Dunn et al.

Parasites & Vectors (2016) 9:31

DOI 10.1186/s13071-016-1310-2

REVIEW Open Access

Epidemiological surveys of, and research

on, soil-transmitted helminths in Southeast
Asia: a systematic review
Julia C. Dunn1,2* , Hugo C. Turner1,2, Aung Tun3 and Roy M. Anderson1,2

Abstract
Soil-transmitted helminth (STH) infections of humans fall within the World Health Organization’s (WHO) grouping
termed the neglected tropical diseases (NTDs). It is estimated that they affect approximately 1.4 billion people
worldwide. A significant proportion of these infections are in the population of Southeast Asia. This review analyses
published data on STH prevalence and intensity in Southeast Asia over the time period of 1900 to the present to
describe age related patterns in these epidemiological measures. This is with a focus on the four major parasite
species affecting humans; namely Ascaris lumbricoides, Trichuris trichiura and the hookworms; Necator americanus
and Ancylostoma duodenale. Data were also collected on the diagnostic methods used in the published surveys
and how the studies were designed to facilitate comparative analyses of recorded patterns and changes therein
over time. PubMed, Google Scholar, EMBASE, ISI Web of Science, Cochrane Database of Systematic Reviews and the
Global Atlas of Helminth Infections search engines were used to identify studies on STH in Southeast Asia with the
search based on the major key words, and variants on, “soil-transmitted helminth” “Ascaris” “Trichuris” “hookworm”
and the country name. A total of 280 studies satisfied the inclusion criteria from 11 Southeast Asian countries;
Brunei, Cambodia, Indonesia, Lao People’s Democratic Republic (Lao PDR), Malaysia, Myanmar, Philippines, Singapore,
Thailand, Timor-Leste and Vietnam. It was concluded that the epidemiological patterns of STH infection by age and
species mix in Southeast Asia are similar to those reported in other parts of the world. In the published studies there
were a large number of different diagnostic methods used with differing sensitivities and specificities, which makes
comparison of the results both within and between countries difficult. There is a clear requirement to standardise the
methods of both STH diagnosis in faecal material and how the intensity of infection is recorded and reported in future
STH research and in monitoring and evaluation (M&E) of the impact of continuing and expanding mass drug
administration (MDA) programmes.
Keywords: Soil-transmitted helminths, Southeast Asia, Systematic review, Neglected tropical diseases, Mass
drug administration, Monitoring and evaluation

Background are four main species of STH; namely, Ascaris lumbri-

Soil-transmitted helminth (STH) infections belong to coides (roundworm), Trichuris trichiura (whipworm) and
the so called neglected tropical diseases (NTDs) that the hookworms (Ancylostoma duodenale and Necator
affect human populations in poorer regions of the world americanus) [6].
[1]. Their presence is a typical marker of poverty where It is estimated that over 1.4 billion people are infected
access to sanitation and clean water is limited and, con- with STHs [2, 7, 8]. According to a study by Pullan et al.
comitantly, standards of hygiene are low [2–5]. There [8], the highest number of STH infections occurs in
Asia, where the People’s Republic of China and India
have the greatest concentration of people infected with
* Correspondence: julia.dunn@imperial.ac.uk
1
London Centre for Neglected Tropical Disease Research, London, UK intestinal worms. Southeast Asia is the region with the
2
Department of Infectious Disease Epidemiology, School of Public Health, highest reported prevalences of STH infection in recent
Faculty of Medicine, Imperial College London, London, UK decades [8, 9].
Full list of author information is available at the end of the article

© 2016 Dunn et al. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Dunn et al. Parasites & Vectors (2016) 9:31 Page 2 of 13

The countries of Southeast Asia have various attri- In this paper we review published epidemiological
butes that contribute to the continually high prevalence studies of STH in the Southeast Asia countries of
of STH. For example, most Southeast Asian countries Brunei, Cambodia, Indonesia, Lao People’s Democratic
have a tropical and moist climate, which is ideal for the Republic (Lao PDR), Malaysia, Myanmar, Philippines,
survival of STH eggs/larvae in the environment [10]. Singapore, Thailand, Timor-Leste and Vietnam. The
This environment acts to promote infection within the overall aim is to evaluate past STH publications from
human population [10, 11]. Socioeconomic factors such studies conducted in Southeast Asia and to help point to
as lack of adequate water resources, sanitation and poor the ideal study design for the M&E of control
hygiene practices have repeatedly been proven to be re- programme impact.
lated to high STH prevalence within a community [5]
since transmission of A. lumbricoides and T. trichiura Review
occurs via the faecal-oral route [6]. Several countries This systematic review was developed in line with the
within Southeast Asia are amongst the poorest in the Preferred Reporting Items for Systematic Reviews and
world, without adequate water and sanitation infrastruc- Meta-Analyses (PRISMA) guidelines (see Checklist in
ture [10, 12] and, therefore, the parasites prosper in such Additional file 1).
environments [13, 14].
The goal set by the World Health Organization Selection criteria
(WHO) for STH control by 2020 is to reduce morbidity We include all published studies in English in which the
from STH in preschool-aged (pre-SAC: 2-5 years) and prevalence and/or intensity of STH infection was mea-
school-aged children (SAC: 5-14 years) to a level below sured in the Southeast Asia countries of Brunei,
which it would not be considered a public health prob- Cambodia, Indonesia, Lao PDR, Malaysia, Myanmar,
lem [15]. Similarly, the target set by the 2012 London Philippines, Singapore, Thailand, and Vietnam (the
Declaration on NTDs, is to achieve preventive chemo- members of the Association of Southeast Asian Nations
therapy (PCT) coverage of 75 % of all pre-SAC and SAC - ASEAN), within the period of January 1st, 1900 to July
at risk of STH by 2020 [16, 17]. To meet this goal, 2015. Timor-Leste was also included due to its proximity
Southeast Asian countries that are endemic for STH to the other Southeast Asian countries and since it is
have been conducting mass drug administration (MDA) often included in public health analyses concerning
campaigns [13, 18], treating pre-SAC and SAC in af- Southeast Asia [8,13]. No studies were found concerning
fected areas with antihelminthic drugs such as albenda- STH in Brunei. Observational and intervention studies
zole and mebendazole at regular intervals [19, 20]. The were eligible for inclusion. We excluded studies that had
current goals and objectives set by the WHO focus on the following criteria: (i) studies that did not report
reducing morbidity in pre-SAC and SAC, the age groups prevalence values for each STH separately (that just re-
most commonly and most severely affected by two of corded prevalence of any STH); (ii) studies where the
the major STH infections; namely, A. lumbricoides and participants were selected from hospital in-patients; (iii)
T. trichiura [15]. Hookworm is found at the highest in- studies where the participants were not permanent resi-
tensities in adults, and hence, its abundance is not greatly dents of the specific country (e.g. refugees or migrants);
affected by only treating pre-SAC and SAC [21–23]. At (iv) duplicate publications or extension of analysis from
present, there is a growing interest in investigating the an original study; and (v) studies where the full publica-
feasibility of interrupting the transmission of STH by tion could not be obtained.
broadening the range of ages targeted for treatment and
increasing coverage in all age groups [24–27]. Search strategy and methodology
To evaluate the impact of MDA, comprehensive epi- We identified published studies using automated data-
demiological studies need to be conducted periodically base searches of EMBASE (1947 to July 2015), ISI Web
to measure changes in the prevalence and intensity of of Science (1900 to July 2015), the National Library of
each STH species over time [28]. With the increasing Medicine’s PubMed (1900 to July 2015) and further
focus on the effect that SAC-targeted MDA has on manual searching was done using Google Scholar, the
prevalence and intensity of STH across all ages [22, 29], Cochrane Database of Systematic Reviews (CDSR) and
ideally monitoring and evaluation (M&E) of control im- the website of the Global Atlas of Helminth Infections
pact should be based on epidemiological studies that are (GAHI - http://www.thiswormyworld.org/). We employed
community wide. Also, to be able to compare progress the following terms and variations on these terms: STH,
between different regions and countries, the methods or soil-transmitted helminth, or Ascaris, or Trichuris, or
and design of M&E should be standardised in terms of hookworm, or Ancylostoma, or Necator, or deworm. A full
the diagnostic method used and the prevalence plus in- list of the search terms is provided in Additional file 1.
tensity measures made in the target population [30]. We also searched the Global Neglected Tropical Diseases
Dunn et al. Parasites & Vectors (2016) 9:31 Page 3 of 13

