The Prevalence of Parasite Contamination of Vegetables and the Risk Factors in Their Transmission in Nsukka Ecological Zone, Enugu State
Chapter One
Objectives of the study
The objectives of this study were to:
- Investigate the prevalence of parasitic contamination of vegetables in Nsukka Ecological Zone.
- Identify the parasites and establish their seasonal distribution on different vegetables.
- Correlate the seasonal distribution of parasites on different vegetables with the prevailing climatic conditions in the ecological zone.
- Establish the major sources of parasitic contamination of vegetables in the area.
- Identify the risk factors in the transmission of these parasites.
- Assess the parasitic quality of water used for the irrigation of these vegetables and establish whether or not they meet the recommended standard.
- Provide surveillance for potential parasitic food-borne illness associated with consumption of raw vegetables in the area.
- Recommend measures and interventions that will minimize the risk of contamination of vegetables and/or transmission of infection to humans.
Chapter Two
Literature Review
Vegetable
In a very broad sense, the term “vegetables” refers to edible plants, commonly collected and/or cultivated for their nutritional value for humans. Most often, the botanical definition of vegetable is the “edible part of a plant” (FAO/WHO, 2005). It is also referred to as the fresh edible portion of herbaceous plants, roots, stems, leaves or fruits; these plants are either eaten fresh or prepared in a number of ways (Damen et al., 2007). Fruits are therefore, a subset of vegetable as the term fruit refers to the mature ovary of a plant which encloses the seed (FAO/WHO, 2005). Some examples of vegetables include cabbage, egg plants, pumpkin, carrot, green, okra, tomatoes, cucumber, etc.
Production systems for vegetables
In recent years, increasing international trade has resulted in globalization of the food supply with the consequent intensification of crop production as well as the introduction of new crop varieties to provide exotic varieties and year-round supplies to importing countries. This has influenced both the type of cultivation system and the distribution of cultivation areas (FAO/WHO, 2008).
Cultivation systems vary considerably between and within countries, but fall into two broad categories: open field, and protected cultivation systems. Within these categories there can be wide variation in terms of inputs, location, size, productivity, target market and the extent to which one is practiced rather than another. Protected cultivations can increase yield, provide year-round supply, and allow greater control of abiotic factors and pests compared to open field culture systems. However, protected cultivation systems require a higher level of inputs per hectare, thus concentration of contaminants may occur (FAO/WHO, 2008).
Cultivation systems can be further divided into soil and soilless culture systems (Johnson, 2008). Soilless systems are suited to produce with short cultural cycles and high plant density. They are often used for the production of high-value-added crops. Plant nutrition can be better controlled in these systems and soil contamination is avoided; however, the universal requirement for safe water and hygiene control of the aquatic systems remains. Plug systems (these begin with seedlings grown in plugs) offer a less labour intensive production system, with reduced use of agrochemicals. Numerous soilless culture systems are in place around the world, such as the Nutrient Film Technique (NFT) system, pot and sacs systems, aeroponics, ebb-and flow system, and floatation systems (Johnson, 2008).
Cultivation systems can also be classified into organic and conventional production systems. Organic farming is the method of farming without using agrochemicals, synthetic mineral fertilizers, and chemical plant protection products in the control of pests and disease (FAO/WHO, 2008; Klapec and Borecka, 2012). Conventional farming, on the other hand, involves the use of agrochemicals, synthetic mineral fertilizers, and chemicals in the control of pests and disease. In Nigeria, however, a blend or mix between organic and conventional farming is also observed.
Global production and trade of vegetables
The vegetables most widely produced and consumed in the world have been examined from 1980 to 2004. Current production of the 15 vegetables studied has risen above 1980 levels e.g. by 74% for green (sweet) corn (maize) to 259% for spinach and eggplant. For 11 of the 15, production has risen over 100%. The rise in production has been relatively steady for almost all the vegetables studied (FAO/WHO, 2005). From 1980 to 2004, the global production per annum (p.a.) of fruit and vegetables grew by 94%. During that period the average yearly production growth of vegetables (4.2% p.a.) was almost twice that of fruits (2.2% p.a.) (FAO/WHO, 2008).
The world harvest area and production of leafy vegetables such as lettuce, chicory and spinach, cabbages and other brassicas has increased progressively since the early 1990s. The harvest area for lettuce and chicory increased by 218% and that for spinach increased by 300% in the period 1986 to 2006. In 2006, the major producers of lettuce and chicory were China (50%) and the United States of America (20%). China also produced 84% of all the spinach produced globally (FAO/WHO, 2008).
