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TMIH549

Tropical Medicine and International Health

volume 5 no 4 pp 302–307 april 2000

Prevalence and distribution of soil-transmitted helminth (STH)


infections in urban and indigenous schoolchildren in Ortigueira,
State of Paranà, Brasil: implications for control
Carla Scolari1, Carlo Torti1, Anna Beltrame1, Alberto Matteelli1, Francesco Castelli1, Maurizio Gulletta1,
Milton Ribas2, Serenella Morana3 and Carlo Urbani4
1 Department of Infectious and Tropical Diseases, University of Brescia, Italy
2 Hospital Sao Francisco, Fundacao Médica Assistencial dos Trabalhadores Rurais de Ortigueira, Brazil
3 Department of Obstetrics and Gynecology, University of Pavia, Italy
4 Service of Infectious and Tropical Diseases, General Hospital of Macerata, Italy

Summary Soil-transmitted helminth (STH) infections represent a major public health problem in poor and developing
countries. During the period September-October 1998 we conducted an epidemiological survey of STH
infections in schoolchildren of an urban area (group A) and an indigenous reserve (group B), in the Muni-
cipality of Ortigueira, State of Paranà, Brazil, to assess potential benefits of mass treatment. Stool samples
were examined for helminth eggs by quantitative (Kato-Katz) technique to determine the prevalence and
intensity of intestinal parasitic infection. Moreover, we examined the relationship between prevalence and
intensity of STH infections and housing/hygienic factors (by means of a 7-item questionnaire). 236 school-
children aged 5–15 years were enrolled, 136 in group A and 100 in group B. The prevalence of STH infections
was significantly higher in group B (93%) than in group A (22%) (P , 0.001). Detected parasites were: A.
lumbricoides (16.1% prevalence in group A, 88% in group B, P , 0.001), hookworms (5.8% in group A,
52% in group B, P , 0.001) and T. trichiura (5.1% in group A, 2% in group B, P 5 0.2). Heavy infections
were detected in 2.9% and 23% of the children in group A and B, respectively (P , 0.001). Housing/hygienic
indicators were significantly poorer in group B. A statistically significant correlation was observed between
total prevalence of STH infections and prevalence of high-intensity infections with most housing/hygienic
variables. On the basis of these results, mass treatment and educational interventions were suggested for the
indigenous community, whereas target treatment and educational interventions were suggested for the urban
community. Even in a geographically homogeneous area different epidemiological realities can be found,
which in turn can influence infection levels and control programmes.

keywords soil-transmitted helminthiasis, epidemiologic survey, control, schoolchildren, Brazil

correspondence Dr Francesco Castelli, Department of Infectious and Tropical Diseases, University of


Brescia. P. le Spedali Civili 1, 25125 Brescia. Italy. E-mail: castelli@master.cci.unibs.it

1997; Geissier et al. 1998; Machado & Costa-Cruz 1998;


Introduction
Olsen 1998).
The World Health Organization (WHO) estimates that more High incidence of parasitic infections and polyparasitism
than one billion of the world’s population is chronically affect the health status (Savioli et al. 1992; Albonico et al.
affected by STH infections, which are closely correlated with 1998; Ferreira et al. 1998). In particular, there is evidence to
poverty, poor environmental hygiene and impoverished health support the relationship between helminth infections, malnu-
services. Intestinal helmintiases are among the most common trition and child development, with negative consequences for
communicable disease of school-age children in certain com- cognitive function and learning ability (Crompton 1992;
munities and tend to occur at highest intensity in this age Nokes & Bundy 1994; Oberhelman et al. 1998; Ray 1998;
group (Albonico et al. 1993; Menan et al. 1997; Urbani et al. Saldiva et al. 1999).

