A Scoping Review and Prevalence Analysis of Soil-
Transmitted Helminth Infections in Honduras
Ana Lourdes Sanchez1*, Jose ´ Antonio Gabrie1, Marı ´a Mercedes Rueda2, Rosa Elena Mejia3,
Maria Elena Bottazzi4, Maritza Canales2
1Department of Health Sciences, Brock University, St. Catharines, Ontario, Canada, 2School of Microbiology, National Autonomous University of Honduras (UNAH),
Tegucigalpa, Honduras, 3National Surveillance Laboratory, Honduras Ministry of Health, Tegucigalpa, Honduras, 4National School of Tropical Medicine, Baylor College of
Medicine, Houston, Texas, United States of America
Background: Honduras is endemic for soil-transmitted helminth (STH) infections, but critical information gaps still remain
on the prevalence and intensity of these infections as well as on their spatial distribution at subnational levels.
Objectives: Firstly, to review the research activity on STH infections in Honduras and secondly, to carry out a national
prevalence analysis and map the geographical distribution of these infections in children.
Methods: A systematic search was conducted of the published and grey literature to identify scientific work on the impact
and prevalence of STH infections done between May 1930 and June 30, 2012. International databases and Honduran
journals were searched. Grey literature was gleaned from local libraries and key informants. Select studies conducted
between 2001 and 2012 were used to produce prevalence maps and to investigate association between STH prevalence
and socio-economic and environmental factors.
Results: Of 257 identified studies, 211 (21.4% peer-reviewed) were retained for analysis and categorized as clinical research
(10.9%), treatment efficacy studies (8.1%) or epidemiological studies (81%). Prevalence analysis and geographical mapping
included 36 epidemiological studies from Honduras’s 18 departments and 23% of its municipalities. Overall STH prevalence
was .50% in 40.6% of municipalities. Prevalences above 20% for each trichuriasis, ascariasis, and hookworm infection were
found in 68%, 47.8%, and 7.2% of studied municipalities, respectively. Municipalities with lower human development index,
less access to of potable water, and with higher annual precipitation showed higher STH prevalences.
Conclusions: This is the first study to provide a comprehensive historic review of STH research activity and prevalence in
Honduras, revealing important knowledge gaps related to infection risk factors, disease burden, and anti-parasitic drug
efficacy, among others. Our decade-long prevalence analysis reveals geographical differences in STH prevalence and these
findings suggest that differential intervention strategies might be necessary in Honduras for the control of these infections.
Citation: Sanchez AL, Gabrie JA, Rueda MM, Mejia RE, Bottazzi ME, et al. (2014) A Scoping Review and Prevalence Analysis of Soil-Transmitted Helminth Infections
in Honduras. PLoS Negl Trop Dis 8(1): e2653. doi:10.1371/journal.pntd.0002653
Editor: Peter Steinmann, Swiss Tropical and Public Health Institute, Switzerland
Received July 31, 2013; Accepted December 6, 2013; Published January 23, 2014
Copyright: ? 2014 Sanchez et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was carried out with support from the Global Health Research Initiative (GHRI, www.ghri.ca), a collaborative research funding partnership of
the Canadian Institutes of Health Research, the Canadian International Development Agency, Health Canada, the International Development Research Centre and
the Public Health Agency of Canada (IDRC Project Number: 103460-050). The funders had no role in study design, data collection and analysis, decision to publish,
or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
* E-mail: email@example.com
Intestinal parasites including soil-transmitted helminths (STH)
have been long recognized as public health problems in much of
the developing world . Soil-transmitted helminthiases are
caused by four species of intestinal worms, namely, Ascaris
lumbricoides, Trichuris trichiura, and the two hookworm species
Ancylostoma duodenale and Necator americanus . Current estimates
show that more than 2 billion people worldwide are infected with
STH, the majority residing in low and middle income countries
(LMICs) [3,4]. Within LMICs, STH endemicity is concentrated in
and around areas where ecological and environmental character-
istics intersect with conditions that facilitate transmission [5,6]. In
addition, recent studies have shown that soil-transmitted helmin-
thiases and other neglected tropical diseases (NTDs) also cause a
great burden among poor populations living in wealthy nations,
including the United States [7,8]. Primarily and due to their
widespread distribution and chronic nature, STH infections pose a
high burden in endemic populations [2,4,9] among which,
children and youth are disproportionally affected [10,11]. Hence,
global efforts are currently focused on this vulnerable population
. As a highly effective and immediate intervention for reducing
STH morbidity in high risk groups, the World Health organiza-
tion (WHO) recommends to all disease-endemic countries periodic
administration of anthelminthic medication (a strategy called
preventive chemotherapy, PC) [12,13]. Implementing PC is,
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however, not without challenges. Barry et al (2013) recently
calculated that for 2011, 875 million children (70% of school age)
lived in high-risk areas worldwide but only 38% of pre-school and
34% of school age children were reached by PC activities .
Aware of this gap, and in support of WHO’s roadmap to guide
implementation of NTD’s control strategies , a number of
private and public partners have agreed to join forces to assure
that anthelminthic drugs and other interventions reach all people
suffering from NTDs including STH infections .
Honduras, as most countries in Latin America, is endemic for
STH infections [4,5,17,18]. Organized efforts to control these
infections in the country can be traced back to the 1990s but the
current nation-wide deworming program for school-age children
was only implemented in 2001 . Honduran data from 2003
onwards is available online on WHO’s Preventive Chemotherapy
(PCT) Databank . Although coverage rates have been sub-
optimal, a steady national coverage of around 70% is reported for
the last three years for which information is available (2009–2011).
Despite this strong commitment to the fight against STH
infections, adequate PC monitoring has yet to be implemented
in Honduras . Moreover, critical information gaps remain on
the prevalence of STH infections as well as on infection intensity
and polyparasitism at subnational levels .
While it is true that there is a paucity of STH research in
Honduras, there is to our knowledge, a wealth of scattered
information that has been produced for decades by a number of
health professionals, scientists, and students (mainly microbiolo-
gists and medical doctors) as well as governmental institutions.
