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Food Control 20 (2009) 942945

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Food Control
journal homepage: www.elsevier.com/locate/foodcont

Prevalence of intestinal helminth eggs on vegetables grown in wastewater-irrigated areas of Titagarh, West Bengal, India
N. Gupta, D.K. Khan, S.C. Santra *
Department of Environmental Science, University of Kalyani, Kalyani 741 235, Nadia, West Bengal, India

a r t i c l e

i n f o

a b s t r a c t
A total of 46 wastewater samples (untreated: 24 and treated: 22), 35 soil samples and 172 vegetable samples were collected from the wastewater-irrigated area of Titagarh to assess its contamination level with intestinal helminth. 83.3% of raw wastewater, 68.2% of treated wastewater, 68.6% of soil and 44.2% of vegetables in the study area were found to be positive for helminth ova. Vegetables grown in this area were found positive for Ascaris lumbricoides (36%), Trichuris trichiura (1.7%) and hookworms (6.4%). A. lumbricoides was the most predominant species observed in all the samples. Of all the vegetables examined, Pudina was most commonly contaminated followed by Lettuce, Spinach, Coriander, Celery and Parsley. High percentage of viable-stage intestinal helminth egg positive vegetable samples grown in the wastewater-irrigated study area may pose serious public health hazards. 2009 Elsevier Ltd. All rights reserved.

Article history: Received 20 February 2008 Received in revised form 5 February 2009 Accepted 10 February 2009

Keywords: Wastewater irrigation Ascaris eggs Trichuris eggs Hookworm eggs

1. Introduction Wastewater reuse in agriculture is an ancient practice that has been generally implemented worldwide. Hussain, Raschid, Hanjra, Marikar, and van der Hoek (2001) estimated that at least 20 million hectares in 50 countries are irrigated with raw or partially treated wastewater. Agricultural deployment of wastewater for irrigation is based on the value of its water content and its constituents, which are used as fertilizers (Kowal, Pahren, & Akin, 1980). However, crop irrigation with insufciently treated wastewater may result in health risks. The use of sewage efuent for irrigation exposes the public to the dangers of infection with a variety of pathogens such as bacteria, viruses, protozoa and helminths. Thus the benet of wastewater reuse is limited by its potential health hazards associated with the transmission of pathogenic organisms from the irrigated soil to crops, to grazing animals and humans (Korentajer, 1991). There is sufcient epidemiological evidence that the agricultural use of untreated urban wastewater leads to an increased risk of infection with intestinal helminth among the exposed farm workers and their families as also consumers of crops that are normally eaten uncooked (Shuval, Fattal, & Yekutiel, 1986). Gaspard, Ambolet, and Schwartzbrod (1997) also reported that the higher health risk is associated with helminth infections compared to other pathogens because helminths persist for longer periods in the environment, its host immunity is usually low to non-existent and the infective dose is small. An important charac-

teristic of these organisms is the production of a cyst or ova stage, which aids their survival. The Titagarh area was selected for this study as the entire agricultural produce cultivated in this area caters to the need of Kolkata city and its suburbs including Titagarh for salad vegetables, and since this area is generally irrigated with raw (untreated) and treated wastewater, the vegetables are likely to pose a threat to public health. A study carried out in wastewater-irrigated area of Titagarh indicated that 18.75% of the studied population which consumed uncooked sewage-irrigated vegetables was infected with Ascariasis as compared to 4.28% of the control population and the difference was signicant. The study also indicated that Ascariasis was the most prevalent helminth infection (18.75%) followed by hookworm infection (4.16%) and Trichuriasis (2.08%) (Gupta, 2008). The objective of the present study was to determine the prevalence of helminth eggs on vegetables grown in wastewater-irrigated area of Titagarh in order to ascertain that the consumption of these vegetables represent a potential hazard to human health, especially when the vegetables are eaten raw. 2. Materials and methods 2.1. Study area The study area, Titagarh is a suburban Industrial town located in 24-Parganas District (North), West Bengal, India. It is situated in the east side of the river Hooghly (a tributary of the river Ganges) 22 km North of Kolkata, the capital city of West Bengal. Titagarh Municipality has an old conventional Sewage Treatment Plant. The system is for treatment of raw sewage from commercial

