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Impact of usership on bacterial contamination of public latrine surfaces in Kathmandu, Nepal

  • Alexis L. Mraz ,

    Contributed equally to this work with: Alexis L. Mraz, Shannon M. McGinnis, Heather M. Murphy

    Roles Formal analysis, Investigation, Writing – original draft, Writing – review & editing

    Affiliations Water, Health and Applied Microbiology Lab (WHAM Lab), Department of Epidemiology and Biostatistics, College of Public Health, Temple University, Philadelphia, Pennsylvania, United States of America, Department of Public Health, School of Nursing and Health Sciences, The College of New Jersey, Ewing, New Jersey, United States of America

  • Shannon M. McGinnis ,

    Contributed equally to this work with: Alexis L. Mraz, Shannon M. McGinnis, Heather M. Murphy

    Roles Data curation, Formal analysis, Investigation, Methodology, Writing – review & editing

    Affiliation Water, Health and Applied Microbiology Lab (WHAM Lab), Department of Epidemiology and Biostatistics, College of Public Health, Temple University, Philadelphia, Pennsylvania, United States of America

  • Dianna Marini ,

    Roles Funding acquisition, Project administration, Writing – review & editing

    ‡ DM and PA also contributed equally to this work.

    Affiliation Aerosan Toilets, Halifax, Nova Scotia, Canada & Kathmandu, Nepal

  • Prakash Amatya ,

    Roles Project administration, Writing – review & editing

    ‡ DM and PA also contributed equally to this work.

    Affiliation Aerosan Toilets, Halifax, Nova Scotia, Canada & Kathmandu, Nepal

  • Heather M. Murphy

    Contributed equally to this work with: Alexis L. Mraz, Shannon M. McGinnis, Heather M. Murphy

    Roles Conceptualization, Funding acquisition, Methodology, Project administration, Resources, Supervision, Writing – review & editing

    heather.murphy@uoguelph.ca

    Affiliations Water, Health and Applied Microbiology Lab (WHAM Lab), Department of Epidemiology and Biostatistics, College of Public Health, Temple University, Philadelphia, Pennsylvania, United States of America, Water, Health and Applied Microbiology Lab (WHAM Lab), Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada

Abstract

According to the United Nations (UN) Sustainable Development Goals (SDGs), community or public toilets shared by more than one household are not considered “safely managed” under SDG 6.2. However, many populations around the globe, particularly in urban settings, lack access to private sanitation facilities. For this reason, there is a need to evaluate the cleanliness of community or public toilets in these settings and examine best practices for maintaining them. This study had three aims: 1) build on previous data collected in March 2018 at public latrines to determine whether cleaning protocols were sustained, 2) examine relationships between latrine cleanliness and usership, and 3) identify latrine surfaces with higher concentrations of bacterial contamination. In March 2018 and December 2019, swab samples were collected from public latrine surfaces in Kathmandu, Nepal. Sampling occurred in “clean” conditions–after cleaning and before the latrine was opened for use–and “dirty” conditions–during operating hours. Samples were analyzed for concentrations of total coliforms (TC) and Escherichia coli (EC). The number of latrine users prior to the “dirty” sample collection was recorded (in December 2019 only). Results found that both TC and EC concentrations were significantly lower during “clean” rather than “dirty” conditions and both TC and EC concentrations increased with the number of users over time. TC and EC concentrations differed by surface type during dirty and clean conditions (p<0.05). Findings suggest cleaning protocols established at this public toilet site were adequately maintained two years later.

Introduction

The United Nations (UN) adopted 17 Sustainable Development Goals (SDG) in 2015 as part of the 2030 Agenda for Sustainable Development, a call to improve the lives and prospects of people globally. SDG 6 focuses on clean water and sanitation, with target 6.2 focusing specifically on achieving “access to adequate and equitable sanitation and hygiene for all and end open defecation, paying special attention to the needs of women and girls and those in vulnerable situations [1].” SDG 6.2 seeks to improve access to “safely managed” sanitation defined as “use of improved facilities that are not shared with other households and where excreta are safely disposed of in situ or removed and treated offsite.” The term “improved” in this context refers to the hygienic separation of human excreta from human contact [2]. A variety of facilities can meet this requirement, including those with sewer connections, septic systems connections, pour-flush latrines, ventilated improved pit latrines, pit latrines with a slab or composting toilets [3]. However, community facilities, facilities shared between households or public toilets are not considered “safely managed” even if the excreta is safely disposed of and treated, and therefore do not count towards meeting the goals outlined in SDG 6.2 [2]. Shared facilities are considered “limited” and fall below “basic” and “safely managed” sanitation on the sanitation ladder. However, the World Health Organization (WHO) does highlight and acknowledge that shared facilities are an incremental and often necessary step towards safely managed sanitation [4].

The Joint Monitoring Programme for Water Supply and Sanitation (JMP), by the WHO and the United Nations International Children’s Emergency Fund (UNICEF) is tasked with monitoring progress towards SDG 6. According to JMP’s 2021 report, 78% of the global population had access to “improved” sanitation in 2020, where 54% of the global population had access to “safely managed” sanitation (defined as a private improved facility, in which fecal matter is safely disposed of on site or transported and treated off-site) and 24% had access to “basic” sanitation (a private improved facility, not shared with other households, which separates fecal matter from human contact) [2, 5]. The percent of the global population using open defecation dropped to 6% in 2020 from 10% in 2015 [5]. Those having access only to “unimproved sanitation”–(pit latrines without slab or platform, hanging latrines or bucket toilets) accounted for 8% of the global population in 2020, dropping from 10% 2015 [5]. While 7% had access to “limited” sanitation which are improved facilities shared between two or more households [2, 5]. Access to improved sanitation is more limited in least developed countries, particularly in sub-Saharan Africa, Oceania, and Central and Southern Asia [3]. Lack of access to clean water and improved sanitation contributes to about 3.3% of global deaths and 4.6% of the global burden of disease [3]. In children under 5 the burden of disease is even higher with 13% of deaths and 12% of disability adjusted life years (DALYs) attributable to water, sanitation and health (WASH) issues [3]. Use of improved sanitation has been demonstrated to promote overall community health. In a study of 41 countries, predominantly in South America and Africa, reduced stunting and childhood death was observed when 80% or more individuals in a village or community were utilizing improved sanitation [6].

