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Parasitología al día

versão impressa ISSN 0716-0720

Parasitol. día v.23 n.3-4 Santiago jul. 1999

http://dx.doi.org/10.4067/S0716-07201999000300002 

TRABAJO DE INVESTIGACION

The distribution of Ascaris lumbricoides infection in
humans from a rural community in Venezuela

GUSTAVO MORALES*, LISBETH LOAIZA** and LUZ PINO*

ABSTRACT

A total of 337 persons (86.8%) were examined by faecal egg count and worm burden by counting expelled parasites following anthelmintic treatment (Oxantel Pyrantel PamoateR) in order to study the prevalence and distribution of Ascaris lumbricoides in the human population of a rural locality from Venezuela. The number of positive diagnosis of A. lumbricoides infection by worm collection was higher than by eggs determination and the degree of infection determined by egg counts resulted well associated with the worm burden (P < 0.001) and so it may used with some confidence. The prevalence and intensity of infection were similar in both sexes. In relation to the age, the highest values for prevalence (P < 0.05), relative risk (P < 0.01) and intensity of infection (P < 0.02) were observed in the 5 to 9 year old children. Within the population, few individual (20.19%) harboured more than 6 roundworms and many of the hosts (38.3%) had only a few (1 to 5 worms) or none worm (41.53%).
Key words: Ascaris lumbricoides, wormy persons, distribution, Venezuela.

*Laboratorio de Parasitología, Instituto de Investigaciones Veterinarias, CENIAP/FONAIAP, Av. Las Delicias, Maracay, Edo. Aragua, Venezuela. e-mail: gamc@cantv.net

** Centro de Investigaciones en Enfermedades Tropicales, Universidad de Carabobo, San Carlos, Estado Cojedes, Venezuela.

INTRODUCTION

Ascaris lumbricoides is the most common and important soil transmitted helminth. This parasite is cosmopolitan and its distribution is largely determined by local habits in the disposal of faeces, because its eggs reach the soil in human faeces and so contaminate the human environment.1, 2 The parasite is present in approximately one - quarter of the world population3 and is one of the major public health problems in many latinoamerican countries.4

The ascariosis infection extends throughout communities of poor and socioeconomically deprived people of the tropics and subtropics5 in areas where inadequate sanitation6, 7 and malnutrition are frequent3 and persits where the limited resources for medical care and poor health awareness in the people prevail.6

The aim of this work is to present and analize some factors affecting the distribution and intensity of A. lumbricoides infection in a rural community from Venezuela in relation to the age and sex of the population.

MATERIALS AND METHODS

Study area: The study was carried out in Mapurite, a rural locality of Cojedes state,Venezuela. The maximum and minimum mean temperatures were 28.4°C in January until 39.8°C in March and April. The average annual relative humidity was 75% and the annual rainfall was 630 mm. The region is classified as semiarid. The soil is constituted by a sandy layer of 20 inches of thickness and has as support a clay compact layer of great plasticity and little permeability. Mapurite contained 388 people in 83 houses of which 81 (98%) were built by the "National Program of Rural Housing" of the Ministery of Health. The houses are provided with indoor water and latrines, but defecation generally occurs in the vicinity of the house (63% of people declared habits of open air defecation).

Description of the population: A total of 337 persons (86.8%) were sampled. A summary of the age and sex of the participants is given in Table 1.

 

Table 1. Summary statistics for the population studied

Age class Male Female Total Percentage
(years)       (%)

0 - 4 21 32 53 15.73
5 - 9 22 21 43 12.76
10 - 14 19 27 46 13.65
15 - 19 18 16 34 10.01
20 - 24 16 14 30   8.90
25 - 29 10 11 21   6.23
30 - 34   6 16 22   6.53
35 - 39 10   9 19   5.64
40 - 44   8   4 12   3.56
> 45 29 28 57 16.91
         
Total 159   178   337   100.00  


The purpose of the research project was explained to community. Adult participated voluntarily and children with their legal guardian authorizations. Strict ethical procedures were followed throughout.

Some obligatory prerequisites and compromises were established:

• No having received any anthelmintic treat-ment at lest during the last six months.

• Collect of total stool for three days post anthelmintic treatment.

Parasitological methods: The prevalence is defined as the proportion of subjects found to be infected at the time the survey and the intensity of the infection as the worm burden per host. Both epidemiological statistics can be measured by eggs determination in faeces or by worm collection after anthelmintic treatment.

