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Regem H.

Lagan
Aleksei L. Fuentes
Noemi D. Rubenecia
Section C

Presence of Enterobius vermicularis ova on the fingernails and risk factors of its infection
among schoolchildren aged 6-9 years in Cabili Elementary School

Abstract
Background Other than transparent tape swab technique, enterobiasis can also be diagnosed in
examining the fingernails of infected children. This research sought to know the presence of E.
vermicularis ova on the fingernails and risk factors associate with infection.
Methods Random samples of schoolchildren resulted to 198 participants aged 6-9 years were
subjected for the collection of fingernails in a cross-sectional study. Schoolchildren have
undergone room to room visitation for the collection of the specimen. After collecting specimen,
each of the participants was given questionnaires. The specimens were prepared in appropriate
laboratory procedures to avoid contamination, and labelled properly. Slide examinations were
done in 4 sets.
Results Presence of E. vermicularis ova on the fingernails was negative on each of the examined
specimen. Zero result was due to the decrease rate of factors that influence enterobiasis such as,
scratching around the anus, habit of thumb sucking, and untrimmed fingernails.
Conclusion Practice of good hygiene among the schoolchildren results a decrease of egg
positive rate on the fingernails. Treatment and preventive measures also decrease the severity of
E. vermicularis infection which affects the result of the study.

Background
Enterobiasis is a disease caused by a small nematode which is the Enterobius
vermicularis (also known as pinworm), a common helminthic infection. Totanes et al. (2009)
mentioned that among the helminthes, pinworm has the widest geographical distribution, usually
in temperate or colder climates and tropical countries such as the Philippines. Bunchu et al.
(2011) added that E. vermicularis is normally the predominant parasite in areas where socio-
economic and environmental conditions, and hygiene practice levels, are lower. Enterobiasis is
generally considered to be a nuisance rather than a fatal disease; the level of morbidity is
significant, particularly in children (Kim et al., 2010). Infection is initiated by the ingestion of
infective eggs which hatch in the caecum region of the large intestine and develop into adult
worms within 4-6 weeks (Gunawardena et al., 2013). The eggs are infective within a few hours
and are easily spread by hands to the mouth, most often through touching contaminated
households objects or food supplies (Cruz et al., 2013). This infection causes irritation and itch
of the perianal surface which usually occurs at night-time; thus, this disrupts the sleep of the
children. There are other effects or symptoms associated with enterobiasis. These are loss of
appetite, loss of weight, dizziness, appendicitis, hyperactivity, perianal itching, abdominal pain,
and nausea (Totanes et al., 2009).
As a result of the extensive distribution of this infection, the mode of transmission and
risk factor of this parasite is significant. Cook (1992) explicated the four methods of
transmission: direct infection from the anal and perianal regions by fingernail contamination;
exposure to viable eggs on soiled bed linen and other contaminated environmental objects; by
contaminated dust containing embryonated eggs; and retro-infection. Moreover, there are factors
that yield enterobiasis infection. Nithikathkul et al. (2001) stated that the infection rate may
include hygiene, levels of parental care, and social interactions at school. In addition, factors
associated with this infection also include playing on the floor, nail biting, failure to wash hands
before meals, and living in non-apartment dwellings (Sung et al., 2001). Since it has a simple
transmission, personal hygiene and sanitary rules can effectively limit its distribution (Nourozian
and Youssefi, 2012).
This infection is more prevalent in children rather than adult ones. Culha and Duran
(2006) asserted that this infection is frequently seen in kindergarten, primary school and
orphanage, where children are crowded. In relation to this, a Taiwanese study reported E.
vermicularis case infection that the prevalence rate of this infection was as high as 16.3% at the
first screening of first-grader admitted in September 1991 (Sung et al., 2001). Another Filipino
study had shown that 33.1% out of 121 children living in institution were infected by Enterobius
vermicularis (Baldo et al., 2004). Bunchu et al. (2011) also reported that among 1,131 children
tested, 19.9% were positive for E. vermicularis eggs. Those statistical results show that the
prevalence of infection is among children particularly schoolchildren.
In indicating the infection, transparent tape swab technique is used in analyzing the ova
of E. vermicularis, and done by applying the tape in perianal region. This is because of the fact
that the eggs, which normally are in the embryo stage when laid by the female worm, are usually
found around the anus of the human host (Royer et al., 1962). However, Cook (1994) asserted
that eggs of E. vermicularis may also be detected from beneath the fingernails. This signifies that
the egg positive rate of E. vermicularis can also be determined by examining fingernails dirt.
We all know that children can easily be infected by E. vermicularis infection because
they have more chance to be transmitted by ingesting the infective egg. To our knowledge, only
transparent tape swab technique is use in diagnosing the infection for detecting the ova of E.
vermicularis. However, there is inadequate information that the infection can also be diagnosed
through fingernail scraping.
The aim of this study is to determine the presence of E. vermicularis ova, by detecting the
ova of the parasite through fingernail scraping, and the risk factors among schoolchildren in our
community.

