Contribution of wastewater irrigated vegetables to the prevalence of soil- transmitted helminth infection among female farmers in Addis Ababa, Ethiopia

doi:10.21203/rs.3.rs-3195259/v1

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Contribution of wastewater irrigated vegetables to the prevalence of soil- transmitted helminth infection among female farmers in Addis Ababa, Ethiopia

https://doi.org/10.21203/rs.3.rs-3195259/v1

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Background

Many farmers in and around Addis Ababa city rely on untreated wastewater for irrigation due to a growing population and limited access to reliable agricultural water sources. However, data on STH contamination of irrigated vegetables and farmer risk are scanty. This study aimed to determine the prevalence of STH in vegetables and female farmer stool samples in Ethiopia, as well as the association between helminths in vegetables and female farmers' stool.

Methods

A cross-sectional study was conducted between November 2021 and February 2022 to investigate the prevalence of helminths in vegetable samples and stool samples of female wastewater irrigated vegetable growers. A stratified random sampling technique was employed to select farming households. The sample size for each district was set by a proportionate allocation to the total number of homes. Two hundred fifty-two composite samples and 101 stool samples from the wastewater-irrigated farm were collected and analyzed. A questionnaire was utilized to collect qualitative data, while vegetable samples were used to obtain quantitative data. Stata version 14.0 was used to process the data. Using Poisson regression, the relationship between helminths in vegetable samples and farmer health was studied. Statistical significance was set at p-value < 0.05.

Result

STH were found in 67.5% of the vegetables and 20.8% of the female farmers' stools. Significant concentrations of Ascaris lumbricoides (vegetable 48.4% and stool 9.9%) were identified in all analyzed samples, followed by hookworm (vegetable 13.1% and stool 8.9%) and Trichuris trichiura (vegetable 5.9% and stool 2%). The presence of helminths in wastewater-irrigated vegetables and the level of infection in exposed farmers had a statistically significant positive association (p < 0.05).

Conclusion

Vegetables grown with wastewater irrigation are contaminated with STH, which could be a source of infections for farmers. Therefore, in addition to reducing occupational exposure, risk reduction programs should target households that have no knowledge how to prevent the spread of helminths.

Helminth

Vegetable

Irrigation

Female

Wastewater irrigation is used to manage water scarcity around the world, with approximately 20 million hectares of agricultural land irrigated using wastewater as of 2017. Due to limited freshwater resources, countries such as Israel (85%), Saudi Arabia (10%), China (55%), Mexico (60%), and Egypt (59.7%) rely extensively on treated wastewater for irrigation [1]. Irrigation is important in agricultural output in East Africa, contributing to food security and economic development. Several nations in the region, notably Ethiopia, Kenya, Tanzania, Uganda, and Sudan, have put irrigation systems in place to supplement rain-fed agriculture and minimize the effects of climate change [2]. According to research, using wastewater for irrigation increases soil transmitted helminth levels in soil and on plants, which can then be transmitted to humans by ingestion of contaminated plants [3, 4]. Female farmers are more vulnerable due to their higher exposure to wastewater during agricultural activities [3].

According to the World Health Organization, soil transmitted helminth infections impact about 1.5 billion people globally, with the largest illness burden occurring in Sub-Saharan Africa, Southeast Asia, and Latin America [5]. STH infections are a major contributor to the global illness burden in these regions, including malnutrition, anemia, and delayed cognitive development in children [6]. In Africa, the frequency of STH infections is notably high among vegetable growers that use wastewater for irrigation, with studies indicating prevalence rates ranging from 10–80% [7].

In Ethiopia, STH infections are a major public health concern, with research revealing high prevalence rates among diverse population groups. A study conducted in Jimma town, for example, reported a prevalence of 18.1% among peri-urban households [8]. Research in the Amhara region reported a prevalence of 60.6 among female vegetable farmers [9].

