|Year : 2016 | Volume
| Issue : 4 | Page : 141-150
Current status of Schistosoma mansoni infection and its snail host in three rural areas in Gharbia governorate, Egypt
Basma M El Sharazly1, Dina M Abou Rayia1, Sanaa N Antonios1, Samia Hanim H Eissa2
1 Parasitology Department, Faculty of Medicine, Tanta University, Tanta, Egypt
2 Zoology Department, Faculty of Science, Tanta University, Tanta, Egypt
|Date of Submission||27-Aug-2016|
|Date of Acceptance||29-Sep-2016|
|Date of Web Publication||8-Mar-2017|
Basma M El Sharazly
Kafr El-Zayat, Gharbia Governorate, 31611
Background Human schistosomiasis is one of the most important neglected tropical diseases. Ongoing control measures have markedly decreased the incidence of the disease. There are currently no data on newly acquired infections.
Aim The aim of the study was to determine the prevalence of Schistosoma mansoni infection among school children in Gharbia governorate and carry out a malacological survey on common snail hosts.
Materials and methods A cross-sectional study was carried out in three rural areas of Gharbia governorate: Tanta, Kafr El-Zayat, and El-Mahala El-Kobra. Parasitological examination of 110 stool samples was performed using direct wet smear, formol–ether concentration technique, and the Kato–Katz method. An immunological test was also performed to detect S. mansoni antigen in urine. Snail vectors were collected from different water streams, identified morphologically, and examined for infection using shedding and crushing methods. Statistical analysis was conducted using SPSS, version 16.
Results The prevalence of S. mansoni infection was found to be 1.8% among school children of the studied areas. Risk factors were age and previous exposure to canal water. In the malacological survey, six species of freshwater snails were found and morphologically identified. Biomphalaria alexandrina was widely distributed but did not show any cercarial shedding.
Conclusion Although the rate of S. mansoni infection among school children is low, they can be a potential infective pool for the rest of the community.
Keywords: Egypt, Gharbia governorate
|How to cite this article:|
El Sharazly BM, Abou Rayia DM, Antonios SN, Eissa SH. Current status of Schistosoma mansoni infection and its snail host in three rural areas in Gharbia governorate, Egypt. Tanta Med J 2016;44:141-50
|How to cite this URL:|
El Sharazly BM, Abou Rayia DM, Antonios SN, Eissa SH. Current status of Schistosoma mansoni infection and its snail host in three rural areas in Gharbia governorate, Egypt. Tanta Med J [serial online] 2016 [cited 2018 Jun 22];44:141-50. Available from: http://www.tdj.eg.net/text.asp?2016/44/4/141/201724
| Introduction|| |
Human schistosomiasis is one of the most important parasitic diseases. It is reported to be endemic in 77 countries in tropical and subtropical regions, leading to infection of about 250 million individuals worldwide . The regions of the Middle East and North Africa represent high endemic spots for schistosomiasis, especially Egypt, which has about 7.2 million infected individuals .
In Egypt, Schistosoma mansoni has nearly completely replaced Schistosoma haematobium in the Nile Delta, and has spread to other regions of the country, especially after construction of the Aswan High Dam .
Since the survey conducted in the year 2000 ,, no surveys have been carried out on the actual current prevalence of schistosomiasis in Gharbia governorate, which is a matter of concern considering the changing spectrum of the disease due to the control measures, which have succeeded in reducing the prevalence of infection all over Egypt, from 3% in 2003 to 0.3% in 2012 .
Detection of S. mansoni eggs in stool samples is the gold standard for the diagnosis of S. mansoni infection, but it has some limitations . Immunodiagnosis of schistosomiasis has been proposed to overcome some of these limitations and assess the active infection .