Method
Design
The study was undertaken in Cabili Elementary School on February 2014 after receiving
approval from the superintendent of DepEd and head of the school. Cross-sectional study was
performed on random samples of schoolchildren whose houses are situated near the dumpsite to
assess the presence of pinworms ova on their fingernails. Basis of pinworms infection, in which
majority of the schoolchildren are exposed and affected, was also identified by evaluating the
risk factors, such as socioeconomic of the parents of the children and practices of the children
inside and outside of their respective houses.

Study Subjects
The study consisted of 198 participants, which are schoolchildren aged 6-9, were
evaluated in the only elementary school (Cabili Elementary School) of Barangay Santiago, Iligan
City that is situated near the dumpsite, as it was randomly selected. The researchers did a room to
room visitation in the school which covered first-grader to fourth-grader classrooms. Participants
were physically well in terms of weight because the feeding program from a food corporation is
sustained. All individuals agreed to participate in the collection of fingernails. The collection was
all gathered for only two consecutive days (afternoons): 55 children were taken samples for the
first visit and 143 children for the second visit. During the last visit, the researchers had collected
the samples two days before the deworming program of the school.

Ethical Consideration
Considering this study will be published, the researchers will protect the privacy of the
respondents, as well as those who are affected by the results of the study and their reputation will
remain confidential.

Protocol/Procedure
Data Collection
The specimens were collected in Cabili Elementary School, Barangay Santiago. Students
records were requested from Guidance Office to obtain necessary information of the students
regarding name, age, BMI and health status. The sample size was calculated resulting 198
schoolchildren had been participated. Each random participants aged 6-9 were visited in thirteen
classrooms, providing permission from the teachers before the collection was started. The
method of collection was introduced to the students first before having their fingernails cut. After
introducing the process, the fingernails in both hands of the participants were clipped, and dirt
was scraped. The specimens (nails and scraped dirt) were put in a small clean container with cap
and label on it. Nail cutters and scrappers were cleaned with 40% isopropyl alcohol every after
use to avoid contamination, and were air dried before using again.
After the collection was performed, each of the students was given questionnaires, asking
them to have it answered by their parents, and to have it passed by the next day. The researchers
went back to school on the next morning to collect the answered questionnaires. With the
cooperation of the teachers, they gathered all the answered data from the students before starting
their class. All questionnaires were collected within five consecutive days because some of the
students didnt pass it promptly.

Time of Sampling
The specimens were collected in the afternoon between 1:00 to 4:00 pm to have a chance
of having the E. vermicularis ova on the fingernails of the participants after taking a bath in the
morning.