Another study conducted in the Southwest Bench Maji Zone indicated that females shared more than 36% of helminth infections as compared to males 33.7% [10]. However, there is a paucity of data on the prevalence of soil transmitted helminth infections among female vegetable farmers using wastewater for irrigation in the capital city of Ethiopia, Addis Ababa. The city is confronting serious wastewater management difficulties, many farmers in and around the cities rely on untreated wastewater for irrigation due to a growing population and limited access to reliable agricultural water sources [11].

Understanding the contribution of wastewater irrigated vegetables to the prevalence of soil transmitted helminths among female farmers in Addis Ababa is crucial for designing effective risk mitigation strategies. In this context, the purpose of the study is to investigate the prevalence of helminths in vegetables and female farmers, as well as the epidemiological link between vegetables and the risk of helminth infection among female farmers.

Study area

The study was conducted in Addis Ababa, Ethiopia's capital. Addis Ababa's current metro area population is 5,461,000 in 2023, a 4.4% increase from 2022 [12]. The city includes both well-designed and constructed modern neighborhoods as well as areas that are in poor condition and lack proper infrastructure. The study includes eleven subcities, such as Nifas silk lafto, Bole, and Akaki Kality. According to demographic predictions from 2014 to 2017, Nifas Silk Lafto's population in 2023 is 445,683, Bole's population is 435,421, and Akaki Kality's population is 255,348 [13]. Wastewater has been exploited for vegetable production in the research region, as it is in other low- and middle-income nations [11]. The vast majority of irrigated land is located around the Tinishu and Teleku Akaki rivers (Fig. 1).

The study area includes seven vegetable-producing locations known locally as Bisrategebrail, Gofa, Lafto, Saries, and Kera, irrigated by the Tinishu Akaki river, and Peacock-Urael and Akaki, irrigated by the Teleku Akaki river (Fig. 1).

Study design and period

A cross-sectional study was conducted from November 2021 to February 2022.

Population

Source population

All female farmers that practice wastewater irrigation for growing vegetables along the Tinishu and Teleku Akaki rivers.

Study population

Selected female farmers that practice wastewater irrigation for growing vegetables along the Tinishu and Teleku Akaki rivers.

Inclusion and exclusion criteria

Inclusion criteria

The wastewater farmers that were selected for the project met the following inclusion criteria: a) being located in one of the seven urban vegetable farming districts; b) being female farmer who has been cultivating for over the years and using wastewater for irrigation.

Exclusion criteria

The following exclusion criteria were considered: a) farmers who cultivate their land using day laborers; and b) farmers who use both alternate water sources and wastewater.

Sample size

The sample size was determined using the single population formula n = Z²P(1-P)/D². By considering a prevalence of 8.02% in a study conducted by Gaidhane et al. in 2022, [28] a marginal error of 5%, a 95% confidence level, and Z_1−α/2 is 1.96. Hence, the calculated sample size becomes 113.

where Z = 95% confidence interval P = Estimated prevalence rate

D = Marginal of sampling error N = Total study population

Sampling technique

A stratified random sampling method was used to sample farming homes, and the sample size for each district was set by a proportionate allocation to the total number of households in the area. The female household provided consent and was included in the study. Finally, 101 female farmers expressed interest in participating in the study. To investigate the prevalence of helminths in vegetable samples, 252 composite samples were obtained from a wastewater-irrigated farm using a random sampling technique. The samples were examined in the Ethiopian Public Health Institutes (EPHI) laboratory.

Data collection

The field farm baseline study employed interviews and observations. Before the survey, a pretest was performed on 5% of the calculated sample size in a nearby farming area that was not included in the study. To determine the prevalence of helminths, a health diary, and a self-reporting sheet were utilized.

Vegetable sample collection

A composite sample of three vegetables (Ethiopian Kale, Lettuce, and Swiss chard) was collected using a random sampling technique between 8:00 a.m. and 10:00 a.m. Each vegetable sample was placed in a sterile polyethylene bag and labeled with a unique number and collection date. The gathered samples were taken to the EPHI laboratory for further analysis on the same day. The vegetables were extracted into a liquid phase by first rinsing them entirely in a physiological saline solution (0.85% NaCl). A sample of 250 g soaking plastic carboys holding the physiological saline solution was sufficient for washing the vegetable sample. After removing vegetable soil-derived fragments and debris from the washing saline solution, wastewater was permitted to settle overnight [14].