database [31] for data collected on STH from studies con- data from two countries [32, 33] and one study included
ducted in Southeast Asia but did not find any results. data from three countries [34]. Most of the studies iden-
Identified studies were exported into EndNote X6 tified were of a cross-sectional design (266 studies, 95 %)
(Thomson Reuters, New York, USA) for management. and the remaining studies were longitudinal (14 studies,
The abstracts of the studies were reviewed against the 5 %). Figure 3 illustrates the distribution of the identified
inclusion and exclusion criteria. The literature selection studies across time – the first study being undertaken in
process is outlined in Fig. 1. Ultimately, 280 studies were 1947. The number of published studies has increased
identified that met the inclusion criteria, a full list of the steadily since 1947 to the present. In 2003 there was a
included studies is provided in Additional file 2. marked increase in STH studies published perhaps due
to an increased focus on the NTDs globally as a result
Data extraction of WHO guidance [18]. Another recent spike in the
Data extraction included country name, study area, year number of STH studies published coincides with the
the study was published, year the study was conducted, London Declaration on NTDs in 2012 [17]. Both of
type of study (cross-sectional or longitudinal/cohort), these events signalled an increase in funding and mate-
sample size, age of participants, prevalence of each STH, rials to combat STH, including for example the donation
intensity of each STH, and diagnostic methods of albendazole tablets by GSK. The surge in published
employed. If the publication did not state which year the studies around these times, plus the longer term increas-
study took place, the year of publication was used in- ing trend, suggests a growing interest in STH control.
stead. Also, if the study was conducted over a range of A large proportion of the selected studies measured
years then the latest year of the stated range was used. STH prevalence and intensity from more than one study
For plotting the age distributions, the mid-point of the area within the same publication. Hookworm was, mar-
stated age range was used. ginally, the most studied STH (256 studies), followed by
A. lumbricoides (251 studies) and T. trichiura was the
Results and discussion least studied (241 studies). This went against the expect-
All identified studies ation that hookworm would be the least studied of the
A total of 280 studies were identified that met the inclu- STHs in Southeast Asia, as the climate of sub-Saharan
sion criteria (Fig. 1). The breakdown of the number of Africa is more suitable for hookworm transmission,
studies by country is provided in Table 1. Figure 2 illus- whereas the warm and humid climate of Southeast Asia
trates the geographical distribution of study areas covered is ideal for A. lumbricoides and T. trichiura [9,10]. Con-
in the selected publications which met the inclusion versely, it seems that most identified studies were inclusive
criteria. of all STH species.
The largest proportion of the identified studies were
conducted in Thailand (55 studies, 20 %), followed by Diagnostic methods
Malaysia (51 studies, 18 %) and Indonesia (48 studies, The differences in the method of STH diagnosis and
17 %). Timor-Leste and Singapore had the fewest studies quantification of intensity used across the selected stud-
(one and two studies respectively). Two studies included ies made it difficult to compare studies. For example,
STH prevalence was measured by 13 different methods
(Fig. 4). Of the 280 studies, 40 reported using more than
one method for diagnosing STH infection, whilst eight
studies did not report the method used at all. The speci-
ficity and sensitivity of the different methods of STH
diagnosis have been analysed in a number of publica-
tions and have been found to vary widely [30, 35–37].
Therefore, it can be inferred that the accuracy of the
prevalence and intensity results in STH studies also var-
ies over time. However, it is difficult to quantify this due
to the lack of standardised procedures.
The Kato-Katz technique was the most frequently
used method of STH diagnosis (128 studies (45.7 %), in-
Fig. 1 Decision tree outlining the inclusion and exclusion criteria of cluding studies that used multiple methods). The pro-
the identified studies. *These papers could not be properly screened portion of studies using each type of diagnostic method
due to being published in non-English language journals and likely has changed over time, with the proportion of studies
include studies in non-included countries such as Japan and
using Kato-Katz and the formalin-ether concentration
South Korea
(FEC) method increasing since the 1980s. The current
Dunn et al. Parasites & Vectors (2016) 9:31 Page 4 of 13

