Parasitic contamination of vegetables marketed in Arba Minch town, southern Ethiopia

Consumption of fruits and vegetables is highly beneficial since they form the major component of a balanced diet [1]. Fruits and vegetables are important sources of carbohydrate, vitamins, minerals and fiber [2‐4]. Considering such nutritional value, it is recommended that individuals should take a minimum of 400 g of fruits and vegetables per day. Fruits and vegetables also protect people from different non-infectious chronic diseases like cardiovascular problems [4, 5]. However; consumption of unwashed, raw or unhygienically prepared fruits and vegetables act as potential sources for the spread of various infectious diseases [2, 3, 6, 7].

Vegetables can be contaminated while growing in fields due to use of organic fertilizer or contaminated irrigation water or during harvesting, processing, distribution, sale and during consumption [8]. As a result, they have been involved in food-borne outbreaks [9]. Infective stages of intestinal parasites (IPs) are the most common contaminants of vegetables, as they are abundant in the environment [10]. Parasites such as Cryptosporidium species (spp), Giardia lamblia (G.lamblia), Entamoeba histolytica (E.histolytica), Ascaris lumbricoides (A.lumbricoides), hookworms, Enterobius vermicularis (E.vermicularis), Trichuris trichiura (T.trichiura), Toxocara spp., Hymenolepis spp., Taenia spp., Fasciola spp. and members of the family Trichostrongylidae could infect humans [11]. Hence, globally, an estimated 3.5 billion people are infected, and 450 million are sick from intestinal parasite infections (IPIs), with an estimated 200,000 deaths each year [12]. Intestinal parasites cause significant morbidity and mortality throughout the world, especially in tropical and sub-tropical countries [13]. Infection with IPs has been known to cause iron deficiency anemia, growth retardation in children and other physical and mental health problems [14, 15].

An effective way of selecting appropriate intervention steps to reduce pathogenic micro-organisms on vegetables is to identify sources of contamination and ecology of the pathogens [16]. However, in developing countries including Ethiopia, the medical impact of food-borne diseases is not known or under estimated because of absence of routine diagnosis and monitoring for the etiologic agents of food-borne infections [17]. The risk has been reported to be higher in towns, where there is poor hygienic and sanitary practice accompanied with overcrowding [5, 13].

Vegetables may get exposed to parasite contaminants in the pre-harvest (cultivation, irrigation, livestock manure) and post-harvest handling (storage, transportation) phases or while processing for consumption [18, 19]. Use of insufficiently treated wastewater and improperly composted manures are responsible for the high rates of parasitic contamination [18, 20]. Bad hygienic practice during production, transport, processing and preparation by handlers including consumers also contribute in vegetable contaminations [21].

Gamo Gofa Zone is known for the production of diverse types of fruits and vegetables that some cover the majority of country level consumption and others are distributed by retailers for local consumption. In Arba Minch (capital of the zone), it is common to see fruits and vegetables being sold in shops, at open markets and more commonly at road sides. It is also common to observe people buying those fruits and vegetables and eating in raw without washing. Despite this, the local health care units have no system to monitor the risks posed by unhygienic marketing and consumption of fruits and vegetables. A study conducted in Arba Minch town in 2014 showed a parasitic contamination rate of 54.4% [22]. Since then, efforts have been made to improve the water supply; sanitation and hygiene (WASH) of the population. Moreover national bi-annual deworming of risk population groups is being implemented since November 2015. Even though we suggest all these efforts indirectly decrease the contamination rate of vegetables, it should be supported by research based evidence. Therefore, this study was designed to determine the level of parasitic contamination of selected vegetables and associated factors in local markets of Arba Minch Town, Ethiopia.

A total of 347 vegetable samples were collected from local markets and examined for parasitological contamination. Vegetables were collected from four local markets namely Sikela (66.3%), Shecha (16.4%), Konso sefer (10.4%) and Yetnebersh (6.9%). Results of parasitological investigation showed that 87 vegetable samples were microscopically positive for at least one parasite. This gives an overall contamination rate of 25.1% (95%CI, 21.0–29.7). Among a total of 87 contaminated samples, 61 (70.1%) and 26 (29.9%) were contaminated with one and two parasite species respectively (Table 1).

The species and stages of parasites detected were ova of A. lumbricoides and hookworms; cysts of G. lamblia, E. histolytica/dispar and Balantidium coli (B. coli); oocysts of Cryptosporidium and Cyclospora species; and larvae of Strongyloides like parasite. Cyst of E. histolytica/dispar (8.4%) was the most frequently detected parasite followed by cyst of G. lamblia (6.9%) and oocyst of Cryptosporidium species (5.8%). Among the five vegetable types included in the study, E. histolytica/dispar was detected only in two vegetables namely tomato (22/29) and carrot (7/29). On the contrary, G. lamblia was abundantly detected in samples of cabbage (16/24) followed by green pepper and carrot (4/24 in each) (Table 2).