Parasite detection

The liquid-phase vegetables were tested using the modified Bailenger method [14]. From overnight settled samples, as much of the supernatant as possible was removed, leaving the sediments at the bottom of the containers. The sediments were then transferred to three 50 ml centrifuge tubes and centrifuged at 1,500 RPM for three minutes. After that, a 15 ml acid/alcohol buffer solution and around 5ml ethyl acetate were added to the sediment and agitated, occasionally letting out the gas. After that, the mixture was centrifuged at 2,200 RPM for three minutes. Finally, as much of the diphasic supernatant as possible was removed, leaving around 1 ml of sediment or suspension for microscopic investigation. The identification of helminth eggs was done using shape and size, which was aided by the diagnosis of intestinal parasites picture available on a workbench.

Stool sample collection and examination

Each participant provided a 2 gm stool sample, which was collected using a clean, leak-proof, screw-cap stool cup labeled with a unique identifier. The specimens were then labeled and delivered to the laboratory. According to WHO recommendations, a Kato-Katz smear was performed for each sample and inspected microscopically to detect helminth eggs and to estimate the degree of infections based on fecal egg count [15]. The Kato-Katz slides were made as soon as the stool samples arrived in the laboratory.

Data quality management

To verify for errors, the generated data were entered into the statistical software EpiData version 3.1. The gathered tools' errors were corrected by revisiting the initial data original questionnaire. To collect lab data, the laboratory data collection sheet or format was employed, and the data were promptly entered into Excel. The laboratory equipment used was calibrated.

Data analysis

The generated data were checked for completeness and consistency. The cleaned data were entered into EpiData Version 3:1 and exported to STATA version 15.0 for analysis. To describe the presence of helminths in stool and vegetable samples, descriptive data analysis was utilized. Additionally, the relationship between helminth loads in vegetable samples and helminth per gram of stool matter from female farmers was evaluated using Poisson regression analysis. Statistical significance was set at p < 0.05.

Prevalence of helminths in vegetable samples

A total of 252 wastewater-irrigated vegetable samples were tested for the presence of helminths. In all vegetable samples, the overall prevalence of helminths identified was 67.5% (170/252). The findings revealed that all three types of vegetables were contaminated with at least one of the three soil transmitted helminths. Ascaris lumbricoides were found to have the highest contamination rate (48.4%), followed by Hookworm (13.1%) and Trichuris trichiura (5.9%) (Table 1).

Table 1

Prevalence of parasites in wastewater irrigated vegetables in Addis Ababa, Ethiopia, from November 2021 to February 2022.
Vegetables	Number of samples examined	Ascaris lumbricoid (%)	Hookworm (%)	Trichris trichiura (%)	Total (%)
Lettuce	84	61(72.6)	15(17.9)	7(8.3)	83(98.8)
Swiss chard	84	43(51.2)	11(13.1)	4(4.8)	58(69.1)
Ethiopian Kale	84	18(21.4)	7(8.3)	4 (4.8)	29(34.5)
Prevalence	252	122(48.4)	33(13.1)	15(5.9)	170(67.5)

Lettuce exhibited the highest rate of contamination for all three helminths, with 98.8% of samples tested found to be positive for at least one STH. Swiss chard had the second-highest prevalence, with 69.1% of samples testing positive, and Ethiopian kale had the lowest prevalence, with 34.5% of samples testing positive (Table 1).

As shown in Table 2, the highest prevalence of Ascaris lumbricoides was found in Bisrategebrail, Kera, and Akaki, with 66.7%, 63.8%, and 63.8% of the vegetables testing positive, respectively. For Hookworm, Peacock Urael and Akaki had the highest prevalence, with 13.8% and 16.6% of the vegetables testing positive, respectively, while Gofa had the lowest prevalence at 5.5% (Table 2).

