epidemiology of soil-transmitted nematode infections in ha nam province, vietnam

Tropical Medicine and International Health

volume 3 no 11 pp 904–912 november 1998

© 1998 Blackwell Science Ltd904

Epidemiology of soil-transmitted nematode infections in HaNam Province,Vietnam

Cathy Needham1, Hoang Thi Kim2, Nguyen Viet Hoa2, Le Dinh Cong2, Edwin Michael1, Lesley Drake1,Andrew Hall1 and Donald A. P. Bundy1

1 Wellcome Trust Centre for the Epidemiology of Infectious Disease, University of Oxford, UK

2 Institute of Malariology, Parasitology and Entomology, Tu Liem, Hanoi, Vietnam

Summary Baseline epidemiological data are presented from a parasitological survey conducted in Thuy Loi commune,

Ha Nam province, Vietnam; a farming community where night soil is routinely used as fertilizer for crops.

177 households were visited and 543 individuals (aged 1–88 years) recruited to the study. Helminth infection

intensity was assessed by Kato-Katz to determine the density of parasite eggs per gram of stool (epg).

Ascaris lumbricoides, Trichuris trichiura and hookworm infections were the only species detected. 83% of

individuals were infected with A. lumbricoides (mean epg 5 11971), 94% with T. trichiura (mean

epg 5 793) and 59% with hookworm (mean epg 5 302). Age-dependent patterns of infection prevalence and

intensity were similar for A. lumbricoides and T. trichiura, but markedly different for hookworm infection.

Similarly, age-dependency in the k-values for the three infections was due to covariance with the respective

mean intensities with age rather than to independent age effects, with similar patterns for A. lumbricoides

and T. trichiura, and a different pattern for hookworm. Three major conclusions can be drawn from the

multiple-species analyses: There is positive interaction between A. lumbricoides and T. trichiura infections;

high-intensity A. lumbricoides infections are significantly associated with high-intensity T. trichiura

infections; and there is positive interaction between these two species such that infection intensity of A.

lumbricoides is higher in individuals with concurrent T. trichiura infection than in individuals without and

vice versa.

keywords Ascaris lumbricoides, Trichuris trichiura, hookworm, aggregation, multiple-species

correspondence Professor D. A. P. Bundy, The Wellcome Trust Centre for the Epidemiology of Infectious

Disease, Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, UK. E-mail:

[email protected]

Introduction

Soil-transmitted nematode infections are highly prevalent in

Vietnam. In northern and central provinces up to 100% of

individuals in some areas may be infected with Ascaris

lumbricoides or Trichuris trichiura, whereas in the south

infection prevalences are lower. In contrast, hookworm

infection occurs at moderate to high prevalence levels

throughout the country, with no marked geographical trend

(Toan 1991; Dr Hoang Thi Kim, unpublished observation).

The geographical distributions of the major soil-

transmitted nematode infections in northern Vietnam suggest

that many areas will be coendemic for these species. It is

likely that such multiple infections may lead to enhanced

morbidity (Abdel-Aal et al. 1970; Buck et al. 1978). Helmiths

may also exhibit specific associations with other helminth

species (Haswell-Elkins et al. 1987; Chamone et al. 1990;

Booth & Bundy 1995; Booth et al. 1996), which may provide

insights into the determinants of multiple species infection

and have implications for the approach to combined control.

The aims of this study were to describe the epidemiological

characteristics of, and to examine the relationships and

associations between soil-transmitted nematode infections in

a northern Vietnam community. This study forms the first

phase of an immunoepidemiological study of reinfection

with soil-transmitted nematodes in Vietnam, which is

intended to support the activities of the Vietnam Partnership

for Child Development.

TMIH324

Tropical Medicine and International Health volume 3 no 11 pp 904–912 november 1998

C. Needham et al. Soil-transmitted nematodes in Vietnam

Methods

Study area and population

The study was conducted in Thuy Loi commune, Kim Bang

District, Ha Nam Province, which is situated approximately

70 km south of Hanoi in northern rural Vietnam. With a total

population of about 4500, Thuy Loi is a farming community

where human faeces, or nightsoil, is routinely used as fertilizer.

High rainfall and warm temperatures results in lush vegetation

and good conditions for rice and vegetable farming in this area.

Houses in the commune are typically made of stone and

cement, with earth, cement or brick floors. There is no piped

water and only a few houses have electricity.