CHAPTER THREE
MATERIALS AND METHODS
Study Area
The study area was Nsukka Ecological Zone, Enugu State (Figure 1). The name “Nsukka” refers to a town and a Local Government Area (L.G.A.) in Enugu State, South-East Nigeria. The town hosts the famous University of Nigeria, Nsukka. It has an estimated population of 167,086 and is blessed with beautiful vegetation dotted with several soft green hills and a cool temperate-like weather. The town has commercial banks, hospitals, schools and network of transportation and communication systems. Other towns that share common border with Nsukka include Enugu Ezike, Orba, Obollo-Afor (formerly centre of the palm oil trade), Ede-Oballa, Uzo Uwani and Nkpologu. Nsukka L.G.A. has a population of 309,633 at the 2006 census (Eyo et al., 2014).
Nsukka Ecological Zone comprises seven L.G.As, Nsukka, Udenu, Igbo Eze North, Igbo Eze South, Uzo Uwani, Igbo Etiti and Isi Uzo (Figure 2), 88 rural communities and the Nsukka urban centre. It is located at the northern boundary of southeastern Nigeria between latitudes 6°30′ to 7°54′ N and longitudes 6°54′ to 7°54′ E. The zone has a total land area of 3,402 km2 and an estimated population of 1,377,001 as at 2007 (Madu, 2007; Ivoke, 2008). The entire study area is ecologically homogenous with the vegetation consisting of the guinea-savannah mosaic type with its characteristic grass-topped hills and dry valleys. For much of the year, the area experiences high temperatures (25ºC – 30ºC) with two distinct seasons, a rainy season of 7 months from April to October and a shorter dry season of 5 months from November to March. The annual precipitation is between 1200 – 3000 mm. Rivers are few but they are natural springs which serve as all-season sources of water. Subsistence agriculture and trading are the dominant occupations of the inhabitants with potatoes, yam, rice, maize, cassava, bananas, palm oil, groundnuts, pepper, citrus fruits, as the major crops (Ofomata, 1979). The soil consists of humus, though relatively not rich in nutrient as it appears to be interlocked in clay particles. Consequently, water does not easily drain through it especially during the rainy season, hence water logged conditions tends to prevail (Ekeh and Ekechukwu, 2009; Ajaero et al., 2013).
Study Design
A total of four hundred and eighty eight (488) samples of six different vegetable types, Solanum marcrocarpon fruit (garden egg), Solanum species leaf (garden egg leaf), Amaranthus species (spinach or green), Telfairia occidentalis (Pumpkin leaf), Ocimum basilicum (scent or basil leaf) and Solanum lycopersicum (tomatoes), were collected from three (3) farms and three (3) markets in both dry and rainy season between January and October, 2013. All dry season samples were collected from January – March 2013 whereas rainy season samples were collected from July – October 2013.
The samples were collected once every forth night within the seven (7) months period. 40, 41, 41, 40, 39 and 40 samples of garden egg, garden egg leaf, spinach, pumpkin leaf, scent leaf and tomatoes respectively were collected from the farms while 39, 42, 40, 42, 41 and 42 samples of garden egg, garden egg leaf, spinach, pumpkin leaf, scent leaf and tomatoes respectively were collected from the markets. A sample was taken as a portion of vegetable weighing 100grams (Uga et al., 2009; Edosomwan et al., 2011). 18 samples of irrigation water were also collected from the three farms during the dry season.
Climatic data for Nsukka Ecological Zone was obtained for both the rainy and the dry seasons within the seven months (7) study period.
CHAPTER FOUR
RESULTS
A total of four hundred and eighty-eight (488) samples of six different vegetable types were examined from three (3) farms and three (3) markets in Nsukka Ecological Zone. Eighteen samples of irrigation water were also examined in the three farms during the dry season. Out of the 488 samples, 253 (51.8%) were contaminated with parasites. Among the contaminated vegetables, 31(39.2%) of Solanum marcrocarpon fruit (garden egg), 50(60.2%) of Solanum species leaf (garden egg leaf), 47(58.0%) of Amaranthus species (spinach or green), 62(75.6%) of Telfairia occidentalis (Pumpkin leaf), 42(51.2%) of Ocimum basilicum (scent or basil leaf) and 20(24.4%) of Solanum lycopersicum (tomatoes) were contaminated.
Ten (10) parasites belonging to ten different genera were encountered. The parasites included some species of protozoa, cestodes and nematodes. The protozoan parasites were Entamoeba histolytica and Cryptosporidium parvum; the cestodes were Taenia and Hymenolepis species; the nematodes were Ascaris species, hookworm, Trichuris trichiura, Strongyloides stercoralis, Enterobius vermicularis and Trichostrongylus species (Plates 1- 10).