Table 2

Prevalence of parasites in vegetable samples from seven wastewater irrigation farming sites in Addis Ababa, Ethiopia, from November 2021 to February 2022.
Site	Number of samples examined	Ascaris Lumricoides (%)	Hookworm (%)	Trichris trichiura (%)	Total (%)
Bisrategebrail	36	24(66.7)	7(19.4)	4(11.1)	35(97.2)
Gofa	36	10(27.8)	2(5.5)	1(2.7)	13(36.1)
Lafto	36	13(36.1)	6(16.6)	1(2.7)	20(97.2)
Saris	36	11(30.5)	4(11.1)	3(8.3)	18(50)
Kera	36	23(63.8)	3(8.3)	1(2.7)	27(75)
Peacock Urael	36	18(52)	13(13.8)	2(5.5)	25(69.4)
Akaki	36	23(63.8)	16(16.6)	3 (8.3)	32(88.8)

Prevalence of helminths in the farmers’ stool

The prevalence of soil transmitted helminths in the population studied was 20.8%, with 21 cases out of 101 samples. The most common helminth infection was Ascaris lumbricoides, which was found in 10 female farmers (9.9%), followed by hookworm in 9 farmers (8.9%), and Trichuris trichiura in 2 farmers (2%) ( Fig. 2).

The female farmer in Bistrategebrale (9.1%) tested positive for the three parasites at the site. Figure 2 shows that the Akaki site has the highest prevalence of Ascaris lumbricoides (20%), hookworm (20%), and Trichuris trichiura (6.6%). Furthermore, the prevalence of Ascaris lumbricoides is higher in Peacock and Bisrategebrail than in other sites.

Relationship between the prevalence of helminths in wastewater irrigated vegetables, and infection in female wastewater vegetable cultivating farmers

The prevalence of helminths in wastewater irrigated vegetables and the level of infection in exposed farmers had a statistically significant positive relationship (p < 0.05), with a regression coefficient of 1.92 (95% CI = 1.56–2.28) (Table 3). When comparing lettuce to other vegetables, the sample exposure resulted in a higher percentage of infection with soil transmitted helminths of 1.88 ( 95% CI = 1.67–2.23) (Table 3).

Table 3

The relationship between the prevalence of helminths in wastewater irrigated vegetables and female farmers in Addis Ababa from November 2021 to February 2022.
STH in vegetable samples versus female farmers’ stool	Coefficient	95% Confidence Interval	P – value
Total vegetables	1.92	1.56–2.28	0.001
Lettuce	1.88	1.67–2.23	0.005
Swiss	1.55	1.28–1.82	0.018
Ethiopian kale	1.22	0.77–1.67	0.024

Vegetable consumption is highly beneficial for health maintenance and disease prevention. On the other hand, they may serve as a source of infection for a variety of parasites. Suppose eaten raw or uncooked and or undercooked. Detecting parasites in vegetables is critical for parasitic illness prevention and control [9].

The level of contamination of vegetables is largely dependent on the quality of the wastewater and the irrigation method [16]. In this study, the prevalence of STH was found in the harvested leafy vegetables. Due to their larger surface area and morphological ability to trap soil and sediment, this creates favorable conditions for STH eggs and larvae to adhere to the surface of vegetables. Moreover, these vegetables are often grown in loose soil, which is more conducive to the survival and growth of STH eggs and larvae [17]. The irrigation methods used during leafy seedling vegetables are often overhead, which means that the contaminated water can come into contact with the leaves and remain there, increasing the risk of STH contamination [19].

vegetables are eaten raw or lightly cooked to preserve taste, and this practice may favor the transmission of STH infections. Lettuce is eaten raw, which was the most frequently contaminated sample in the study sites. The leaves of lettuce have a favorable structure for the retention of soil particles, as thsy have numerous crevices and folds and can provide shelter and protection to helminth eggs and larvae [17]. Moreover, the present helminth egg in irrigated wastewater can get onto green and leafy vegetables up to 90% [20]. In addition, vegetables are often contaminated with parasites during growth, harvesting, handling, or distribution, which poses a significant occupational health risk.