There are several barriers to the use of community latrines or public toilets such as: safety issues, cleanliness and challenges associated with operation. Concern for physical safety, particularly at night and for women, is one barrier in using public toilets [7, 8]. Unhygienic conditions resulting in a health concerns and/or a feeling of disgust is another barrier [9, 10]. Operational considerations include distance and time to a latrine, user fees, maintenance, and access to running water and soap [911]. These concerns are reported less frequently in those that use communal latrines in comparison to those who rely on open-defecation [10]. In many urban centers, private household latrines are not only cost-prohibitive but space prohibitive, highlighting the need for shared sanitation options to end open defecation [12, 13]. Furthermore, it could be argued that some forms of shared sanitation may be more “safely managed” if the waste is emptied and disposed of appropriately or treated on-site compared to households who may empty their latrines illegally into the environment [14]. For instance, the public toilets in the current study treated the waste with an anaerobic digester prior to discharging the small liquid fraction of waste into the receiving environment. The log removal of pathogens in an anerobic digester is expected to be higher than typical household sanitation systems such as a pit latrine, cesspit/ soakpit or septic system [4, 1518].

As population growth increases in cities around the world, shared toilets are a necessary intervention for providing access to sanitation when there is inadequate space and resources for households to have their own individual toilet facilities. One argument against community latrines or public toilets is that they are not adequately cleaned and maintained. Consequently, for shared sanitation to be considered “safely managed”, it is important to also understand the cleanliness of shared latrines to see if they can provide an effective and clean alternative to privately owned toilets.

To date there is limited research on the microbiological cleanliness of shared sanitation in low-income countries although there is some work in high income countries demonstrating contamination in public flush toilets [19]. What appears to be lacking is evidence supporting frequency of cleaning and cleaning methods required to reduce microbial contamination specifically in toilet facilities.

In response to the 2015 earthquake, Aerosan Toilets, a Canadian Non-Governmental Organization (NGO) with operations in Nepal, began assessing community and public toilets in Kathmandu, Nepal, to determine how to meet the urban sanitation need, particularly for women. Aerosan built biogas latrines utilizing an anaerobic digester which provides power to local businesses. All latrines are sex-segregated, operated by trained staff, are cleaned regularly, and have hand washing facilities with soap. Latrines were built and initially operated by Aerosan before transitioning ownership and operations to local private operators. Aerosan worked with the Sanitation Workers’ Cooperative (Co-op) to provide training to and elevate the social status of those who work in sanitation-related jobs (including operating Aerosan toilets). The Co-op supported sanitation workers’ upwards mobility and improved working conditions and financial well-being. McGinnis et al. (2019) sampled Aerosan’s pilot latrines in 2018 which were overseen by Aerosan at the time of the study. Later in 2018, the operations of the pilot latrines fully transitioned to private operators. We returned nearly two years later to collect additional data to achieve the following aims:

  1. Determine if cleaning protocols and standards established and evaluated in March 2018 were sustained by private operators ~2 years later.
  2. Understand the relationship between usership and bacterial contamination of the latrine surfaces to advise cleaning frequency.
  3. Identify surfaces in the latrine facilities that had the highest levels of microbiological contamination

This work fills an important gap in knowledge on whether cleaning practices can be maintained over time by public toilet operators as well as how frequently latrines should be cleaned based on usership.

Methods

Definition of shared sanitation

There are many forms of shared sanitation as outlined by Evans et al. (2017) including: (a) shared household toilet (toilet in one household also used by other households); (b) compound toilets (toilets used only by the people living in a particular compound); (c) community toilets (non-household toilets used by a restricted group of households); and (d) public toilets (open to anybody) [20]. The management and operation of these different shared sanitation facilities differs, which can affect the cleanliness of toilet facilities. For clarity in the current manuscript, the toilets studied herein were public toilets.

Study site

The study took place in Kathmandu, the capital city of Nepal. Nepal is ranked as 142 out of 189 countries on the Human Development index [21]. Since the 1950s Nepal’s population has trended towards urbanization with the urban population increasing from 2.9% in the 1951 census to 21.4% in 2020 [22, 23]. This urbanization trend is expected to continue with an estimate of 36% of Nepal’s population residing in urban areas by 2050 [24]. Roughly 1.42 million people, or 4.9% of Nepal’s population were living in Kathmandu in 2020 [25]. Rapid urbanization combined with limited economic resources and infrastructure issues persisting from the 2015 earthquake have resulted in a lack of sanitation facilities within Kathmandu [26, 27]. As per the 2016–2017 Annual Household Survey, 11.5% of all Nepalese are lacking access to a toilet and 31% of the poorest Nepalese are without sanitation [28].