Table 1 Breakdown of the identified studies

Country Number Number of prevalence studies Number of studies with Number of studies with Number of studies with full
of studies that measured intensity prevalence by age groups age groups and intensity age distribution and intensity
Cambodia 22 1 4 0 0
Indonesia 48 9 30 6 4
Lao PDR 26 2 10 1 1
Malaysia 51 11 20 6 1
Myanmar 22 4 9 4 4
Philippines 37 7 13 1 1
Singapore 2 0 1 0 0
Thailand 55 4 13 4 4
Timor- 1 0 0 0 0
Leste
Vietnam 20 5 5 2 2
TOTAL 280a 43 105 24 17
a
Includes two studies that had components in two different countries, and one study that had components in three different countries

Fig. 2 Map of identified STH studies in Southeast Asia. Red circles indicate the location of published STH studies
Dunn et al. Parasites & Vectors (2016) 9:31 Page 5 of 13

Fig. 3 Number of identified studies published by year

decade has also seen the first studies using more ad- However, prevalence as an indicator [21, 44, 45] is far from
vanced molecular and immunological diagnostic tools ideal given the highly non-linear relationship between this
such as the polymerase chain reaction (PCR) [38–40] measure and the average intensity of infection when
and enzyme-linked immunosorbent assay (ELISA) [41]. parasite distributions of worms or eggs per gram (EPG)
In each decade there was a small proportion of studies output per host is aggregated (negative binomial) in
that do not specify which method the authors used to form [46].
diagnose STH infection. Figure 5 shows overall STH prevalence plotted against
There was also variation in how the diagnostic average intensity for the studies that measured intensity
methods were applied. For example, variation between by EPG counts. There are clearly discernible relation-
studies is apparent where the Kato-Katz method was ships between STH prevalence and average intensity dis-
used as the primary diagnostic method. Studies varied in played in these plots. Prevalence is non-linearly related
how many Kato-Katz thick smears were prepared from to average intensity where the former changes rapidly at
each participant, how many times these slides were read low intensities, but slowly at high intensities. The im-
(for quality control) [42] and whether or not readings portance of this relationship lies in the observation that
were by the same operator or different people. Out of large changes in intensity, possibly caused by the effects
the 128 studies that used Kato-Katz, 97 (75.8 %) did not of MDA, are not well measured by changes in preva-
clearly state that any repetition had been made, 11 lence. Therefore, M&E for MDA programmes must be
(8.6 %) studies stated that they prepared/read Kato-Katz based on intensity. The precise relationship between the
slides once, 19 (14.8 %) studies in duplicate and one study two epidemiological measures is determined by the mag-
in the Philippines [43] read Kato-Katz slides six times. nitude of the negative binomial aggregation parameter k
(which varies inversely with the degree of aggregation).
Prevalence and intensity metrics For high aggregation prevalence plateaus well below
Most control programmes use prevalence as their main 100 %, while for low degrees of aggregation of worms it
epidemiological indicator, as advised by the WHO [15, 19]. quickly saturates to high prevalence figures [46]. The
Dunn et al. Parasites & Vectors (2016) 9:31 Page 6 of 13

Fig. 4 Number of studies that used each STH diagnostic method. Multiple = studies that reported using multiple methods of diagnosis

heterogeneity displayed in this non-linear relationship only. Five studies used the more direct method of mean
may be due in part to the inclusion of data from different worm burden based on worm expulsion in faeces post
settings, countries and decades on the same graph. The chemotherapy. A single study used eggs per millilitre
vertical lines on Fig. 5 indicate the boundaries of the in- (EPM) of faeces as the measure of intensity.
tensity groupings defined by the WHO as low, medium
and high [15]. Note that for values within one intensity Age distributions of prevalence and intensity of infection
classification (low, medium or high) the prevalence of in- The current focus of STH control, determined by the
fection varies widely. This reflects differing degrees of goals set by the WHO [15], is reducing morbidity in
worm aggregation within the various human communities pre-SAC and SAC, the age groups that suffer the highest
studied. For example, the prevalence values for hookworm morbidity from heavy A. lumbricoides and T. trichiura
in the low intensity group (low intensity group mean EPG infection [18, 47]. Consequently, most studies are focussed
414.42) ranged from close to 0 to 94 %. on STH infection in these age groups. However, recent
As specified in the inclusion criteria, all of the studies mathematical model-based studies of STH transmission
selected reported at least one prevalence value for a species dynamics [23, 29, 44, 48, 49] have helped focus attention
of STH. Of these 280 studies, only 43 (15 %) also measured onto the burden of infection in adults and how it affects
STH intensity of infection in the study participants. Table 1 overall STH transmission in a given community. These
details the number of studies that measured intensity of studies concluded that in many settings, transmission
STH in participants. Similar to prevalence, STH intensity could not be interrupted by only SAC-focussed MDA, this
was measured using a variety of different methods between is especially true for hookworm where prevalence and in-
studies. In 29 studies intensity was measured using the in- tensity is highest in the adult age groups [21,50]. There-
direct method of mean EPG of faeces. Eight additional fore, in many instances morbidity control will not lead to
studies used EPG but presented the geometrical means elimination, as adults will not be treated and transmission
Dunn et al. Parasites & Vectors (2016) 9:31 Page 7 of 13

