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Revista da Sociedade Brasileira de Medicina Tropical
24(4):217-221, out-dez, 1991
ASCARIS L UMBR1C01DES: REINFECTION IN CHILDREN
BEARING AN ESTABLISHED WORM BURDEN
Fausto E. Lima Pereira, Andrea P. Sampaio,
Carlos Musso and Jane S. Castelo.
To clarify the existance of reinfection in children bearing an established Ascaris
lumbricoides infection, the authors evaluated the weight and the length of worms collectedfrom
ten cases of ascaridiasis. The worm burden was greater than 27 worms in nine cases. In seven
cases the weight and the length of worms showed little variation, with unimodal distribution of
values, suggesting that all the worms in each case belong to the same population, originated
from a single brood infection or from successive infections over small time intervals. In three
cases there was great variation in worm size indicated by the different values for the means and
medians and by the high values for the standard deviation and coefficient of variation. In these
three cases there was a bimodal distribution of worm's size suggesting the coexistance of two
distinct populations: one, less numerous, composed of mature worms and the other, more
numerous, composed ofimmature worms, in two cases, and two distinctpopulations of immature
worms in one case. The existance of worms in different stages of maturation indicates that the
less mature population was acquired when the mature worms were established in the gut. These
results indicate that the reinfection with Ascaris in children bearing an established infection is
not rare and resistance induced by a preexisting infection is not the rule.
Key-words: Ascaris lumbricoides. Ascariasis.
Previous reports evaluating the size of Ascaris
lumbricoides worms expelied after treatment or
collected at autopsy have demonstrated that the
size distribution (weight and length) is unimodal
in each patient26. This observation suggested the
predominance of a single brood infection or
successive infections over small time intervals in
human ascariasis. It has been hypothesized that
successful development of Ascaris within the host
occurs only in the absence of an established infection
in the small intestine. The protective effect of an
extant worm population against subsequent invaders
has been confirmed in experimental infection with
Ascaridia galli in chickens4 and acquired resistance
against Ascaris larvae has been demonstrated in
experimental infections in mice5. Studies of
chemotherapeutic elimination of established human
Ascaris lumbricolides infection in endemic areas
Departamento de Patologia do Centro Biomédico, Universidade
Federal do Espírito Santo e Serviço de Patologia do Hospital
Infantil Nossa Senhora da Glória, Vitória, ES.
Endereço para correspondência: Dr. Fausto E. Lima Pereira.
Dept° de Patologia/CBM/UFES. Caixa Postal 780, 29000
Vitória ES.
Recebido para publicação em 02/08/91.
have shown that the clearance of worms is followed
rapidly by reinfection, indicating a loss of reistance
against reinfection after elimination of a pre-existing
worm burden3.
Recently Baird et al1 reported a fatal Ascaris
infection in a child with a massive worm burden
composed of two populations: a small number of
heavy worms (male and female) and a large number
of lighter worms (male and female). The authors
suggested that the heavier worms represented an
older pre-existing population, while the smaller,
more numerous worms with umimodal size
distribution, represented a younger population
acquired as a single brood infection. According to
the authors, this was the first report of superimposed
Ascaris reinfection in man.
To clarify the existance of reinfection in children
bearing an established Ascaris lumbricoides infection,
we studied the weight and length of worms colected
at autopsy (nine cases) or after surgery (one case)
from children with Ascaris infection. The worm
burden was greater than 27 worms in nine of ten
cases. Two distinct populations were observed in
three cases, indicating that reinfection with Ascaris
217
Pereira FEL, Sampaio AP, Musso C, Castelo JS. Ascaris lumbricoides; reinfection in children bearing an
established worm burden. Revista da Sociedade Brasileira de Medicina Tropical 24:217-221, out-dez, 1991
occurs more frequently than previously suspected.
RESULTS
MATERIAL AND METHODS
Ascaris collected from nine autopsy and from
one surgical case were rinsed in tap water and stored
in 10% formalin. The worms were grouped by
gender and individually weighed and measured.
When necessary a dissecting microscope was used
for identification of males and females. The age and
sex distribution of the ten children are in Table 1.
For each case the mean, the median and the
standard deviation were calculated for the weight
and length of worms. The “z” scores were calculated
to indicate the largest worm which would be
considered a member of the same population with
99% confidence level (p<0.01). All the worms
with “z” scores higher than 2.33 were grouped and
compared with the others with “z” scores lower
than 2.33. For comparison of the means the Student
“t” test was used.
The results are shown in Tables 1, 2 and 3 in
Figures 1 and 2. Analysis of the distribution of the
weight and length (Tables 1 and 2) identified seven
cases in which the mean and the median were
similar, and in which the standard deviation and the
coefficient of variation (Table 3) indicated a
relatively small dispersion of values around the
mean. However in four of these seven cases, one or
two worms were found with “z” scores above 2.33
(Table 3). The Figure 1 shows clearly the unimodal
distribution of worm's size in those cases.