Slide Examination
After the collection, the specimens were brought in MSHC Student Medical Technology
Laboratory in Iligan for microscopic examination. Before examining it, the specimens in each of
the containers were added 2 to 3 ml of normal saline solution as diluents to detach the dirt from
the nails. The dilution took less than 24 hours, and specimens were stored in a box at room
temperature. The diluted specimens were transferred in a labelled sterile test tube on the same
amount of saline solution, excluding the fingernails. The test tubes were centrifuge for 20
minutes to ensure that the sediments have separated from the fluid. After the centrifugation, the
fluid from the test tubes were decanted back to the small container, and the decanted test tubes
were place to the other test tube rack ready for examination. Slide examinations were made by
set for the specimens were not diluted at a time. Slide examinations were done with a total of 4
sets. Just a small drop of sample was use in the slide examination using light microscope. Low
power objective was used to identify the ova of parasite and high power objective for
confirmation.

RESULTS
Profile in Terms of Age and Gender
Table 1
Variable Frequency Percentage (%)
Gender
Male 83 41.92
Female 115 58.08
Total 198 100

Age
6 26 13.1
7 56 28.3
8 67 33.8
9 49 24.8
Total 198 100

Table 1 presents the frequency and percentage distribution of respondents in terms of


gender and age. It shows that the majority of the respondents were female which has a frequency
of 115 and a percentage of 58.08%, while the male has a frequency of 83 and a percentage of
41.92%. In terms of age, 26 (13.1%) were 6 years old, 56 (28.3%) were 7 years old, 67 (33.8%)
were 8 years old and 49 (24.8%) were 9 years old.

Proper Hygiene and other Possible Risk Factors


Table 2
Variable Male Perce Female Perce Total Total
Frequency ntage Frequency ntage Frequency Percentage
(%) (%) (%)

Taking a Bath
Regularly 55 66.3 91 79.1 146 73.74
Seldom 28 33.7 24 20.9 52 26.3
Total 83 100 115 100 198 100

Hand Washing
before and after
meal
Regularly 68 81.9 97 84.3 165 83.3
Seldom 15 18.1 18 15.7 33 16.7
Total 83 100 115 100 198 100

Thumb Sucking
Yes 10 12 14 12.1 24 12.12
No 69 83.1 93 80.9 162 81.82
Sometimes 4 4.8 8 7 12 6.06
Total 83 100 115 100 198 100

Playing on the
Ground
Yes 17 20.5 11 9.6 28 14.14
No 43 51.8 76 66.1 119 60.10
Sometimes 23 27.7 28 24.3 51 25.76
Total 83 100 115 100 198 100

Nail Cutting
Regularly 69 83.1 105 91.3 174 87.9
Seldom 14 16.9 10 8.7 24 12.1
Total 83 100 115 100 198 100

Kind of Flooring in
the House
Soil (Yuta) 7 8.4 10 8.7 17 8.59
Wood (Kahoy) 33 39.8 38 33 71 35.86
Semento 36 43.4 59 51.3 95 47.98
(Cement)
Kawayan 7 8.4 8 7 15 7.58
(Bamboo)
Total 83 100 115 100 198 100

Scratching Near the


Anal Area
Yes 8 9.6 6 5.2 14 7.1
No 75 90.4 109 94.8 184 92.9
Total 83 100 115 100 198 100

Taking Deworming
Drugs
Yes 70 84.3 97 84.3 167 84.3
13
No 83 15.7 18 15.7 31 15.7
Total 100 115 100 198 100
Nail Bitting 4
Yes 59 4.8 3 2.6 7 3.5
Never 20 71.1 94 81.7 153 77.3
Sometimes 83 24.1 18 15.7 38 19.2
Total 100 115 100 198 100