Much of this information is, however, not only unpublished but
inaccessible to interested stakeholders (e.g., scientific research
community, civil society, and decision and policy makers). As
shown previously by others, active in-country searches of
unpublished data are essential to obtaining epidemiological
information to assist in decision-making processes . Therefore,
to bring to light this important Honduran information, we carried
out a systematic revision of the available published and
unpublished literature pertaining STH infections produced in
Honduras from 1930 to 2012. Our first objective was to examine
the research activity on STH infections, synthesize research
evidence, and identify research gaps. Secondly, we selected key
data from 2001–2012 to carry out a prevalence analysis for the last
decade and map the geographical distribution and prevalence in
children #15 years old of the three most common intestinal
helminths in Honduras, Ascaris lumbricoides, Trichuris trichiura and
the hookworms (predominantly Necator americanus ).
We conducted a scoping review, a method useful for exploring
questions where little knowledge has been established [22,23], and
followed the 5-stage methodological framework proposed by
Arksey and O’Malley (2005). Briefly, the process included: (1)
identifying the research question; (2) identifying relevant studies;
(3) study selection; (4) charting the data; and (5) collating,
summarizing and reporting the results . We also conducted
a stakeholders consultation, previously considered optional 
but strongly recommended by Levac et al. (2010) to add
methodological rigor to these types of studies . Part of the
consultation process preceded the literature search and took place
in April 2012. The literature search was carried out in Canada and
in Honduras from May 2 to June 30, 2012. Analysis and charting
of the data was done through an iterative process as defined by
Levac et al , between July and December 2012.
1. What has been studied in Honduras in regards to STH
infections; what are the extent, range, and nature of this
research? Derived from these findings, what are the research
2. What is, for the last decade, the prevalence and geographical
distribution of pre-school and school-age STH infections in
Honduras? Is STH geographical distribution linked to
municipal specific characteristics?
Literature search strategy
The information search was constrained to the major STH
species circulating in Honduras: Ascaris lumbricoides, Trichuris
trichiura and the hookworms. No restrictions in terms of study
design, authorship, institutional affiliation, or year of publication
were set. For online searches, language was restricted to Spanish
and English (the most likely languages to be utilized for
international publication by Honduran authors). If review studies
were identified, a search of the listed primary sources was done,
and if retrieved, they were included in the study.
To identify potentially relevant information (i.e., studies and
reports pertaining STH infections in Honduras), we followed the
strategy described below.
researchers and other stakeholders.
the ‘‘Strategic plan for the control, elimination and prevention of
neglected infectious diseases in Honduras, 2012–2017’’ (PEEDH
for its Spanish abbreviation) was officially announced in
Tegucigalpa. In light of the scarcity of STH research evidence
mentioned in PEEDH’s inaugural report , the need of
undertaking the present study became evident. Shortly after, we
discussed this collaborative effort with representatives of the
Honduran Ministry of Health (MoH) and researchers at the
National Autonomous University of Honduras, UNAH. An
agreement to share MoH survey data was reached by end of
On April 12, 2012,
Soil-transmitted helminthiases are infections of public
health importance in Honduras. Although research data
on this topic in the country is somewhat inconsistent and
scattered, a wealth of information has been produced by
Honduran researchers and practitioners over the years. The
vast majority of this information, however, remains
inaccessible in the gray literature, thus missing its potential
to inform research, policy, and practice. We undertook a
thorough review of the literature produced from 1930 to
2012 in order to identify research gaps and, based on a
select number of studies, conducted a prevalence analysis
with data generated between 2001 and 2012. Our study
reveals that these parasitic infections have not been a
focus of sustained research efforts in Honduras. Literature
analysis identified current knowledge gaps related to
infection risk factors, disease burden, and anti-parasitic
drug efficacy, among others. Evaluating and monitoring
the national control program also emerged as a priority.
Our study also reveals geographic areas of very high
endemicity, suggesting that targeted interventions might
be appropriate in localized areas of the country. Honduras
is at present expanding the deworming program to
include pre-school children and the data presented here
could serve as a baseline for future monitoring and
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May 2012. Therefore, from June 4–15, 2012, individuals
representing the following institutions were approached to discuss
their current activities related to STH infections: MoH, World
Food Program, Pan American Health Organization (PAHO),
Healthy Schools Program, and Parasitology section of the School
of Microbiology, UNAH.
We searched electronic databases including the
National Library of Medicine’s PubMed (http://www.ncbi.nlm.
nih.gov), the Thomson Reuters’ Web of Knowledge (http://www.
webofknowledge.com) and Google Scholar (http://scholar.google.
ca). We also searched databases integrated to the Virtual Health
Library, VHL (http://www.bvs.hn) of the Latin American and
Caribbean Center on Health Sciences Information (BIREME):
LILACS, SciELO, DESASTRES, PAHO, WHOLIS, IBECS and
English terms and their Spanish equivalents were used as
keywords. In English, the following keywords were used: soil-
transmitted, geohelminth, helminth, Ascaris lumbricoides, round-
worm, ascariasis, Trichuris trichiura, whipworm, hookworm, Ancy-
lostoma duodenale, Necator americanus, intestinal disease, intestinal
obstruction, biliary, diarrhea, parasitism, parasitic, eosinophil,
nutrition. Each keyword/term was entered independently into the
following search syntax: , keyword or term . AND ,
Honduras. OR , Honduran .. Each search was done twice
on different days to ensure accuracy and maximum return.
Online search of literature published in Honduran
We searched for data available in several online
Honduran peer-reviewed periodicals (all affiliated with UNAH,
and available at http://www.bvs.hn/RMHS/html/RMH.html).
Firstly, we searched Revista Me ´dica Honduren ˜a, (Honduran
Medical Journal, established in 1930 and indexed in Medline only
until 1965); the most important medium for biomedical research
dissemination in Honduras. Secondly, we searched online issues of
these more recently established journals: Revista de la Facultad de
Ciencias Me ´dicas (est. 2004) Revista Ciencia y Tecnologı ´a,
UNAH (est. 1997); Revista Me ´dica de los Postgrados de Medicina,
UNAH (est. 1996); and Revista Honduras Pedia ´trica (est.1963 and
discontinued 2007). None of the journals supported keyword
searches; therefore, potentially relevant articles were identified by
screening each available issue.