The aim of this study was to determine the prevalence of S. mansoni infection among school children in three rural areas in Gharbia governorate using direct parasitological microscopic examination, the Kato–Katz technique, and immunodiagnosis of S. mansoni antigen. The distribution of the intermediate snail host in the water streams of these regions was also investigated.
| Materials and methods|| |
This study was conducted in three rural areas of Gharbia governorate, named Tanta, Kafr El-Zayat, and El-Mahala El-Kobra, which are endemic for schistosomiasis. In each area, two rural districts were selected. Gharbia governorate is an agricultural area that is located in the middle of the Nile Delta on the Rosetta branch of the river Nile in Egypt. The climate in these areas varies from hot and highly humid in summer to cold in winter. Relative humidity ranges from 70 to 90% . These rural areas depend on water streams as the main source of water for domestic and irrigation purposes, which create favorable snail-breeding conditions ([Figure 1]).
|Figure 1 Exposure of children to canal water in the studied area in Kafr El-Zayat. The upper left photo shows living Biomphalaria alexandrina snails collected from the same area.|
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This study was conducted on 110 school children living in these rural areas, aged 6–15 years, after getting approval from their parents and from the head of their schools. A questionnaire was administered and history was taken from the children’s parents regarding name, sex, age, type of water supply, parents’ occupations, canal water contact, and previous schistosomiasis treatment.
A cross-sectional parasitological and malacological study was conducted. Permission and official approval to carry out the study and ethical approval were obtained from the Research Ethics Committee of the Faculty of Medicine, Tanta University.
Stool samples were collected from school children from the six rural districts in clean plastic containers. The samples were processed in the Parasitology Laboratory, Faculty of Medicine, Tanta University. Other pathogenic parasites detected during microscopic stool examination were also recorded. The Kato–Katz technique was applied following the protocol of Katz et al. . Urine samples were also collected from some children (35 children) with a history of frequent water contact activities and subjected to a rapid immunological diagnostic test called circulating cathodic antigen (CCA) cassette test obtained from Rapid Medical Diagnostics (Pretoria, South Africa). According to the manufacturer’s instructions, the valid test should be read within 20 min and is considered positive if two bands appear, a control band and a positive band. If only the control band appears, the test is considered negative and if the control band does not appear the test is considered invalid. All remnants of stool and urine samples were discarded following safe disposal measures in the Tanta Faculty of Medicine general incinerator according to the faculty research and safe disposal rules. The children who were positive for S. mansoni and other intestinal parasites were referred to the Health Unit to receive free treatment.
Snail vectors were collected from water streams in the study area by two trained field collectors using long-handled nets. They were collected over a period of 1 year, and during all seasons of the year. During snail collection, physical characteristics of the habitat were observed, such as vegetation abundance, water turbidity, and speed of the water current. Snails collected from each water stream were transferred into labeled plastic buckets with water and vegetation. The number of captured snails was recorded. They were identified morphologically on the basis of shell morphology .
Snails were kept in plastic containers; each one contained 25 snails at a time in 1.5 l of dechlorinated water; they were fed with lettuce leaves. The containers were maintained at 27–29°C. Water in the containers was changed every 2 days. To verify S. mansoni infection, the snails were examined using the traditional techniques of shedding and crushing methods. In the shedding method, 4–5 snails were put in a beaker containing about 5 ml of clear, dechlorinated water. They were then exposed to artificial light for 1 h and checked for shedding of cercariae. In the crushing method, the snails were squeezed between two glass slides and examined under a light microscope for the presence of sporocysts .
The data were analyzed using SPSS, version 16 (SPSS Inc., Chicago, Illinois, USA), and P-values less than 0.05 were considered significant.
| Results|| |
Prevalence of S. mansoni infection
Microscopic examination of stool samples detected no positive cases of S. mansoni infection on applying the direct smear method. The use of formol–ether concentration revealed one (0.9%) positive case, whereas the Kato–Katz method revealed two (1.8%) positive cases. The urine CCA method revealed four (11.4%) positive cases of S. mansoni infection. Two of them were also positive by the Kato–Katz technique and one was positive by the three diagnostic procedures (formol–ether, Kato–Katz, and CCA). There was a statistically significant difference between CCA and the other diagnostic techniques (formol–ether and Kato–Katz) (P=0.003 and 0.013, respectively) ([Table 1] and [Figure 2] and [Figure 3]).
|Table 1 Prevalence of Schistosoma mansoni infections in the studied group as determined by different diagnostic tests|
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|Figure 2 Stool smear by Kato–Katz technique showing Schistosoma mansoni egg (×400).|
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|Figure 3 Circulating cathodic antigen rapid immunochromatographic test: the first two cards to the left show positive results for Schistosoma mansoni; the third card shows only the control line in a negative sample.|
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Factors affecting the prevalence of S. mansoni infection in the studied group are presented in [Table 2]. Only age and canal water exposure had a significant statistical relation with the prevalence of S. mansoni infection (P=0.021 and 0.037, respectively).
