Frequency of parasitic infections in Arachishypogaea L (groundnuts), Citrulluslanatus seeds (watermelon seeds), and Ziziphusspina-christi (nabag) sold by street vendors in Khartoum State, Sudan: a cross-sectional study

Introduction

Intestinal parasitic infections can be transmitted orally through the ingestion of infective agents from infected food, water, or contaminated hands.^1,2 Food contamination and food borne parasitic diseases frequently occur globally. These are estimated to amount to 23.2 million cases and 45,927 deaths annually.³ Fresh fruits and vegetables could be a source of dissemination of foodborne parasitic diseases.^4,5 A study in Ghana revealed Ascaris lumbricoides (roundworm), Ancylostoma duodenale (nematode), Necator americanus (hookworm), and Strongyloides stercoralis (threadworm) contaminations in tiger nuts.⁶ Another study on tiger nuts reported other contaminants such as animal droppings, fungi toxins and bacteria.⁷ Groundnuts, Ziziphus spina-christi (nabag), and watermelon seeds (tasali) are widely consumed in Africa and the Middle East.⁸ Nabag and tasali are widely eaten in Sudan.

These crops are natural sources of carbohydrates, proteins, fats, -iron, calcium, ascorbic acid, thiamine, riboflavin, and niacin.^9-12 Groundnuts in Sudan are mainly used for oil extraction, but can be eaten as a snack: raw, or after roasting without its external cortex envelop.¹³ Nabag is eaten after the sweet pulp of the fruit is dried to produce fine flour.¹⁴ The flour is placed in small metal cups and steamed. Dried pulp flour and water are also mixed with sesame and shaped into small balls.¹⁵ Fruit pulp prepared in these two ways can be consumed either immediately or stored for future use. In addition to groundnuts, nabag, and tasali,¹⁶ many crop products represent an important and for some, the only source of income in Sudan.¹⁵

Intestinal parasitic infections are very common worldwide. They are often not diagnosed and hence not treated, leading to harmful effects which can be lethal in some cases. Food contamination may occur when food is prepared, stored, or handled; this is a common phenomenon in public places like the streets.¹⁵ Identifying parasitic contamination will help fight these infections, because knowing contamination rates allows to take the necessary preventive measures. The objective of this study was to identify parasitic contamination rates in Arachis hypogaea L (groundnuts), Citrullus lanatus seeds (watermelon seeds), and Ziziphus spina-christi (nabag) sold by street vendors in Khartoum State, in Sudan.

Method

Results

The participants in this study were 15 street vendors selling groundnuts, nabag, and tasali. The population was divided into six age groups: 10–20, 21–30, 31–40, 41–50, 51–60, and over 61 years. The most common age group was 31–40 (46.7%), followed by 41–50 (20%), 21–30 (13.3%), 10–20 (6.7%), 51–60 (6.7%), and more than 61 (6.7%). Eight (53.3%) of the 15 subjects were women, while seven (46.7%) were men.

The total parasitic contamination rate was 60% (27 samples), divided as follows: 20% (n = 9) for groundnut, 22.2 % (n = 10) for nabag, and 17.8 % (n = 8) for tasali. A Chi-squared test was used to test the relationship between crop type and detection of parasites, revealing an insignificant relationship with P = 0.757 (Table 1). The presence of both E. histolytica and G. lamblia accounted for 11.1% of the positive results.

The contamination rate assessed using FECT was 53.3% (24 samples), while the sugar floatation technique detected a contamination rate of 48.9% (21 samples); the correlation between detection and technique used was found to be highly significant at P = 0.000 (Table 2). Using FECT, the detected prevalence of E. histolytica, G. lamblia, and mixed contamination of E. histolytica and G. lamblia were 33.3% (15), 11.1% (5), and 8.9% (4), respectively; when using the sugar floatation technique, the detected prevalence of E. histolytica, G. lamblia, and mixed contamination of E. histolytica and G. lamblia were 37.8% (17), 8.9% (4), and 2.2% (1), respectively (Table 2). The prevalence rates of E. histolytica in groundnuts, nabag, and tasali were 15.6% (7), 8.9% (4), and 8.9% (5), respectively, and for G. lamblia were 2.2% (1), 6.7% (3), and 6.7% (3) (Table 3). Mixed contamination was found in groundnuts, nabag, and tasali in the following proportions: 2.2% (1), 6.7% (3), and 2.2% (1), respectively. Contamination rates for groundnut, nabag, and tasali detected by FECT were 20% (9), 20% (9), and 13.3% (6), respectively, while those detected using the sugar floatation technique were 20% (9), 13.3 % (6), and 15.5% (7).