* Corresponding author. Tel.: +91 33 2580 8749; fax: +91 33 2582 8282. E-mail address: scsantra@yahoo.com (S.C. Santra). 0956-7135/$ - see front matter 2009 Elsevier Ltd. All rights reserved. doi:10.1016/j.foodcont.2009.02.003

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as well as domestic sources as discharged by the people of Titagarh and parts of Barrackpore municipality. In the Sewage Treatment Plant, raw sewage is being treated in the activated sludge treatment plant where the sewage rst enters into primary sedimentation tank. From primary sedimentation tank, the efuent is sent to the aeration tanks. After mechanical aeration, the efuent is sent to the secondary settling tanks. From the settling tank, the nal efuent is directly taken to the adjoining agricultural land through concrete pipe. Both untreated and treated sewage water are used for irrigation purpose in the study area. Sewage treatment plant operators are often to release raw wastewater due to pressing demand of the farmers of the surrounding agricultural land. The common vegetables grown in the study area are Pudina, Lettuce, Spinach, Coriander, Parsley etc. Most of these vegetables cultivated in this site are supplied to wholesale vegetable markets in Kolkata and the rest enter the local markets. The present study was carried out during January and August 2006. 2.2. Detection of helminth eggs in vegetables Lettuce (Lactuca sativa), Pudina (Mentha viridis), Celery (Apium graveolens), Coriander (Coriandrum sativum), Spinach (Spinacia oleracea) and Parsley (Carum petroselinum) were selected for this experiment because these are generally eaten uncooked. A total of 172 vegetable samples were collected randomly from the periurban area of Titagarh. A portion of the vegetables were weighted (100 gm for all vegetables) into plastic bag and washed with 2 L of physiological saline solution (0.95% NaCl). The washing water was then left for about 10 h for sedimentation to take place. The top layer was discarded and the remaining washing water was centrifuged at 2164g for 15 min. The supernatant was discarded and the residue was collected carefully. The concentration of helminth eggs in the residue was investigated using the technique of Tlman Rivas modied by Bailenger (1962). Microscopic observation of helminth eggs in sample was performed in Mac Master Counting cell at 100-fold magnication. 2.3. Detection of helminth eggs in irrigation water and soil A total of 46 wastewater samples (untreated: 24 and treated: 22) and 35 soil samples were collected from the wastewater-irrigated area of Titagarh to assess their contamination level with intestinal helminth. For soil analysis, 100 gm of soil samples were collected in plastic bag. In case of irrigation water, a volume of 2 L was analyzed for untreated wastewater and that of 10 L for treated wastewater. The water and soil samples were also examined by the technique of Bailenger (1962). The helminth eggs at different stages of maturation were identied (Suzuki, 1981). 2.4. Analysis of data Data were compiled in a spreadsheet (Microsoft Excel, Version 2000) and analyzed as appropriate using descriptive statistics.

Table 1 Status of helminth contamination in analyzed samples of wastewater, soil and vegetables. Samples Raw wastewater Treated wastewater Wastewater-irrigated soil Wastewater-irrigated vegetables No. of samples examined 24 22 35 172 No. and (percentage) of positive samples 20 15 24 76 (83.3) (68.2) (68.6) (44.2)

Table 2 Occurrence of Ascaris, Trichuris and hookworm eggs in raw and treated wastewater. Sample No. of eggs [range and (mean)]/l A. lumbricoides Raw wastewater Treated wastewater 1872 (38.12) 1060 (23.72) T. trichiura 0.34 (1.19) 0.22 (0.39) Hookworms 215 (8.08) 19 (4.68)