Egg count determination: Prechemotherapy stool sample cup (10 g/person) which were distributed with instructions to a member of each house in Mapurite locality. Containers were clearly marked with the name of each house member and collected following day. The stool samples were processed within 24 hours using the Stoll egg counting technique.8, 9

Worm burden determination: the most reliable measure of the intensity of infection is to count all the A. lumbricoides expelled by the subjects for a known period (48 to 72 hours) following the anthelmintic treatment with a proven efficacious drug.1 The worm expulsion was obtained by mean of Oxantel Pyrantel Pamoate (QuantrelR, Pfizer). It was administrated in a single dose of 10 mg/kg in children under 12 years old and 12 mg/kg for the individuals of the others ages. Plastic containers labelled were inmediatelly given to treated individuals with instructions to pass all stools in the container for the following 72 hours the expelled worms were collected according to Magalhaes procedure.10 The worm were isolated and washed in physiological solution and preserved in 7% formalin. The total worm burden in each individual was estimated on the basis of the number of A. lumbricoides expelled. The intensity of infection was stratified according the following classes:

0 worms = 0 (negative); 1 to 3 worms = 1; 4 to 5 worms = 2; 6 to 8 worms = 3; 9 to 12 = 4; 13 to 20 = 5; 21 to 28 = 6; 29 to 40 = 7; 41 to 50 = 8.

Intensity of infection: the intensity of infection was measured on the basis of eggs counts, expressed as eggs per gram of stool (epg)9:

• light

:
<
2600 epg

• moderate

:
2600 <
12559 epg

• heavy

:
12600 <
25599 epg

• very heavy

:
>
26000 epg

Data analysis: Considering that the data do not present a normal distribution the following non parametric statistical analysis were used: a) the Mc Nemar test b) the Chi square test c) the Mood Median test d) the test for k independent samples of Kruskal-Wallis.11, 12 In the following the test used is indicated by "a", "b", "c" or "d".

In order to establish the possibility to become infected with A. lumbricoides in relation to the age and sex, the relative risk was calculated13 and the significance of values over 1 was determined by mean of Student t test.14

RESULTS

The number of positive diagnostic of A. lumbricoides infection by worm collection after anthelmintic treatment was higher than by egg determination (a; X² = 12.1 P < 0.0005). The stool diagnosis provided a prevalence value of 54.30% while the detection of worms in the stool passed by the same subjects following anthelmintic treatment revealed a prevalence of 58.45%. The results by sex are presented in Table 2. The percentage of infection was similar in both sexes (b; by egg determination X² = 0.34; N.S.; by worm recuperation X² = 0.05 N.S.) (Table 2).

 

Table 2. Prevalence of infection with Ascaris
lumbricoides
in relation to the sex of the individuals
sampled from the locality of Mapurite (Cojedes State,
Venezuela)

EGG DETERMINATION
Sex Not infected Infected %

Male 70 89 55.97
Female 84 94 52.81
       
X² = 0.34 (N.S.)  

WORM COLLECTION
Sex Not infected Infected Prevalence

Male 65 94 59.12
Female 75 103   57.86
       
X² = 0.05 (N.S.).
X² = Chi Square statistic.
N.S. = Not significant.

Host sex did not influence the intensity of infection (b; X² = 3.3 N.S.) (Table 3).

 

Table 3. Frequency distribution of Ascaris
lumbricoides
burden per person in relation
to the host sex (Mapurite locality, Cojedes
State, Venezuela)

Worm burden Male Female

1 - 3 65 75
4 - 5 37 49
6 - 8 16 10
9 - 12   8 11
13 - 20   5   5
25 - 49   6   7
     
X² = 3.3 (N.S.)
     
     
X² = Chi Square statistic  
N.S. = Not significant.  


The Table 4 show that the 5 to 9 years old class had the highest prevalence and relative risk for A. lumbricoides infection by eggs deter-mination and by worm recuperation. The intensity of A. lumbricoides infection in male and female children within the 5-9 years old class was not significantly different (c; X² = 0.01).

 

Table 4. The frequency (F) and the relative risk
(Rr) of Ascaris lumbricoides infection in
relation to the age class (Mapurite locality,
Cojedes State, Venezuela)

EGG DETERMINATION
(Stoll technique)

Age class n F Rr P value

0 - 4 53 21 0.49 N.S.
5 - 9 43 32 3.07 0.01*
10 - 14 46 27 1.10 N.S.
15 - 19 34 23 1.86 N.S.
20 - 24 30 14 0.71 N.S.
25 - 29 21 11 0.92 N.S.
30 - 34 22 14 1.51 N.S.
35 - 39 19   9 0.74 N.S.
40 - 44 12   5 0.59 N.S.
> 45 57 27 0.76 N.S.
         