Toilet facility

This study took place at a privately owned pay per use public toilet site in the busy center of Ratna Park in Kathmandu. The toilet facility was initially rehabilitated and operated by Aerosan toilets in 2017 and then transitioned to a private operator in mid-2018 with no oversight by Aerosan. While managing the facility, Aerosan implemented and oversaw cleaning protocols. The toilet facility was sex segregated and featured two female cabins, five male cabins, male urinals, and three handwashing stations. There were more cabins for males than females as the toilet facility was in a busy urban marketplace with a large proportion of male workers. Each cabin contained a private latrine with slab, a bucket used for anal cleansing, and a tap to fill the bucket. The cabins were equipped with interior locks and lights to ensure privacy and visibility in the early morning and at night. The handwashing stations were shared by male and female customers and included soap and water. The toilets served upwards of 1,500 people a day (S1 Table). The facility was generally clean with no obvious odours and all the cabins and handwashing stations were in good working condition.

The same toilet facility was visited in March 2018 by McGinnis et al. while it was being operated by Aerosan. In the present study we revisited the toilet facility 21 months later, to see if cleaning practices were sustained even after the intervening organization had stopped managing the public toilets. The cleaning protocol developed in collaboration with Aerosan is presented in S2 Text. The operators were not aware of the study prior to our arrival and throughout the week of sampling. Cleaning occurred daily after the toilet facility closed and focused on the latrine slab, urinals, walls, mirrors, handwashing, door, and anal cleansing tap handles, and the anal cleansing bucket.

Site swabbing and usership data collection

Samples were collected from both female cabins, three male cabins, and all three handwashing stations. In each cabin, the following surfaces were swabbed: the pit latrine slab, the rim of the anal cleansing bucket, the handle of the anal cleansing tap, and the interior door handle of the latrine cabin. The handle for the water tap was also sampled at each handwashing station. Samples were taken at varying times throughout the day, accounting for both “clean” and “dirty” conditions. Clean samples were taken at 5:00 am, prior to the facility opening for the day. “Dirty” samples were any samples collected after users had started using the latrines. Latrines were cleaned thoroughly by the operators only at the end of the day. When visibly soiled, operators also cleaned dirty cabins in a more abbreviated manner than the end of day cleaning.

Samples were collected as per McGinnis et al. 2019 [29]. Sterile swabs stored in a sterile tube with a sponge containing 1 mL of Amies solutions (BD CultureSwab BBL, Franklin Lakes, NJ, USA) were used for sample collection. An additional 2 mL of sterile phosphate buffer solution (PBS) with 0.2% sodium thiosulfate was added to the collection tube, prior to swabbing. Swabs were removed aseptically from the transport tube and swabbed completely over the sample area, while rotating the swab. The swab was returned to the labeled transport tube. The entire surface area of the small surfaces, including the rim of the anal cleansing bucket, the handwashing and latrine taps, and the doorhandles, were swabbed [30]. An area of 100 cm2 was swabbed for the latrine slabs (a standardized 10 cm x 10 cm square was used). The surfaces swabbed, including their dimensions, are described in Table 1 and images presented in S1 Fig. After collection, swabs were transferred on ice and stored at 4°C until processing (within 30 hours).

Lab methods

Swabs were processed at the Environment and Public Health Organization (ENPHO) lab, in Kathmandu, Nepal, using membrane filtration and culture-based methods [29, 31]. Swabs were vortexed in the sterile collection tube for 30 seconds to remove bacteria from the swab tip into the surrounding solution. The solution was then emptied into a sterile test tube with the sponge squeezed aseptically to remove any additional liquid. Next, 1 mL of the sample liquid was filtered through a 47 mm, 0.45-micron mixed cellulose fiber membrane. Membranes were incubated on Brilliance Total Coliforms/E. coli Selective Agar (Oxoid Microbiology Products, Cheshire, United Kingdom) for 24 hours at 35°C [29, 31]. All samples were processed in duplicates. For latrine swab samples, a serial dilution was performed and processed in duplicate. Blank filters were performed daily during sample processing for Quality Assurance / Quality Control purposes. All blanks contained no measurable coliforms or E. coli.

Usership data collection

Usership data were collected by two enumerators located on site who counted the number of users entering the facility for each hour of observation. Usership was recorded from opening until all “dirty” samples were collected for each day. Due to the high usership at this facility, enumerators were unable to count the number of users entering each individual latrine and instead were only able to count the total number of users that entered the male urinals, male latrine cabins, or female latrine cabins per hour. Data were also collected on the number of individuals who used the handwashing stations per hour. These data were used to determine the number of individuals who had used the latrine cabins between the beginning of the day (when cabins were clean) to the time of swabbing each day for the “dirty” conditions. “Dirty” was defined as anytime point after opening. This was the time period when the facility was being used by patrons following the last full cleaning.

Statistical methods

We were limited in our ability to run numerous serial dilutions and some of our dataset includes non-detects (NDs) and too numerous to count (TNTC) plates. In our statistical analyses, we replaced NDs with half of our estimated limit of detection (LOD) of 1 Colony forming unit (CFU)/ plate and set TNTC to 200 CFU/ plate which is in line with the maximum number of colonies that can be reliably counted on a plate [31]. Our estimated LOD was established as the lowest number of colonies that we recovered on our plates. All analyses were performed in R version 4.0.2. Kruskal-Wallis tests were used to determine if there were differences in bacterial contamination across different surface types. Wilcoxon Signed Rank tests were used to compare data between clean (immediately after cleaning) and dirty (after any number of individuals had used the latrines) conditions. Finally, Spearman Rank tests were used to assess relationships between the number of users since cleaning and bacterial contamination across latrine surfaces.

