Abstract
Water is an essential resource required for various human activities such as drinking, cooking, and other recreational activities. While developed nations have made significant improvement in providing adequate quality water and sanitation devoid of virus contaminations to a significant percentage of the residences, many of the developing countries are still lacking in these regards, leading to many death cases among the vulnerable due to ingestion of virus-contaminated water and other waterborne pathogens. However, the recent global pandemic of COVID-19 seems to have changed the paradigm by reawakening the importance of water quality and sanitation, and focusing more attention on the pervasive effect of the use of virus-contaminated water as it can be a potential driver for the spread of the virus and other waterborne diseases, especially in developing nations that are characterized by low socioeconomic development. Therefore, this review assessed the socioeconomic inequalities related to the usage of virus-contaminated water and other waterborne pathogens in developing countries. The socioeconomic factors attributed to the various waterborne diseases due to the use of virus-contaminated water in many developing countries are poverty, the standard of living, access to health care facilities, age, gender, and level of education. Some mitigation strategies to address the viral contamination of water sources are therefore proposed, while future scope and recommendations on tackling the essential issues related to socioeconomic inequality in developing nations are highlighted.
Keywords: Drinking water, Inequality, Developing countries, Socioeconomic, Virus contamination
Graphical abstract
1. Introduction
Water is regarded as the epicenter of human activities as it is required for drinking, irrigation of crops, recreational activities and industrial use. Protecting this essential natural resource against any contaminants is critical to forestalling its potential avenue for outbreaks of diseases. Unfortunately, water quality and sanitation remain elusive, with conspicuous occurrences in the developing countries (Célia da Silva Lanna et al., 2019; Montgomery and Elimelech, 2007). Available data indicate that more than 30% of the developing and less developed countries have no access to quality drinking water sources (WHO and UNICEF, 2015). Consequently, leading to an upsurge in the use of any available water resources including reclamation and reuse of treated wastewater for domestic activities and irrigation purpose, considering the rapid population growth, climate change, and increased water demand (Morrison et al., 2020; Bougnom et al., 2019; Santos et al., 2017). An estimate of 663 million people is reportedly consuming untreated water obtained from different sources including groundwater and surface water (WHO and UNICEF, 2015). While the current treatment procedures have achieved excellent results in treating physical, chemical and selected microbiological contaminants (Adelodun et al., 2019; Tandukar et al., 2020), the removal of human enteric viruses in the wastewater remains unsatisfactory, with less attention giving to virus contaminations in water sources and their health impact (Gall et al., 2015). Moreover, there is no regulatory standard procedures for the treatment of virus-contaminated water and wastewater at the moment (Gerba et al., 2018; Qiu et al., 2015). The ability of some of the viruses to travel a much greater distance than bacteria in the soil and eventually to groundwater source due to their sizes and their persistence for a more considerable period making their removal difficult and high risk of waterborne gastroenteritis virus infections (Gerba, 1984; Schwab, 2007). A recent global review of groundwater-related enteric disease outbreaks identified 649 events within the published literature from 1948 to 2015 with an alarming increase in groundwater-related Acute Gastrointestinal Infections (AGI) (Murphy et al., 2017).