302 © 2000 Blackwell Science Ltd


13653156, 2000, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-3156.2000.00549.x by Republic of Moldova Hinari NPL, Wiley Online Library on [30/10/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Tropical Medicine and International Health volume 5 no 4 pp 302–307 april 2000

C. Scolari et al. Soil-transmitted helminth infections in schoolchildren in Ortigueira, Brasil

The WHO has developed a clear policy for the control of A questionnaire composed of seven questions to assess
STH infections (Montresor et al. 1998), recommending that housing/hygienic indicators (i.e. number of cohabiting
any programme aimed at controlling morbidity due to STH people, number of rooms in the house, presence of toilet, in-
infections should begin with a baseline survey. Baseline sur- or outside toilet, sharing the latrine or not, presence of safe
veys provide a sound basis for estimating current status and water, presence of sewage) was filled for each subject. These
needs for future interventions and produce essential data to specific questions were chosen as easily verifiable indicators
guide the development of control programmes at national, of hygienic conditions, rather than as specific risk factors for
regional and district levels (Montresor et al. 1998). Childhood STH infections. Safe water was defined as running treated
diarrhoea has been recognized as public health priority in water. The ratio number of people per house/number of
Ortigueira Municipality, especially among local indio com- rooms per house (i.e. index of overcrowding) has been con-
munities. The main cause was believed to be STH infections, sidered in the analysis. The threshold of 2 for this ratio was
but no data were available to guide public health inter- chosen as it represented the median value for the frequency
ventions. Therefore we conducted an epidemiologic survey to distribution.
determine what kind of interventions should be performed. A field assistant who knew every person in their school
verified answers of the children to the questionnaire. Chil-
dren’s addresses were recorded in order to conduct a sub-
Materials and methods
group analysis within the urban population, with the
The study was conducted in Ortigueira, with 2548 km2 one of objective of verifying any difference between children living
the largest municipalities of Paranà State. The estimated in a large suburban shanty town called Vila Andradina and
number of inhabitants is 55 000, 76% living in rural areas. An other urban children. Sex and age were also recorded for each
indigenous reserve with a population of 400 Queimadas child. Age of each child was verified in the schools’ registers.
indios is located 1 km from the urban centre. Statistical analysis of the data was performed with EpiInfo
Schoolchildren aged 5–15 years were recruited from the (CDC). Continuous data were compared by Anova test; cat-
urban area (group A) and from the indigenous reserve (group egorical data were analysed by use of the Chi square test with
B). Since no more than an estimated 5–10% of school-age Mantel-Haenszel stratified analysis or by use of Fischer’s
children do not attend school regularly, the sample popu- exact test as appropriate. A P-value , 0.05 was considered
lation could be considered representative. The study was car- significant. Individuals with A. lumbricoides, hookworms, or
ried out during the months of September and October 1998. T. trichiura infections were treated with albendazole 400 mg
The sample size was calculated in order to demonstrate a single dose.
difference of 20% in the prevalence of STH infections
between the two study groups (assuming 40% prevalence in
Results
group B and 20% in group A) with a confidence interval of
95% and a precision of 80%. Stool examination was offered to 140 children of group A
To reach target samples we recruited the whole population and 105 children of group B. A total of 236 schoolchildren,
in the indigenous reserve and a randomly selected sample in
the urban area. There is only one school in the indigenous
reserve; the urban sample was selected from the two public
Table 1 Sex and age of urban (Group A) and indigenous (Group B)
schools in town. Within each of these two schools two classes schoolchildren
were selected using a lottery method as suggested by the
WHO guidelines (Montresor et al. 1998). At the beginning of Group A Group B
the study the reasons for the survey and the procedure for n (%) n (%) P-value
stool sample collection were explained to all the participants
and their parents, whose informed consent was obtained. Children 136 100
Each individual was provided with a plastic container Sex
marked with an identification number and with the name of Male 070 (51.4%) 44 (44%)
the subject. Each subject gave one stool sample. Stool Female 066 (48.6%) 56 (56%) 0.25*
samples were examined within 12 h for the evidence of para- Age (years)
05–7 020 (14.7%) 31 (31%)
sitic infections by the Kato-Katz quantitative technique
08–11 100 (73.6%) 52 (52%)
(Montresor 1998). The Kato-Katz slides were examined 12–15 016 (11.7%) 17 (17%) 0.002†
within 1 h to avoid missing evidence of hookworm eggs.
Results are expressed as classes of intensity following recom- *Calculated by Mantel-Haenszel stratified analysis. †Calculated by x2
mendations by WHO (Montresor 1998). uncorrected test.