Results

A total of 230 swab samples were collected from the public toilet site in Kathmandu, Nepal between December 8–12, 2019, of which 69 were taken during “clean” conditions and 161 of which were taken during “dirty” conditions. Pictures of sampled surfaces are available in the supporting information. “Clean” samples were collected at 5:00 am first before the facility opened and after the facility was thoroughly cleaned the night before. Dirty samples were taken throughout the day with the facility in use. All samples were taken from the same public toilet site; 120 were taken from the male cabins, 80 were taken from the female cabins, and 30 were taken from the handwashing stations. Total coliform (TC) and E. coli (EC) concentrations recovered from surfaces are summarized in Table 2. The tap at the handwashing station had the highest median TC counts in clean conditions, while the latrine slab had the highest median EC counts in clean conditions and the highest TC and EC counts in dirty conditions.

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Table 2. Total coliform and E. coli concentrations measured across public toilet surfaces 08–12 December 2019 during clean and dirty conditions.

https://doi.org/10.1371/journal.pwat.0000091.t002

Fig 1 summarizes TC and EC concentrations measured per square centimeter on the various surface types during clean (after cleaning before any users entered the site) and dirty conditions (after some number of users).

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Fig 1. Bacterial concentrations (log10 colony forming units (CFU) per square centimeter (sq cm)) by surface type for public toilets in “clean” and “dirty” conditions.

Boxplots represent the interquartile range (IQR) and median of the bacterial concentrations. Whiskers represent the concentration ranges while dots represent outliers (anything greater than 1.5 x IQR). LS = latrine slab, AC = anal cleaning tap, DH = door handle, B = anal cleansing bucket rim, HW = handwashing station tap.

https://doi.org/10.1371/journal.pwat.0000091.g001

Difference in bacterial levels between clean and dirty conditions

The results of the Wilcoxon Signed Rank Test comparing the bacterial concentrations measured during “clean” and “dirty” conditions across each surface type are summarized in Table 3. Results of Kruskal-Wallis tests found the TC and EC concentration on each type of latrine surface (AC, B, DH, LS, and HW) differed significantly among surface types during dirty and clean conditions (p<0.05). No significant differences were found using Kruskal-Wallis tests between individual latrine cabins during clean or dirty conditions on AC, B, and LS surfaces. There was a significant difference in both the EC concentrations (p = 0.028) and the TC concentrations (p = 0.007) amongst individual handwashing sinks (HW) in dirty conditions, potentially a result of proximity to the male latrines and differences in use. There was also a significant difference in both EC concentrations (p = 0.001) and TC concentration (p = 0.005) between the door handles of different cabins in dirty conditions. In addition, no significant differences were found between bacterial contamination (both TC and EC) measured in male compared to female latrine cabins during both clean and dirty conditions using Wilcoxon Rank tests.

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Table 3. Results of the Wilcoxon Signed Rank Test comparing the bacterial concentration of the public toilet surfaces during dirty and clean conditions (bolded if significant).

https://doi.org/10.1371/journal.pwat.0000091.t003

The anal cleansing tap and the latrine slab had statistically significant different levels of TC and EC between the clean and dirty samples collected. The rim of the anal cleansing buckets had statistically significant different levels of EC, but not TC between the clean and dirty samples collected. The door handles and handwashing taps did not have a significant difference between the clean and dirty conditions for either TC or EC.

How usership affected bacterial levels on latrine surfaces

Figs 25 display the relationships between the number of users since cleaning and log10-transformed concentrations of TC and EC measured on latrine surfaces. These plots include linear trend lines to display associations separated by gender for all surfaces except for handwashing stations. For latrine slabs and the cleansing taps (Figs 2 and 3) there is a positive association between usership and bacterial contamination.

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Fig 2. Scatterplots and linear regression line displaying bacterial concentrations on latrine slabs by usership.

The shaded area represents the 95% confidence interval of the line of regression.

https://doi.org/10.1371/journal.pwat.0000091.g002

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Fig 3. Scatterplots and linear regression line displaying bacterial concentrations of the handle of the anal cleansing tap and the rim of the anal cleansing bucket by usership.

The shaded area represents the 95% confidence interval of the line of regression.

https://doi.org/10.1371/journal.pwat.0000091.g003

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Fig 4. Scatterplots and linear regression line displaying bacterial concentrations on the handwashing tap by usership.

The shaded area represents the 95% confidence interval of the line of regression.

https://doi.org/10.1371/journal.pwat.0000091.g004

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Fig 5. Scatterplots and linear regression line displaying bacterial concentrations on the interior doors handle of the latrine cabin by usership.

The shaded area represents the 95% confidence interval of the line of regression.

https://doi.org/10.1371/journal.pwat.0000091.g005

Spearman Rank correlations were used to measure significant associations between the number of users since cleaning and bacterial contamination on latrine surfaces. Significant positive correlations were found between the number of users and concentrations of TC and EC on the latrine slab (rho = 0.55 for TC, rho = 0.57 for EC, p<0.05) and the cleansing tap (rho = 0.36 for TC, rho = 0.44 for EC, p<0.05). No significant correlations were found for the other surfaces.

Fig 2 shows the scatterplot and linear regression of the TC and EC concentrations on the latrine slab. The TC and EC had a significant positive correlation with users in both the male and female cabins. Fig 3 represents the linear regression of the TC and EC on the anal cleansing tap and rim of the anal cleansing bucket plotted against usership. There was a positive correlation between both the TC and EC concentrations and usership on the anal cleansing tap, which was significant for EC in female cabins. There was a positive, non-significant relationship between both TC and EC and usership on the bucket in both male and female latrines. Fig 4 represents the correlation between the TC and EC concentrations and usership on the handwashing tap. There was a positive, non-significant relationship between TC and EC concentration and usership. Lastly, Fig 5 shows the relationship between the TC and EC concentrations on the interior door handles and usership. There was a non-significant negative relationship between TC and EC concentration and usership for the door handles in female cabins and no relationship between TC or EC concentrations and usership on door handles in male cabins.