In recent years, the federal ministry of health, in collaboration with concerned non-governmental organizations, is showing strong commitment to combat the public health impact of human parasites. However, the burden of intestinal parasitosis is still unacceptably high due to favorable climatic conditions, unsanitary conditions and little awareness by the community about the transmission and prevention of parasitic diseases. Open defecation is common in Ethiopia which, in turn, contaminates raw edible fruits and vegetables as well as water [26].

The overall parasitic contamination rate in the present study was 25.1% which is in line with findings from Nigeria and Iran [10, 27]. However it is lower than many of the previous findings elsewhere [22, 28‐34]. On the other hand, it is higher as compared to studies from Iran, Turkey, Maiduguri (Nigeria) and Sudan [34‐36]. These variations between the present study and previous results might be due to variations in geographical locations, climatic and environmental conditions, the kind of fruit and vegetable samples examined and number of fruits/vegetables examined, laboratory methods used, and sanitary status of the community.

As compared to similar study conducted in Arba Minch town in 2014, the present study showed a decrease in contamination rate by more than half (54.4% vs 25.1%) [22]. These differences might be due to ongoing bi-annual deworming program targeting helminthiasis. Moreover, improvements in the implementation of WASH program accompanied with continuous health education by the health extension workers to avoid open defecation might also play an important role. Differences in kind and number of fruits and vegetables assessed could also be responsible for the discrepancy.

In this study, tomato (35.0%) was the most frequently contaminated vegetable. On the contrary, tomato was the least contaminated vegetable according to previous studies [30, 32]. Leafy vegetables and/or those with uneven surfaces (salad, cabbage) make the parasitic stages more easily attach to their surfaces unlike to those having smooth surface (green pepper, tomato) [37]. Our finding is against the logic because we didn’t include equal number of the vegetables from each kind and very few numbers of samples were examined especially for salad. However, compared to green pepper, tomato was 32.1% less likely to be contaminated with parasites, similarly with study findings in Nigeria [10].

In the present study, cyst of E. histolytica/dispar (8.4%) was the most frequently detected parasite followed by G. lamblia (6.9%) which is in line with previous finding from Sudan [33]. However it varies among many other studies [10, 30‐33, 35]. Iodine wet mount was examined in the present study which increases the sensitivity of stool microscopy for detection of protozoa cysts. Ova of A.lumbricoides were the predominant contaminants according to previous similar study done in Arba Minch. The national deworming program against soil transmitted helminths might bring this shift. In addition to this, variation in the season and kind of fruits and vegetables considered also matters.

Cryptosporidium spp (5.8%) was the third most common parasitic contaminant in the present study. However, the rate of contamination was lower as compared to findings from Ghana (17%), Egypt (29.3%) and Jimma, Ethiopia (12.8%) [4, 7, 30]. It is common to use animal excreta as fertilizer in the study area that we had expected higher rate of Cryptosporidium contamination. However, variations in the laboratory methods used might bring this variation as we used only ziehl Neelson staining technique.

Double contamination by two parasite species was observed in all kinds of vegetables (7.5%) but the rate of double infection is much lower as compared to studies conducted in different parts of Ethiopia. In addition, unlike to the previous studies, no more than two parasites have contaminated the same vegetable sample at a time [22, 26]. This is an indication that the level of contamination of vegetables is decreasing owing to implementation of parasite control activities in the country.

Vegetables directly supplied by farmers to vendors were 3.5 times more likely to be contaminated with parasites as compared to vegetables supplied by large scale vendors. Large scale vendors receive vegetables on the farm land, pack and transport to Arba Minch town using their vehicle, store it properly and distribute to small scale vendors. On the other hand, small scale vendors who receive vegetables directly from farmers transport it either via back of animals or human labor; vegetables are readily exposed to contamination in this case.

In the present study, display of vegetables without washing was not significantly associated with parasitic contamination (p = 0.232) with probable reason of few number of washed vegetables included in the study (n = 49). However, previous studies in Turkey and Iran showed that washing of vegetables contributes for significant decrease in the rate of parasitic contamination [37, 38]. According to study results by Fallah et al, traditional washing with tap water reduces rate of parasitic contamination (32.6% vs 1.3%) but does not totally remove parasites from vegetables. Pre-washing could not inactivate viable infectious parasitic stages. Hence, in order to totally remove parasites, vegetables need to be washed following standard technique using chemicals like calcium hypochlorite and automated fruit-vegetable washer [38].

Previous studies have identified that means of display, type of water used for washing before display and contamination extent of irrigation water were significantly associated with parasitic contamination of vegetables [10, 30, 34]. In order to identify potential sources or factors which contribute for parasitic contamination of vegetables, large scale follow up study starting from farm to in-house consumption is recommended.