Study design and protocol

All households within a certain area in the commune were

visited, and all occupants were encouraged to participate in

the study. Willingness to participate and compliance were a

priority as this survey formed the baseline survey of a

longitudinal immunoepidemiological study. For each

household, a questionnaire was completed to record potential

household-related risk factors for helminth infection.

Occupants were asked to provide a stool sample for

microscopical examination and for each individual recruited to

the study, a questionnaire was completed giving details of

potential risk factors for infection at individual level. The

Kato-Katz technique was used to estimate helminth infection

intensity by counting the number of parasite eggs in 50 mg of

stool, with 10% of slides re-examined as quality control. Slides

were prepared immediately on receipt of each stool sample and

examined on the same day.

Data analysis

The aims of this study were to firstly describe the epidemiology

of A. lumbricoides, T. trichiura and hookworm infections in

the study site, and secondly to examine the interactions

between these helminths in individuals.

Age-infection patterns

Age-prevalences of each helminth infection (as assessed by egg

counts) were analysed using logistic regression (Kleinbaum

et al. 1982). The analysis of the effects of age and gender on

egg intensity data, however, required consideration of the

significant overdispersion in the data. We addressed this

empirically using quasi-likelihood Poisson regression models,

which estimate and use the overdispersion parameter from such

data to provide statistically valid tests for the significance of

posited predictors (McCullagh & Nelder 1991). Note that the

intention here is not to examine how the extra-variation in the

data is brought about but simply to statistically account for

such variation in the data analysis.

Egg count frequency distributions

To be consistent and for comparisons with previous work, this

was studied via the fits of the negative binomial probability

distribution model to the observed egg count data (Anderson

1982; Bundy & Cooper 1989; Guyatt et al. 1990). Stepwise

regression was used to ascertain if the dispersion parameter k

from this model (and thus overdispersion) varied with age

independently of the mean egg count (an independent increase

in k with age for instance would be indicative of the operation

of acquired immunity (Woolhouse et al. 1994; Grenfell et al.

1995).

Multiple–infection interactions

These were studied by the construction of the appropriate

Poisson log-linear models, contingency tables and in the case of

egg intensity data (logarithmically transformed), by the

analysis of variance as detailed in the Results section below.

Results

Characteristics of the study sample and area

We visited 177 households and recruited 543 individuals to the

study (71% compliance). Descriptive analysis of the question-

naire data revealed the following reported characteristics of the

study site and sample:

91% of households had a latrine with all occupants using

the household latrine if present.

92% of households grew their own vegetables, and of these

93% used night soil as fertilizer in household gardens.

Rainwater was the principal source of drinking water (76%

of households) and reported to be boiled in all cases before

drinking.

96% of children aged 5–15 attended school and all schools

had latrines.

92% of adults with an occupation were farmers, and all

farmers used night soil as a fertilizer in the field. 98% of

farmers did not wear shoes in the fields and 76% of farmers

defecated outside when working.

91% of individuals had been treated for worms at some

stage using locally available anthelmintics, with 1% reporting

treatment within the last 6 months. Treatment was

predominantly self-administered.

Parasitology

Table 1 summarizes the prevalence and intensity of helminth

infections in Thuy Loi commune. Ascaris lumbricoides,

© 1998 Blackwell Science Ltd 905




Trichuris trichiura and hookworm infections were the only

helminth species found, with prevalences of 83%, 94% and

59%, respectively. Mean egg counts were moderate for A.

lumbricoides and light for T. trichiura and hookworm

infections. The species of hookworm infection was not

determined in this study, however, previous studies have shown

that over 95% of hookworm infections in north Vietnam are

Necator americanus (Nguyen Thi Kim, personal

communication).

Age- and sex-dependent infection prevalence and intensity

Figure 1 shows the age patterns of A. lumbricoides, T.

trichiura and hookworm prevalence. A. lumbricoides and T.

trichiura exhibit very similar profiles with 80% of children

infected by the age of 5, and a high proportion of individuals

infected in all age classes. In contrast, the proportion of those

infected with hookworm increases with age to reach a plateau

after the age of 20. Logistic regression analysis showed no

significant relationship between host age and prevalence of A.

lumbricoides (P 5 0.46) or T. trichiura infection (P 5 0.25),

whereas there was a highly significant relationship between

host age and hookworm prevalence (P 5 0.0001). There was

no significant relationship between host sex and infection

prevalence (A. lumbricoides, P 5 0.06; T. trichiura, P 5 0.34;

hookworm, P 5 0.11).