When we analyzed the results using Spearman Rank correlations by gender, significant positive correlations were found between the number of users and concentrations of TC and EC on the latrine slabs of male (rho = 0.57 for TC, rho = 0.58 for EC) and female (rho = 0.53 for TC, rho = 0.55 for EC) cabins (p<0.05). The anal cleansing tap had significant positive correlation between EC and usership for males and females (rho = 0.47 for males, rho = 0.47 for females) and TC (rho = 0.41) for female cabins. No other significant correlations were found after accounting for gender. It should be noted that men had access to urinals, which were separate from the latrines, meaning male cabins were likely used primarily for defecation while female latrines were used for both urination and defecation. Consequently, contamination of male cabins with fecal material may occur more rapidly than in female cabins when urinals are present.

Sustainability of cleaning protocols

Data collected during December 2019 was compared to data collected at the same site during March 2018 as reported previously in McGinnis et al. (2019). March 2018 data were collected after a cleaning protocol was established by latrine operators in partnership with Aerosan toilets. In December 2019, Aerosan no longer provided oversight at the public toilet site and the latrine operator was left to continue the cleaning protocol. Data collected during these time points are displayed in Fig 6. These data include TC and EC concentrations measured during dirty and clean conditions from the latrine slab (LS), anal cleansing tap (AC), door handle inside the latrine cabin (DH), and handwashing tap (HW). Data from the bucket (B) presented in this paper was not available in previous data collection so it is not included on the plots below.

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Fig 6. Bacterial concentrations by surface type for community latrines in “clean” and “dirty” conditions in March 2018 and December 2019.

Boxplots represent the interquartile range (IQR) and median of the bacterial concentrations. Whiskers represent the concentration ranges while dots represent outliers (anything greater than 1.5 x IQR). LS = latrine slab, AC = anal cleaning tap, DH = door handle, HW = handwashing station tap.

https://doi.org/10.1371/journal.pwat.0000091.g006

Results presented in Fig 6 show similar reductions in bacterial contamination from “dirty” to “clean” conditions in March of 2018 and December of 2019. Although bacterial concentrations measured during clean conditions were higher on the handwashing station (HW) in 2019 as compared to 2018 for both TC and EC, and higher on the latrine slab (LS) and door handle (DH) for TC, overall reductions in bacterial contamination between clean and dirty samples were still significant 21 months after the cleaning protocol was established and Aerosan no longer oversaw operations at the facility. There was not a significant change in terms of visual cleanliness, and the operators appeared to be maintaining the same cleaning protocols. These results suggest that the cleaning protocol established by Aerosan was somewhat sustainable and adequate to ensure the cleanliness of public toilets at the facility studied.

Discussion

Efficacy of cleaning protocol

When considering SDG 6.2 and whether shared sanitation facilities, such as those sampled in this study, should count towards safely managed sanitation, it is important to consider whether those facilities have the capacity to be cleaned adequately and regularly. This study demonstrated that the end of day cleaning was effective in reducing the bacterial load in the latrines. The “clean” samples, taken before the latrines opened for the day were statistically significantly lower for E. coli on the anal cleansing tap, the latrine slab, and the rim of the anal cleansing bucket. The anal cleansing tap and latrine slab were also significantly lower during the clean conditions for total coliforms. This site had a guard that stayed at the site overnight, and presumably used the latrines during that time. We did notice that the same handwashing tap and latrine had consistently higher E. coli and total coliform counts than the other latrines or taps during the “clean” sampling events. This may be a result of a single user (security guard) overnight.

Though there is a demand for cleaner latrines and anecdotal evidence that use would increase with higher sanitation standards [3236], few studies have examined how frequently public toilets should be cleaned based on usership including in developed countries. Additionally, in the literature, there does not seem to be an acceptable upper limit of bacteria for what would be considered clean [37]. There is one paper from 1976 that defined heavy contamination as greater than 103 CFU/ cm2 of total bacteria counts [30]. Our work showed TC levels between 2-3log during the dirtiest conditions on the latrine slabs that seem to align with this work. Although public toilets are used globally, and cleaning protocols have been established [38], there is a lack of scientific evidence outlining the frequency of cleaning required to maintain hygienic standards. There are studies that outline the effectiveness of certain cleaners on bacteria found on bathroom surfaces, however we were unable to recover any articles in the literature that focused specifically on frequency of cleaning [39]. For example, a search of all articles containing “toilets” AND “cleaning” or “latrines” AND “cleaning” in PubMed yielded only 97 and 34 articles, respectively. Two articles focused on cleaning of surfaces in hospital settings to assess microbial contamination, and one of these assessed daily cleaning [37, 40]. In our work, the latrine slabs, and anal cleansing tap showed increased bacterial contamination with increased usership. This work fills a knowledge gap and highlights the importance of understanding user traffic at public toilets and cleaning throughout the day at user-based intervals.