The impact of using unsafe water on public health is of great universal concern with the frequent detection of pathogens in various water bodies. The ingestion of contaminated water, which is most often caused by poor sanitation and hygiene often results in various waterborne diseases (Adelodun et al., 2020b; Pooi and Ng, 2018; Nasser, 1994). Yang et al. (2020) found an association between drinking water and poor sanitation and the risk of disease infections among children (under five years of age) with the poor socioeconomic condition in sub-Saharan Africa. In 2012, 1.8 billion people which is almost 25% of the world population were estimated to consume contaminated water containing viruses, protozoa, and bacteria (WHO and UNICEF, 2015), that have led to various kind of diseases in human especially gastroenteritis (Bosch et al., 2008). One of the significant reoccurring waterborne diseases is diarrhea with 1.7 billion reported cases annually (WHO, 2017a), resulting in the death of 525,000 children below the age of 5 years annually (Pooi and Ng, 2018). UNICEF (2012) documented that about 90% of diarrhea death globally is a result of poor hygiene, inadequate sanitation and unsafe water. The general knowledge is that microbes are the primary organisms leading to the spread of diarrhea. Some of the contracted viruses through drinking water and their impact on human health is often neglected (Mantovani et al., 2015a). Based on the guidelines on drinking water, WHO classified water transmitted virus-related pathogens as exhibiting an average and to a great health significance on human health, and these viruses include enteroviruses, adenovirus, rotavirus, norovirus and other caliciviruses, astrovirus, hepatitis A, polioviruses and coxsackieviruses (WHO, 2017b). Besides, other viruses like cytomegalovirus and polyomaviruses can also be proliferated via water (WHO, 2017a,b; Cannon et al., 2011), as well as coronaviruses and influenza that have been alluded to spread through potable water with inconclusive evidence (WHO, 2017b). Unfortunately, some of the viruses may result in acute illnesses such as hepatitis (hepatitis A and E viruses), cancer (polyomavirus), meningitis, encephalitis, and myocarditis (enteroviruses) (WHO, 2017b).
While developed nations have made significant progress in water treatment systems to address viruses and pathogens contaminations in water and wastewater, the majority of people have access to improved drinking water, thereby averting waterborne related diseases. However, the use of contaminated water for various human activities continues by many people living in developing and less developed nations due to the wide differential inequality in socioeconomic development. So, the importance of accessibility to potable water cannot be overemphasized as it plays a vital role in the present global efforts to address the prevalent poverty and poor health, specifically in developing countries. Previous studies proved that those living below $1.25 per day (those living in abject poverty) correspond almost with those lacking access to potable water (Sambu, 2016; Rijsberman, 2006). In order to prevent and contain diseases, accessibility to water and sanitation is essential to combating the virus and maintaining the good health and well-being as contained in the Sustainable Development Goal 3. Thus, to attain the United Nations (UN) sustainable development goal 6 “Clean Water and Sanitation” by 2030, a substantial attempt in the creation and management of wastewater treatment plants (WWTPs) should be put into operation in these less developed countries in the subsequent years (Gallego-Schmid and Tarpani, 2019; Nhamo et al., 2019; UN-Water, 2017). Considering the current global pandemic caused by the novel coronavirus (SARS-CoV-2) with several studies indicating its possible persistence and potential risk in water environment coupled with the existing endemic of waterborne related infections and diseases, especially those resulting from the ingestion of virus-contaminated water, a review focusing on the assessment of differential inequality of virus-contaminated water use in developing countries is essential.
In an attempt to provide an outline of the status quo of socioeconomic disparities on the basis of virus-contaminated water use in developing nations, the paper is structured as follows. Firstly, there is a review of the water pollution status in developing countries. Also, virus associated with water pollution and their human health impacts are expatiated. More importantly, this paper assessed the socioeconomic inequality factors relating to virus-contaminated water usage in developing countries. Further, some possible mitigation strategies were proffered based on the existing literature that can be adopted for the developing countries, especially those characterized by low level social and economic development. Finally, this review concludes with future research needs to curb the viral contamination in water in developing countries and put forward recommended policies.
We employed three-stage procedures in order to address the objectives of this study adequately. Firstly, the peer-reviewed articles published only in the English language were searched for and retrieved from the Scopus database (www.scopus.com), which has the most extensive abstract and citation of peer-reviewed literature. The relevant keywords corresponding to the topic and objectives of this study including “contamination”, “water”, “socioeconomic”, “drinking water”, “virus”, which were combined with the Boolean search words of ‘AND’, ‘OR’ were used. The selected articles include original and review articles published within the last 20 years (1999–2019). The articles that mainly on water pollution without pathogenic contaminations and attributed waterborne diseases were not considered. Secondly, to avoid the omission of important key papers that capture the objectives of this study, relevant articles from the references of the retrieved papers were manually screened for relevance, after which they were retrieved. Lastly, all the retrieved articles were thoroughly reviewed, synthesized, and included in this study.