CHAPTER FIVE
DISCUSSION, CONCLUSION AND RECOMMENDATIONS
Discussion
Prevalence of parasites in vegetables
Out of 488 samples of vegetables examined, 253 were contaminated, representing a contamination rate of 51.8%. This shows a considerable high level of parasitic contamination of raw edible vegetables in Nsukka Ecological Zone. This finding was consistent with previous reports from Tripoli, Libya (Abougrain et al., 2009), Abuja, Nigeria (Malam and Soso, 2012), Metro Manila, Philippines (Su et al., 2012) and Southern Iran (Olyaei and Hajivandi, 2013), where the contamination rates were 58%, 51.60%, 45.0% and 43.7% respectively. Similarly, Ekwunife et al. (2014) reported parasitic contamination rate of 42% in local food drinks (soya milk, kunu-zaki and zobo) sold in open markets in Enugu Municipality, Nigeria. Lower contamination rates of 16.2% and 11.0% were detected in Saudi Arabia (Al-Megrin, 2010) and Zamfara State, Nigeria (Shehu and Amina, 2014) respectively while higher contamination rates of 65%, 75.9% and 79% were detected in Tehran, Iran (Gharavi et al., 2002), Kisii Municipality, Kenya (Nyarango et al., 2008) and Khorramabad, Iran (Ezatpour et al., 2013) respectively. The observed differences in the rate of contamination may be due to differences in agricultural practices, varying degrees of environmental contamination with faeces in the different regions, methods used for detection of the parasites, accessibility of vegetable farms to infected livestock and wild animals, types and number of vegetables sampled as well as post-harvest handling of vegetables.
The rate of parasitic contamination was higher in vegetables collected from the markets than those collected from the farms. This could be as a result of cross-contamination between market vegetables. Vegetable vendors in the ecological zone usually buy different vegetables, possibly from different farmers, and packed them in the same bag while conveying them to the market. This could lead to the contamination of those vegetables that were not contaminated in the farm. Furthermore, vendors in the market used the same water to wash/rinse different vegetables which could also lead to the contamination of those vegetables that were not contaminated from the farm, thus increasing the contamination rate. This finding agreed with Beuchat and Ryu (1997) and FAO/WHO (2008), but contrasted with previous work by Gharavi et al. (2002) who reported a higher prevalence in farm than in market samples.
The farm within the University of Nigeria, Nsukka (UNN) had higher rate of contamination than the other two farms. The farm was located close to human habitation (Male hostel) and some of the students practiced open defecation. This, faeces could be carried to the farm, especially through flood during rainy season, and contaminate the vegetables. This agreed with FAO/WHO (2008) which reported that vegetable and herbs grown in urban, peri-urban, heavily industrialized or populated areas are more prone to potential contamination. Ikpa market also had higher rate of contamination than the other markets. This may be attributed to the poor drainage systems in the market. The waterlogged stinking gutters may contain parasites that could contaminate the environment especially after rainfall. These vegetables are usually heaped on small bags or polythene spread on the ground. As customers select to buy them some fall to the ground and may be contaminated with parasites with the consequent higher rate of contamination in this market. This is in consonance with Edosomwan et al. (2011) who reported higher contamination rates in markets where the vegetables were heaped on bare ground which might have been contaminated with eggs and cysts of parasites.
The leafy vegetables, Telfairia occidentalis (pumpkin leaf), Amaranthus species (green or spinach), etc. were significantly more contaminated than the fruit vegetables, Solanum lycopersicum (tomatoes) and Solanum marcrocarpon (garden egg) because they have uneven surfaces which facilitate sticking of parasites’ eggs, larvae, cysts and oocysts more readily to the surface of the leaves either in the farm or when washed with contaminated water. On the other hand, the fruit vegetables have smooth surfaces which reduce the rate of parasitic attachment. This finding was consistent with previous reports (Eneanya and Njom, 2003; Damen et al., 2007; Uga et al., 2009; Amaechi et al., 2011; Uttah et al., 2013; Eraky et al., 2014). Furthermore, the dense foliage of the leafy vegetables would protect the helmith eggs against unfavorable condition to their survival and persistence, such as sunlight, drying, and wind (Benti and Gemechu, 2014). Telfairia occidentalis was significantly more contaminated than the other vegetables because it is a creeper and as such in regular contact with the contaminated soil. It can also become heavily infested as a result of flooding or run offs during the rainy seasons in the farms. This is in agreement with the reports of Ogban et al. (2010) and Edosomwan et al. (2011).
The month of August recorded the highest rate of contamination while the least contamination was observed in the month of January and February for farm and market samples respectively. This was not absolutely consistent with previous work by Al-Binali et al. (2006) who reported that the months of November, January, February and May had the least prevalence of 8% while the months of December and April had the highest prevalence of 15.9%.