|Table 2 Factors affecting the prevalence of Schistosoma mansoni infection in the studied group|
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Other parasites were accidentally detected in 24 children during this study. Eight (7.3%) children had Entamoeba histolytica cysts, six (5.5%) had Giardia lamblia cysts, six (5.5%) had Enterobius vermicularis eggs, and two (1.8%) had Hymenolepis nana eggs ([Table 3] and [Figure 4]).
|Figure 4 Stool smears of other accidentally detected parasites (×400). (a) Hymenolepis nana egg. (b) Giardia lamblia cyst. (c) Enterobius vermicularis eggs. (d) Entamoeba histolytica cyst.|
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A total of 1500 random snail samples were collected during this study. Examination of the physical characteristics of the water bodies showed that water streams were moderately turbid and covered by large amounts of weeds, algae, and other garbage such as plastic, clothes, and fallen leaves. Six species of freshwater snails were identified morphologically according to the procedure followed by Brown  and Ibrahim et al.  ([Table 4]).
|Table 4 Prevalence of Biomphalaria alexandrina snails in relation to other freshwater snails in Gharbia governorate|
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Diagnostic features of the detected discoidal snail species
The shell is discoidal, thin to rather thick, and sometimes fragile. It has spirally coiled whorls that are rounded at both sides. It is umbilicated on the left side and has a more depressed spire with a deep suture on the right side. The shell sculpture is smooth in texture and includes slightly curved regular growth lines. The aperture is suboval, clearly wider than high. The umbilicus is open and wide.
The shell is thin, flattened, and discoidal. It has spirally coiled whorls, which increase slowly in diameter outwards. The upper right side of the shell is convex, whereas the lower left side is flattened. Usually a carination is present near the base of the shell. The whorls at the apex are depressed, forming a depression, which is almost as deep as the suture. The sculpture consists of a fine closely curved growth line.
H. duryi is distinguishable from Biomphalaria spp. by having a higher shell, more angular whorls, and a deeply and wider umbilicus on the left side. The number of whorls varies from four to five and their sculpture comprises slightly curved regular growth lines. The aperture is suboval, and slightly higher than wider with a thin sharp outer lip ([Figure 5]).
|Figure 5 Discoidal snail species isolated from the studied area. (1) Biomphalaria alexandrina. (2) Planorbis planorbis. (3) Helisoma duryi.|
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Other accidentally discovered snail species
The shell is sinistral and globose ovoid to elongate. It has a sharply pointed apex. The whorls are generally convex and more rounded at the periphery and are separated by shallow sutures. The shell of P. acuta is easily confused with that of Bulinus truncatus but it can be distinguished by sharply pointed spires, whorls without shoulder angles, and absence of umbilicus in the body whorl.
The shell is sinistral and globose. The whorls are generally convex and rounded at the periphery and are separated by deep sutures. The uneven curvature of the whorls tends to produce a blunt shoulder. The spire is clearly shorter than the aperture and the apex is usually blunt or obtuse. The umbilicus is visible and varies from small to rather big.
The shell is dextral, thin, somewhat fragile and transparent, and ovoid in its outline. The whorls are tightly coiled, convex, and separated by deep sutures. The spire is much shorter than the aperture, not exceeding half the height of the aperture. The sculpture is more distinct on the body whorl and includes fine transverse lines of growth only.