The age profiles of infection intensity are also similar for A.

lumbricoides and T. trichiura, with peak egg counts in school-

age children (Figure 2a,b). For hookworm infection, egg counts

increased steadily with host age, reaching maximal levels in the

oldest age group (Figure 2c). Poisson regression using quasi-

likelihood estimation to account for overdispersion in the data

(McCullagh & Nelder 1991) showed no significant effects of

host sex on egg intensity of A. lumbricoides (P 5 0.61) or T.

trichiura (P 5 0.76) infection, but a significantly higher

hookworm egg intensity in females than in males (P 5 0.007;

Figure 2c). Egg counts varied significantly with age in a

nonlinear fashion for all three infections: A. lumbricoides,

P 5 0.0004; T. trichiura, P 5 0.0004; hookworm, P 5 0.001.

Frequency distributions of egg counts and comparison of age-

intensity with age-k

The frequency distributions of egg counts for all three

infections are typically aggregated (not shown) and can be

described empirically by the negative binomial distribution in

which the parameter ‘k’ is an inverse measure of the degree of

aggregation (Bliss & Fisher 1953). For each species, k was

estimated by maximum likelihood for all data and within each

age class. The degree of aggregation for A. lumbricoides

(k 5 0.297) and hookworm (k 5 0.217) is similar to estimates

of k derived from other studies. A k-value of 0.592 for T.

trichiura in our study is slightly higher (5 less aggregated)

than values estimated from other studies (Bundy & Cooper

1989).

A comparison of age-dependent changes in parasite

aggregation and intensity (Figure 3), shows a remarkable

similarity between the age-profiles of k and the age-profiles of

egg intensity for each of the three species. Stepwise regression

was used to determine whether there were any independent

effects of age on k (Table 2). The results support the

impression given in Figure 3 that the age-dependency in the

k-values for the three infections is due to covariance with the

respective mean egg intensities with age rather than

independent age effects.

Multiple species infection prevalence

A high prevalence for individual species typically leads to a

high proportion of individuals concurrently infected with

more than one species. Table 3 shows that 47.7% of the

Table 1 Summary of helminth infections in Thuy Loi Commune

Prevalence Intensity (epg)

———————

Mean S.D. Max.

A. lumbricoides 83.4% 11971.9 18676.9 173604

T. trichiura 94.3% 00793.1 01208.2 008880

Hookworm 59.1% 00302.7 00698.8 008473

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100

00

Mean age (years)

10

50

90

50

40

30

20

10 20 30 40

Pre

vala

nce

(%

) 70

80

60

Figure 1 Age-dependent infection prevalence for A. lumbricoides

(m ), T. trichiura (j) and hookworm (d). Sample sizes are as

follows: 0–4 years, n 5 26; 5–9 years, n 5 98; 10–14 years,

n 5 87; 15–29 years, n 5 92; 30–44 years, n 5 154; $45 years,

n 5 86.




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Figure 2 Age-dependent infection intensity (as assessed by density

of eggs per gram of stool; epg) for (a) A. lumbricoides, (b) T.

trichiura and (c) hookworm. s all individuals; d females; j males.

Vertical bars represent standard errors of the mean values. For

sample sizes, refer to legend of Figure 1.

Figure 3 Age-dependency of the negative binomial distribution

parameter ‘k’(d) for (a) A. lumbricoides, (b) T. trichiura and (c)

hookworm infection. For comparative purposes, age-intensity

profiles are overlaid for each (j, dotted line). Vertical bars represent

standard errors of the mean values. For sample sizes, refer to legend

of Figure 1.




sample harboured all three infections, with 32.2%

harbouring both A. lumbricoides and T. trichiura infections.

Poisson log linear analysis was used to test specifically for

interactions between species prevalence (Table 4) (Booth &

Bundy 1995). There were no significant interactions between

hookworm infection and either A. lumbricoides or T.

trichiura, suggesting that hookworm infections occurred

largely independently of the other two species. In contrast, a

statistically significant interaction is evident between A.

lumbricoides and T. trichiura infections, with a greater

probability of concurrent infection than would be expected

by chance.

Multiple species infection intensity

For each pair of infections (A. lumbricoides-T. trichiura

(n 5 434); A. lumbricoides-hookworm (n = 269); T.

trichiura-hookworm (n 5 307)), egg counts from individuals

were arbitrarily categorized according to the method used by

Forrester et al. (1988), with ‘high’ infection defined as egg

counts in the top 20% of the range for each species. The

nature of the association between ‘high’ infection with one

species and ‘high’ infection with the other, for each paired

infection, was investigated using contingency tables and x2

analysis (Table 5). If high egg counts were associated

randomly with each other (i.e. . if a ‘high’ infection of one

species was equally likely to be associated with a ‘high’ or not

‘high’ infection for the other), then there would be no

significant difference between observed and expected values.