eggs (Table 1). The helminth eggs identied from wastewater, soil and vegetable samples of the study area included those of Ascaris lumbricoides (round worm), Trichuris trichiura (whip worm) and hookworm. Data obtained by analyzing raw and treated wastewater used for vegetable irrigation are summarized in Table 2. The result showed that in both raw (untreated) and treated wastewater, concentration of Ascaris eggs was found to be highest, followed by hookworm eggs and Trichuris eggs. After treatment of the raw wastewater in the Titagarh Sewage Treatment Plant, the load of helminth eggs decreased to some extent but considerable level of helminth egg contamination still remained in the treated wastewater used for irrigation. Of the 172 vegetables tested, 62 (36%) were found positive for A. lumbricoides, 3 (1.7%) for T. trichiura and 11 (6.4%) for hookworm (Table 3). Of all the examined vegetables, Pudina was most commonly contaminated followed by Lettuce, Spinach, Coriander, Celery and Parsley. The study also indicated that the most common parasite in vegetables examined was A. lumbricoides. 4. Discussions The present survey has demonstrated the contamination of wastewater-irrigated vegetables with Ascaris eggs, Trichuris eggs and hookworm eggs. This study shows that viable-stage ova are present in the raw (83.3%) and treated (68.2%) wastewater used for irrigation and cause soil contamination. Helminth eggs present in wastewater constitute a risk when used in irrigation. These eggs are very resistant in the environment and they can survive in water, soil and crops for several months/years (Feachem, Bradely, Garelick, & Mara, 1983). Bryan (1977) observed that eld vegetables were directly contaminated with irrigation water or indirectly by contact with contaminated soil. Many epidemiological studies have revealed an excess of parasitic contamination associated with raw wastewater reuse in irrigation (Al Salem & Tarazi, 1992; Bouhoum & Schwartzbrod, 1997; Bradely & Hadidy, 1981; Cifuentes, Blumenthal, Ruiz-Palacios, & Bennet, 1992; Srivastava & Pandey, 1986). Of the 172 vegetable samples that were collected, processed and examined, 76 of them were contaminated with parasites. From the study it is found that Pudina samples are most commonly contaminated with helminth eggs. This could be attributed to the dense foliage of these vegetables offering a large contamination surface. This foliage also protects cysts and eggs against hostile environmental factors (Shuval et al., 1986). High percentage of helminth contamination found in Lettuce and Spinach samples could be explained by the fact that broad-

3. Results A total of 46 wastewater (24 untreated and 22 treated), 35 soil and 172 vegetable samples were examined for ascertaining the presence of helminth eggs in wastewater-irrigated area of Titagarh, West Bengal, India. This study showed that high percentages of examined samples were positive for embryonated helminth eggs. It is noted that 83.3% of untreated wastewater samples, 68.2% of treated wastewater samples, 68.6% of wastewater-irrigated soil and 44.2% of vegetable samples were found positive for helminth

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Table 3 Helminth egg distribution in vegetables grown in wastewater-irrigated area of Titagarh, West Bengal, India. Vegetables No. of samples examined No. and (percentage) of positive samples A. lumbricoides Lettuce Parsley Spinach Pudina Celery Coriander Total 32 30 30 32 28 20 172 14 (43.8) 7 (23.3) 11 (36.7) 16 (50) 7 (25) 7 (35) 62 (36) T. trichiura 0 0 1 1 0 1 3 (0) (0) (3.3) (3.1) (0) (5) (1.7) Hookworm 3 (9.4) 1 (3.3) 2 (6.7) 3 (9.4) 1 (3.6) 1 (5) 11 (6.4)

