Human excreta is a low cost source of nutrients vital to plant growth, but also a source of pathogens transmissible to people and animals. We investigated the cost-savings and infection risk of soil transmitted helminths (STHs) in four scenarios where farmers used either inorganic fertilizer or fresh/composted human excreta supplemented by inorganic fertilizer to meet the nutrient requirements of rice paddies in the Red River Delta, Vietnam. Our study included two main components: 1) a risk estimate of STH infection for farmers who handle fresh excreta, determined by systematic review and meta-analysis; and 2) a cost estimate of fertilizing rice paddies, determined by nutrient assessment of excreta, a retailer survey of inorganic fertilizer costs, and a literature review to identify region-specific inputs. Our findings suggest that farmers who reuse fresh excreta are 1. 24 (95% CI: 1. 13–1. 37, p-value<0. 001) times more likely to be infected with any STH than those who do not handle excreta or who compost appropriately, and that risk varies by STH type (Ascaris lumbricoides RR = 1. 17,95% CI = 0. 87–1. 58, p-value = 0. 29; Hookworm RR = 1. 02,95% CI = 0. 50–2. 06, p-value = 0. 96; Trichuris trichiura RR = 1. 38,95% CI = 0. 79–2. 42, p-value = 0. 26). Average cost-savings were highest for farmers using fresh excreta (847,000 VND) followed by those who composted for 6 months as recommended by the WHO (312,000 VND) and those who composted for a shorter time (5 months) with lime supplementation (37,000 VND/yr); however, this study did not assess healthcare costs of treating acute or chronic STH infections in the target group. Our study provides evidence that farmers in the Red River Delta are able to use a renewable and locally available resource to their economic advantage, while minimizing the risk of STH infection.
Application of human excreta onto rice paddies as fertilizer is a common practice in northern Vietnam, where many farmers use single or double vault latrines, lack access to wastewater infrastructure, and have variable access to commercial inorganic fertilizers [1]. Using organic waste to fertilize fields has clear benefits for crop yield [2]; however, this practice increases certain health risks for farmers and consumers, such as infection by soil transmitted helminths (STHs) [3,4]. The STH group includes Ascaris lumbricoides, Trichuris trichiura, and hookworm spp. , which are intestinal parasites that spread between people when sanitation is inadequate or when good hygiene is not practiced [4]. People are infected when they accidentally ingest infective eggs or when their skin contacts infective larvae in contaminated soil. These parasites are particularly prevalent in regions with warm, moist climates, and are included in the category of tropical neglected diseases associated with poverty. World Health Organization (WHO) guidelines recommend that farmers compost human excreta for six months prior to application in order to inactivate STH eggs and larvae, and thereby reduce spread between people [5]. This practice is not feasible for all Vietnamese farmers, in particular those who harvest multiple crops per year or have single vault latrines that lack a chamber for long-term excreta storage. Current evidence suggests that only one-third of farmers who use human excreta follow the six-month recommendation [6], and that STH infection remains an occupational hazard associated with handling human excreta [3]. It is common practice for household members to add a handful of kitchen ash after using a latrine, as this reduces smell. A recent study characterizing A. lumbricoides egg die-off during excreta composting suggests that adding lime reliably accelerates egg inactivation so that WHO criteria for safe handling (<1 viable egg/g total solids) are met by 153 days [7]. Ascarid eggs can survive longer periods in adverse environmental conditions than other STHs, and for that reason we chose A. lumbricoides die-off as a proxy for overall STH die-off [8]. Rice farmers in some agricultural regions of Vietnam have shifted their source of fertilizer from human excreta to commercial inorganic products, either wholly or in part. It is unclear whether this trend will become universal as not all farmers are able to afford or access commercial fertilizer, and others consider human excreta a superior source of long-term nutrition for plants and soil [9]. Inorganic fertilizers are primarily imported, and their costs are influenced by a wide range of factors, including energy prices [10]. Using human waste to fertilize crops is recognized as a way to decrease household expenditures; however, it is unclear how costs and health risks associated with STH infection interact. The goal of this study was to compare the costs and STH risk associated with fertilizing rice paddies in the Red River Delta (RRD).
The RRD encompasses eight provinces and two major urban municipalities (Hanoi and Haiphong) in northern Vietnam. The RRD is an agriculturally intense area that produces approximately 15% of the national annual rice output [11]. Throughout the region, farmers use various combinations of human excreta, inorganic fertilizers, and animal manure to replenish soil nutrients and maximize rice yield. To generate cost estimates, we chose four fertilization scenarios: (A) Fresh human excreta (≤ 139 day storage without lime); (B) Composted human excreta (153 day storage with 10% lime as per [7]); (C) Composted human excreta (181 day storage without lime; WHO standard [5]); (D) Inorganic fertilizer. Although three scenarios (A-C) involved human excreta, we assumed that only farmers who handled fresh excreta (A) would experience STH infection risk, as the composting scenarios (B and C) met WHO standards for helminth inactivation. Risk of STH infection for Vietnamese farmers handling fresh excreta was evaluated by systematic review and meta-analysis. Our economic analysis of the four scenarios included the direct costs incurred for composting human excreta (i. e. lime) and supplementing excreta with inorganic fertilizers. Capital costs (i. e. cost to build a double vault latrine) were not included because differences in factors such as materials and design cause costs to vary substantially in the RRD, and would add a high level of uncertainty to our analysis. To estimate the direct costs, we determined nutrient content of organic fertilizer scenarios, conducted a retailer survey of inorganic fertilizers in the study area, and collected economic inputs from published sources specific to the RRD (e. g. household size, excreta production per household, annual harvest frequency, average paddy size).