Concerning the site distribution of the snail species, B. alexandrina had the highest distribution in Kafr El-Zayat (66.2%), followed by Tanta (17%) and El-Mahala El-Kobra (16.8%) ([Table 5]). Regarding the seasonal variation of snail species, B. alexandrina was more abundant in summer (47.1%) and autumn (28.6) rather than in spring (18.2%) and winter (6.1%) ([Figure 6] and [Table 6]).
|Table 5 Distribution of the collected snail species in the three cities of Gharbia governorate|
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|Figure 6 Other freshwater snails isolated from the studied area. (4) Physa acuta. (5) Bulinus truncates. (6) Lymnaea natalensis.|
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Examination of the collected B. alexandrina snails by shedding and crushing methods revealed that none of them was infected.
| Discussion|| |
Control of schistosomiasis using mass drug administration of praziquantel in Egypt was extremely successful. It succeeded in reducing both prevalence and morbidity. However, these reports were, in most cases, collected from the whole country or region-wide, thus neglecting the potential impact of focal high-risk areas of transmission, which becomes masked by results from larger areas in other parts of the country with currently negligible rates . The presence of these focal areas of high-risk transmission may necessitate the modification of local control programs taking into consideration the fact that praziquantel is ineffective against schistosomula and immature worms .
The present work revealed that the prevalence of infection with S. mansoni was 1.8% in children aged 6–15 years. These results are in accordance with other reports from governorates of the Nile Delta that have the same agricultural conditions as those of Gharbia governorate. El-Sahly et al.  found that the prevalence of S. mansoni infection in the Nile Delta was 3–7%. Also, Zaher et al.  detected S. mansoni ova in 0.33% of outpatients in Sharqia governorate. The Egyptian Ministry of Health report indicated that the percentage of S. mansoni infection has decreased to 4% compared with 45% in 1960 . Similarly, Bahbah and El-Shikhsalem  found that the rate of schistosomiasis among children in Menoufia governorate was 0.8%.
However, this study is not in agreement with that of El-Khoby et al.  and El-Hawey et al. , who found that the prevalence of S. mansoni in Gharbia governorate was 37.7%. The results of this work show that there is a decrease in the prevalence of intestinal schistosomiasis in the Nile Delta, which suggests that control programs in Egypt are having a good impact on schistosomiasis in this region.
Identifying the local risk factors of infection at multiple levels is crucial to understand how transmission varies within small spatial scales and how it changes over time . In this study the association between schistosomiasis and water contact is well documented as a significant risk factor for schistosomiasis. Swimming in water streams, washing clothes and utensils using infected stream water, crossing the water with bare feet, and fishing activities were the determinant factors for infection. Similar findings have been reported in previous studies among rural children and adolescents in different countries .
In the present study, although the female participants had a relatively lower infection rate compared with their male counterparts, the difference was statistically nonsignificant. This may be attributed to recent changes in the work engaged in by the female population in rural areas. At present, most members of the female community in rural areas share agricultural work with their male counterparts. In addition, they wash utensils and clothes in infected water. Previously, male exposure to infected water was higher than that of women, leading to a high incidence of infection in the male population .
The present work revealed that the age group 11–15 years had significantly higher infection prevalence than the age group 6–10 years. The increase in infection rate in this study as age increases may be attributed to more contaminated water contact over time among the students as they engage in activities such as irrigation, farming, fishing, and swimming. This result is in agreement with that of El-Khoby et al. , who reported that the risk factors in Gharbia governorate for S. mansoni infection were age more than 10 years and male sex . In contrast, El-Morshedy et al.  found higher prevalence rate among young children (below 10 years). They attributed this to partial immunity . This discrepancy in results may be due to the difference in the habits of people. In our study, frequent water contact was noted to be higher among older children.
Diagnosis of schistosomiasis by microscopic examination of stool samples could be time-consuming and expensive. The Kato–Katz technique has been the backbone of intestinal schistosomiasis diagnosis. However, it shows low sensitivity for detecting low-intensity infections, which are commonly seen in children . Recent studies have shown that a commercially available, urine-based cassette test (CCA) is a promising method for the diagnosis of S. mansoni infection .
In our work, four cases gave positive results by CCA, whereas only two were positive by microscopic examination. It was suggested by Stothard et al.  that CCA-positive, microscopy-negative specimens could be due to recently acquired (i.e. pre-egg patent) infections or low-intensity infection in this young age group. These could remain largely undetected by direct egg detection methods such as microscopy, owing to a temporal lag in diagnostic patency as worms mature to fecundity . In this work a single CCA performed on urine samples showed higher sensitivity for S. mansoni diagnosis than multiple Kato–Katz thick smears obtained from stool samples. Since CCA are only released from living worms, the rapid tests can be used to monitor the dynamics of existing worm burdens, as well as post-treatment clearance .