© 2000 Blackwell Science Ltd 303


13653156, 2000, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-3156.2000.00549.x by Republic of Moldova Hinari NPL, Wiley Online Library on [30/10/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Tropical Medicine and International Health volume 5 no 4 pp 302–307 april 2000

C. Scolari et al. Soil-transmitted helminth infections in schoolchildren in Ortigueira, Brasil

Table 2 Total prevalence of soil-transmitted infections by age in groups remained in all age groups as shown in Table 2.
urban (Group A) and indigenous (Group B) schoolchildren Double infections were found in 2.9% of group A and in
49% of group B (P , 0.001); only one urban child presented
Group A (n 5 136) Group B (n 5 100)
a triple infection.
Age prevalence (%) prevalence (%) P-value
The most common soil-transmitted helminths were A.
lumbricoides, followed by hookworms and T. trichiura. As
05–7 years 03/20 (15%) 26/31 (84%) , 0.001*
shown in Table 3, the prevalence of each parasite in group A
08–11 years 19/100 (19%) 50/52 (96%) , 0.001*
12–15 years 08/16 (50%) 17/17 (100%) , 0.001*
and B, respectively, was: A. lumbricoides 12.1% and 88%
(P , 0.001); T. trichiura 5.1% and 2% (P 5 0.2); hookworms
*Calculated by Mantel-Haenszel stratified analysis. 5.8% and 52% (P , 0.001).
The percentage of heavy infections was 2.9% in group A
and 23% in group B (P , 0.001). The prevalence distribution
of the parasites in the two groups by classes of intensity is
136 in group A and 100 in group B, were examined for soil- shown in Table 3. The association of heavy infections with
transmitted infection and interviewed. Compliance was 97% age was further analysed. While no statistically significant
and 95.2% for group A and B, respectively (P 5 0.43). The difference was found between the prevalence
main characteristics for each of the two groups are shown in of heavy infections in 5–7-year-old children of group A
Table 1. The distribution by sex within the groups was homo- (1/20 5 5%) and of group B (4/31 5 12.9%) (P 5 0.35), a
geneous, while the distribution by age was not (Table1). statistically significant difference was found both in the 8–11
Environment and housing conditions varied between the (3/100 5 3% and 13/52 5 25% in group A and B, respec-
groups: All houses in the indigenous reserve had earth floors, tively; P , 0.0001) and 12–15 (0/16 5 0% and 6/17 5 35.3%;
the urban dwellings had wood floors. Soil also differed in that P 5 0.001) year old children.
in the indigenous reserve there were many basins of stagnant Housing and hygienic conditions also differed significantly
water in which children played. in the two groups (Table 4). By means of a univariate analysis
The prevalence and intensity of STH infections varied sig- we found a correlation between STH infections and housing-
nificantly between the two groups. 22% of group A children /hygienic variables, with the only exception of sharing
and 93% of group B were infected by one parasite or more latrines between families (Table 5). We also found a corre-
(P , 0.001). The difference in the prevalence between the two lation between the prevalence of heavy intensity infection and

Table 3 Total prevalence and prevalence by


Group A Group B P-value class of intensity of soil-transmitted infec-
tions in urban (Group A) and indigenous
(Group B) schoolchildren
N° examined 136 100
A. lumbricoides
Prevalence (%) 012.5 088 , 0.001*
Class of intensity (%)
Light (1–4999 epg^) 007.3 026
Moderate (5000–49 999 epg†) 005.8 044
Heavy (> 50 000 epg) 002.9 018 , 0.001§
T. trichiura
Prevalence (%) 005.1 002 0 00.2‡
Class of intensity (%)
Light (1–999 epg) 004.4 002
Moderate (1000–9999 epg) 000.7 000
Heavy (> 10 000 epg) 0000 000 0 00.4*
Hookworms
Prevalence (%) 005.8 052 , 0.001§
Class of intensity (%)
Light (1–1999 epg) 005.8 038
Moderate (2000–3999 epg) 0000 009
Heavy (> 4000 epg) 0000 005 , 0.001*

†epg, Eggs per gram of faeces. *Calculated by x2 uncorrected test. ‡Calculated by Fisher’s
exact test. §Calculated by Mantel-Haenszel stratified analysis.

