Health system profile Paraguay. Washington, D.C.:
Pan American Health Organization / World Health Organization.
Pan American Health Organization. (2013). Health situation analysis and trends summary:
Pelletier, D., Frongillo, E., Jr, Schroeder, D., & Habicht, J. P. (1994). A methodology for
estimating the contribution of malnutrition to child mortality in developing countries.
Journal of Nutrition, 124(10), 2106S-2122S.
Raj, S., Sein, K., Anuar, A., & Mustaffa, B. E. (1996). Effect of intestinal helminthiasis on
intestinal permeability of early primary schoolchildren. Transactions of the Royal Society of
Tropical Medicine and Hygiene, 90(6), 666-669.
Reddy, M., Gill, S., Kalkar, S., Wu, W., Anderson, P., & Rochon, P. (2007). Oral drug therapy
for multiple neglected tropical diseases: A systematic review. Journal of the American
Medical Association, 298(16), 1911-1924.
PARASITES IN PARAGUAY
Savioli, L., Engels, D., & Endo, H. (2005). Extending the benefits of deworming for
development. Lancet, 365(9470), 1520-1521. doi:10.1016/S0140-6736(05)66433-1.
Scherrer, A., Sj, öberg, M., Allangba, A., Traor, M., & Utzinger, J. (2009). Sequential analysis of
helminth egg output in human stool samples following albendazole and praziquantel
administration. Acta Tropica, 109(3), 226-231.
Simeon, D., Grantham-McGregor, S., Callender, J., & Wong, M. S. (1995). Treatment of
trichuris trichiura infections improves growth, spelling scores and school attendance in some
children. Journal of Nutrition, 125(7), 1875-1883.
Smits, H. L. (2009). Prospects for the control of neglected tropical diseases by mass drug
administration. Expert Review of Anti-Infective Therapy, 7(1), 37-56.
Spiegel, A., Tall, A., Raphenon, G., Trape, J., & Druilhe, P. (2003). Increased frequency of
malaria attacks in subjects co-infected by intestinal worms and plasmodium falciparum
malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene, 97(2), 198
Stephenson, L., Holland, C., & Cooper, E. S. (2000). The public health significance of trichuris
trichiura. Parasitology, 121, S73–95.
Stephenson, L., Latham, M., Adams, E., Kinoti, S., & Pertet, A. (1993). Physical fitness, growth
and appetite of kenyan school boys with hookworm, trichuris trichiura and ascaris
lumbricoides infections are improved four months after a single dose of albendazole.
Journal of Nutrition, 123(6), 1036-1046.
Stephenson, L., Latham, M., & Ottesen, E. A. (2000). Malnutrition and parasitic helminth
infections. Parasitology, 121, S23-38.
PARASITES IN PARAGUAY
Stoltzfus, R., Chwaya, H., Tielsch, J., Schulze, K., Albonico, M., & Savioli, L. (1997).
Epidemiology of iron deficiency anemia in Zanzibari schoolchildren: The importance of
hookworms. American Journal of Clinical Nutrition, 65(1), 153-159.
Sundar, S., More, D., Singh, M., Singh, V., Sharma, S., Makharia, A., . . & Murray, H.
(2000). Failure of pentavalent antimony in visceral leishmaniasis in India: Report from the
center of the Indian epidemic. Clinical Infectious Diseases, 31(4), 1104-1107.
Tanumihardjo, S., Cheng, J., Permaesih, D., Muherdiyantiningsih, Rustan, E., Muhilal, . . &
Olson, J. (1996). Refinement of the modified-relative-dose-response test as a method for
assessing vitamin A status in a field setting: Experience with Indonesian children. American
Journal of Clinical Nutrition, 64(6), 966-971.
Taylor-Robinson, D., Jones, A., & Garner, P. (2009). Does deworming improve growth and
school performance in children? PLoS Neglected Tropical Diseases, 3(1), e358.
The Global Fund to Fight AIDS Tuberculosis and Malaria. (2010). The global fund 2010:
Innovation and impact. Geneva: The Global Fund to Fight AIDS Tuberculosis and Malaria.
Thein-Hlaing, Thane-Toe, Than-Saw, Myat-Lay-Kyin, & Myint-Lwin. (1991). A controlled
chemotherapeutic intervention trial on the relationship between ascaris lumbricoides
infection and malnutrition in children. Transactions of the Royal Society of Tropical
Medicine and Hygiene, 85(4), 523-528.
U.S. Department of Health & Human Services. (2013). Guidance on satisfying the safe harbor
method. Retrieved April 27, 2013, from
PARASITES IN PARAGUAY
United Nations (U.N) (2005). The millennium development goals report 2005. New York, NY:
United Nations. United Nations Millennium Declaration, 55/2., 8th plenary meeting.
Urbani, C., & Albonico, M. (2003). Anthelminthic drug safety and drug administration in the
control of soil-transmitted helminthiasis in community campaigns. Acta Tropica, 86(2-3),
Utzinger, J., Becker, S., Knopp, S., Blum, J., Neumayr, A., Keiser, J., & Hatz, C. (2012).
Neglected tropical diseases: Diagnosis, clinical management, treatment and control. Swiss
Medical Weekly, 142, w13727.