Table 5 shows that ‘high’ A. lumbricoides infections are

significantly more likely to be associated with ‘high’ T.

trichiura than would be expected by chance.

The effect of concurrent infection on mean egg intensities

is shown in Figure 4. Mean A. lumbricoides egg intensity is

significantly higher in individuals with dual A. lumbricoides/

T. trichiura infections than in individuals without concurrent

T. trichiura infection (Figure 4a). The converse is also true –,

i.e. that mean T. trichiura egg intensity is significantly

higher in individuals with dual A. lumbricoides/T. trichiura

infections than in individuals without a concurrent A.

lumbricoides infection. There are no significant differences in

host age between these groups.

For A. lumbricoides and hookworm, mean egg intensity of

A. lumbricoides is significantly lower in dual infections than

in infections without concurrent hookworm (Figure 4b),

whereas there is no effect of the presence of A. lumbricoides

on the mean intensity of hookworm. However, there is a

highly significant difference in host age between these two

groups, with the majority of A. lumbricoides/no hookworm

infections occurring in young individuals as would be

expected from the differing age-profiles of these species. For

T. trichiura and hookworm, there is no significant effect of

the presence of one species on the mean intensity of the other

(Figure 4c). Again, there is a significant age effect, with T.

trichiura/no hookworm infections occurring in younger

individuals than dual T. trichiura/hookworm infections.

Discussion

Soil-transmitted nematode infections are highly prevalent in

this rural community. This high prevalence occurs in spite of

high levels of drug treatment and the fact that latrines are

common and reportedly well used both in households and in

schools. However, the environmental and climatic conditions

in the community favour transmission, and farming practises

(especially the routine use of night soil as fertilizer), are likely

Table 2 Stepwise regression analysis of the relationships between the degree of aggregation (k) and the mean intensity of infection, host age

and the interaction between intensity and age, for A. lumbricoides, T. trichiura and hookworm infections (n 5 543)

Factor d.f. A. lumbricoides T. trichiura Hookworm

——————————— ——————————— ———————————

F P F P F P

Mean intensity 1,5 49.23 0.0009 85.99 0.0003 20.07 0.007

Age 1,4 05.54 0.1100 01.01 00.38000 03.87 0.140

Mean intensity 3 age 1,3 02.15 0.2400 03.34 00.17000 08.29 0.060

Table 3 Contingency table showing observed and expected (in

parentheses) prevalences of single and multiple infections (expressed

as percentage) for all individuals (n 5 543)

A. lumbricoides

—————————————

Hookworm T. trichiura Present Absent

Present Present 47.7 (47.2) 8.8 (9.4)

Absent 01.8 0(2.2) 0.7 (0.4)

Absent Present 32.2 (31.5) 5.5 (6.3)

Absent 01.7 0(2.6) 1.5 (0.6)




to expose most people to faecal-borne, soil-transmitted

nematode infections.

The epidemiological characteristics of A. lumbricoides,

T. trichiura and hookworm infection with respect to host

age are typical of those described elsewhere, with peak

infection intensity occurring in school-aged children for

A. lumbricoides and T. trichiura, and in adults for hook-

worm (Elkins et al. 1986; Bundy et al. 1987; Pritchard et al.

1990; Bradley et al. 1992). Paradoxically, convexity in age-

intensity patterns occurs for A. lumbricoides and T. trichiura

in this community despite the very high transmission and

despite the exceptional exposure of adults. This could reflect

the operation of density-dependent factors, such as acquired

immunity, although the analysis of between-host variability

in egg counts by age (as discussed below) suggests that other

factors may also need to be considered in explaining the egg

count patterns.

Interestingly, hookworm egg counts were higher in adult

females than in males. This contrasts with the typical pattern,

such as that observed by Bradley et al. (1992) and Pritchard

et al. (1990), where on average, males exhibited higher worm

burdens than females. Why this is so, is unclear. There appear

to be no occupational biases in this Vietnam community: over

90% of adult women and men are farmers and thus both

sexes are likely to be highly (and equally?) exposed to hook-

worm larvae in the rice fields. The alternative hypothesis –

that hormonal-induced immunosuppression increases sus-

ceptibility in women especially during pregnancy, is plausible

but unlikely to be the dominant factor in this community, as

birth rates are low. The study sample was not truly random

by design as compliance and willingness to participate in the

study were a priority, given that this survey formed the initial

phase of a longitudinal immuno-epidemiological study. This

resulted in a slight over-representation of females (mothers)

in the 25–44 year age classes, suggesting that the documented

adult female bias in hookworm egg intensity in this study

may also reflect peculiarities of sampling. Whatever the

cause, it is clear that the present observation may have

important public health significance for north Vietnam as

females tend to suffer more serious manifestations of hook-

worm infection than males (Miller 1979; Bundy 1988). More

detailed studies in the area of gender-related predisposition

to infection are clearly required in Vietnam.