304 © 2000 Blackwell Science Ltd


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Tropical Medicine and International Health volume 5 no 4 pp 302–307 april 2000

C. Scolari et al. Soil-transmitted helminth infections in schoolchildren in Ortigueira, Brasil

Table 4 Housing/hygienic factors in urban


(Group A) and indigenous (Group B) school- Housing/hygienic factors Group A Group B P-value
children
N° of cohabiting people (mean) 04.5 06.2 , 0.001*
N° of rooms in the house (mean) 03.4 02 , 0.001*
Presence of toilet in the house (%) 98.5 80 , 0.001§
Inside toilet (%) 81.6 05 , 0.001§
Shared toilet (%) 12.5 02 00 0.003§
Safe water (%) 97 01 , 0.001§
Sewage (%) 97.7 54 , 0.001§

*Calculated by Anova test. §Calculated by x2 uncorrected test.

housing/hygienic variables, with the exception of presence of lence and intensity of intestinal helminth infections than
toilet (Table 5). indio children. STH infections represented a more serious
In a subgroup analysis, 23 children living in a shanty-town health problem among children in the indigenous reserve,
called Vila Andradina presented a higher prevalence of STH 76% of whom had moderate/heavy infections. This preva-
infections. The overall prevalence of children infected with at lence rate is higher than that of other studies in indigenous
least one parasite in this community was 60.8%, while the communities in Brazil (Santos et al. 1995; Miranda et al.
overall prevalence in the other urban agglomerates was 14.1% 1998). Interestingly, the difference in the prevalence of heavy
(P , 0.001). The prevalence of high-intensity infections was intensity infections between the two groups was limited to
significantly higher in children living in Vila Andradina older children (> 8 years). This suggests that chronic expo-
(3/23 5 11.1%) than in other urban children (1/113 5 0.9%) sure to infection in the indio community may lead to
(P 5 0.001). The subgroup of children living in Vila increased intensity of infections.
Andradina was not significantly different from the other The most prevalent parasite was A. lumbricoides in all
urban children considering sex and age, but it was with analysed groups, in agreement with Bundy (1986),
respect to the house and hygienic conditions. Hanitrasoamampionana et al. (1998) and Saldiva et al.
(1999). While the prevalences of A. lumbricoides and hook-
worms were higher in indigenous than in urban school-
Discussion
children, the prevalence of T. trichiura was higher in the
The schoolchildren in Ortigueira city had lower overall preva- urban population, though not to a significant level (P 5 0.2).

Table 5 Correlation of the total prevalence of STH infections and the prevalence of heavy intensity STH infections with housing/hygienic
variables in the study population

Total prevalence of STH infections Prevalence of heavy intensity STH infections


Housing/hygienic ————————————— ————————————————
factors Values RR* CI† RR* CI†

No. of cohabiting people/no. >2 2.62 1.90, 3.61 03.71 1.46, 9.47
of rooms in the house ratio ,2 1
Toilet No 1.78 1.43, 2.21 0§ §
Yes 1
Inside toilet No 3.99 2.77, 5.75 04.25 1.67, 10.85
Yes 1
Shared toilet Yes 0.79 0.46, 1.37 00.91 0.23, 3.57
No 1
Safe water No 4.19 3.02, 5.81 10.33 03.2, 33.36
Yes 1
Sewage No 2.05 1.69, 2.50 01.61 0.75, 3.45
Yes 1

*RR: relative risk. †CI: confidence interval. §data not available because of a null value in the analysis.