Fig. 5 STH prevalence (% infected) plotted against the average intensity for studies that measured intensity in eggs per gram (EPG) of faeces. Red
line indicates the upper threshold for low intensity, purple line indicates the upper threshold for medium intensity, above purple line is high
intensity as defined by the WHO [15]. a = Ascaris lumbricoides, (b) = Trichuris trichiura, (c) = Hookworm

will not be broken. To break transmission, country MDA (Fig. 6a and b). A. lumbricoides prevalence peaks in the
programmes may have to adapt to include all age groups. SAC groups in both the Philippines and Thailand stud-
As such, there is a need for comprehensive epidemio- ies. Hookworm prevalence for both Philippines and
logical studies measuring prevalence and intensity across Thailand increases to a peak around the 20-29 age
all age groups. groups (Fig. 6c and f ), and remains high across the older
Table 2 presents the details of the 17 studies that mea- age groups. However, T. trichiura prevalence varies be-
sured STH prevalence and intensity of infection in all tween the two countries; prevalence in the Philippines
age groups within a community (6 % of the total number study is lower for pre-SAC (Fig. 6b) but remains at high
of identified studies). The small number of these studies level for the other age groups, whereas in the Thailand
is indicative of the lack of comprehensive epidemio- study (Fig. 6e) prevalence is similarly lower in pre-SAC
logical M&E of control impact of MDA on STH in the but then peaks in SAC and decreases over the older age
Southeast Asia region. Cambodia, Singapore and Timor- groups. Additional file 1: Figure S1 presents these data
Leste did not have any studies that fit these criteria. Even for each country included in the review.
within these 17 studies, there is substantial variation in Figure 7 records the age distributions of the mean in-
how prevalence and intensity are measured and sum- tensity of infection for the studies that recorded faecal
marised (Table 2). EPG, the most commonly used measurement excepting
Figure 6 shows the prevalence age distribution of each a few studies that employed worm expulsion methods.
STH for two example countries, the Philippines [51] and The plots contain data from studies in all Southeast Asia
Thailand [52–55]. Prevalence of A. lumbricoides and T. countries included in the analysis (except for Singapore
trichiura is higher for the included Philippines study and Timor-Leste which did not have any studies that
Dunn et al. Parasites & Vectors (2016) 9:31 Page 8 of 13

Table 2 Details of the studies that measured intensity across all ages
First Author Year Country Sample size Parasite species Diagnostic method Intensity measure
Bakta 1993 Indonesia 2331 hk KK EPG
Higgins 1984 Indonesia 227 asc, tri, hk MM EPG
Joe 1959 Indonesia 664 asc, tri, hk AUT Mean worm burden
Margono 1983 Indonesia 276 asc, tri, hk KK EPG
Phongluxa 2013 Lao PDR 574 asc, tri, hk KK EPG (geo mean)
Rahman 1994 Malaysia 204 asc, tri, hk KK EPG
Yogore 1953 Philippines 229 asc, tri, hk DM EPM
Preuksaraj 1983 Thailand 43341 asc, tri, hk KK/ST EPG
Sadun 1953 Thailand 219 hk DM/ST EPM
Sadun 1955 Thailand 13469 hk DM/ST EPG
Bethony 1998 Thailand 641 hk NS EPG
King 2005 Vietnam 201 asc ELISA EPG
Needham 1998 Vietnam 543 asc, tri, hk KK EPG
Hlaing 1990 Myanmar 2826 asc DM/FEC/KK EPG
Hlaing 1984 Myanmar 783 asc DM/FEC/KK EPG
Hpay 1970 Myanmar 571 asc, tri DM/FEC/ST Mean worm burden
Tu 1970 Myanmar 671 asc, tri DM/FEC/ST Mean worm burden
EPG eggs per gram, EPG (geo mean) geometric mean of eggs per gram, EPM eggs per millilitre. Asc Ascaris lumbricoides, tri Trichuris trichiura, hk Hookworm. KK
Kato-Katz method. MM McMaster method. NS Not stated. AUT Autopsy method. DM Direct microscopy method. ST Stoll technique. ELISA Enzyme-linked immunosorbent
assay. FEC Formalin-ether concentration method

Fig. 6 Age distribution of the prevalence of infection for studies in the Philippines (a, b and c) and Thailand (d, e and f) that measured intensity
and prevalence across all age groups. Figure (f) includes data from more than one study and data points were plotted against the mid-point of
the reported age group. A = Philippines, Ascaris lumbricoides. B = Philippines, Trichuris trichiura. C = Philippines, hookworm. D = Thailand, Ascaris
lumbricoides. E = Thailand, Trichuris trichiura. F = Thailand, hookworm. Note different scales on figure (e) and (f)
Dunn et al. Parasites & Vectors (2016) 9:31 Page 9 of 13

Fig. 7 Age distribution of the intensity of infection for studies that measured intensity in eggs per gram (epg), by decade the study was conducted in.
a = Ascaris lumbricoides, (b) = Trichuris trichiura, (c) = Hookworm. Orange = 1950–1959, Red = 1970–1979, Green = 1980–1989, Purple = 1990–1999,
Blue = 2000–2009. There were no studies from 1960–1969 or 2010-present

included intensity values). A. lumbricoides and T. tri- prevalence and intensity of infection across a broad range
chiura show convex curves with higher mean intensities of age classes – and yet this period to the present is when
in the younger age groups (pre-SAC and SAC), which MDA coverage has been rising. M&E programmes in
then decreased with increasing age. Hookworm inten- Southeast Asia, to record the impact of MDA, need to
sities increased with age and then plateaued in older age focus on intensity across all age groupings.
groups. However, in a few studies there are several data Intensity of infection can also be measured by a more
points that denote high intensities in pre-SAC and SAC direct method, mean worm burden, based on worm
age groupings. Past comprehensive epidemiological stud- expulsion post-chemotherapy (Fig. 8). As this method
ies have indicated that there is usually a higher intensity directly counts the number of worms harboured by a
of hookworm in adult age groups [21, 50]. A possible participant, there is perhaps little uncertainty of the per-
reason for this pattern not being seen in this analysis is son’s intensity level, assuming that stool collection is
due to the under-representation of adults in the people complete and lasts for many days post-treatment. However,
sampled in the included studies. For example four stud- there are far fewer studies that use mean worm burden as
ies included hookworm intensity values for SAC [56–59] the intensity measure as well as reporting these intensities
and none for adults. Also, the age groupings are usually by age and including a representation of the entire commu-
much larger for the adults (e.g. all ages above 40 years nity [60–63]. All but one of these studies are in Myanmar.
or all ages above 50 years) and so may not represent the The remaining study [60] was carried out in Indonesia and
variation between different adult age groups on a finer was the only case in this review to collect data via autopsy.
age range and the possible increase in hookworm burden The data for T. trichiura was not included in Fig. 8 be-
in the later years of life. It is relevant to note that very cause, in two studies, the adult age groups were grouped in
few studies have been conducted post-2000 that record a manner that does not adequately reflect the variation
Dunn et al. Parasites & Vectors (2016) 9:31 Page 10 of 13