The relationship between crop type positivity to contamination and technique used was negligible for both FECT (P = 0.655) and sugar floatation technique (P = 0.591) (Table 4). The 31-40 age group had the highest contamination rate (33.3%), followed by 41–50 (13.3%), more than 61+ (6.7%), 51–60 (4.4%), 21–30 (2.2%), and 10–20 (0%) groups. There was a significant association between seller age group and outcome positivity (P = 0.028). Contamination rates were 24.4%, 20%, and 15.6% in Khartoum state cities, i.e. Khartoum, Bahri, and Omdurman, respectively. There was no relation between city and contamination rate (P = 0.329). The results revealed that E. histolytica was the dominant parasite across all city, with prevalence rates of 17.8%, 17.8%, and 8.9 % in Khartoum, Bahri, and Omdurman, respectively; while G. lamblia had lower prevalence rates in Khartoum, Bahri, and Omdurman, at 13.4%, 4.4%, and 8.9%, respectively. Relationship testing between city and species detected yielded insignificant results (P = 0.460).

Discussion

Groundnut and watermelon seeds are important cash crops. They respectively represented 43,532 USD (59,620 tons) and 49,355 USD (74,149 tons) of Sudanese exports in 2018.¹⁸ To the best of our knowledge, this study was the first to look into the parasitic contamination of groundnuts, nabag, and tasali sold by Sudanese street vendors. Two studies in Ghana and Nigeria estimated parasitic infections in the root plant Cyperus esculentus L. (tiger nuts); those studies were similar to some degree, and found contamination to be significant.^6,7 The overall contamination rate in the previous study was 60%, which is considered significant. This rate was expected, because vendors sold their products unprotected and handled them with their bare hands. Contamination does not necessarily happen at the selling stage; it can happen during crop farming, harvesting, storage and transport, and even at home, according to Idahosa, 2011¹⁹ and Porter et al., 1990.²⁰ Contamination may occur during the planting phase as a result of polluted irrigational water, as mentioned by Keraita et al., 2002,²¹ which is contaminated as a result of inadequate or insufficient sanitation infrastructures to cope with the rate of urbanization.²² In our study, the most contaminated crop was nabag (22.2%), followed by groundnut (20%), and finally tasali. This may be due nabag being sold raw, which also exposes it to the previously mentioned contamination factors, particularly during the growing and harvesting phases; When nuts fall to the ground, they may come into contact with potentially polluted soil, as well as other external contaminants carried by wind, humans, or animals.

However, because groundnuts grow beneath the soil surface,¹³ they might be damaged if the nuts comes into contact with soil that has been contaminated, or with polluted irrigational water.

Despite this, salting and roasting may help to reduce contamination. Tasali had the lowest contamination rate in comparison to others. This could be explained by it being protected by the fruit (watermelon) during growing and harvesting, as well as the washing, salting, and roasting processes that occur before it is eaten. In our study, the parasites detected belonged to two species: E. histolytica (44.4%) and G. lamblia (26.7%). E. histolytica was the most common of both in all sampled crops (groundnut: 17.8% vs 4.4%, nabag: 15.6% vs 15.6%, and tasali: 11.1% vs 8.9%). Groundnuts had the highest rate of E. histolytica contamination (44.4%). This finding is consistent with a Nigerian study on tiger nuts, which are similar to groundnuts in their cultivation process, and in which E. histolytica was identified as the only protozoan parasite (25% contamination rate).^6,7,13 The precise prevalence rates of E. histolytica and G. lamblia in Khartoum State are unknown; however, some studies may help to provide a more concise view. E. histolytica and G. lamblia were found to be common parasites in the following areas: Alhag-yousif (G. lamblia: 46.4% and E. histolytica: 15.50%), Elengaz (G. lamblia: 33.4% and E. histolytica: 3.6%), and Alkalakla (G. lamblia: 33.4% and E. histolytica: 3.6%).^17,23,24 These results suggest that contaminated crop products could be a major source of infection.

Between the saturated sugar floatation technique (prevalence rate: 48.9%) and FECT (prevalence rate: 53.3%), the FECT was the found the most efficient technique for crop examination (P = 0.000). This finding was supported by Abdalazim et al., (2019)¹⁷ (P = 0.000). FECT outperformed the saturated sugar floatation technique in detecting both parasites, with FECT detecting 44.2% of E. histolytica and G. lamblia while the sugar floatation technique detected 40% of E. histolytica and 11.1% of G. lamblia. According to our study, seller sex and location (stationed vehicle or no vehicle) did not affect the positivity of crop samples to contamination (P-value: 0.807 and 0.329 respectively), while the age group played a role in the occurrence of contamination.²⁵

Conclusions

The population in Sudan should be alerted about the diseases that could be caused by consumption of contaminated crops or foods whether from local street venders or shops. People should be careful before they consume any food or crop and either consume clean foods or cook well before consumption to get rid of any possible pathogens. The farmers, street venders and anyone related to the food should be educated about food hygiene and the health authorities should undergo regular health checks and maintain control on crops, foods, restaurants, shops and street vendors to minimize possible exposure of individuals to parasites and other microorganisms or toxins due to consumption of contaminated foods. Future studies should address contamination of foods and crops from streets, markets, restaurants and if possible homes.

Data availability