  X² = 18.2 (P < 0.05)  

  WORM COLLECTION  
Age class n F Rr P value

0 - 4 53 33 1.21 N.S.
5 - 9 43 34 3.04 0.01*
10 - 14 46 27 1.01 N.S.
15 - 19 34 23 1.55 N.S.
20 - 24 30 14 0.55 N.S.
25 - 29 21 11 0.77 N.S.
30 - 34 22 14 1.26 N.S.
35 - 39 19   9 0.62 N.S.
40 - 44 12   5 0.49 N.S.
> 45 57 27 0.55 N.S.
 
X² =16.5 P < 0.05.
n = number of individual sampled
N.S. = not significant* = level of signification


Differences in the intensity of infection were tested for the all age class. It was evidenced that a significantly number of individuals infected with high worm burden belonged to 5 to 9 age group (d; H = 19.5 P < 0.02) (Table 5).


Table 5. Frequency distribution of Ascaris lumbricoides burden in different age groups in
Mapurite locality (Cojedes State, Venezuela)

  Worm burden code
Age 0 1 2 3 4 5 6 7 8 AR Z
class                      

0 - 4 20 22 4 4 1 0 1 1 0 160.9 0.66
5 - 9   9 15 1 3 8 5 1 0 1 213.5 3.21
10 - 14 19 11 6 4 3 1 0 2 0 171.1 0.16
15 - 19 11   8 6 4 2 1 0 2 0 189.8 1.31
20 - 24 16   8 4 0 1 1 0 0 0 140.4 - 1.7
25 - 29 10   4 2 2 1 0 0 2 0 165.0 - 0.2
30 - 34   8   5 4 0 2 1 0 1 1 185.0   0.8
35 - 39 10   3 4 1 0 1 0 0 0 150.0   0.8
40 - 44   7   0 2 1 1 0 0 0 1 159.4 - 0.3
> 45 30 10 10   7 0 0 0 0 0 147.5 - 1.8
                       
  H = 19.51 P < 0.02 (adjusted for ties)
   
H = Kruskal-Wallis statistic
AR = Average rank
Z = Z statistic (this value indicate how the mean rank R for each age group differ from the mean rank R for all N observations).

When the worm burden is over 9 parasites all the classes diagnosticated by egg counts were classified as heavy or very heavy intensity of A. lumbricoides infection (d; H = 293.6 P < 0.0001) (Table 6). Only 14 individuals of the sample diagnosticated as negatives by egg determination, resulted positives by worm collection. These individuals harboured few worm burden (1 to 3 worms) with only male parasites (Table 6).

 

Table 6. Relationship between the degree of intensity of Ascaris lumbricoides infection established
by egg count and frequency distribution of worm burden per individual (Mapurite locality,
Cojedes State, Venezuela)

Degree of Worm burden code
infection 0 1 2 3 4 5 6 7 8 AR Z

Negatives 140 14 0 0 0 0 0 0 0   80.8 - 15.3
Light     0 53 21   2 0 0 0 0 0 203.9     3.6
Moderate     0 16 18   11   0 0 0 0 0 233.5     4.8
Heavy     0   2 3 8 6 1 0 0 0 276.0     5.1
Very heavy     0   1 1 5 13   9 2 8 3 309.2     9.9
                       
  H = 293.6 (P < 0.0001)
   
H = Kruskal Wallis statistic
AR = Average rank
Z = Z statistic (this value indicate how the mean rank (R) for the group differ from the mean rank R for all N observations.

The cumulative percentage distribution (Table 7) of worms burdens showed that few persons (68) harbour more that 6 worms (20.19%) and many of the hosts (128) have less than 6 worms (38.3%).

Table 7. The cumulative percentage distribution of Ascaris lumbricoides
burden in a human population of locality of Mapurite (Cojedes State,
Venezuela)

Worm burden

n

Percentage Cumulative percentage

Not infected 140   41.53 41.53
1 - 3 86 25.52 67.05
4 - 5 43 12.76 79.81
6 - 8 26   7.72 87.53
9 - 12 19   5.64 93.17
13 - 20 10   2.97 96.14
  21 - 28  2  0.59 96.73
29 - 40   8   2.38 99.11
 41 - 50   3  0.89 100.00  
       
n = number of individuals.