Handwashing taps, interior cabin door handles, and the rim of the anal cleansing bucket did not show clear increase in bacterial contamination with increased usership. These surfaces were small and not flat, for that reason a lack of statistical difference may be due to limitations on the overall ability of the method to recover bacteria from small surface areas [41]. It is possible that bacteria were being transferred to individuals’ hands, shirt sleeves, or other materials used to cover hands, from the doorhandles when they were closing or opening the door. If a latrine was particularly dirty, customers would avoid using it, even if it meant waiting longer for a cleaner latrine. Operators would spot clean latrines throughout the day if they were visibly dirty, but these quick cleans were not recorded as a cleaning as the whole cleaning protocol was not executed. Therefore, some of the surfaces were cleaned between users, which may affect some of the trends in the data. It should also be noted that TC and EC are indicator species and are not necessarily a result of human fecal contamination. Higher EC concentrations are a better indicator of fecal contamination than TC concentrations [42]. Higher TC levels, particularly on the latrine slabs may have been the result of dirt transferred from users’ shoes to the latrine slabs.

Public toilets and SDG 6.2

The results of this study suggest that private operators can effectively clean and maintain public latrines over time, however that cleaning needs to occur throughout the day. For public latrines to be a sustainable solution for improved sanitation and decreased open defecation, it is vital that private operators can maintain the latrines. This study demonstrates private operators’ ability to do so after transitioning from an NGO’s oversight.

Public toilets equipped with an anaerobic digester, like those sampled in this study, may be a viable solution for meeting SDG 6.2 due space constraints in certain contexts and because they will achieve a higher reduction of pathogens in the fecal waste than most household latrine options [4, 1518]. Previous literature demonstrates the potential hygiene and health issues that may occur with shared latrines, particularly those in low-income housing or slums [4345]. It is important to recognize that these issues are occurring in both private and shared toilets. Additionally, McGinnis et al. (2019) demonstrated that the contamination in public toilets was not higher than the contamination in private or shared latrines in Kathmandu, Nepal [29]. In situations where private latrines are not feasible, community or public, pay per use latrines, like the ones sampled in this study may be a hygienic alternative. Over half of the women in a 2018 survey in Kathmandu reported that they would not use toilets more frequently if they were free-of-charge, indicating the fee is not the main barrier of use [46]. The fee provides the resources to monitor and clean the facilities, in addition to having female-specific cabins may make public toilets safer than other latrine options for women and girls.

Cleaning recommendations

Using the results of our study and accounting for practical implications of implementing cleaning throughout the day at public toilets (and not just at the end of the day), we recommended to Aerosan that the toilets should be cleaned after every 50 users. This recommendation was based on an approximate 0.5 log increase in E.coli on latrine slab surfaces after every ~50 users. The results are specific to a site with male urinals and five male cabins and two female cabins. The usage of the Aerosan toilets varied over the course of the day with busy times occurring in the morning and late afternoon. Consequently, scheduling cleaning based on usership as opposed to at a regular time intervals seemed most appropriate for the context. This is in line with recommendations in the “2022 Guide to Better Public Toilet Design and Maintenance” produced by the Restroom Association in Singapore and an 2010 document produced by the British Toilet Association [38, 47]. It is important to create site-specific sustainable cleaning protocols considering which materials are available locally, the cost of water, and the type of toilet. If biogas latrines are being used, like those in the current study, cleaning materials should be picked with care to not interfere with gas production. It is recommended that public toilets are audited on a regular basis to ensure continued cleanliness.

Study limitations and recommendations for future cleaning studies

There are several limitations of this study including that it was limited in scope and duration which makes it virtually impossible to generalize these results to other contexts. The project was limited due to financial constraints and logistical challenges in conducting microbiological research in a field setting (e.g sterilization, access to sterile lab space, travel time in urban environment, safety concerns) in a low-income country. Due to these constraints, we were unable to collect and process samples at more than two time points each day from all the surfaces, meaning we had to vary the time of day that we collected the samples. Consequently, we don’t have daily repeated measures for each sampling time point. We chose to swab multiple surfaces instead of fewer so we could better understand the extent of contamination in the latrines. We were unable to collect usership data by individual cabin and only collected data in aggregate across all female and all male cabins prior to a specific sampling event. Additionally, we designed the study to develop site specific recommendations for Aerosan, a local NGO. Therefore, the study design was tailored to meet their needs, including that they wanted use to generate recommendations on cleaning frequency by users (instead of by time) as they planned to implement turnstiles to count users at public toilets they were implementing in Kathmandu.

There is limited data in the literature on the cleanliness of public toilets in low-income settings, and therefore our work helps to fill that data gap. Given our experience, we have several recommendations for future cleaning studies where possible:

  1. Samples should be collected at the same times over multiple days and always include samples from “clean” conditions
  2. Utilize a structured observation questionnaire to capture other behavioural events at the study site (i.e. people avoiding certain cabins, impromptu cleanings, handwashing etc)
  3. Enumerate individuals entering each cabin (instead of block of cabins) prior to sampling
  4. Collect and analyze the microbiological quality of the water used for cleaning the latrines
  5. Perform 2–3 serial dilutions for culture-based studies
  6. Analyze for pathogens and not only indicator organisms to better understand potential health risks

Supporting information

S1 Text. Summary of total coliform (TC) and E. coli (EC) concentrations stratified by number of users.

https://doi.org/10.1371/journal.pwat.0000091.s003

(DOCX)

S2 Text. Community latrine cleaning protocols.

https://doi.org/10.1371/journal.pwat.0000091.s004

(DOCX)

S2 Data. Latrine slab data file used for figures and analysis.

https://doi.org/10.1371/journal.pwat.0000091.s006

(CSV)

S3 Data. Small surfaces data file used for figures and analysis.

https://doi.org/10.1371/journal.pwat.0000091.s007

(CSV)

Acknowledgments

The authors would like to thank the Environment and Public Health Organization (ENPHO) lab for allowing us to use their space for sample processing and analysis, as well as the public toilet operators who allowed us access to the sampling sites and the Aerosan staff that counted the latrine users during the study period.