The seasonal variability of parasites showed that the rate of contamination was generally higher in the rainy season than in the dry season. This finding was consistent with previous reports (Al-Megrin, 2010; Said, 2012; Olyaei and Hajivandi, 2013; Eraky et al., 2014). It is therefore assumed that parasitic stages, eggs, cyst, oocyst, and larvae, on the surfaces of vegetables were not washed off by rain. Anuar and Ramachandran (1977) had reported that the eggs of Ascaris lumbricoides were difficult to wash off due to their adhesive nature. Rainfall could also be a major source of contamination as some of the vegetables are likely to be submerged under flood after heavy rainfall; there is a tendency that the flood must have carried with it parasitic stages and faecal waste from the surrounding environment since open defecation is a common practice (FAO/WHO, 2008; Edosomwan et al., 2011). Casteel et al. (2006) reported that faecal contamination is an important factor in the spread of disease caused by enteroparasites; helminth eggs might also remain viable for longer periods in moist environments than in dry ones (Simoes et al., 2001). Water does not interfere with the viability of eggs, and allows for the survival of the resistant forms (cysts) of parasitic protozoan (Simoes et al., 2001). These findings, however, contrasted the reports of Al-Binali et al. (2006) and Uga et al. (2009) who recovered more parasites in the dry than in the rainy season.
Conclusion
Raw edible vegetables are important vehicles of transmission of intestinal parasites, such as Ascaris species, Entamoeba histolytica, Taenia species, hookworm, Trichuris trichiura, Hymenolepis species, Strongyloides stercoralis, Enterobius vermicularis, Trichostrongylus species and Cryptosporidium parvum, in Nsukka Ecological Zone. There is also a possibility of transmission of zoonotic parasite, such as Echinococcus which causes hydatid disease and A. suum, through raw edible vegetables in the area. The large number of persons potentially at risk of infection with these parasites, both within and outside the ecological zone where the vegetables are exported to, makes it of significant public health importance.
Water used for irrigation purposes, in the ecological zone, did not meet the WHO recommended standard of ≤ 0.1 helminth egg per litre and thus is a source of contamination of vegetables. Other important sources of contamination are the use of animal manure, defecation on cultivated farmland and environmental pollution with faeces. Contamination from wild and domestic animals might also be possible. The use of wastewater and animal manure in the production of vegetables posed an occupational risk to the famer and is a health hazard to both the farmers and the consumers of such vegetables (Ayres and Mara, 1996; Damen et al., 2007; Tomass and Kidane, 2012; Shehu and Amina, 2014).
Climatic variables or factors such as rainfall, temperature and relative humidity influence the prevalence and abundance (intensity) of parasites in vegetables.
Raw consumption of vegetables without adequate washing and the habit of eating already prepared fruits and vegetables outside the home are important risks factors in the transmission of intestinal parasites to man via vegetables in the ecological zone. Another important anthropogenic attitude which has increased the risk of infection to farmers is that most of the farmers do not wear shoes and gloves during planting and harvesting of vegetables.
Recommendations
Vegetables cannot be removed from human diet, but can be excluded from the cycle of transmission and dispersion of parasites (Shehu and Amina, 2014). Control or elimination of pathogenic microorganisms from fresh fruits and vegetables can be achieved only by addressing the entire system, from the field to the point of consumption (Beuchat and Ryu, 1997).
It is therefore recommended that farmers should adequately treat wastewater and animal manure before using them to irrigate and fertilize raw edible vegetables. They should also wear personal protective equipments (PPEs) such as shoes and gloves. The application of treated animal manure should stop at least 120 days before harvesting an edible product that does come into contact with the soil (FAO/WHO, 2008). Alternatively, the government can subsidize the cost of environmentally friendly inorganic fertilizers to discourage the use of untreated animal manure by vegetable farmers.
Environmental pollution with human and animal faeces should be avoided to prevent consequent parasitic contamination of vegetables. Similarly, mass treatment of people infected with intestinal parasites is necessary to reduce the reservoir of infection.
Adequate washing of raw edible vegetables before consumption is highly recommended. Soaking vegetables in water containing common salt, vinegar, etc. for at least 10 minutes before washing was recommended (Fawzi et al., 2004). Washing raw edible vegetables severally in clean water has also been reported to be effective in decontamination (Beuchat and Ryu, 1997; Fallah et al., 2012). Reducing the rate of consumption of already prepared fruits and vegetables outside the home can reduce an individual’s potential risk of infection with intestinal parasites.
Health education of farmers, vegetable vendors and the general public on the public health importance of wastewater irrigation, the use of untreated animal manure in the production of vegetables, open defecation and environmental contamination with faeces as well as the need for adequate personal hygiene and washing of vegetables before consumption is advocated.
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