The degree of aggregation (k) of the three species in Thuy

Loi commune is similar to previous estimates of k (Bundy &

Cooper 1989), with the exception that the frequency

distribution for T. trichiura is slightly less aggregated than

that observed elsewhere. This may be due to the very high

prevalence of T. trichiura in this community, as k is highly

variable at such prevalences (Guyatt et al. 1990). The use of

egg count data in the present study may also affect

comparisons with other studies.

Our study has shown that for A. lumbricoides, T. trichiura

and hookworm infections in the same community, the age-

dependency in k-values is due to covariance with the

respective mean intensities, with similar patterns for

A. lumbricoides and T. trichiura, and a different pattern for

hookworm. Many processes may underlie these patterns in

aggregation (Woolhouse et al. 1994; Grenfell et al. 1995;

Michael et al. 1998). In the present study, although generated

Table 4 Interactions between species prevalence: Poisson log-linear model results. Note that the sign of the regression coefficient of the model

indicates the direction of the specific parasite association

Regression Likelihood

Interaction d.f. coefficient ratio statistic P

A. lumbricoides 1 T. trichiura 1 20.302 9.24 0.002

A. lumbricoides 1 hookworm 1 20.090 0.08 0.778

T. trichiura 1 hookworm 1 20.181 2.60 0.107

A. lumbricoides 1 T. trichiura + hookworm 1 20.109 1.21 0.270

Table 5 Observed and expected numbers of individuals with ‘high’ infection for species in paired infections with A. lumbricoides and

hookworm (n 5 269), A. lumbricoides and T. trichiura (n 5 434) and T. trichiura and hookworm (n 5 307). ‘High’ is defined as egg counts in

the top 20% of the range observed for each species. The observed occurrence of paired ‘high’ is compared with expected values using x2 statistic

(degrees of freedom 5 1)

Infection pairs Observed Expected x2 P

A. lumbricoides ‘high’ – T. trichiura ‘high’ 40 17.4 29.4 0.001

A. lumbricoides ‘high’ – hookworm ‘high’ 15 10.8 1.63 0.25

T. trichiura ‘high’ – hookworm ‘high’ 16 12.1 1.26 0.50




1400

0TH

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Figure 4 Comparison of mean infection intensity and host age in (a) A. lumbricoides [A] – hookworm [H] dual infections and A no H, or H no

A infections, and similarly for (b) A. lumbricoides [A] – T. trichiura [T] and (c) T. trichiura [T] – hookworm [H] combinations. Sample sizes are

as follows: AH, n 5 269; A no H, n 5 184; H no A, n 5 52; AT, n 5 434; A no T, n 5 19; T no A, n 5 78; TH, n 5 307; T no H, n 5 205; H no

T, n 5 14. Vertical bars represent standard errors of the mean values. Infection intensity and host age were compared statistically between

groups using the Mann Whitney test; P-values are given in the boxes.



from a relatively small sample where sampling biases may be

significant, the trend of decreasing infection intensity and

increasing aggregation observed after the peak in infection

intensity in children for A. lumbricoides and T. trichiura may

reflect either the consequence of an age-dependent exposure

or infection rate or of two groups diverging in immunological

heterogeneity with age (Anderson 1982; Bundy et al. 1988;

Grenfell et al. 1995). The latter hypothesis is currently being

investigated empirically in these individuals.

Three main conclusions may be drawn from the

examination of the associations between species. Firstly, in

accordance with previous studies (Booth & Bundy 1995;

Booth et al. 1996), a statistically significant relationship is

evident between A. lumbricoides and T. trichiura prevalence.

This means that an individual infected with A. lumbricoides

is more likely to be infected with T. trichiura than would be

expected by chance, and vice versa. In contrast, infection with

hookworm was largely independent of the other two species.