DISCUSSION

The ascariosis fluorishes in communities where the prevailing social environment is characterized by poverty, poor housing, inadequate sanitaries practices and overcrowding7 and its distribution is largely determined by the local habits in the disposal of faeces.3, 15 Infections may be prevalent in areas apparently enjoying good sanitation facilities. This is due mainly to promiscuos excretory habits of people and to the dispersal stool contaminate around

he home4, that means that the prevention of soil-transmitted helminth infections is in large part a problem of faeces disposal.

The highly percentage of open air defecation habits (63%) for the Mapurite inhabitants, undoubtely favourish the A. lumbricoides infection and suggest a common and constant exposure to infective eggs.

The prevention of geohelminths begin with the installation of latrines, this measure was carried out in Mapurite but the results showed that this facility are not being properly used.

Field data on A. lumbricoides consistently show that infection prevalence as assessed by the presence of eggs in a stool sample unders-estimate the true proportion of individual infected16 and diagnosis by stool examination is rarely 100% sensitive17 as was demostrated in this work. It can be explained because in fourteen people amongst infected no female worm were present, since female worms are very prolific, laying thousand of eggs daily and produce eggs even if unmated.17, 18

It is known that certain group of people within population are more at risk to infection whether due to their sex, age, religion or occupation.19 However there is no consistent evidence to indicate that there is a difference in susceptibility to helminth infection between both sexes in humans1, 18, 34 and the differences may be due to behavioural or occupational causes.18 Similar results were obtained for the intensity of infections, since both sexes have the same epidemiological importance within the community.

The prevalence and the intensity of infection were highest in the 5 to 9 years old group, this showed that age had strong effects on both epidemiological statistics and give a great importance to this group as environmental contaminator within the community. Other authors have obtained similar results.18, 20 The children are perhaps particularly a risk of ingesting eggs through playing on the ground in defecation areas and throughout eating soil contaminated with eggs.1

The differences which occurs in the prevalence, relative risk of infection and intensity of infection by A. lumbricoides at various ages may be due to behavioural differences superimposed on probable physiological inmunological and genetic differences.1, 21, 22 These observations suggest that a child targeted approach to chemotherapy may be effective and may also have an economic advantage because children are more accesible due to attendance at school.20, 23

Due to low cost easy of application and diagnostic capability quantitative faecal egg counts have been widely used in epidemiological studies of intestinal nematode infections.24 A good indication of the degree of infectation with roundworms may be obtained from the egg counts, because a good correlation was found between the average worm burden and the intensity of infection determined by egg counts and with certain limits it is feasible to have an idea of worm burden according to the abundance of eggs in the faeces,25 as occured in the present work, where a good association was found between the degree of infection established by eggs counting and worm recuperation.

The large variation observed in the number of parasites between the host individuals is a commun feature in helminth infections, attributed to variation in susceptibility or behaviour of the hosts and correlated with different infection chances.26 As in the present study where it was found that intensity of infection is high in some individuals (21.19%), while others living in the same community in apparently identical situation are free (41.58%) or harbour few parasites (38.3%).

Current opinions suggest that the observed predisposition of some individuals to given intensities of A. lumbricoides will have a genetical basis.1 It has been established for some host helminth systems that the specificity of the antibody responses varies according to the strain of the animal hosts.27 The finding of predisposition to infection either to heavy or light intensity of infection is of practical importance in designing chemotherapeutic strategies for the control of ascariasis in order to use the resources most effectively.28

Suggested treatment strategies include targeting the most heavily infected families29 or the most heavily infected age group,21 because mathematical model given evidence that selective treatment of only the heavily infected persons in a community may be superior to mass chemotherapy as a control measure, both in terms of reducing parasite loads and decreasing number of necessary treatments.18, 30 This selective chemotherapy offers an alternative approach to control.30

When the predisposal individuals to harbour high worm burden or wormy person31 are identified, drug treatment can be repeatedly focussed on these individuals,22 until reach a critical average worm burden below which mating frequency to be low to maintain transmission within the human community18 this break point is very low, being of the order of an average worm burden of 0.3 to 0.5 worms per host.32 In the locality under study the individuals of the 5 to 9 age group can be submitted to periodical coprological examination for the evaluation the succes of control programme.

As general conclusion the provision of sanitation facilities not protect the population against geohelminth infection if the over-all level of faecal contamination is high.33

The reduction of environmental contamina-tion with viables eggs of A. lumbricoides can be reached by the selective treatment of the most heavy infected people or wormy persons 31 and by the properly use of latrines by the community.4

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