The prevalence of helminths detected in the vegetable sample was 67.5% (95% CI = 0.50–0.75) which is comparable with previous findings of Desta et al., 61% (95% CI = 0.52% − 0.64 ) [11]and a study conducted in Dessea, Ethiopia 63.4% (95% CI = 0.54% − 0.72 ) [20]. But this result is higher than studies conducted in different parties of Ethiopia; in Bardar, the prevalence of STH was 39.1% (95% CI = 0.34% − 0.44) [21], Dire Dawa, 47.3% (95% CI = 0.42% − 0.52) [22], Arba Minch 54.4% (95% CI = 0.49% − 0.59) [23]. The difference could be due to variations in sanitation and hygiene practices, geographical locations, climatic and environmental conditions, methods used for the detection of intestinal parasites, and socioeconomic status.

This study provided information on the prevalence of helminth infection among urban female vegetable farmers in Addis Ababa city. Ascaris lumbricoides and hookworm were the most prevalent infections in the population studied, consistent with global trends. Eight hundred and 600 million people are infected with Ascaris lumbricoides and hookworm at the global level, [24]. The low-frequency Trichuris trichiura observed might be due to their minimal dispersion as a single female worm of Trichuris liberates relatively fewer numbers eggs (20,000 eggs per day) [20].

The current study found a helminth prevalence of 20.8% among female farmers growing vegetables using wastewater as an irrigation source (95% CI = 0.16–0.26). This figure is similar to a study conducted in Babile, Eastern Ethiopia, which reported a prevalence of 20.8% (95% CI = 0.16–0.26) [4] and comparable to a study in rural Vietnam 19.2% (95% CI = 0.13–0.25) [16]. According to studies, female farmers in general are more vulnerable to soil transmitted helminth infections due to their frequent contact with soil through agricultural activities, such as planting, weeding, and harvesting [24, 25]. They have less access to sanitation facilities and hygiene education than their male counterparts, which may increase their risk of STH infections.

In addition, female farmers may be responsible for caring for children and other family members, which may limit their time and resources to practice good personal hygiene [26].

In the current study, a statistically significant ( p < 0.05) positive regression coefficient suggests that there is a positive association between STH prevalence in the three vegetable and female vegetable farmers. The coefficient indicates that an increase in STH prevalence in the vegetable sample is associated with an increase in the number of cases of STH infection among female farmers. The positive association is due to poor sanitation practices in the surrounding areas. The absence of proper sanitation facilities for female farmers and their families, combined with their defecation practices in nearby bushes, has led to contamination of the irrigation water and soil. The contaminated water and soil have then contributed to the higher number of helminths found in vegetables. Our observation during the survey was that farmers consume raw lettuce without properly washing or preparing it. This is also one factor that increases the risk of ingesting the helminths and other contaminants present in the vegetables. There was an increase in parasitic prevalence in the surrounding areas through stool surveys further supports that poor sanitation practices contribute to the contamination of vegetables.

Female farmers who grew lettuce with wastewater had a 1.88 (95% CI = 1.67–2.23) greater likelihood of having STH than those who grew lettuce with another type of water. Furthermore, the prevalence of STH infection among female farmers who use wastewater for cultivating Swiss had 1.55 (95% CI = 1.28–1.82), and Ethiopia kale 1.22 (95% CI = 0.77–1.67) times higher frequency than alternative water users for irrigation, respectively. The higher prevalence of STH infection among female farmers farming vegetables with wastewater irrigation may be attributed to a combination of factors related to the vegetable species’ ability to absorb STH from the soil, wastewater, and farmers’ agricultural practices. According to a study conducted in Iran, the prevalence of STH was more significant in organic lettuce (13.09%) than in conventional lettuce (8.33%) [27]. This implies that the prevalence of STH in lettuce varies based on the farm soil and agricultural practices adopted.

However, it is important to note that the analysis only captures the relationship between wastewater cultivated vegetables and STH infection among female farmers. Other factors may also influence the prevalence of STH infection. Therefore, further robust research is needed to better understand the complex relationships between STH in vegetables and the prevalence of STH infection among female farmers.