Secondly, for those individuals harbouring dual A.

lumbricoides/T. trichiura infections (i.e. eliminating indi-

viduals uninfected with either species), ‘high’ A. lumbricoides

infections are significantly more likely to be associated with

‘high’ T. trichiura infections than would be expected by

chance. Previous studies have used rank correlation analyses

to investigate the relationship between the intensity of two

concurrent infections, and many have reported highly sig-

nificant correlations between the intensity of A. lumbricoides

and T. trichiura (Haswell-Elkins et al. 1987; Holland et al.

1989; Robertson et al. 1989). The analysis used in this paper

specifically tests for associations between defined ‘high’

infections of two species by adopting the arbitrary cut off

used by Forrester et al. (1988). Again, no similar trends were

observed for associations with hookworm infection.

These results can be interpreted in a number of ways. The

population dynamics of A. lumbricoides and T. trichiura are

similar: both species are transmitted via the faecal-oral route.

In a community such as Thuy Loi commune, where both

species are endemic, behavioural patterns and social factors

leading to risk of infection with one species are likely to

lead simultaneously to infection with the other. Similar

epidemiological characteristics of A. lumbricoides and T.

trichiura will act to concentrate the infection intensity within

certain groups of individuals. Therefore associations between

A. lumbricoides and T. trichiura are perhaps not surprising,

compared to the lack of associations between these infections

and hookworm infection, where transmission occurs via the

percutaneous route and the epidemiological characteristics

are different.

The third and perhaps most interesting conclusion, partly

predictable from the analysis of the paired-species ‘high’

infections above, is that infection intensity of A. lumbricoides

is significantly higher in individuals with concurrent T.

trichiura infection than in those without concurrent T.

trichiura infection and vice versa. There are no differences in

host age between these groups. This may merely reflect the

similar routes of transmission for these parasites: people

build up heavy infections with both because they get infected

the same way, or it could imply a two–way synergistic

interaction such that the presence of one species favours the

survival, growth or fecundity of the second species. In this

respect, as A. lumbricoides and T. trichiura occupy different

spatial locations in the gut, it is unlikely that competitive

factors play a role, which suggests that the most plausible

mechanisms could be cross-immunity or the inducement of a

general nonspecific immunosuppressive response. Whatever

the mechanism, the implication is that parasite transmission

and host morbidity is likely to be greater in individuals with

dual infections. A caveat in this analysis is the unbalanced

sample due to the high prevalence of A. lumbricoides and T.

trichiura in the community; however, similar findings have

been reported in children by Slade (1991), where infection

prevalences were lower and sample sizes were more balanced.

Interestingly, the presence of hookworm infection appears to

have a negative effect on concurrent A. lumbricoides infection

intensity. However, this is likely to be a consequence of the

highly significant age difference between these groups;

individuals without hookworm are younger and have higher

A. lumbricoides infection intensity.

To summarize, as elsewhere, descriptive analyses in a high-

transmission community of northern Vietnam have shown

similarities between the epidemiological characteristics of A.

lumbricoides and T. trichiura on the one hand and

hookworm infection on the other. In accordance with

previous work, we found positive associations between the

prevalence and intensity of A. lumbricoides and T. trichiura,

in marked contrast to a negative association between

hookworm and these parasite species. Individuals with

simultaneously high intensities of infections of more than

one parasite species are at risk of morbidity associated with

each species, and possibly at risk of greater morbidity since

there may be synergism in pathogenesis. These results

confirm the good sense of the school-based community

treatment approach, and why the Partnership for Child

Development is relevant for Vietnam, particularly in areas of

high Ascaris and Trichuris transmission. Studies are now

required to investigate whether morbidity is indeed greater in

those individuals with dual infections, and whether the

associations described in this study persist after effective

treatment and a period of natural reinfection.

Acknowledgements

We gratefully acknowledge the Wellcome Trust for financial

support of this study. The study was carried out under the





auspices of the Vietnam Partnership for Child Development

programme. The hard work, enthusiasm and commitment of

many individuals in Vietnam made this study possible. In

particular, we thank Nguyen Thi Dang, Nguyen Thi Loan,

Nguyen Thi Mai, Nguyen Thi Duc and Hoang Van Tan from

IMPE; Nguyen Thi Hanh and Nguyen Thi Hoa from Ha

Nam Province; Nguyen Thi Van and Nguyen Thi Phin from

Kim Bang District; and Hoang Thi Nhan, Nguyen Thi

Nhuan, Nguyen Thi Chu and Nguyen Thi Xuyen from

Thuy Loi Commune. E.M. is a recipient of a MRC

Fellowship.

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