The result shows that more than half of the total respondent says that they take a bath
every day. It also shows that females tend to take a bath every day than males. By this, it proves
that females are more hygienic than males. In terms of hand washing before and after eating, out
of 198 respondents 165 (83.3%) says they wash their hands regularly and 33 (16.7%) answered
seldom. It summarizes that most of the respondents wash their hands before and after eating. The
school teaches the students on how to practice proper hand washing to ensure the students safety
on eating. Assuming that those respondents who answered seldom forgot proper hand washing
due to hastiness or they were not properly thought by their parents.
In terms of thumb sucking habit, 24 (12.12%) of the total respondents says yes and 162
(81.82%) says no. It demonstrates that most of the respondents are not practicing thumb sucking
habit. We believe that those respondents who answered yes previously practiced thumb sucking
habit since their infant stage. Only 28 (14.14%) of the total respondents says that they are
playing on the ground. It summarizes that majority of the respondents are not playing on the
ground. Parents these days are stricter on where and how their children play. Also, they are now
knowledgeable enough about the diseases that their children might get.
87.9% or more than half of the parents of the respondents are regularly cutting their
child's fingernails. Parents believe that having nicely trimmed nails can keep their children from
biting or picking at them, which can lead to infections and for their children to look neat and
clean. Out of the total respondents, 17 (8.59%) says soil, 71 (35.86%) says wood, 95 (47.98%)
says cement and 15 (7.58%) says bamboo. It summarizes that almost half of the respondents are
using cement as their type of house flooring. Houses and buildings nowadays are made up of
concrete materials and almost all of the grounds are covered with cements.
The table also shows that the majority of the respondents are not scratching near the anal
area. Only 14 (7.1 %) answered yes and those respondents whose answer is yes might have some
skin irritations or other skin problems that causes them in scratching the area near the anus.
Majority of the respondents are taking deworming drugs. 167 (84.3%) of the total respondents
says. Nearly every parent these days are more aware of the benefits of taking deworming drugs
against parasitic infections. The government also takes action and responsibility of the students
health concerns. Out of 198 respondents, only 7 (3.5%) answered yes in nail biting habit and
majority or 77.3% of them answered never. This illustrates that most of the respondents are not
practicing nail biting and we believe that those who answered yes makes nail biting their
childhood habit.

Table 3
Factors affecting the presence of E. vermicularis ova on the fingernails
Variable Frequency Percentage (%)
Regular hand washing in
relation to scratching the
anus

Scratching the anus but hand 14 100


washed regularly

Scratching the anus but 0 0


seldom hand washing

Total of participants that


scratched around the anus: 14 100

Regular nail trimming in


relation to scratching the
anus

Scratching the anus but nail


trimming regularly 9 64.3

Scratching the anus but


seldom nail trimming 5 35.7

Total of participants that


scratched around the anus: 14 100

There are 14 of the respondents total population answered that they were scratching their
anus. In table 3, the researchers identify the factors that may affect the presence of E.
vermicularis ova on the fingernails which are hand washing and nail trimming. It shows that
100% were scratching their anus but regularly practicing hand washing. On the other hand, there
were 9 (64.3%) out of 14 respondents answered that they were scratching their anus but regularly
trimming their nails while 5 (35.7%) were scratching their anus but trimmed their nails
occasionally. The results illustrate that proper hand washing and regular nail trimming affects the
presence of E. vermicularis in the fingernails.