References

  1. 1. United Nations. Water and Sanitation. In: United Nations Sustainable Development [Internet]. [cited 21 Sep 2020]. https://www.un.org/sustainabledevelopment/water-and-sanitation/
  2. 2. World Health Organization, United Nations International Children’s Emergency Fund. Sanitation. In: Joint Monitoring Programme [Internet]. [cited 21 Sep 2020]. https://washdata.org/monitoring/sanitation
  3. 3. World Health Organization, United Nations International Children’s Emergency Fund. Progress on drinking water, sanitation and hygiene: 2017 update and SDG baselines. 2017.
  4. 4. World Health Organization, others. Guidelines on sanitation and health. World Health Organization; 2018.
  5. 5. World Health Organization, United Nations International Children’s Emergency Fund. Progress on household drinking water, sanitation and hygiene 2000–2020: five years into the SDGs. Geneva; 2021.
  6. 6. Geere J-AL, Hunter PR. The association of water carriage, water supply and sanitation usage with maternal and child health. A combined analysis of 49 Multiple Indicator Cluster Surveys from 41 countries. International Journal of Hygiene and Environmental Health. 2020;223: 238–247. pmid:31488359
  7. 7. Ellis A, McClintic EE, Awino EO, Caruso BA, Arriola KRJ, Ventura SG, et al. Practices and Perspectives on Latrine Use, Child Feces Disposal, and Clean Play Environments in Western Kenya. The American Journal of Tropical Medicine and Hygiene. 2020;102: 1094–1103. pmid:32124727
  8. 8. Hirve S, Lele P, Sundaram N, Chavan U, Weiss M, Steinmann P, et al. Psychosocial stress associated with sanitation practices: experiences of women in a rural community in India. Journal of Water, Sanitation and Hygiene for Development. 2015;5: 115–126.
  9. 9. Obeng PA, Keraita B, Oduro-Kwarteng S, Bregnhøj H, Abaidoo RC, Awuah E, et al. Usage and barriers to use of latrines in a Ghanaian peri-urban community. Environmental Processes. 2015;2: 261–274.
  10. 10. Shiras T, Cumming O, Brown J, Muneme B, Nala R, Dreibelbis R. Shared latrines in Maputo, Mozambique: exploring emotional well-being and psychosocial stress. BMC International Health and Human Rights. 2018;18: 30. pmid:30045729
  11. 11. Sara S, Graham J. Ending open defecation in rural Tanzania: which factors facilitate latrine adoption? International Journal of Environmental Research and Public Health. 2014;11: 9854–9870. pmid:25247427
  12. 12. O’Keefe M, Messmer U, Lüthi C, Tobias R. Slum inhabitants’ perceptions and decision-making processes related to an innovative sanitation service: Evaluating the Blue Diversion Toilet in Kampala (Uganda). International journal of environmental health research. 2015;25: 670–684. pmid:25684115
  13. 13. Patinet J. Dry toilets in urban crises: the case of Kabul. Proceedings of the 4th International Dry Toilet Conference, Tampere, Finland. 2012. pp. 22–24.
  14. 14. Capone D, Buxton H, Cumming O, Dreibelbis R, Knee J, Nalá R, et al. Impact of an intervention to improve pit latrine emptying practices in low income urban neighborhoods of Maputo, Mozambique. International Journal of Hygiene and Environmental Health. 2020;226: 113480. pmid:32086016
  15. 15. Oakley von S. Anaerobic Sludge Blanket Reactors. In: Global Water Pathogen Project [Internet]. Michigan State University, UNESCO; 13 Mar 2017 [cited 16 Dec 2022]. https://www.waterpathogens.org/http%3A//www.waterpathogens.org/book/anaerobic-sludge-blanket-reactors
  16. 16. Adegoke S. Septic Systems. In: Global Water Pathogen Project [Internet]. Michigan State University, UNESCO; 13 Mar 2017 [cited 16 Dec 2022]. https://www.waterpathogens.org/book/septic-systems
  17. 17. Adegoke S. Cesspits and Soakpits. In: Global Water Pathogen Project [Internet]. Michigan State University, UNESCO; 15 Feb 2018 [cited 16 Dec 2022]. https://www.waterpathogens.org/book/cesspits-and-soakpits
  18. 18. Orner N. Pit Toilets (Latrines). In: Global Water Pathogen Project [Internet]. Michigan State University, UNESCO; 23 Aug 2018 [cited 16 Dec 2022]. https://www.waterpathogens.org/book/pit-toilets-latrines
  19. 19. Abney SE, Bright KR, McKinney J, Ijaz MK, Gerba CP. Toilet hygiene—review and research needs. Journal of Applied Microbiology. 2021;131: 2705–2714. pmid:33899991
  20. 20. Evans B, Hueso A, Johnston R, Norman G, Pérez E, Slaymaker T, et al. Limited services? The role of shared sanitation in the 2030 Agenda for Sustainable Development. Journal of Water, Sanitation and Hygiene for Development. 2017;7: 349–351.
  21. 21. United Nations Development Programme. Human Development Reports. 2020 [cited 8 Jun 2021]. http://hdr.undp.org/en/countries/profiles/NPL
  22. 22. The World Bank. Nepal Data. In: Urban Population [Internet]. 2019 [cited 3 Sep 2020]. https://data.worldbank.org/indicator/SP.URB.TOTL?locations=NP
  23. 23. Bista R. Push and Pull Factors of Urbanization in Nepal: Its impacts on Household Perspectives. 2019.