leaved vegetables such as Lettuce, Spinach, and Cabbage etc are having large surface areas which are in direct contact with the sewage contaminated soil surface (Larkin et al., 1978). It is found that among three different intestinal helminth parasites identied in the study, A. lumbricoides was the most predominant species observed in all samples and recorded the highest prevalence (36%). This is consistent with the ndings in metropolitan region of Sao Paulo, Brazil (de Oliveira & Germano, 1992). Ascaris (round worm) is one of the most resistant of the enteric pathogens and it is often used as a parasitological indicator (Watson, Satchwell, & Jones, 1983). About 25% of the world population is infested with Ascaris and the infection is more prevalent in the developing world (Blumenthal, Strauss, Mara, & Cairncross, 1989). Bryan (1974) reported three epidemics of Ascariasis in Germany associated with food contaminated with wastewater. A study in Jerusalem (Shuval, Yekutiel, & Fattal, 1984) provided strong evidence that massive infection of both Ascaris and Trichuris may occur when salad and vegetable crops are irrigated with wastewater. A study in Hamdan, Iran showed 90% Ascaris contamination in vegetables (Sayyed Tabai & Sadjjadi, 1998). Choi and Chang (1967) in Korea found 56% and 40% Ascaris contamination in Cabbage and Radish samples, respectively. In Ghana, Amoah, Drechsel, Abaidoo, and Ntow (2006) reported that contamination rates with Ascaris in Lettuce, Cabbage and Spring onion were 60%, 55% and 65%, respectively. 1.7% of the total vegetables examined in the study area found contaminated with T. trichiura. A previous study on parasitic contamination of vegetables in Ghana showed 3% of Lettuce and 2% each of Cabbage and Spring onion were Trichuris affected (Amoah et al., 2006). Another study in Nigeria revealed 5.1%, T. trichiura contamination in examined vegetables (Damen, Banwat, Egah, & Allanana, 2007). In this study, 6.4% of the total vegetables examined were found contaminated with hookworm. Amoah et al. (2006) in a study on vegetables in Ghana showed that 5% of Lettuce and 3% each of Cabbage and Spring onion samples were contaminated with hookworm. A study in Brazil reported 6.4%, 10.2%, 7.7%, 28.6% and 4% hookworm contamination in Lettuce, Wild Chicory, Chicory, Arugula and Parsley samples, respectively (Simes et al., 2001). In Nigeria, hookworm contamination rate in vegetables was found 19.8% (Damen et al., 2007). The result obtained in this study supports previous research on the contamination of vegetables with intestinal helminth parasites and suggests that there is a great potential of acquiring intestinal helminth infection from ingesting raw produce (Amahmid, Asmama, & Bouhoum, 1999; Choi & Lee, 1972; Coelho, Oliveira, Milman, Karasawa, & Santos, 2001; da Silva, Marzochi, CamilloCoura, Messias Ade, & Marques, 1995; de Oliveira & Germano, 1992; Erdogrul & Sener, 2005). High percentage of helminth contamination of vegetables observed in the wastewater-irrigated area of Titagarh might have severe public health implications. The parasites found in the

vegetables of the study area were considered pathogenic to man and the consumption of such contaminated vegetable crops might constitute a health risk for the consumers of these produce. Both crop consumers and agricultural workers are at high risk of parasite infection in the study area. This is because the wastewater being used in irrigation in the study area does not meet the WHO standard for unrestricted irrigation and is therefore unsafe for use in the production of green leafy vegetables which are generally eaten raw. For agricultural irrigation of crops that are eaten uncooked, it recommends a value of 61 helminth egg/l (WHO, 1989), and recent epidemiological research work shows that a limit of <0.1 helminth egg/l is needed if children under 15 years are exposed (Blumenthal, Mara, Peasey, Ruiz-Palcios, & Stott, 2000). The prevention of this risk can be achieved by an integrated set of approach which may include proper wastewater treatment, crop restriction and appropriate wastewater application techniques. Beside these, practice of basic food safety rules in the use of wastewater-irrigated vegetables may ensure safety. Prior to consumption, thorough washing and disinfecting of vegetables are highly recommended. To be more precise, it is advisable to wash vegetables with tap water to remove the mud, then to soak them in a solution with 3060 ppm concentration of iodine for 30 min and nally rinse them again carefully (Nematian, Nematian, Gholamrezanezhad, & Asgari, 2004). A comprehensive health education program should also be undertaken for creating awareness of the risk involved among the farming community and general population in the use of untreated or partially treated wastewater for irrigation of agricultural crops. Acknowledgement The authors gratefully acknowledge University of Kalyani for providing nancial support and necessary facilities for the research work. References
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