Utzinger, J., Raso, G., Brooker, S., De Savigny, D., Tanner, M., Ornbjerg, N., & N'goran, E.
(2009). Schistosomiasis and neglected tropical diseases: Towards integrated and sustainable
control and a word of caution. Parasitology, 136(13), 1859-1874.
van den Biggelaar, A. H., Rodrigues, L. C., van Ree, R., van der Zee, J. S., Hoeksma-Kruize, Y.
C., Souverijn, J. H., & Yazdanbakhsh, M. (2004). Long-term treatment of intestinal
helminths increases mite skin-test reactivity in Gabonese schoolchildren. The Journal of
Infectious Diseases, 189(5), 892-900. doi:10.1086/381767.
Watkins, W., Cruz, J., & Pollitt, E. (1996). The effects of deworming on indicators of school
performance in Guatemala. Transactions of the Royal Society of Tropical Medicine and
Hygiene, 90(2), 156-161.
Watkins, W., & Pollitt, E. (1997). "Stupidity or worms": Do intestinal worms impair mental
performance? Psychological Bulletin, 121(2), 171-191.
Weiss, M. G. (2008). Stigma and the social burden of neglected tropical diseases. PLoS
Neglected Tropical Diseases, 2(5), e237.
PARASITES IN PARAGUAY
World Health Organization (WHO). (1995). WHO model prescribing information. Drugs used in
parasitic diseases. Geneva, Switzerland: World Health Organization.
World Health Organization (WHO). (2002). Prevention and control of schistosomiasis and soil-
transmitted helminthiasis. WHO Technical Report Series, 912, i-57. Retrieved April 4, 2013
World Health Organization (WHO). (2004). The world health report 2004: Changing history.
Geneva, Switzerland: World Health Organization.
World Health Organization (WHO). (2006). Preventative chemotherapy in human helminthiases:
Coordinated use of anthelminthic drugs in control interventions: A manual for health
professionals and programme managers. Geneva, Switzerland: World Health Organization.
World Health Organization (WHO). (2013). Soil-transmitted helminthiasis: Country indicators -
Paraguay. Retrieved April 4, 2013, from
Yang, Y., Kim, S., Jung, S., Huh, S., & Lee, J. (1997). Chemotherapeutic trial to control
enterobiasis in schoolchildren. Korean Journal of Parasitology, 35(4), 265-269.
PARASITES IN PARAGUAY
Appendix A: Patient History & Physical Form
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Appendix B: IRB Exempt Study Approval
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Appendix C: List of Tier 1 Core Public Health Competencies Met
Domain #1: Analytic/Assessment
Identify the health status of populations and their related determinants of health and illness (e.g., factors contributing to health promotion and disease prevention, the quality, availability and use of health services) Describe the characteristics of a population-based health problem (e.g., equity, social determinants, environment) Use variables that measure public health conditions Use methods and instruments for collecting valid and reliable quantitative and qualitative data Identify sources of public health data and information Recognize the integrity and comparability of data
Identify gaps in data sources Adhere to ethical principles in the collection, maintenance, use, and dissemination of data and information Describe the public health applications of quantitative and qualitative data
Collect quantitative and qualitative community data (e.g., risks and benefits to the community, health and resource needs) Use information technology to collect, store, and retrieve data
Describe how data are used to address scientific, political, ethical, and social public health issues
Domain #2: Policy Development and Program Planning
Gather information relevant to specific public health policy issues
Domain #3: Communication
Identify the health literacy of populations served Solicit community-based input from individuals and organizations Participate in the development of demographic, statistical, programmatic and scientific presentations
Domain #4: Cultural Competency
Recognize the role of cultural, social, and behavioral factors in the accessibility, availability, acceptability and delivery of public health services Respond to diverse needs that are the result of cultural differences Describe the need for a diverse public health workforce
Domain #5: Community Dimensions of Practice
Recognize community linkages and relationships among multiple factors (or determinants) affecting health (e.g., The Socio-Ecological Model) Describe the role of governmental and non-governmental organizations in the delivery of community health services
Domain #6:Public Health Sciences
Describe the scientific evidence related to a public health issue, concern, or, intervention Retrieve scientific evidence from a variety of text and electronic sources Discuss the limitations of research findings (e.g., limitations of data sources, importance of observations and interrelationships) Describe the laws, regulations, policies and procedures for the ethical conduct of research (e.g., patient confidentiality, human subject processes)
Domain #7: Financial Planning and Management
Report program performance
Domain #8: Leadership and Systems Thinking
Incorporate ethical standards of practice as the basis of all interactions with organizations, communities, and individuals Identify internal and external problems that may affect the delivery of Essential Public Health Services Use individual, team and organizational learning opportunities for personal and professional development
Source: http://corescholar.libraries.wright.edu/cgi/viewcontent.cgi?article=1108&context=mph
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Informationen und Neuigkeiten zum Thema Urologievon Universitätsdozent Dr. Andreas Jungwirth HEUTE ERHALTEN SIE DAS NEUE „UROLOSKOP", die erste und einzige urologische Patientenzeitschrift in Österreich! Ich habe auch heuer wieder Neuigkeiten und Testosteron und das Herz Trends aus der Welt der Urologie und Andrologie zusammengestellt und ich hoffe, dass so mancher Artikel Ihr Interesse findet. Gerade die Patientengruppe,