This study adds to current knowledge about the opportunities and risks associated with reusing human excreta to fertilize rice plants in one region of Vietnam. Our finding that handling fresh excreta increases the risk of STH infection in farmers (RR = 1. 24,95% CI: 1. 13–1. 37) emphasizes the importance of adequately treating excreta to inactivate STH life stages. Furthermore, the risk is not limited to farmers as fresh excreta reuse facilitates STH spread to other commune residents, and ultimately to consumers, through food, water, and environmental transmission routes. This practice is one factor contributing to the high prevalence of A. lumbricoides (44. 4%; N = 34 million), T. trichiura (23. 1%; N = 17. 6 million) and hookworm (28. 6%; N = 21. 8 million) infections in Vietnam [23]. Our study did not assess healthcare costs associated with STH prevention, treatment, or chronic disability. Individuals with low intensity infections are often asymptomatic; however, those with high intensity infections can experience a variety of acute or chronic conditions (e. g. diarrhea, abdominal discomfort, anemia and rectal prolapse) that reduce quality of life and may require costly medical interventions to treat [4]. Long-term sequelae of chronic infections, such as impaired cognitive development and growth faltering, can negatively impact lifelong earnings and contribute to the cycle of poverty in low resource communities. Although our study showed that farmers using fresh excreta benefitted from the largest cost-savings in fertilizer expenditure, the direct and indirect societal costs incurred due to prolonged STH infection would likely outweigh these savings. Despite laws that prohibit use of human excreta for agriculture in Vietnam, this practice remains common among certain farming groups [24]. Human excreta is perceived as more valuable than animal manure due to differences in dietary protein content, and it is believed to improve soil structure more sustainably than inorganic fertilizers [9]. Although many farmers compost excreta, WHO recommendations for hygienic composting are not commonly followed, as farmers harvest multiple crops per year and are unwilling or unable to store excreta for six months prior to use [5,6]. Some misperceptions about the reasons for safe composting might influence farmer willingness to use fresh excreta. For example, focus group participants in the RRD emphasized ease of application and benefits to soil structure, rather than the benefits of composting to protect human health [1]. Our alternative to the WHO standard, composting for 153 days with 10% lime to accelerate STH inactivation, was not a reasonable alternative for farmers prioritizing cost savings. However, for farmers less concerned about cost savings, the 10% lime compost strategy could be further accelerated to 111 days by adding aeration to latrines, which would allow excreta to be safely handled at more frequent intervals [7]. Human excreta use in crop agriculture was previously estimated to represent 83 million USD in fertilizer import savings to the Vietnamese economy [6], which is one-fifth of the 2014 net expenditure on inorganic fertilizer importation (384 million USD) [25]. Our cost analysis indicated that farmers could save 37,000–847,000 VND/yr (1. 48–37. 28 USD, $2017) [26] by using human excreta. While these savings might appear low, they represent 1–22% of a farmer’s average annual income in the RRD [27]. Furthermore, the savings could represent a higher percent of annual income in regions that are less fertile, where rice yields are lower, or in remote locations where transportation challenges result in higher commercial fertilizer costs. Another report, suggesting that household excreta traded on the domestic market could contribute up to 15% of household income for those in the lowest income quintile, is in line with our analysis [6]. Therefore, it is unlikely that low-income rural farmers would be willing to universally replace organic fertilizers of human origin with inorganic commercial fertilizers. This was previously demonstrated by farmers who were given non-composting latrines and who ultimately broke the seals open to access the excreta [24]. Our nutrient analysis of human excreta originating from the RRD and composted over time demonstrated excreta to be an adequate organic source of phosphorus and potassium, but not nitrogen, for plant growth. Therefore, all of the scenarios using human excreta (A-C) required additional inorganic fertilizer in order to meet the recommendations for optimizing rice yield. It is not clear how far outside Vietnam these results should be extrapolated as differences in dietary intake directly influence NPK excretion, and soil supplementation requirements vary regionally. Furthermore, our analysis was based on total excreta collected in a double vault latrine, rather than waste separated into liquid and solid components, as occurs in some other regions that use excreta. However, beyond the immediate economic and agricultural gains to reusing excreta, there are global benefits to nutrient recycling. It is estimated that the demand of phosphate rock will outweigh supply by the mid-21st century, which has important consequences for food security as phosphorus is essential for plant growth [28]. As access to a hygienic toilet (flush, pour flush, sulabh or double vault latrine) is still regionally variable in Vietnam (61. 6–96. 