The current study's major strength is demonstrating the epidemiological link between wastewater-irrigated vegetables and helminth infection among female farmers, which of course, can be passed on to other members of the community through produce, contributing to endemic infection. The detailed collection of vegetable samples along the river line provides valuable information for environmental and community health surveillance. However, the study's limitations, such as its focus on only leafy vegetables, and farmers, and the absence of helminth infection identification in vegetable market sellers, may impact the generalizability of the findings.

The study found a high prevalence of helminth contamination in wastewater-irrigated vegetables, with all three types of vegetables showing contamination with at least one of the three STHs. Ascaris lumbricoides were found to be the most prevalent helminth, followed by hookworm and Trichuris trichiura. The prevalence of helminth infections varied between study sites, with the highest prevalence of Ascaris lumbricoides, hookworm, and Trichuris trichiura being observed in Akaki. Moreover, the study found a statistically significant positive relationship between vegetable production and female farmers’ chance infections. The farmers had a 1.92 times higher chance of developing STH infections by working on the farm.

The findings suggest a high risk of helminth contamination in wastewater-irrigated vegetables and the need for regular monitoring of helminth infections in the population, particularly in areas with a high prevalence of infection. Improved hygiene practices during vegetable production and processing are also needed to reduce the risk of contamination and ensure the safety of the food supply. Furthermore, comprehensive health education programs should be implemented among the farming community and general population to raise awareness of the dangers of working and living in a helminth-contaminated environment. Further research may be necessary to understand the risk factors associated with helminth infections among farmers who practice wastewater irrigation and the potential effects of helminth infection further down the supply chain.

STH

Soil Transmitted Helminths

WHO

World Health Organization

EPHI

Ethiopian Public Health Institute

FDRE

Federal Democratic Republic of Ethiopia

UNDP

United Nations Development Programme

Ethical considerations

The Addis Ababa University College of Natural and Computational Sciences Institutional Review Board Committee approved the research. An official permission letter was received from each municipal agriculture and health subcity admiration. After the objective and contents of the study were clarified to all participants, written consent was obtained from each participant. Confidentiality of the study results was maintained, and no other tests were done on the stool samples collected other than those mentioned in the data collection section.

Consent for publication

Not applicable

Conflict of interest

The authors declare that they have no conflicts of interest sented in this study are available from the principal author upon reasonable request.

Funding

This work was supported by the Water Security and Sustainable Development Hub, which is funded by the UK Research and Innovation’s Global Challenges Research Fund (GCRF), Grant no.: ES/S008179/1.

Authors’ contribution

BK conceived and designed the study, carried out data collection and laboratory examination, and finalized the writing of the manuscript. BM, SR, and ET designed the study and revised the manuscript. ML, CL, and BK revised the manuscript. The drafted manuscript was revised, and all authors read and approved the final manuscript.

Acknowledgments

We are grateful to the Water Security and Sustainable Development Hub for their valuable comments on the manuscript and to the staff of the EPHI Laboratory for their assistance. We also wish to acknowledge the fieldwork support of development agents at various subcity administrative areas of Addis Ababa.

Availability of Data

The data used in this manuscript are not publicly available due to ongoing analyses. Data presented in this study are available from the corresponding author upon reasonable request.

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No competing interests reported.

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Contribution of wastewater irrigated vegetables to the prevalence of soil- transmitted helminth infection among female farmers in Addis Ababa, Ethiopia

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Abstract

Background

Methods

Result

Conclusion

Figures

Background

Methods

Study area

Study design and period

Population

Source population

Study population

Inclusion and exclusion criteria

Inclusion criteria

Exclusion criteria

Sample size

Sampling technique

Data collection

Vegetable sample collection

Parasite detection

Stool sample collection and examination

Data quality management

Data analysis

Results

Prevalence of helminths in vegetable samples

Prevalence of helminths in the farmers’ stool

Discussion

Conclusion

Abbreviations

Declarations

Ethical considerations

Conflict of interest

Funding

Authors’ contribution

Acknowledgments

Availability of Data

References

Additional Declarations

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