In case 10, as showed in Tables 1, 2 and 3, the
standard deviation and coefficient of variation
were great but there were not worms with “z”
scores above 2.33. However the bimodal
distribution of worm's size (Figure 2) showed
clearly the existance of two distinct populations.
The student's “t” test showed a significant
difference between the means of worm size of
these two distinct populations.
Table 1 - Weight (g) of worms colected from children with ascariasis.
Case
Age
Sex
N of worms Mean
s
Median
Range
1
6
m
m 51 0.55 0.19 0.54
0.19 - 1.02
f
90
1.34 0.53 1.35
0.23
- 2.93
2
3
f
m
32 0.65 0.18 0.64
0.35 - 1.48
f 41 1.71
0.32 1.78
0.92 - 2.56
3
5
f
m
82 0.90
0.14 0.90
0.76
- 1.21
f 65 2.76 0.52
■ 2.80
1.50 - 4.50
4
2
f
m
22 0.97
0.17
0.99
0.70 - 1.31
f
22 2.37 0.42
2.53
0.58
- 3.22
5
2
f
m
13 0.35 0.11 0.35
0.20
- 0.66
f
14 0.74 0.53 0.71
0.25
- 2.15
6
7
f m
4 1.20 0.14 1.12
1.12 - 1.42
f 4 3.73
0.09 3.73
3.65
- 3.82
7
11
m
m
19
1.57 0.23 1.55
1.25 - 2.12
f
13 4.21
0.35 4.12
3.42 - 4.88
8
4
m m
126 0.27 0.23 0.20
0.05 - 1.33
f 229
0.47 0.74 0.30
0.07
- 5.34
9
2
f
m
11 0.13
0.12 0.08
0.01 - 0.46
f
32 0.29
0.44 0.07
0.01 - 1.55
10
5
m
m
24 0.65 0.54
0.37
0.17
- 1.72
f 32 2.73 1.62 3.47
0.32
- 5.28
m = male f = female
218
Pereira FEL, Sampaio AP, Musso C, Castelo JS. Ascaris lumb rico ides; reinfection in children bearing an
established worm burden. Revista da Sociedade Brasileira de Medicina Tropical 24:217-221, out-dez, 1991
In cases 8 and 9 the worm analysis revealed
different values for the mean and the median, and
the standard deviation was great, with values near
or above the values for the mean. In these two cases
17 and 8 worms respectively were identified with
“z” scores above 2.33, and thus could be considered
as distinct populations at a confidence level of 99 %
(p < 0,01). Comparison of the means of weigths
and lengths of worms with “z” scores greater than
2.33 with the means observed for the worms with
“z” scores less than 2.33 revealed significant
differences.
219
Pereira FEL, Sampaio AP, Musso C, Castelo JS. Ascaris lumbricoides; reinfection in children bearing an
established worm burden. Revista da Sociedade Brasileira de Medicina Tropical 24:217-221, out-dez, 1991
Table 2- Size of worms (cm) collected from children with ascariasis.
Case
N of worms
Mean s
Median
Range
1
m
51
11.6 1.64
12.0
7.5 - 15.5
f 90
16.8
3.05 17.5
7.0 - 22.5
2
m 32
12.0
1.30 12.0
9.5 - 17.0
f 41 18.9
1.59 19.0 15.0 - 22.0
3
m
82
13.6 1.07 14.0
12.0 - 16.5
f 65
21.9 2.07 22.0
18.0 - 29.5
4
m
22
14.8
1.38
14.5 12.5 - 17.2
f 22 21.8
1.77
21.7
17.0 - 24.0
5
m 13
8.9
1.04
8.8
7.0 - 10.5
f
14
12.5
2.77 12.8
8.3 - 18.5
6
m
4
14.3
2.42 16.2
13.0 - 17.5
f 4
24.5
1.91
23.0
23.0 - 27.0
7
m
19
15.5 1.48
15.5 12.5 - 18.3
f 13
24.0 2.08
24.0
21.9 - 29.0
. 8
m 126
7.9
2.10 8.0
5.5 - 15.5
f 229
10.7
3.03
10.5
6.0 - 28.0
9
m
11
6.5
2.06
6.2
3.5 - 10.5
f 32
7.7
4.61 6.7
3.0 - 18.5
10
TO
24
10.5
2.66
9.5
7.5 - 15.5
f 32
19.5 4.36
20.0
10.6 - 26.0
m = male f = female
DISCUSION
Our results showed that in seven of ten cases of
ascariasis in children there was a regular distribution
of worm’s size. In these cases the variation in size
observed was similar to that reported by Jung2 and
by Takata et al6 although these authors provided the
range of values and not the standard deviation. Thus
in six cases, our observations are in agreement with
the concept of a single brood infection in human
ascariasis. Althoug we observed in four cases at
least one worm with “z” score greaterthan2.33, we
believe that these worms are the remnant of a
previous infection which declined through
senescenceor, perhaps, in the faceofanew infection.