7% of homes containing a latrine), an opportunity currently exists to optimize nutrient recovery infrastructure in homes requiring sanitation upgrades [27]. Our systematic review and meta-analysis found a statistically significant higher risk of infection with any STH among Vietnamese farmers who use human excreta, and highlighted the limited volume of evidence to describe this association. Only four studies met our inclusion criteria, despite searching academic and grey-literature sources in Vietnamese and English. Of these, only three were included in meta-analysis due to poor reporting quality. Out of a possible score of 13, two studies achieved a quality score of 50% or lower. Our findings showed that studies often did not report descriptions of appropriate sample size determinations, confounders controlled for, sample size for positive exposure and/or outcomes, as well as risk estimates or associated p-values. However, aside from one study, all studies were from the RRD study area, included participants of similar age and gender, and estimated exposure and outcomes using similar methods. Each study had slightly different definitions for agricultural use of human excreta, and therefore our meta-analysis included both individuals whose primary occupation was rice farming, but also those who worked with human excreta in other ways aside from direct field application. Inclusion of Yajima et al. , 2009 in the meta-analyses of both T. trichiura and A. lumbricoides produced significant heterogeneity in the estimates of infection risk. This study had a small sample size and very low prevalence of STHs (i. e. one case of A. lumbricoides detected), leading to low risk ratios and wide confidence intervals. The study did not provide information on approaches used to measure or control for potential confounders, further adding to the difficulty in interpretation of protective properties of human excreta use in STH. Pooled results by STH type revealed the lowest risk for hookworm infection, and significant variation in studies combined in meta-analysis for this outcome. It was not possible to examine potential factors contributing to heterogeneity in hookworm risk estimates due inclusion of only two studies in meta-analysis. Therefore, in order to better understand factors influencing infection and to substantiate the limited body of evidence on STH risk in the RRD of Vietnam, additional research employing high methodological rigour is warranted. Although our study attempts to represent the typical situation in the RRD, much of our data comes from Ha Nam province exclusively which may differ in relevant ways from other RRD provinces. The estimate of risk was limited by the number of estimates reported in the literature and we assumed that STH risk was equal in scenarios B-C. Human excreta was collected from various households and mixed before analysis. Thus, results may not accurately reflect the nutrient and moisture content of unmixed excreta if collected and analysed from time of defecation. Costs related to the removal of excess human excreta, latrine construction and maintenance, and personal safety equipment were not explored.
Our study confirmed that human excreta is a significant and sustainable source of nutrients needed for crop fertilization. Its use as agricultural fertilizer, a common practice in Vietnam, offers direct benefits to rice farmers. Human health, agricultural productivity, household earnings are optimized when farmers follow WHO standards for excreta use and government standards for crop fertilization; however current policies prohibit excreta use altogether and therefore may need to be revisited. Furthermore, our results suggest that farmers and the Vietnamese economy would benefit by forward thinking public health messaging promoting STH prevention, such as safe excreta handling strategies, personal protective equipment (e. g. gloves and boots) and regular anthelmintic prophylaxis, rather than an outright ban on excreta use. This study highlights agricultural policies needing further attention, and demonstrates the value of promoting research that provides innovative solutions for safely and economically extracting nutrients from human excreta.
Each year, hundreds of millions of people worldwide are infected with intestinal worms spread by contaminated soil, also known as soil transmitted helminths (STHs). These worms are most common in tropical climates in areas lacking good hygiene and sanitation, and negatively impact child development, quality of life, and economic wellbeing. Reuse of human excreta for fertilizer is a common practice in many low to middle income countries because farmers require a low cost source of nutrients to grow food crops eaten by people and animals. Excreta can contain microbes, such as STHs, that cause disease in people; however, composting is a known method of killing STHs. Therefore, our goal was to determine if Vietnamese rice farmers involved in this practice are at higher risk of STH infection, and to calculate the amount of money saved by farmers composting for different lengths of time, and supplementing with various commercial fertilizers. We suggest that farmers compost excreta for six months to reduce disease exposure and optimize household savings. Optimizing practices to improve food production and protect farmer health is critical for poverty alleviation in low to middle income countries.
invertebrates
medicine and health sciences
helminths
tropical diseases
parasitic diseases
animals
rice
ascaris lumbricoides
mathematics
ascaris
statistics (mathematics)
experimental organism systems
neglected tropical diseases
plants
research and analysis methods
agrochemicals
grasses
mathematical and statistical techniques
fertilizers
agriculture
people and places
helminth infections
professions
eukaryota
plant and algal models
meta-analysis
nematoda
biology and life sciences
population groupings
physical sciences
soil-transmitted helminthiases
statistical methods
organisms
agricultural workers
Turning poop into profit: Cost-effectiveness and soil transmitted helminth infection risk associated with human excreta reuse in Vietnam