A newer university journal established in 2011 and devoted to
undergraduate and graduate research, Revista Portal de la Ciencia
(https://www.unah.edu.hn/?cat=3539), was not included in our
search since was not available online. To our knowledge, there are
not in Honduras other periodicals -peer-reviewed or otherwise-
likely to publish STH research.
For verification, we also searched an online inventory of
Honduran national and international publications on intestinal
parasites hosted by VHL (http://www.bvs.hn/E/Parasitos.html).
Hand search of the grey literature produced locally in
Grey literature (i.e., studies that are unpublished,
have limited distribution, and/or are not included in public
bibliographical retrieval systems ) was obtained through site
visits and meetings with key informants (parasitology faculty
members from UNAH, graduate students, government represen-
tatives (primarily from the Ministry of Health–some of which took
part in the consultation process). From June 4–15, 2012, two
libraries affiliated with UNAH, the main Honduran university,
were visited to identify potentially relevant research theses and
monographs produced by students undertaking professional
degrees (i.e., medical sciences, nursing, and microbiology) as well
as by graduate students in infectious diseases, public health and
epidemiology master in science programs. Prior to visiting the
libraries, we found through VHL 72 medical students’ theses on
intestinal parasites, 69 of which were potentially relevant.
Librarians also provided access to library intranets where medical
students’ monographs had been catalogued. Keyword search was
not possible within the intranet so researchers reviewed lists of
titles to identify key terms listed above and request access to the
documents. Hard copies of theses and monographs selected were
retrieved by the librarians for researchers’ perusal. Other printed
or online material on the subject published by Honduran authors,
such as parasitology laboratory manuals and books were
scrutinized for primary research data. Key informants were
approached to obtain primary data contained in research theses,
surveys and field trips reports.
Hand search of reference lists on publications by the Pan
American Health Organization.
PAHO-related publications known to the researchers or those
found through VHL were screened for primary sources of
Online searches of STH international databases.
bases of GAHI’s Global Atlas of Helminth Infections (http://
www.thiswormyworld.org) and the Global Neglected Tropical
Diseases (http://www.gntd.org) were searched for Honduran
Reference lists of PAHO or
All available studies and reports capturing information related
to the major STH species circulating in Honduras were assessed
by two researchers and two research assistants. Potentially relevant
studies were scrutinized and only those providing primary data
involving humans and conducted in Honduras were retained for
Retained studies were analyzed, charted, and organized into
three categories: those reporting clinical cases or investigating
medical outcomes (clinical research); those reporting treatment
efficacy, and those with an epidemiological scope. Data were
entered twice for accuracy into spreadsheets (MS-Excel 2010) and
summary tables were produced for each category.
Objective 1. Research activity assessment.
activity was assessed by analyzing published studies in both the
peer-reviewed literature and in the form of official reports, theses,
and scientific abstracts. Data considered not stemming from
research work were excluded from this assessment (i.e., partially
processed data derived from parasitology courses field trips and
microbiology social service reports summarizing a mandatory one-
year professional practice at clinical laboratories of the public
Objective 2. Prevalence analysis.
ical studies were utilized to meet the second research objective.
Primary data presented by studies were disaggregated into datasets
according to date of study, age of population (i.e., children or adult)
and outcomes under investigation. Also, as Honduras is organized
into 18 departments and 298 municipalities , when available,
datasets were disaggregated into these first or second administra-
Studies meeting the following criteria were selected for
Sub-sets of epidemiolog-
Providing primary data
Population- or school-based and dated since 2001, the year
national deworming was launched
Conducted among children (#15 years old), the target at risk
population of PC programs
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d) Used Kato-Katz for stool examination, the diagnostic method
recommended by WHO
Epidemiological studies were reviewed and data extracted into a
standardized MS-Excel database. Data extracted included: source
of data, author(s), date and location of the study, sample size,
characteristics of the surveyed population, parasitological methods
performed, and positivity for investigated parasites. Prevalence
figures provided by studies were verified or calculated by the
researchers conducting the review. Averages of overall and species-
specific prevalences were calculated for departmental and
municipal levels, and maps were generated to depict their
Statistical analysis and prevalence mapping
Descriptive statistics were used to express frequencies. Preva-
lence of STH infections was calculated from epidemiological
studies meeting selection criteria for prevalence analysis. Datasets
from surveys done in the same department were averaged to
obtain overall prevalence by any STH at the first administrative
level. For municipalities, if multiple data were available for the
same location, a weighted average prevalence was calculated
(accounting for the sample size in each survey). Based on the
geographical coordinates of surveys’ sites, prevalence maps were
generated using ArcGIS 10.1 (ESRI Inc., California, USA). For
surveys that had been conducted in small villages nearby
municipal capitals, the available geographical coordinates of the
latter were used as geo-reference. Prevalence was expressed in
risk categories (i.e., low, ,20%; moderate, $20% and ,50%;
high, $50%), corresponding to WHO’s categories of risk for
morbidity to determine preventive chemotherapy administration
A multivariable linear regression model was used to assess
association between STH prevalence and socio-economic and
environmental variables at the municipality level. Socio-economic
variables included Human Development Index (HDI), household
overcrowding (defined as $3 individuals per room, excluding
bathrooms and kitchen), households with potable water, and
household with sanitary facility [28,29]. Environmental variables
included the average annual temperature and average annual
precipitation . Other characteristics considered for analysis
were dropped from the model because they were either already
included in the HDI calculation (e.g., literacy, unsatisfied basic
needs, poverty) or because they showed high collinearity with
other variables (e.g., altitude). Statistical analyses were carried out
using IBM SPSS Statistics for Windows version 20.0 (Armonk,
Figure 1. Process of identification and selection of relevant studies (May 1930 to June 30, 2012). Clinical studies included 17 peer-
reviewed articles (1 international), 5 medical theses, and 1 conference abstract. Treatment efficacy studies included 6 peer-reviewed articles (3
international), and 11 medical theses. The 36 epidemiological studies used for prevalence mapping included 3 national surveys by the Honduras
Ministry of Health, 1 technical report by the Honduras Ministry of Natural Resources and Environment, 28 parasitology courses field trips reports, and
4 undergraduate theses.