Fig. 8 Age distribution of intensity for studies that measured intensity in mean worm burden. a = Ascaris lumbricoides, (b) = Hookworm

across adult groups (all ages above 14 years). For A. lum- plots the average (over the reviewed Southeast Asian
bricoides mean worm burden has a small peak around countries) change in MDA coverage as recorded in the
SAC, decreases around 30–50 years old and then increases WHO PCT database in pre-SAC and SAC. The raw data,
again at the oldest ages (Fig. 8a). Therefore, in terms of as extracted from the WHO PCT databank interactive re-
worm intensity, the older age groups also suffer from a port, is presented in Additional file 3. Note that average
high worm burden, although the morbidity in adults may coverage increases from 2003 to 2013 in both age group-
be less damaging than in SAC. However for hookworm, for ings as a trend in the region. However, considerable differ-
which there is only one study [60], mean worm burden ences exist between countries as recorded in the raw data.
peaks in the 30–40 years individuals (Fig. 8b). It seems likely that this overall rise in coverage is the main
driver behind the trend for a decrease in prevalence and
Limitations intensity of STH infection in most countries in the region.
The first limitation of our review, which has been Finally, whilst every effort has been made to make this
highlighted earlier in this paper, is our inability to directly review comprehensive and inclusive of all the studies
compare studies due to the differences in diagnostic tech- published on STH in Southeast Asia, it is inevitable that
niques and units of measurement. However, despite this some studies will have been missed due to them not be-
lack of standardisation, when the studies were pooled and ing published in English language journals. In the future,
analysed, trends in prevalence and intensity across the age it would be useful to have these papers translated to add
classes could be determined. The age distributions of A. further information to the review. It is likely however,
lumbricoides, T. trichiura and hookworm prevalence that the inclusion of these papers would have supported
(Fig. 6) displayed a similar pattern to those recorded in the conclusions drawn in this paper. In general, STH
past studies and reviews [46, 50, 61, 64]. However, in fu- studies are difficult to compare and contrast due to a
ture research and in M&E appraisals it is obviously highly lack of standardisation in diagnostic methods.
desirable to place greater emphasis on the standardisation
of the methods of measurement. Conclusions
Secondly, the significance of changes in the prevalence Since 1947 there have been a large number of epidemio-
and intensity of STH infection over time can best be logical studies on STH in Southeast Asia, increasing in
interpreted when examined in conjunction with know- numbers over the years to the present day. However,
ledge of the history of control efforts, specifically MDA, in only a small proportion of these studies can be truly
the area under consideration. It is possible to determine deemed comprehensive in the sense of good coverage of
this history at country-level via the WHO PCT databank prevalence and intensity data over a broad range of age
[20], but the data only extends as far back as 2003 and is classes in the studied communities or areas. Only 17
incomplete for a number of countries. Regional-level studies (6 %) measured both STH prevalence and inten-
MDA data and information on other interventions, such sity across all age groups. It is imperative for the future
as water and sanitation hygiene (WASH) and behaviour of STH control in Southeast Asia that more studies are
change, is required before the cause of any changes in completed with much better, standardised M&E design.
prevalence and/or intensity can be established. Figure 9 Ideal M&E design should include a consistent diagnostic
Dunn et al. Parasites & Vectors (2016) 9:31 Page 11 of 13

Fig. 9 Mean mass drug administration (MDA) coverage for pre-school aged children (pre-SAC) and school-aged children (SAC) in the Southeast
Asian countries. Red = pre-SAC, Blue = SAC. Data collated from the World Health Organization preventive chemotherapy databank [20]. Country-specific
data is included in Additional file 3

method. Currently Kato-Katz is recommended by the effective targeting by age group and frequency of MDA to
WHO due to its ease of use in the field and low cost interrupt transmission of STH in different populations
[19]. However, methods with higher sensitivity and spe- and settings.
cificity are desirable as the impact of expanded MDA Perhaps the most important message arising from this
programmes drive infection to low levels. M&E should review is that public health workers must place greater
use STH intensity as the primary measure to determine emphasis on the standardisation of diagnostic methods
the effectiveness of MDA programmes, including those for determining STH prevalence and intensity. The
integrated with WASH, education and nutrition compo- achievement of some degree of uniformity in epidemio-
nents. Large changes in intensity, reflecting effective treat- logical methods would mean that studies can be directly
ment, are not well measured by changes in prevalence. compared both within and between countries to effect-
M&E should also cover the different ecological areas of a ively evaluate and compare the progress of control efforts.
country and should be repeated at set intervals. They To achieve this, guidance and support from organisations
should be continued for a specified time after MDA, and such as WHO to endemic countries would be useful for
any other control activities, have been stopped. The data emphasising the importance of comprehensive and con-
is of obvious importance in evaluating the progress and ef- tinuous M&E. Indeed it would be desirable if WHO
fectiveness of MDA programmes, plus the impact of treat- played the lead role in setting standardisation guidelines.
ing pre-SAC and SAC on transmission within the total Training in best practice and uniform methods could help
community. Finally, this data can also be of great value in lower income countries optimise M&E. It has proven diffi-
mathematical modelling studies to determine the most cult in the past for researchers to agree on one method of
Dunn et al. Parasites & Vectors (2016) 9:31 Page 12 of 13