DISCUSSION
E. vermicularis is a common intestinal parasite that is still an issue of childrens
parasitism. Intestinal parasitism is one indicator of poor personal hygiene, lack of adequate
environmental sanitation, overcrowding, and poverty (Sung et al., 2001). Enterobiasis is not a
major disease but a disturbance accompanied with itchiness on the anus that is experienced by
the infected child. Female worm of E. vermicularis tends to lay eggs in the perianal area which
causes irritation and itchiness. In order to ease the itchiness, the child scratches the perianal areas
were embryos are deposited. Autoinfection occurs when the contaminated hands or fingernails
are not washed before and after eating.
There are different factors that are associated with enterobiasis. In Korean study, among
personal hygiene factors involving children, thumb-sucking and fingernail-trimming were highly
associated with enterobiasis (Kim et al., 2010). Thumb sucking is one of the factors that
contribute autoinfection. Totanes et al. (2009) also asserted that untrimmed nails can influence
the transmission of E. vermicularis ova. A case-control study had demonstrated that children who
bite their fingernails or who do not wash their hands before meals are at higher risk for ingesting
eggs from the environment (Sung et al., 2001). In the current study, it showed that only few of
the schoolchildren in Cabili Elementary School were having those kinds of factor that highly
associated with enterobiasis. In the results, 12.12% out of 198 were having a habit of thumb
sucking, 12.1% have seldom trimmed their fingernails, 3.5% were nail biting and 16.7% have
seldom washed their hands. But it doesnt mean that they have enterobiasis. The child will only
be infected unless his/her fingernails are contaminated with E. vermicularis ova. Scratching the
perianal area and exposing the hands to the infected environment are some ways to transfer the
ova on the fingernails. Fingernails pick up the embryos during scratching from the perianal
region (Royer et al., 1962). Kim et al., (2010) said that children with the habit of scratching
around the anus were more infected by E. vermicularis than those who do not have this habit.
Moreover, infection occurs when the eggs in infective stage are accidentally ingested from a
contaminated environment (Kang et al., 2006). The individuals with the contaminated fingernails
are susceptible with the infection for they have the more chance of ingesting the ova.
The infection can be diagnosed by a method known as transparent tape swab technique
where transparent adhesive tape is put on skin around the anus. Since the embryos are also found
on the fingernails during scratching, the infection could also be diagnosed by trimming the
fingernails where the E. vermicularis ova reside. In the current study, the researchers were
undergone laboratory procedures and slide examination using the dirt on the fingernails as
specimen to identify the presence of E. vermicularis ova. However, there were no E.
vermicularis ova or ova of other parasite detected on each of the specimens.
In the current study, only 14 out of 198 schoolchildren (7.07%) were scratching around
the anus. This could be the reason that lessens the chance of detecting the E. vermicularis ova on
the fingernails. Even if the fingernails of 14 participants were contaminated with ova, factors that
include washing of hands and trimming of nails can eliminate the presence of ova if done
regularly. As a result, out of 14 schoolchildren who were scratching the around the anus, 14
(100%) were washing hands regularly and only 9 (64.3%) were trimming nails regularly. Though
5 out of 14 (35.7%) were not trimming their fingernails regularly, they still wash their hands
during and after eating that also contribute the elimination of ova on the fingernails. Hand
washing and nail trimming are considered to be the basic of proper hygiene. Totanes et al. (2009)
stated that the spread of enterobiasis can be limited by proper hygiene and sanitation. Therefore,
proper hygiene affects the presence of E. vermicularis ova on the fingernails.
Other than proper hygiene, there is still another factor that could affect the result of the
current study. The school administrators mentioned that DepEd had conducted deworming
program in the school on the past months. However, they could not tell the specific anthelmintic
drug and treating schedule. DOH (2011), in partnership with DepEd, prescribing 400 mg of
albendazole or 500 mg of mebendazole, single dose on schoolchildren (Grade 1-6) in public
school every January and July. This means that the treating schedule is on every 6 months with
albendazole or mebendazole as anthelmintic drugs. Anthelmintic therapies for enterobiasis are
successful that includes mebendazole and albendazole (St Georgiev, 2001). Horton (2000)
illustrated the albendazoles cure rate in 27 studies involving children aged 2-15 years old with
enterobiasis that is 98% effective with a recommended single dose of 400 mg. Other than
albendazole, mebendazole is also effective. Lormans et al. (1975) conducted a study of 94
subjects treated with mebendazole. In a post-treatment examination, patients were found
negative of enterobiasis (Lormans et al., 1975). In the current study, 84.3% have participated in
deworming program. Since the anthelmintic drugs are found to be effective, therefore the 167
participants were not infected with E. vermicularis. Hence, the treated anthelmintic drugs to the
schoolchildren contributed to the absence of E. vermicularis ova on the fingernails.
Our study has several limitations. First, there were just few of the participants have done
scratching in perianal region. Besides, 100% of them were practicing good hygiene as they are
hand washing regularly. Second, the participants were not really having enterobiasis because
many of them were taking anthelmitic drugs.
Based on the study, children who have a good hygiene in terms of hand sanitation give a
negative result for the presence of E. vermicularis ova on the fingernails. In addition, deworming
program of the school prevents the participants from getting infected with E. vermicularis.

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