© 2000 Blackwell Science Ltd 305


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C. Scolari et al. Soil-transmitted helminth infections in schoolchildren in Ortigueira, Brasil

Indeed, a series of data has demonstrated that T. trichiura is Physicians, Province of Pavia, Italy. We thank Dr Antonio
a typically urban parasite (Bundy 1986; Saldiva et al. 1999). Montresor for suggestions and WHO for providing labora-
WHO guidelines for the evaluation of STH infections at tory kits for Kato-Katz technique. We also wish to thank the
community level (Montresor 1998) recommend periodic treat- Queimadas for their support.
ment rounds for groups with a prevalence of high-intensity
infections of 10% or above, regardless of the prevalence of
overall infections. Therefore our results provide a clear basis References
for periodic mass treatment in the indigenous population, as Albonico M, De Carneri I, Di Matteo L et al. (1993) Intestinal para-
we suggested to local health authorities. A different approach sitic infection of urban and rural children on Pemba Island: implica-
(i.e. treatment of positive cases diagnosed by the health unit) tions for control. Annals of Tropical Medicine and Parasitology 6,
is suggested in case of prevalence , 50% and percentage of 579–583.
high intensity infections , 10% (Montresor 1998). This was Albonico M, Stoltzfus RJ, Savioli L et al. (1998) Epidemiological evi-
recommended for the urban population. dence for a differential effect of hookworms species, Ancylostoma
However, urban children in Vila Andradina had poorer duodenale or Necator americanus, on iron status of children.
International Journal of Epidemiology 27, 530–537.
housing-hygienic conditions (i.e. answers to the question-
Bundy DAP (1986) Epidemiological aspects of Trichuris trichuriasis in
naire) and higher prevalence/intensity of intestinal helminth
Caribbean communities. Transaction of Royal Society of Tropical
infections. These children live in a shantytown where a mass Medicine and Hygiene 80, 706–718.
treatment could be applied, even if the small size of the Crompton DWT (1992) Ascaris and childhood malnutrition.
sample did not allow us to suggest clear recommendations. Transaction of Royal Society of Tropical Medicine and Hygiene 86,
Our data are consistent with a direct effect of the lack of 577–579.
sanitation on prevalence/intensity of intestinal helminth Feachem RG, Bradley DJ, Garelick H & Mara DD (1983) Sanitation
infections as suggested by others with more powerful and Disease: Health aspects of excreta and wasterwater manage-
methods (Feachem et al. 1983; Schulz & Kroeger 1992). ment. Work Bank Study in Water Supply and Sanitation. John
Indeed our observation underscores the importance of reduc- Wiley. New York.
Ferreira RF, Souza W, Perez E et al. (1998) Intestinal helminthiasis and
tion of transmission through interventions based on inform-
anemia in youngsters from Matriz da Luz, District of Sao Laurenco
ation, education and communication strategies and
da Mata, state of Pernambuco, Brazil. Memorias Do Instituto
improvement of sanitation for all community categories Oswaldo Cruz, Rio de Janeiro 93, 289–293.
(Montresor et al. 1998). Geissier PW, Mwaniki D, Thiong’o F & Friis H (1998) Geophagy as a
Populations living close to each other may have different risk factor for geohelminth infections: a longitudinal study of
risks for STH infections if their social economic status and Kenyan primary schoolchildren. Transactions of the Royal Society
their living conditions differ. For an appropriate control strat- of Tropical Medicine and Hygiene 92, 7–11.
egy it is important to conduct epidemiological surveys which Hanitrasoamampionana V, Brutus L, Hebrard G et al. (1998) Etudie
are able to detect these differences. Our study has certain épidémiologique des principales nématodoses intestinales humaines
limitations, inherent in the representativity of the selected dans le Moyen-ouest de Madagascar. Bulletin de la Societé de
sample and the type of analysis. Results concerning urban Pathologie Exotique 91, 77–80.
Machado ER & Costa-Cruz JM (1998) Strongyloides stercoralis and
schoolchildren should not be extended to the child popu-
other enteroparasites in children at Uberlandia City, State of Mina
lation living in the municipality as a whole. School-age chil-
Gerais, Brazil. Memorias Do Instituto Oswaldo Cruz 93, 161–164.
dren not attending schools were excluded from the analysis, Menan EIH, Nebavi NGF, Adjetey TAK, Assavo NN, Kiki Barro PC &
although their proportion was low. Multivariate analysis was Kone M (1997) Profile des helminthiases intestinales chez les enfants
not performed, and this does not allow us to determine the d’age scolaire dans la ville d’Abidjan. Bulletin de la Societé de
exact risk of each considered housing-hygienic factors in Pathologie Exotique 90, 51–54.
determining STH prevalence. However, our survey was basi- Miranda R, Branches Xavier F & Camurca de Manezes R (1998)
cally aimed at providing the basis for practical public health Parasitismo intestinal em uma aldeia indigena Parakana, sudeste do
interventions to decrease STH infections. The cross-sectional Estado do Parà, Brazil. Cadernos de Saùde Pùblica 14, 507–511.
study design does not allow us to determine the efficacy of Montresor A, Crompton DWT, Bundy DAP, Hall A & Savioli L (1998)
Guidelines for the Evaluation of Soil-Transmitted Helminthiasis
mass-treatment in this population. A longitudinal cohort
and Schistosomiasis at Community Level. WHO, Geneva.
study will be necessary to provide this crucial next piece of
WHO/CTC/SIP/98.1.
information. Nokes C & Bundy DAP (1994) Does Helminth Infection Affect Mental
Processing and Educational Achievement? Parasitology Today 10,
Acknowledgements 14–18.
Oberhelman RA, Guerrero ES, Fernandez AM et al. (1998) Correlation
Funding for this project was provided by College of between intestinal parasitosis, physical growth and psychomotor