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Table 1. Summary of identified and screened studies on soil-transmitted helminth infections done in Honduras between May
1930 and June 30, 2012.
Type of sourceSource Online access
N6 issues or
N6 potentially relevant
studies (No. retained)
Published studies Honduran journals*
Yes1930–2011 53158 (41)
International journals Yes1930–2012 Not applicable18 (14)**
Grey literature Medical theses#
No1950–1992 72 69 (60)
Medical monographs No1993–2012 11400 (0)
Microbiology thesesNo2000–2012 106 (6)
Microbiology monographsNo 2006–201289 4 (1)
Abstracts in scientific conferences No1983–2011 28 13 (9)
Ministry of Health national surveysNo 2001–20113 3 (3)
Other governmental technical reportsNo Not applicable1 1 (1)
Microbiology social¥service reportsNo1990–199257 47 (38)
Parasitology field tripsNo 1999–201238 38 (38)
Total 257 (211)
*Honduran journals reviewed: 382 issues (from 1930 to 2011) of Revista Me ´dica Honduren ˜a; 20 issues (from 2004 to 2011) of Revista de la Facultad de Ciencias Me ´dicas;
20 issues (from 1997 to 2009) of Revista Ciencia y Tecnologı ´a; 29 issues (from 1996 to 2008) of Revista Me ´dica de los Postgrados de Medicina; and 80 issues (from 1963
to 2007) of Revista Honduras Pedia ´trica.
**Of 14 international articles, 1 was in Spanish and 13 in English.
#Catalogued by the Virtual Health Library (Biblioteca Virtual en Salud) as theses done on ‘‘Intestinal Parasites’’ at the Faculty of Medical Sciences (http://www.bvs.hn/E/
¥OtherMicrobiology Social Service reports had been sent back from the library to the School of Microbiology and discarded by the School due to the lack of storage space.
Figure 2. Honduran studies on soil-transmitted helminth infections by category (May 1930 to June 30, 2012). This graph represents
211 studies, either published or in the grey literature, retained for analysis.
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NY: IBM Corp.) and Stata 13 (College Station, TX: StataCorp
As initial step, the consultation with stakeholders revealed great
interest in harmonizing STH infection control efforts, in partic-
ularly the operative aspects of the deworming program. Various
stakeholders emphasized the need for monitoring and evaluation
of the PC program, while all agreed that integrated, multi-sectoral
efforts were needed for STH control to be sustainable. University
faculty members highlighted the importance of research capacity
strengthening and the need for international collaboration to boost
STH research in the country.
The consultation also yielded key data as follows: 3 MoH
national surveys [20,31,32]; 1 technical report by the Ministry of
Natural Resources and Environment ; 4 BSc thesis [34–37], 1
MPH thesis , and 1 PhD thesis . In addition, we obtained
38 datasets with partially processed primary data from parasitol-
ogy field trips. For a complete list of retained studies and reports,
see supporting file Text S1.
On the basis of our consultation efforts and the fact that the
Honduran Medical Journal is the oldest Honduran biomedical
periodical in which STH-relevant data was likely to be found, our
search time period spanned from May 1930, the date this journal
was established, to June 30, 2012. A flow chart with details of the
literature search and process is shown in Figure 1, and a summary
of literature sources and identified, screened, and retained studies
is shown in Table 1.
Searches of international databases were unproductive. GAHI’s
Global Atlas of Helminth Infections yielded two data sources
already identified through our search: data from national surveys
and identified on the website as authored by Zu ´niga, and a paper
published internationally . The Global Neglected Tropical
Diseases (GNTD) did not contain any data for Honduras.
Likewise, searches of PAHO reports or publications [11,41,42]
did not yield additional primary data.
Studies identified and selected
As shown in Table 1, of 257 initially identified studies, 76
(29.6%) were scientific peer-reviewed articles published in national
or international journals. The remaining 70.4% studies were in the
grey literature, most of which only existed in paper on library
shelves or researchers’ filing cabinets. None of the grey literature
was available online. Of the 257 studies selected for scrutiny, 47
(18.3%) were either not found or deemed ineligible. In total, 211
studies comprising 329 datasets were retained. Of 211 studies
retained, 23 (10.9%) fell in the clinical research category, 17
(8.1%) focused on treatment efficacy, and 171 (81%) had an
epidemiological scope. It was observed that the number of studies
on clinical outcomes and treatment efficacy has gradually declined
since the 1990s (Figure 2).
Figure 3. Honduran publication productivity on soil-transmitted helminth infections by source (May 1930 to June 30, 2012). This
graph represents 135 documents in both the peer-reviewed and grey literature. Reports from parasitology courses field trips and microbiology social
service were excluded from this analysis.
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STH research activity in Honduras
We retrieved a total of 135 publications, 81.5% of which were
dated before 2000. The oldest article found containing STH data
was published in 1930 . Figure 3 shows an analysis of research
productivity by decade and source of publication. Temporal trends
were observed in publication activity. Interest in conducting STH
research in the faculty of medical sciences is reflected by a 3-
decade publications activity. After 1980s, however, a sharp decline
in STH publications can be observed. According to library
records, no medical theses or monographs related to STH have
been written since 1992. Peer-reviewed publications, on the other
hand, were more numerous in the late 1950s and again in the
1990s. In the latter decade, 20 publications were produced, 17 of
which were articles in Honduran and International journals (of 14
international articles, 13 were in English and one in Spanish. Five
were published between 1950 and 1956; six in the 1990s, and
three in each 2001, 2002, and 2004. Figure 2 depicts all studies
found by category and period of time.
Clinical research studies.
clinical research publications dating from 1932 to 2010 is shown in
A summary of 23 STH-related
Table 2. Single-patient or case series were reported by 21
publications (91.3%); the vast majority (n=17, 80.9%) describing
A. lumbricoides pathology in children and adults (Table 2A). Four
cases involved severe T. trichiura pathology (n=1) or hookworm
pathology (n=3). Altogether, these cases involved 156 patients,
nine of whom died. In eight patients, the cause of death was
related to A. lumbricoides intestinal obstruction or perforation, while
in one patient, massive gastrointestinal bleeding due to heavy
hookworm infection was reported as the contributory cause.