The accidental detection of other parasitic infections among school children such as E. histolytica, G. lamblia, E. vermicularis, and H. nana raises a serious health concern. It signifies the fact that children are the highest risk groups in the community and serve as sources of infection and transmission. Therefore, targeting children, through school-based programs, is mandatory to control a variety of infections, especially helminths.
As regards snail survey, the Egyptian freshwater snail fauna and its geographical distribution are changing over time. In the last few decades, changes have occurred in the water habitats that have influenced the snail distribution in Egypt. These changes may cause alterations to the epidemiology of schistosomiasis in Egypt . In the present study, B. alexandrina was the dominant snail species in the three rural areas of Gharbia governorate. In addition, it was more abundant in Kafr El-Zayat rather than in Tanta and El-Mahala El-Kobra. Similar results were reported by Eissa et al. , who found that snails of the family Planorbidae are characteristically common among freshwater snails throughout Gharbia governorate. This may be attributed to the fact that Gharbia governorate is characterized by a wide range of water habitats − from large lakes and ponds to small rainwater pools and sluggish streams. These habitats, which mainly have stagnant or slowly running water and fairly dense aquatic vegetations, are the preferred habitats for most of the species of freshwater snails, especially Biomphalaria .
Regarding the seasonal variation in the distribution of B. alexandrina snails, it was found that they were more abundant in summer and autumn than during spring and winter. This may be due to favorable environmental conditions during this period, which include physical, chemical, and biological elements. This result comes in agreement with that of Karimi et al. , who stated that late summer and autumn had the optimal temperature required for breeding and reproduction of snails. El-Khayat et al.  mentioned nearly similar results. They reported that B. alexandrina was most abundant during autumn and summer. Hussein et al.  reported that the snail population was high in autumn. The present result partially agrees with that of Abd El-Wakeil et al. , who reported that the highest number of snails was during spring and summer.
In the present study there was no cercarial shedding by B. alexandrina snails at any of the sites of collection. This indicates that there is very low transmission potential of S. mansoni infection in the study area. A complete absence of infected snails may be attributed to the effective control measures and the continuous monitoring carried out by the snail control field workers of the Egyptian Ministry of Health and Population in these locations. Similarly, Tucker  mentioned that the actual number of infected snails in nature may be very low and cercariae may be shed for only a limited period of time. Moreover, cercarial release from field-collected snails may also be inhibited by a variety of contaminants and invertebrates harbored by the snails .
In this study a negative correlation was noted between H. duryi and the schistosomiasis snail host, Biomphalaria. These results concur with those of Yousif et al. . Therefore, H. duryi may negatively affect the distribution of Biomphalaria snails in the future and further studies are needed to evaluate the impact of H. duryi on the aquatic biota.
One of the dominant snail species in the study areas was P. acuta. This snail transmits avian schistosomes, causing cercarial dermatitis, which has recently been reported as an emerging infection. It is expected that cercarial dermatitis will become an issue of increasing public health concern for people in contact with freshwater in Egypt .
| Conclusion|| |
Despite the low prevalence of S. mansoni infection among school children in Gharbia governorate, Egypt, they could act as a potential infected pool for the rest of the community. The risk factors for S. mansoni infection were revealed to be age older than 10 years and frequent contact with canal water. In addition, antigen detection rapid test (CCA test) is a promising diagnostic tool for the diagnosis of S. mansoni infection and we recommend its use in prevalence surveys. Moreover, this work sheds light on the common species of freshwater snails in the Nile Delta region. B. alexandrina is widely spread, but fortunately all collected snails were uninfected. However, its continuous presence indicates that the environmental conditions are favorable for it and that there is still a risk for schistosomiasis transmission and continuous monitoring is still needed. Lastly, our work identified Kafr El-Zayat as a site of S. mansoni infection where most of the positive cases were found and where the snail vector (B. alexandrina) was established. Hence, it could be the cause of spread of the disease into new areas. Therefore, control interventions are essential in this area.
The authors thank the Head of Medical Parasitology, Faculty of Medicine, Tanta University, for his general support. They also gratefully acknowledge Abdel Moaty, in the Medical Parasitology Lab, for his technical assistance in collecting and maintaining the snails used for the tests.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]