STH diagnosis. There have been numerous recent papers References

evaluating the sensitivity and specificity of the various 1. Pullan RL, Brooker SJ. The global limits and population at risk of soil-transmitted
helminth infections in 2010. Parasit Vectors. 2012;5(1):81.
methods [30, 65, 66]. However, the new technologies of 2. Hotez PJ, Fenwick A, Savioli L, Molyneux DH. Rescuing the bottom billion
quantitative PCR, multiplex PCR and ELISA offer great through control of neglected tropical diseases. Lancet. 2009;373(9674):1570–5.
potential especially in low prevalence areas, as MDA impact 3. Esrey SA, Potash JB, Roberts L, Shiff C. Effects of improved water supply and
sanitation on ascariasis, diarrhoea, dracunculiasis, hookworm infection,
increases, to identify the remaining pockets of transmission. schistosomiasis, and trachoma. Bull World Health Organ. 1991;69(5):609–21.
4. Ziegelbauer K, Speich B, Mäusezahl D, Bos R, Keiser J, Utzinger J. Effect of
sanitation on soil-transmitted helminth infection: systematic review and
Additional files meta-analysis. PLoS Med. 2012;9(1):e1001162.
5. Strunz EC, Addiss DG, Stocks ME, Ogden S, Utzinger J, Freeman MC. Water,
Additional file 1: PRISMA checklist, full list of search terms and sanitation, hygiene and soil-transmitted helminth infection: a systematic
Supporting Figure 1. (DOCX 1462 kb) review and meta-analysis. PLoS Med. 2014;11(3):e1001620.
Additional file 2: Full list of the included studies. (XLSX 56 kb) 6. Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, et al.
Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm.
Additional file 3: Preventive chemotherapy data for the Southeast Lancet. 2006;367(9521):1521–32.
Asian countries. (XLSX 13 kb) 7. Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Ehrlich-Sachs S, Sachs
JD, et al. Control of neglected tropical diseases. New Engl J Med. 2007;
357:1018–27.
Abbreviations 8. Pullan RL, Smith JL, Jasrasaria R, Brooker SJ. Global numbers of infection and
Asc: Ascaris lumbricoides; ASEAN: Association of Southeast Asian Nations; disease burden of soil transmitted helminth infections in 2010. Parasit
AUT: autopsy method; CDSR: Cochrane Database of Systematic Reviews; Vectors. 2014;7(1):37.
DM: Direct Microscopy method; ELISA: enzyme-linked immunosorbent assay; 9. Utzinger J, Bergquist R, Olveda R, Zhou XN. Important helminth infections in
EPG: eggs per gram of faeces; EPG (geo mean): eggs per gram of faeces Southeast Asia. Diversity, potential for control and prospects for elimination.
(geometric mean); EPM: eggs per millilitre of faeces; FEC: formalin-ether Adv Parasitol. 2010;72(C):1–30.
concentration; GAHI: Global Atlas of Helminth Infections; Hk: hookworm; 10. Brooker S, Singhasivanon P, Waikagul J, Supavej S, Kojima S, Takeuchi T, et
KK: Kato-Katz method; Lao PDR: Lao People’s Democratic Republic; al. Mapping soil-transmitted helminths in Southeast Asia and implications
M&E: monitoring and evaluation; MDA: mass drug administration; for parasite control. Southeast Asian J Trop Med. 2003;34(1):24–36.
MM: McMaster method; NS: not stated; NTD: neglected tropical disease; 11. Matsusaki G. Influence of low temperature, sunshine, desiccation and
PCR: Polymerase Chain Reaction; PCT: preventive chemotherapy; Pre- excreta upon the eggs of Ancylostoma Duodenale and Necator Americanus.
SAC: Preschool-aged children; PRISMA: Preferred Reporting Items for ii. Sunshine. Yokohama Med Bull. 1963;14:123–6.
Systematic Reviews and Meta-analyses; SAC: school-aged children; SE 12. WHO. Report of the informal consultation on scaling up treatment of soil
Asia: Southeast Asia; ST: stoll technique; STH: soil-transmitted helminth; transmitted helminthiasis in the South-East Asia region: 10–11 October
Tri: Trichuris trichiura; WASH: water and sanitation hygiene; WHO: World 2011, New Delhi, India. New Delhi: World Health Organization; 2012.
Health Organization.
13. Jex AR, Lim YAL, Bethony JM, Hotez PJ, Young ND, Gasser RB. Soil-transmitted
helminths of humans in Southeast Asia-towards integrated control. Adv
Competing interests Parasitol. 2011;74(C):231–65.
Roy M Anderson is a non-executive Director of GlaxoSmithKline (GSK). 14. Hotez PJ, Ehrenberg JP. Escalating the global fight against neglected
GlaxoSmithKline played no role in study design, data collection and analysis, tropical diseases through interventions in the Asia Pacific Region. Adv
decision to publish, or preparation of the manuscript. Parasitol. 2010;72(C):31–53.
15. WHO. Eliminating soil-transmitted helminthiases as a public health problem
Authors’ contributions in children: progress report 2001–2010 and strategic plan 2011–2020.
JCD conducted the literature search, data collection and analysis. JCD and Geneva: World Health Organization; 2012.
HCT drafted the first version of the manuscript. JCD, HCT and RMA 16. WHO. Neglected tropical diseases - prevention, control, elimination and
contributed to the design of the study. JCD, HCT, AT and RMA contributed eradication. WHA 66.20. In: Sixty-Sixth World Health Assembly. Geneva:
to the writing of the paper. All authors read and approved the final version World Health Organization; 2013.
of the manuscript. 17. The London Declaration [http://unitingtocombatntds.org/resource/london-
declaration]. Accessed 14 May 2015.
18. WHO. In: Crompton D, Montresor A, Nesheim M, Savioli L, editors. Controlling
Acknowledgements disease due to helminth infections. Geneva: WHO; 2003.
Roy Anderson gratefully acknowledges funding of the NTD Modelling 19. WHO. Helminth control in school-age children - Second Edition. Geneva:
Consortium by the Bill and Melinda Gates Foundation in partnership with World Health Organization; 2012.
the Task Force for Global Health. The views, opinions, assumptions or any 20. WHO. PCT databank: soil-transmitted helminthiases. Geneva: World Health
other information set out in this article are solely those of the authors. Organization; 2014.
21. Anderson RM, Schad GA. Hookworm burdens and faecal egg counts: an analysis
Funding of the biological basis of variation. Trans R Soc Trop Med Hyg. 1985;79(6):812–25.
JCD and HCT are supported by the London Centre for Neglected Tropical 22. Anderson RM, Truscott JE, Easton A, Oliveira R, Brooker S, Hollingsworth D.
Disease Research (funded by GSK). RMA is supported by the Bill & Melinda How frequently and to whom should mass chemotherapy be administered
Gates Foundation (#OPP1053230).The funders had no role in study design, to control soil transmitted helminths? In: American Society for Tropical
data collection and analysis, decision to publish, or preparation of the Medicine and Hygiene Annual Meeting Presentations, November 2013.
manuscript. Washington DC, USA; 2013. 151.
23. Turner H, Truscott J, Bettis A, Shuford K, Dunn J, Hollingsworth T, et al. An
Author details economic evaluation of expanding hookworm control strategies to target
1
London Centre for Neglected Tropical Disease Research, London, UK. the whole community. Parasit Vectors. 2015;8(1):570.
2
Department of Infectious Disease Epidemiology, School of Public Health, 24. Boatin BA, Basañez MG, Prichard RK, Awadzi K, Barakat RM, Garcia HH, et al.
Faculty of Medicine, Imperial College London, London, UK. 3Worm Free A research agenda for helminth diseases of humans: towards control and
Myanmar Kids Program, Tun Khit Foundation, Yangon, Myanmar. elimination. PLoS Negl Trop Dis. 2012;6(4):e1547.
25. Brooker SJ, Nikolay B, Balabanova D, Pullan RL. Global feasibility assessment
Received: 12 November 2015 Accepted: 8 January 2016 of interrupting the transmission of soil-transmitted helminths: a statistical
modelling study. Lancet Infect Dis. 2015;15(8):941–50.
Dunn et al. Parasites & Vectors (2016) 9:31 Page 13 of 13