Among these case-reports, special attention should be given to one
documenting for the first time the presence of Ancylostoma duodenale
in Honduras. The case involved a two-month old infant in whom
vertical transmission was suspected given the patient’s age,
exclusive breastfeeding, and maternal hookworm infection .
As shown in Table 2B, three clinical research studies (all
predating 1970) focused on anemia or nutrition. It is worth
highlighting a nutrition study by Borjas (1957), done in a
population living in a large area of banana plantations in
Northern Honduras. This was a comprehensive collaborative
study with the Institute of Nutrition of Central America and
Table 2. Clinical studies on soil-transmitted helminth infections published in Honduras from May 1930 to June 30, 2012 (n=23).
A. Case report/Case Series
SpeciesClinical findingsPopulationN6 reportsN6 Cases CommentsRef.
Ascaris lumbricoides Biliary ascariasisChildren34 Hepatic abscesses were also found in one
case. One deceased.
Adults5 35Ultrasound was the most common
diagnostic method; only approx. 55% had
a positive stool sample
Pleural ascariasisChildren11Stools were negative for Ascaris;
secondary to hepatic abscess due to
migration of adult worm (Autopsy report)
Pseudo-appendicitis Adults1 11 Light-moderate chronic abdominal pain
was the most frequent symptom.
Intestinal obstruction/perforationChildren4 77 Abdominal pain, vomiting and
constipation were the most frequent
symptoms. Four deceased.
Adults3 20 Intestinal perforation was the most
frequent complication. Four deceased.
Trichuris trichiuraAnemia and malnutritionChildren14 Severe anemia and malnutrition were
observed due heavy T. trichiura infection.
HookwormsAnemiaInfant11 Two-month old female patient. Anemia,
leukocytosis and eosinophilia. First case
of A. duodenale reported in Honduras.
Vertical transmission suspected.
Gastrointestinal bleedingInfant12 Massive gastrointestinal bleeding due to
heavy hookworm infection. One
Anemia Adult11Severe anemia and edema in extremities.
B. Other clinical focus
Purpose of the studyPopulationN6 reportsN CommentsRef.
Treatment of iron deficiency anemia Children with
125 STH infections were found in 72% of cases
Determine nutritional statusAdult inmates1 2323% of inmates were infected with at least one
General population 1 198 90% of participants were infected with at least
STH: Soil-transmitted helminth.
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Panama (INCAP) and involved an in-depth clinical examination,
anthropometric measurements, and laboratory analyses. The
study reports a high prevalence of stunting and anemia among
children, as well as 90% of STH infection prevalence in the
studied population. Almost half of STH infections were caused by
multiple parasite species .
Treatment efficacy studies.
ing on STH treatment efficacy were found (Table 3). Publication
dates ranged from 1954 to 1990. Studies varied greatly in their
design but most (73%) were done in children. Altogether, these
studies tested the efficacy of 12 different drugs by estimating cure
rate (CR), defined as the percentage of individuals who became
stool-negative 7–21 days after treatment. Parasite detection in pre-
and post-treatment stool samples was done with direct smear (41%
Seventeen publications focus-
of studies), Stoll egg counting technique (41%) or the Kato-Katz
method (18%). A pioneer on drug efficacy studies in Honduras was
Dr. Mark T. Hoekenga, an American physician who later became
the president of the American Society of Tropical Medicine and
Hygiene . He tested in humans a variety of drugs against STH
and other parasites while stationed in northern Honduras as the
Director of Medical Research, United Fruit Company Hospital,
La Lima. Hoekenga obtained excellent cure rates for piperazine
citrate against A. lumbricoides but very poor for hookworms and T.
trichiura . Albendazole efficacy against all three STH species
was reported by two studies in the late 1980s showing CRs ranging
from 66% for T. trichiura and 100% for hookworms. Conversely,
Bustamante and Herna ´ndez (1990) studied Albendazole efficacy
for hookworms in children, finding a CR of 80% .
Table 3. Treatment efficacy studies on soil-transmitted helminth infections conducted in Honduras from May 1930 to June 30,
Drug DoseYear Population
n CR (%)n CR (%)n CR (%)
Albendazole400 mg (single dose)1986 General 8280.575 66.716100.0
1989Children40 90.040 92.640100.0 
1990 Children———— 20 80.0 
Mebendazole100 mg BID/3 days 1983Children21 90.51894.44100.0
1986 General 8378.3 7565.3 11100.0 
1987Children8144.4 5870.7 219.5
1989Children 3786.53767.9 3788.9
Piperazine citrate75 mg/kg BID/2 days1987Children 2462.5———— 
1989Children 3773.037 68.837 20.0
75 mg/kg BID/3 days1983 Children21 90.5200.01 0.0 
75 mg/kg BID/7 days 1989Children 2387.0————
100 mg/kg (single dose)1987Children 24 58.3————
1989 Children 8842.0———— 
1 g BID/6 days1955Adults 3497.0 220.0 15 26.4
2 g (single dose)/6 days1955 Adults 5192.1525.7 33 15.1
3 g (single dose)/2 days 1956Children30 96.6———— 
Thiabendazole 50 mg/kg BID/3 days1969 Children——76 85.51752.9
1969 Children4327.5 1080
Levamisole 3 mg/kg (single dose) 1970Children 4297.6 18 44.410 80.0
Pyrantel10 mg/kg (single dose)1975Children 13 92.033 8.0—— 
1983Children21100.0 190.02 100.0 
20 mg/kg/3 days1975Children———— 15100.0 
Pyrantel-Oxantel100 mg (single dose)1987 Children8125.9 6080.0 20 10.0
Dithiazanine iodide20 mg/kg/5 days1960Children 4195.03898.0 10 89.0
600 mg/5 days1967General——5172.5—— 
Diethylcarbamazine25 mg/kg/4 days1954General30 80.0————
Sodium santoninate250 mg/6 days 1954General38 35.3————
Hexylresorcinol1 g (single dose)1954 General8042.0————
Chenopodium-chloroform15 mL in castor oil1954General 8040.0————
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211, 81%) found through our search were epidemiological in
nature; they comprised 272 datasets containing coproparasitolo-
gical results of 342,898 individuals. Thirty-three (19.3%) of these
studies were peer-reviewed publications while the rest were
unpublished surveys done by either the government or university
faculty members. Table 4 shows the characteristics of epidemio-
logical studies included.