306 © 2000 Blackwell Science Ltd


13653156, 2000, 4, Downloaded from https://onlinelibrary.wiley.com/doi/10.1046/j.1365-3156.2000.00549.x by Republic of Moldova Hinari NPL, Wiley Online Library on [30/10/2022]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Tropical Medicine and International Health volume 5 no 4 pp 302–307 april 2000

C. Scolari et al. Soil-transmitted helminth infections in schoolchildren in Ortigueira, Brasil

development among infants and children from rural Nicaragua. Santos RV, Coimbra CEA, Flowers NM & Silva JP (1995) Intestinal
American Journal of Tropical Medicine and Hygiene 58, 470–475. parasitism in the Xavante Indians, Central Brazil. Revista Do
Olsen A (1998) The proportion of helminth infections in a community Instituto de Medicina Tropical de Sao Paulo 17, 145–148.
in western Kenia which would be treated by mass chemotherapy of Savioli L, Bundy D & Tomkins A (1992) Intestinal parasitic infections:
schoolchildren. Transaction of Royal Society of Tropical Medicine a soluble public health problem. Transactions of the Royal Society
and Hygiene 92, 144–148. of Tropical Medicine and Hygiene 86, 353–354.
Ray SM (1998) Intestinal geohelminthiasis and growth in pre- Schulz S & Kroeger A (1992) Soil contamination with Ascaris
adolescent primary school children in Northeastern Peninsular lumbricoides eggs as an indicator of environmental hygiene in urban
Malaysia. Southeast Asian Journal of Tropical Medicine and Public areas of north-east Brazil. Journal of Tropical Medicine and
Health 29, 112–117. Hygiene 95, 95–103.
Saldiva SR, Silveira AS, Philippi ST et al. (1999) Ascaris – Trichuris Urbani C, Touré A, Hamed AO et al. (1997) Parasitoses intestinales et
association and malnutrition in Brazilian children. Paediatric and schistosomiases dans la vallee du fluve Senegal en republique
Perinatal Epidemiology 13, 89–98. Islamique de Mauritanie. Médecine Tropicale 57, 157–160.

© 2000 Blackwell Science Ltd 307

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