26. Global Partners are taking the “Neglect” out of “Neglected Tropical Diseases” 46. Anderson RM, May RM. Helminth infections of humans: mathematical
[http://www.gatesfoundation.org/Media-Center/Press-Releases/2014/04/ models, population dynamics, and control. Adv Parasitol. 1985;24.
Global-Partners-Are-Taking-the-Neglect-out-of-Neglected-Tropical-Diseases] 47. Sayasone S, Utzinger J, Akkhavong K, Odermatt P. Multiparasitism and
27. Lo NC, Bogoch II, Blackburn BG, Raso G, N’Goran EK, Coulibaly JT, et al. intensity of helminth infections in relation to symptoms and nutritional
Comparison of community-wide, integrated mass drug administration strategies status among children: a cross-sectional study in southern Lao People’s
for schistosomiasis and soil-transmitted helminthiasis: a cost-effectiveness Democratic Republic. Acta Trop. 2015;141(PB):322–31.
modelling study. Lancet Glob Health. 2015;3(10):e629–38. 48. Truscott J, Turner H, Anderson R. What impact will the achievement of the
28. Ohta N, Waikagul J. Disease burden and epidemiology of soil-transmitted current World Health Organization targets for anthelmintic treatment
helminthiases and schistosomiasis in Asia: the Japanese perspective. Trends coverage in children have on the intensity of soil transmitted helminth
Parasitol. 2007;23(1):30–5. infections? Parasit Vectors. 2015;8:551.
29. Truscott JE, Hollingsworth TD, Brooker SJ, Anderson RM. Can chemotherapy 49. Anderson RM, Turner HC, Truscott JE, Hollingsworth TD, Brooker SJ. Should
alone eliminate the transmission of soil transmitted helminths. Parasit the goal for the treatment of doil transmitted helminth (STH) infections be
Vectors. 2014;7(1):266. changed from morbidity control in children to community-wide
30. Levecke B, Behnke JM, Ajjampur SSR, Albonico M, Ame SM, Charlier J, et al. transmission elimination? PLoS Negl Trop Dis. 2015;9(8), e0003897.
A comparison of the sensitivity and fecal egg counts of the McMaster egg 50. Bradley M, Chandiwana SK, Bundy DAP. The epidemiology and control of
counting and Kato-Katz thick smear methods for soil-transmitted helminths. hookworm infection in the Burma Valley area of Zimbabwe. Trans R Soc
PLoS Negl Trop Dis. 2011;5(6):e1201. Trop Med Hyg. 1993;87(2):145–7.
31. Hürlimann E, Schur N, Boutsika K, Stensgaard A-S, Laserna de Himpsl M, 51. Yogore Jr M. Intestinal parasitism from health and welfare conditions at the
Ziegelbauer K, et al. Toward an open-access global database for mapping, Victorias Milling Company, Inc. Edited by Lara H. 1953.
control, and surveillance of neglected tropical diseases. PLoS Negl Trop Dis. 52. Sadun EH. Studies on the distribution and epidemiology of hookworm,
2011;5(12), e1404. Ascaris, and Trichuris in Thailand. Am J Epidemiol. 1955;62(2):116–55.
32. Jatanasen S. A brief survey of parasitic helminth in south Laos and 53. Sadun EH, Vajrasthira S. Studies on intestinal parasitic infections in Cholburi
Cambodia with a comparison to the state in Thailand. Jpn J Med Sci Biol. Province (Thailand). Am J Trop Med Hyg. 1953;2(2):286–97.
1961;14(5–6):257–62. 54. Bethony JM. Epidemiology and immunology of Necator americanus
33. Cross JH, Basaca-Sevilla V. Intestinal parasitic infections in Southeast Asia. infection in rural Thailand: the role of acquired immunity in determining
Southeast Asian J Trop Med. 1981;12(2):262–74. infection intensity. PhD Thesis: State University of New York at Buffalo; 1998.
34. Kabayashi J, Socheat D, Phommasack B, Tun A, Huy Nga N. The Asian 55. Preuksaraj S, Jeradit C, Sathitayathai A, Kijvannee S, Seedonrusmi T. Studies
Center of International Parasite Control (ACIPAC): Five years of achievement. on prevalence and intensity of intestinal helminthic infections in the rural
IV: Activities in partner countries (Cambodia, Lao PDR, Myanmar and population of Thailand 1980–1981. Collected papers on the control of
Vietnam): small scale pilot project (SSPP) and other impacts. Southeast Asian soil-transmitted helminthiases. 1983;2:54–8.
J Trop Med. 2005;36(S3):28–40. 56. Pegelow K, Gross R, Pietrzik K, Lukito W, Richards AL, Fryauff DJ. Parasitological
35. Sayasone S, Utzinger J, Akkhavong K, Odermatt P. Repeated stool sampling and nutritional situation of school children in the Sukaraja district, West Java,
and use of multiple techniques enhance the sensitivity of helminth Indonesia. Southeast Asian J Trop Med. 1997;28(1):173–90.