Prevalence determination and/or infection intensity was the
sole objective of 140 studies (81.9%), while 10 (5.8%) and 21
(12.3%) explored associations with either infection risk factors or
clinical outcomes, respectively. Half of the studies were conducted
in community settings, whereas 42.7% were carried out with
hospitalized or outclinic patients in public health care facilities. As
shown in Table 4, parasitic infections were determined using
various methodologies, mainly the direct smear (52.6%) and Kato-
Katz (31.6%). Usage of the Kato-Katz method was traced back to
1993  and by the year 2000, it had become the method of
choice. Intensity of infection was assessed in about 34% of the
studies. Not all studies using Kato-Katz reported infection
The majority of studies (171 of
intensity. Due to great variability of diagnostic procedures, we
did not attempt to analyze infection intensity data.
Ten studies (9 theses and 1 peer-reviewed article) explored risk
factors for STH infection. Statistical significance was found
between STH infection and low socio-economic status [50,51]
low human development index in the community , lack of
sanitary infrastructure [50,52–56], and overcrowding . The
most recent study examining risk factors for STH in Honduras
showed that the number of children in the household with recent
history of diarrhea, and infection of household members with T.
trichiura were associated with ascariasis, and that the number of
children 6–14 years old in the household was associated with both
A. lumbricoides and T. trichiura infection .
Additionally, two studies reported that older children were more
likely to be parasitized with STH than their younger counterparts
[56,58]. Only one study examined the impact of intestinal
parasites on school performance .
Prevalence and geographical distribution
Of the 171 epidemiological studies, 36 met the inclusion criteria
for prevalence and geographic distribution analysis. We were able
to disaggregate these studies by datasets and municipal level and
obtained 108 datasets studying 9,336 children from all the
country’s 18 departments and 69 of the 298 (23%) municipalities.
Not all datasets were complete: 12 lacked information on the
number of negative samples examined. For this reason, overall
STH prevalence was based on only 96 datasets. The majority of
municipal datasets derived from single cross-sectional surveys but
multiple studies had been done in 18 (26%) municipalities (in
which case weighted averages were calculated to estimate
prevalence). Also, only 15% of the surveys had been conducted
outside municipal capitals. Thus, such data was geo-referenced to
the respective capitals’ coordinates. Most datasets (70%) were
obtained from surveys done by the MoH but additional datasets
provided by other authors doubled the sample size and increased
the number of municipalities by 15%. Almost half (42%) of the
data represented three departments located in central and western
Honduras: Francisco Moraza ´n, Santa Ba ´rbara and Copa ´n.
Scarcity of data was notorious for departments in the north and
east of the country.
Altogether, half (49.1%) of the children studied were positive for
at least one STH, and 27.8%, 35.3%, and 5.1% were positive for
A. lumbricoides, T. trichiura, and hookworms, respectively. Consis-
tently, T. trichiura prevalence was higher (in average, up to 2.5
times) than that of A. lumbricoides.
At the departmental level, A. lumbricoides and T. trichiura
prevalence were above 20% in 16 (89%) departments. Among
those, six departments had prevalences of $20–50% for both
parasites, whereas in two departments (Atla ´ntida and Gracias a
Dios) these prevalences exceeded 50%. Hookworm prevalence was
more dispersed, ranging from 0–1% and up to 5% in seven and
five departments, respectively. The remaining six departments had
prevalences ranging from 6% to 23.6%. One Department (Gracias
a Dios) had the highest prevalences for all three parasite species:
51.5%, 63.8% and 23.6% for A. lumbricoides, T. trichiura, and
Figure 4 shows the overall and species-specific prevalence as
well as the geographic distribution of STH infections according to
data from studies done between 2001 and 2012. Map 4A shows
that overall STH prevalence was $20% in 84% of the municipal
data and also that this prevalence was 50% or higher in 40.6% of
represented municipalities. As shown in maps 4B and 4C,
prevalence data above 20% were common for both A. lumbricoides
and T. trichiura (47.8% and 68% of represented municipalities,
Table 4. Epidemiological studies on soil-transmitted
helminth infections conducted in Honduras from May 1930 to
June 30, 2012 (n=171).
Number of studies identified171
Grey literature138 (80.7)
Total number of individuals included in the studies342,898
Children 87 (50.9)
General population72 (42.1)
Community based85 (49.7)
Health-care based 73 (42.7)
Special population based13 (7.6)
Parasite species of focus
Hookworm only4 (2.3)
A. lumbricoides only2 (1.2)
All 3 species of STH165 (96.5)
Primary outcome of the study
STH prevalence only140 (81.9)
STH prevalence and risk factors association 10 (5.8)
STH prevalence and pathology association 21 (12.3)
Stool examination method
Direct smear only (with or without egg counting)90 (52.6)
Stoll egg counting technique 2 (1.2)
Direct smear and/or Zinc sulphate, sugar flotation, formalin-
Included Kato-Katz method 54 (31.6)
Intensity of infection
Not established 112 (65.5)
STH: Soil-transmitted helminth.
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PLOS Neglected Tropical Diseases | www.plosntds.org9January 2014 | Volume 8 | Issue 1 | e2653
respectively). Moderate and high-risk areas for these two parasites
overlapped in less than 50% of cases. Hookworm infection was
observed throughout the country with prevalence $20% in 7.2%
of municipalities (Fig. 4D). Half of the study sites had reports of
0% prevalence for hookworm infection. It is important to note that
compared with the rest of the country, municipalities in the South,
typically with dryer climate and hotter temperature, had
consistently lower STH prevalences.