  24. 24. United Nations, Department of Economic and Social Affairs, Population Division. World urbanization prospects: the 2014 revision. 2014.
  25. 25. Nepal Population (2020)—Worldometer. [cited 3 Sep 2020]. https://www.worldometers.info/world-population/nepal-population/
  26. 26. Behera B, Sethi N. Analysis of household access to drinking water, sanitation, and waste disposal services in urban areas of Nepal. Utilities Policy. 2020;62: 100996.
  27. 27. Sekine K, Roskosky M. Emergency response in water, sanitation and hygiene to control cholera in post-earthquake Nepal in 2016. Journal of Water, Sanitation and Hygiene for Development. 2018;8: 799–802. pmid:33384868
  28. 28. Central Bureau of Statistics. Annual Household Study 2016/17. In: Nepal in Data [Internet]. 2017 [cited 3 Sep 2020]. https://nepalindata.com/resource/annual-household-survey-201617/
  29. 29. McGinnis S, Marini D, Amatya P, Murphy HM. Bacterial contamination on latrine surfaces in community and household latrines in Kathmandu, Nepal. International journal of environmental research and public health. 2019;16: 257. pmid:30658441
  30. 30. Mendes M, Lynch D. A bacteriological survey of washrooms and toilets. Epidemiology & Infection. 1976;76: 183–190. pmid:1063213
  31. 31. United States Environmental Protection. Method 1604: total coliforms and Escherichia coli in water by membrane filtration using a simultaneous detection technique (MI Medium). Stand Methods. 2002. pp. 4–7.
  32. 32. Kwiringira J, Atekyereza P, Niwagaba C, Günther I. Gender variations in access, choice to use and cleaning of shared latrines; experiences from Kampala Slums, Uganda. BMC Public Health. 2014;14: 1180. pmid:25407788
  33. 33. Nakagiri A, Kulabako RN, Nyenje PM, Tumuhairwe JB, Niwagaba CB, Kansiime F. Performance of pit latrines in urban poor areas: A case of Kampala, Uganda. Habitat International. 2015;49: 529–537.
  34. 34. Le TT, Luu NH, Rheinländer T, Dalsgaard A, Konradsen F. Sanitation behavior among schoolchildren in a multi-ethnic area of Northern rural Vietnam. BMC Public Health. 2012;12: 140. pmid:22353490
  35. 35. Garn JV, Sclar GD, Freeman MC, Penakalapati G, Alexander KT, Brooks P, et al. The impact of sanitation interventions on latrine coverage and latrine use: A systematic review and meta-analysis. International Journal of Hygiene and Environmental Health. 2017;220: 329–340. pmid:27825597
  36. 36. Tumwebaze IK, Orach CG, Niwagaba C, Luthi C, Mosler H-J. Sanitation facilities in Kampala slums, Uganda: users’ satisfaction and determinant factors. International Journal of Environmental Health Research. 2013;23: 191–204. pmid:22873693
  37. 37. Hambraeus A, Malmborg A-S. Disinfection or cleaning of hospital toilets—an evaluation of different routines. Journal of Hospital Infection. 1980;1: 159–163. pmid:6182206
  38. 38. British Toilet Association (BTA). BTA Guidance–Toilet Cleaning. 2010 Nov.
  39. 39. Rusin P, Orosz-Coughlin P, Gerba C. Reduction of faecal coliform, coliform and heterotrophic plate count bacteria in the household kitchen and bathroom by disinfection with hypochlorite cleaners. J Appl Microbiol. 1998;85: 819–828. pmid:9830117
  40. 40. Dharan S, Mourouga P, Copin P, Bessmer G, Tschanz B, Pittet D. Routine disinfection of patients’ environmental surfaces. Myth or reality? J Hosp Infect. 1999;42: 113–117. pmid:10389060
  41. 41. Griffith C. Surface Sampling and the Detection of Contamination. Handbook of Hygiene Control in the Food Industry. 2016; 673–696.
  42. 42. Edberg SC., Rice EW., Karlin RJ., Allen MJ. Escherichia coli: the best biological drinking water indicator for public health protection. Journal of Applied Microbiology. 2000;88: 106S–116S. pmid:10880185
  43. 43. Heijnen M, Routray P, Torondel B, Clasen T. Shared sanitation versus individual household latrines in urban slums: a cross-sectional study in Orissa, India. The American journal of tropical medicine and hygiene. 2015;93: 263–268. pmid:26123953
  44. 44. Ramlal PS, Stenström TA, Munien S, Amoah ID, Buckley CA. Relationships between shared sanitation facilities and diarrhoeal and soil-transmitted helminth infections: an analytical review. Journal of Water, Sanitation and Hygiene for Development. 2019;9: 198–209.
  45. 45. Potgieter N, Aja-Okorie U, Mbedzi RL, Traore-Hoffman AN. Bacterial Contamination on Household Latrine Surfaces: A Case Study in Rural and Peri-Urban Communities in South Africa. Current Microbiological Research in Africa. Springer; 2020. pp. 175–183.
  46. 46. Monsell L, Dullaghan N, Krastev S, Pilat D. Applying Behavior Change to Promote Gender—Symmetrical Public Toilet Usage in Nepal; Aerosan Behavioral Diagnostic Report. Montreal, QC, Canada: The Decision Lab; 2018.
  47. 47. Restroom Association (Singapore). A Guide to Better Public Toilet Design and Maintenance. 5th ed. 2022. https://www.toilet.org.sg/articles/GuideBetterPublicToilet.pdf