diagnosis: a cross-sectional survey in southern Lao People’s Democratic 57. Al-Mekhlafi MSH, Azlin M, Aini UN, Shaikh A, Sa’iah A, Fatmah MS, et al.
Republic. Acta Trop. 2015;141(PB):315–21. Prevalence and distribution of soil-transmitted helminthiases among Orang
36. Tarafder MR, Carabin H, Joseph L, Balolong Jr E, Olveda R, McGarvey ST. Asli children living in peripheral Selangor, Malaysia. Southeast Asian J Trop
Estimating the sensitivity and specificity of Kato-Katz stool examination Med. 2006;37(1):40–7.
technique for detection of hookworms, Ascaris lumbricoides and Trichuris 58. Norhayati M, Zainudin B, Mohammod CG, Oothuman P, Azizi O, Fatmah MS.
trichiura infections in humans in the absence of a ‘gold standard’. Int J The prevalence of Trichuris, Ascaris and hookworm infection in Orang Asli
Parasitol. 2010;40(4):399–404. children. Southeast Asian J Trop Med. 1997;28(1):161–8.
37. Nikolay B, Brooker SJ, Pullan RL. Sensitivity of diagnostic tests for human 59. Rahman WA. Helminthic infections of urban and rural schoolchildren in
soil-transmitted helminth infections: a meta-analysis in the absence of a Penang Island, Malaysia: implications for control. Southeast Asian J Trop
true gold standard. Int J Parasitol. 2014;44(11):765–74. Med. 1998;29(3):596–8.
38. Schär F, Odermatt P, Khieu V, Panning M, Duong S, Muth S, et al. Evaluation 60. Joe LK, Siang TK. Human intestinal helminths obtained from autopsies in
of real-time PCR for Strongyloides stercoralis and hookworm as diagnostic tool Djakarta. Indonesia Am J Trop Med Hyg. 1959;8(4):122–5.
in asymptomatic schoolchildren in Cambodia. Acta Trop. 2013;126(2):89–92. 61. Hlaing T, Than S, Htay Htay A, Myint L, Thein Maung M. Epidemiology and
transmission dynamics of Ascaris lumbricoides in Okpo village, rural Burma.
39. Wiria AE, Hamid F, Wammes LJ, Kaisar MMM, May L, Prasetyani MA, et al.
Trans R Soc Trop Med Hyg. 1984;78(4):497–504.
The Effect of Three-Monthly Albendazole Treatment on Malarial Parasitemia
62. Tu M, El-Zawahry MM, Kyi DO, Hlaing K, Hla-Gyaw S, Kyaw-Myint, et al.
and Allergy: A Household-Based Cluster-Randomized, Double-Blind,
Epidemiological features of intestinal parasitoses in the inhabitants of Okpo
Placebo-Controlled Trial. PLoS ONE. 2013;8(3):e57899.
village, Burma. Union Burma J Life Sci. 1970;3:247–67.
40. Gordon CA, McManus DP, Acosta LP, Olveda RM, Williams GM, Ross AG, et
63. Hpay D, El-Zawahry MM, Maung L, Kyi DO, Dwe RS, Sein T, et al.
al. Multiplex real-time PCR monitoring of intestinal helminths in humans
Epidemiological features of intestinal parasitoses in Dayebo village, Burma.
reveals widespread polyparasitism in Northern Samar, the Philippines. Int J
Union Burma J Life Sci. 1970;3:289–307.
Parasitol. 2015;45(7):477–83.
64. Croll NA, Anderson RM, Gyorkos TW, Ghadirian E. The population biology
41. King E, Kim H, Dang N, Michael E, Drake L, Needham C, et al. Immuno‐
and control of Ascaris lumbricoides in a rural community in Iran. Trans R Soc
epidemiology of Ascaris lumbricoides infection in a high transmission
Trop Med Hyg. 1982;76(2):187–97.
community: antibody responses and their impact on current and future
65. Becker SL, Lohourignon LK, Speich B, Rinaldi L, Knopp S, N’Goran EK, et al.
infection intensity. Parasite Immunol. 2005;27(3):89–96.
Comparison of the Flotac-400 dual technique and the formalin-ether
42. Speich B, Ali SM, Ame SM, Albonico M, Utzinger J, Keiser J. Quality control
concentration technique for diagnosis of human intestinal protozoon
in the diagnosis of Trichuris trichiura and Ascaris lumbricoides using the
infection. J Clin Microbiol. 2011;49(6):2183–90.
Kato-Katz technique: experience from three randomised controlled trials.
66. Sinniah B. Daily egg production of Ascaris lumbricoides: the distribution of eggs
Parasit Vectors. 2015;8(82):25652120.
in the faeces and the variability of egg counts. Parasitol. 1982;84(1):167–75.
43. Papier K, Williams GM, Luceres-Catubig R, Ahmed F, Olveda RM, McManus
DP, et al. Childhood malnutrition and parasitic helminth interactions. Clin
Infect Dis. 2014;59(2):234–43.
44. Anderson RM, Truscott JE, Pullan RL, Brooker SJ, Hollingsworth TD. How
effective is school-based deworming for the community-wide control of
soil-transmitted helminths? PLoS Negl Trop Dis. 2013;7(2), e2027.
45. Pullan RL, Kabatereine NB, Quinnell RJ, Brooker S. Spatial and genetic
epidemiology of hookworm in a rural community in Uganda. PLoS Negl
Trop Dis. 2010;4(6):e713.