Prevalence and associated factors
Table 5 shows the results from the multivariable linear
regression model testing for associations between selected
municipal characteristics and STH prevalence. Human Devel-
opment Index (HDI) was significantly inversely associated with
overall STH prevalence (adjb=219.3, 95% CI=236.12 to
22.48, p=0.025) and A. lumbricoides infections (adjb=214.2,
95% CI=227.16 to 21.24, p=0.032). A decrease in about 19%
and 14% of overall STH and ascariasis prevalence, respectively,
was observed per a 0.1 increase in the HDI value. Likewise,
access to potable water in the household was significantly
associated with a decrease in the overall STH prevalence
(adjb=20.57, 95% CI=21.01 to 20.12, p=0.014). A similar
effect, although only marginally significant, was observed for
hookworm infections (p=0.069). Conversely, the average annual
precipitation was significantly associated with increased overall
STH prevalence (adjb=0.02, 95% CI=0.01 to 0.03, p=0.006),
as well as with the individual species prevalence [A. lumbricoides
(adjb=0.01, 95% CI=0.00 to 0.02, p=0.013), T. trichiura
(adjb=0.01, 95% CI=0.00 to 0.03, p=0.014); hookworm
(adjb=0.01, 95% CI=0.00 to 0.01, p=0.023)].
The present study provides for the first time, a detailed portrait of
past and present efforts to document, research, and define the
epidemiological situation of soil transmitted helminthiases in
Honduras. This study also provides a 10-year analysis of the
geographical distribution and prevalence of STH infections in
children #15 years of age, the population sector most at risk for
Figure 4. Mapping of observed overall and species-specific prevalence of soil-transmitted helminth infections in Honduras. Data
were pooled from 36 epidemiological studies (up to 108 datasets) done between 2001 and 2012. If multiple data were available for the same site
(26%), a weighted average prevalence was calculated taking into account the sample size in each survey. Overall prevalence (map A) calculation was
done from 96 datasets due to missing data. Prevalences of A. lumbricoides (map B), T. trichiura (map C), and hookworms (map D), were calculated
based on all 108 datasets. Honduras is divided into 18 departments (boundaries defined by black lines on the maps) and 298 municipalities
(boundaries defined by gray lines on the maps).
A Review of Geohelminth Infections in Honduras
PLOS Neglected Tropical Diseases | www.plosntds.org 10January 2014 | Volume 8 | Issue 1 | e2653
these infections. We believe this information is an important first step
in understanding the spatial distribution of STH prevalence in
Honduras and may assistin the decision-making processin regards to
deworming activities or other control and research activities [41,60].
Other studies have reported that publications on STH infections
are scarce in Honduras [11,41] and our results confirms this to
some extent. However, our search identified numerous data
sources that had been previously inaccessible to other researchers.
The majority (76%) of publications we found were oriented to
either clinical research or case-study reports and were found in the
Honduran Medical Journal. Unsurprisingly, these clinical reports
tended to describe severe pathology and/or death, which is a
common publication bias . Our search also revealed that
interest in publishing these types of findings was higher in the
1950s and 1960s, which probably coincided with the heightened
attention to tropical medicine in Honduras during that time .
Interest in anti-parasitic treatment efficacy was high during the
1950s through the 1970s, but this interest gradually declined in the
following decades probably due to the widespread acceptance of
benzimidazoles as treatment of choice. Epidemiological studies
were found mostly unpublished as the majority were surveys
carried out by the government or experiential learning activities in
parasitology at a public university.
Our prevalence analysis based on select epidemiological studies
shows that most of the Honduran population lives in STH
endemic areas. A previous publication provides STH prevalence
data for children 1–14 years of age ranging from 11.7%–89.2%
, while another present an overall national average of .20%
. Our study confirms that the prevalence in most of the
territory is indeed .20% but more importantly, reveals high-risk
geographic areas where STH endemicity is greater than 50%. As
pointed out previously , spatial distribution analysis is
indispensable to understand parasitic disease’s transmission
dynamics, and the findings presented here provide a valuable
insight into Honduras’s STH geographical distribution.
The multivariable analysis showed that STH prevalence was
significantly associated with lower HDI (a composite index of life
expectancy, education, and income). This finding is consistent with
previous observations by Cilie ´zar 2003  and indicates that it is
not just poverty what drives STH transmission but other inequities
. In addition, higher prevalence of STH infections was observed
in municipalities with less access to potable water. Altogether,
these findings underscore the importance of integrated approaches
to STH control . The overall higher prevalence of T. trichiura
over A. lumbricoides merits further research. The number of infected
people globally has been traditionally larger for the latter , but
it is also well established that benzimidazole drugs’ efficacy is
significantly lower for T. trichiura than for other STH . Due to
the annual rounds of single-dose Albendazole currently in place, it
is possible that T. trichiura will become the predominant species in
Honduras. Hence, regular monitoring and research are essential to
determine the frequency and schedule of deworming by
geographic areas. It also is important to remain vigilant of
potential development of drug resistance . In terms of
hookworm infections, while the overall national prevalence was
scarcely 5.1%, there was great variability not only between
municipalities but between studies done in the same location.
Overclarification of Kato-Katz preparations leading to loss of
hookworm diagnostic reliability could explain, at least partially,
this variability. We recently verified this effect during a study in
Honduras whereby inadvertent clarification time of .90 minutes
reduced Kato-Katz hookworm diagnostic sensitivity by almost
50% . This shows that under-reporting needs to be considered
when analyzing national data. It also underscores the need for
Table 5. Association between municipal characteristics and prevalence of soil-transmitted helminth infections in Honduras. 2001–2012.
adjb (95% CI)
adjb (95% CI)
adjb (95% CI)
adjb (95% CI)
Human Development Index
219.3 (236.12, 22.48)
214.2 (227.16, 21.24)
210.28 (226.23, 5.66)
22.93 (28.25, 2.39)
20.37 (21.41, 0.67)
0.04 (20.74, 0.81)
20.34 (21.17, 0.48)
20.08 (20.38, 0.22)
Potable water in the household
20.57 (21.01, 20.12)
20.32 (20.75, 0.12)
20.34 (20.8, 0.12)
20.10 (20.21, 0.01)
Sanitary facilities in the household
0.03 (20.71, 0.76)
20.01 (20.54, 0.53)
20.02 (20.61, 0.58)
0.08 (20.13, 0.29)
Annual precipitation (mm)
0.02 (0.01, 0.03)
0.01 (0.00, 0.02)
0.01 (0.00, 0.03)
0.01 (0.00, 0.01)
Annual temperature (uC)
20.27 (22.86, 2.31)
21.79 (24.07, 0.49)
0.68 (21.33, 2.68)
0.11 (20.46, 0.68)
STH, soil-transmitted helminth; adjb, adjusted coefficient; CI, confidence interval.