In these four cases it is possible that the apparent
reinfection occurred at the end of the life-span of a
pre-existing worm burden.
In two cases (cases 8 and 9) the great variation
in worm's size indicated by the high value of
coefficient of variation and the great number of
worms with “z” scores above2.33 show clearly the
coexistence of two distinct worm's populations:
one composed of numerous small imature worms
and the other of large mature worms in case 8 and
composed of two populations of imature worms in
case 9.
In case 10 the standard deviation and coefficient
of variation were great but there were not worms
with “z” scores above 2.33: the existance of two
distinct populations was clearly demonstrated by
the bimodal distribution of the values for the weigth
and the length. In this case the two populations were
composed of imature and mature worms.
Our observations are in agreement with those
of Baird et al1 in that, in the cases 8, 9 and 10 the
patients appear to have acquired a reinfection with
Ascaris while hosting a light but significant worm
burden. While the mechanisms of reinfection in
these cases is unknown. Baird et al1 invoked
undemutrion as a possible predisposing factor in
their single case, and we found evidence of
220
Pereira FEL, Sampaio AP, Musso C, Castelo JS. Ascaris lumbricoides; reinfection in children bearing an
established worm burden. Revista da Sociedade Brasileira de Medicina Tropical 24:217-221, out-dez, 1991
Table 3 - Coefficient of variation for length and
weigth of worms and number of worms
and number or worms with "z" scores
above 2.33 in ten cases ofascariasis in
children
Case
Length
Weight
CV (%) z > 2.33 CV(%)
z > 2.33
1
m 14
0 36 0
f 18 1 40 1
2 m 10 0
28 1
f
8 0 19
1
3 m 7
1 16
0
f 9
0
19
1
4 m
9
0
19 0
f 8
0 18 0
5
m
11
0
33 1
f 22 0 71 1
6 m 16 0
11 0
f 7 0
3 0
7
m
9
0 14 0
f 9
0
8
0
g
m 26
7
90 7
f 31
9 158 10
9 m 31 1 91 1
f 59 7 147 7
10
m
18 0
83 0
f
22 0
56 0
CV = coefficient of variation
undemutrion in two of three children with
reinfection. It remains possible that other factors
are responsible for this phenomenon. In conclusion
our results demonstrate that reinfection in ascariasis
is not rare, and that the resistance observed with a
pre-existing worm burden is not invariable.
RESUMO
Para tentar esclarecer a existência de reinfecção
em crianças portadoras de ascaridíasejá estabelecida,
foram avaliados o peso e o comprimento dos vermes
colhidos em lOcasosde ascaridíase, em nove dos quais
a carga parasitária foi maior do que 27 vermes. Em
sete casos o peso e o comprimento dos vermes
apresentaram pouca variação, com distribuição
unimodal dos valores, sugerindo assim pertencerem
todos a uma mesma população originada de uma única
infecção ou de infecções repetidas com intervalos
muito curtos. Em três casos, o peso e o comprimento
dos vermes mostraram grande variação, indicada
pelos valores diferentes para as médias e as medianas
e dos altos valores dos desvios padrão e dos coeficientes
de variação. Nesses casos, a distribuição dos valores
para o comprimento e para o peso foi bimodal, sugerindo
a coexistência de duas populações diferentes de vermes:
uma, menos números a, composta de vermes já maduros
e outra, mais numerosa composta de vermes imaturos
em dois casos e duas populações de vermes imaturos
em um caso. A presença de populações distintas de
vermes, com diferentes graus de maturidade, indica
que a população mais imatura foi adquirida quando a
população mais desenvolvida já estava estabelecida no
intestino. Esses resultados demonstram que a reinfecção
com Ascaris em crianças portadoras de ascaridíase
estabelecida não é rara equea resistência induzida por
uma infecção pré-existente não é um fato invariável.
Palavras-chaves: Ascaris lumbricoides. Ascaríase.
REFERENCES
1. Baird JK, Mistrey M, Pimsler M, Connor DH.
Fatal human ascariasis following secondary
massive infection. The American Journal of
Tropical Medicine and Hygiene 35:314-318,
1988.
2. Jung RC. The predominance of single brood
infection in human ascariasis. Journal of
Parasitology 48:405-407, 1984.
3. Otto GF. Ascaris lumbricoides: treatment and
loss of worms and reinfection. Journal of
American Medical Association 95:194-195,
1930.
4. Sadun EH. Resistance induced in chickens by
infection with the nematode Ascaridia galli.
The American Journal of Hygiene 47:282-289,
1948.
5. Sprent JFA, Chen HH. Immunological studies
in mice infected with larvae of Ascaris
lumbricoides. In: Criteria of immunity and
immunizing effects of worm tissues. Journal of
Infectious Diseases 84:111-124, 1949.
6. Takata I. Experimental infection with Ascaris
of pig and man. Kitasato Archives of
Experimental Medicine 23:49-59, 1951.
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