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PLOS Neglected Tropical Diseases | www.plosntds.org 11January 2014 | Volume 8 | Issue 1 | e2653
innovative and standardized diagnostic tools as well as for
maintaining adequate training of laboratory personnel .
Our study has identified important gaps and challenges in STH
research and control in Honduras. Studies on the health, nutrition
and cognitive impact of these helminthiases in children are greatly
needed. Equally important are studies that accurately determine
prevalence and infection intensity by ecological zones along with
associated risk factors for infection. Research gaps were also
revealed around benzimidazoles efficacy. From the policy and
practice perspective, an important challenge at present is the lack
of a monitoring and evaluation (M&E) component to the PC
program. If implemented, M&E performance indicators would be
useful in tracking progress towards the morbidity target recom-
mended by the WHO (i.e., reduce STH infections of moderate and
high intensity below 1%) .
Strengths and limitations
Major strengths of this study are its breadth and depth. We
made every possible effort to identify, locate, and retrieve a vast
amount of work and data from both published and unpublished
sources, thereby reducing many of the well-known biases that
affect systematic review studies . Importantly, by conducting
our search in two languages and not excluding the grey literature
in our analysis, we reduced biases in location , selective
publication  and dissemination . Almost certainly,
however, there may remain many other studies or data sources
that we were not able to identify (e.g., from non-governmental
organizations providing deworming). As well, our prevalence
analysis has unavoidable limitations inherent to pooling of
historical data, as indicated in recent publications [69,70]. Aware
of the diverse quality of studies included (in terms of sampling
strategies and diagnosis accuracy [71,72]), we aimed at reducing
bias by selecting within the epidemiological studies those that
were less dissimilar, namely, using data gathered from 2001
onwards, avoiding pooling data from different age groups, and
restricting provenance of studies to community and school-based
only. Further, to mitigate diagnostic differences, we only selected
studies utilizing single-stool examination by the Kato-Katz
method. Still, it is widely known that Kato-Katz is subject to
variations, and while our prevalence data for A. lumbricoides and T.
trichiura are probably reliable, the same cannot be said for
Limitations notwithstanding, we provide further evidence that
STH infections are widespread in Honduras and are likely
affecting the quality of life of the poorest of the poor [3,73].
Moreover, we reveal prevalence differentials at sub-national
administrative levels, which can prove useful for establishing a
historical trail of these infections, and most importantly help
design better interventions for their prevention and control .
Five-year outlook and conclusions
Honduras is making good strives toward sustained implemen-
tation of a nation-wide deworming program of both pre-school
and school-age children. Here, we propose a five-year outlook of
the types of strategies and activities that Honduras as a country
could prioritize (Table 6). Implementing such strategies would help
Table 6. A five-year outlook of strategies that could be implemented in Honduras to achieve sustainable control of soil-
transmitted helminth infections.
Integrated, inter-sectoral interventions Apply collaborative, integrated and multi-sectoral approaches especially prioritizing
communities where focal transmission shows singular patterns
Evaluate the feasibility of deploying complementary interventions such as improved
sanitation, vector control, and health promotion
Integrate communities and municipalities to play a bigger role in sanitation, health
education, and treatment uptake
Regular evaluation and monitoring of control efforts Studies to monitor and evaluate the performance and reach of the national soil-
transmitted helminth infections control program
Fill critical clinical knowledge gaps Studies around benzimidazole efficacy for the three soil-transmitted parasites species
prevalent in Honduras
Research into the co-management of these and other diseases
Expand epidemiology research effortsStudies on the health, nutrition and cognitive impact of these helminthiases in
Determine prevalence and infection intensity by ecological zones along with
associated risk factors for infection
Update the mapping of STH prevalence and intensity, including estimates of
populations at risk and disease burden
Research capacity strengtheningReinforce the training and capacity of medical, laboratory, and other health
Enhance statistical analysis capability including geospatial mapping
Seek international research collaboration
Knowledge transfer and disseminationImprove coordination and information dissemination to gain local and international
financial and political support
Disseminate research findings to local and international stakeholders using
Share information with the scientific community through peer-reviewed journals and
other accessible media
A Review of Geohelminth Infections in Honduras
PLOS Neglected Tropical Diseases | www.plosntds.org12 January 2014 | Volume 8 | Issue 1 | e2653
Honduras not only overcome current challenges for sustainable
control but also to fill the knowledge gaps identified in the present
In conclusion, we believe the way forward is to increase the
amount and quality of STH research done in Honduras and to
make this knowledge publicly available to the scientific community
as well as to national and international policy and decision makers.
At the same time, efforts directed to STH control and prevention
should continue with firm determination and more diversification.
As PC coverage reaches the national goal, we advocate for
integrated, multi-sectoral approaches [5,63,74] prioritizing com-
munities where focal transmission shows singular patterns.
Differential endemicity is possible because even though Honduras
is a small country (112,492 km2); it is characterized by a
mountainous territory comprising distinct ecological areas with
important variations in precipitation, temperature, soil composi-
tion, etc. It is also a nation of diverse cultures and ethnicities, and
with profound social inequalities . Ultimately, with strong
support from the national and international community, Hondur-
as’s strategic plan for NTD control has the potential to greatly
reduce the health burden of STH infections and other neglected
diseases in the country.
Studies retained for analysis.
We would like to thank Doris Quan, Wilfredo Sosa, Vilma Espinoza,
Eunice Espinoza, Irina Jovel, Karla Herna ´ndez, and Carol Rodriguez,
School of Microbiology, UNAH, for providing prevalence data. We are
grateful to UNAH’s libraries staff for their valuable cooperation. Brock
University library staff is also acknowledged for ArcGIS training.
Conceived and designed the experiments: ALS MC JAG. Performed the
experiments: ALS JAG MMR REM MC. Analyzed the data: ALS JAG
MEB. Wrote the paper: ALS JAG MEB.
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