2. Status of water pollution in developing countries
Water quality indicators of an area are usually defined based on physical, chemical and biological parameters and the choice of which is dependent on water use. The physicochemical properties of water have been reported to influence the development of biological life in water, thereby affecting water quality (Adelodun et al., 2020b; Soja and Wiejaczka, 2014). Thresholds are allocated to each indicator, and when such permissible limits are exceeded, there is a high risk of threat to human health (Mukate et al., 2019). Recent studies on analyses of river water pollution in Ethiopia considered some physicochemical water quality parameters (pH, dissolved oxygen, biochemical oxygen demand, total nitrogen, total phosphorus, and electrical conductivity) and bio-indicators (macroinvertebrate and diatom indices) by obtaining water samples from agriculture, forest, and urban landscapes within the Nile, Omo-Gibe, Tekeze and Awash River basins (Awoke et al., 2016).
Water policy frameworks and interviews were also employed to ascertain the effectiveness of the study. The study concluded that there was a significant water quality deterioration in the study areas in all the four basins. It was concluded that the river water pollution poses a great challenge to human health and immediate solutions should be proffered to prevent future health deterioration. A good look at available literature centered on water pollution in the South Asian region, predominantly in Bangladesh, Nepal, and India, showed that high pollution loads discharged in rivers as a result of industrial wastes, population growth, pesticides, fertilizers, domestic sewage, domestic effluent and urban activities had offered more severe and adverse effects on the health of inhabitants. Karn and Harada (2001) performed regression analysis on their study data to evaluate annual pollution trends in average biochemical oxygen demand (BOD) and dissolved oxygen (DO) at Bagmati, Yamuna and Buriganga rivers and discovered that the BOD increase rate in Bagmati was highest and most rapid than the others. Average annual BOD was found to be at least five times higher than standards in the rivers of Dhaka and Delhi and as much as 15 times higher in the Bagmati if the standards for Nepal were on the same scale as those in India and Bangladesh.
As a continent, Africa is endowed with substantial water resources, including a huge interconnected river water network (Fig. 1 ), which are often serve as a reservoir for domestic, industrial, and agricultural wastes, thereby leading to significant economic scarcity of the water resources in the region. Some studies have assessed and confirmed the viral contamination of river systems in selected countries in Africa. Marie and Lin (2017) evaluated the presence of viral causing waterborne in the Umhlangane River of South Africa, which serves as the main drinking water catchment as well as reservoir for domestic, industrial and agricultural wastes. Some infectious viral groups, including human adenovirus, polyomavirus and hepatitis A and C virus were identified, which may pose a significant health risk to the many populations using the water from the River source for various domestic and agricultural uses. Also, the section of Nile River up to 300 km south of Egypt was reported to contain enteroviruses and (coxsackieviruses) with a frequency of 60% (Rabeh, 2009), which indicates potential health risk for the rural communities who majorly use the River water for domestic consumption and recreational purposes. Likewise, Virus-like particles were reported in the Umgeni River water samples in South Africa, indicating potential health risk implications for human consumption (Ganesh et al., 2014). Similarly, the high prevalence of Human astrovirus was identified from both Rivers Mboone and Mbagathi in Kenya (Kiulia et al., 2010). Further, the enteric viruses like adenoviruses and enteroviruses were also confirmed from the water samples taken from the Lake Victoria in Kenya (Opere et al., 2020). Although some of the tested samples only confirmed the genetic materials of the viruses with no possible viability, the reported viral infections associated with drinking water supplies cannot be entirely ignored (Verheyen et al., 2009; Sekwadi et al., 2018).
Fig. 1.
Topographic map of African River network.
Developing countries, mainly in Africa, are currently faced with adoption, implementation and valuation of water for ecosystem conservation and water quality management practices are still in the juvenile stage. This situation has strengthened the consumption of untreated water and enhanced untreated water discharged into rivers. Similar reported cases have been documented in Ethiopia, and findings have been concluded that gross pollution of many rivers is a consequential result of rapidly increasing urban populations and intense industrial and agricultural activities (Beyene et al., 2012). The ultimate goal of drinking water supply as declared by water resources engineers in developing countries is to provide good water quality, not only on the verge of leaving the treatment plant but at the customer's tap and point of discharge. However, most researches have failed to assess water pollution in the course of distribution. According to Prest et al. (2016), treated drinking water enters a distribution system containing physical particles, microbial loads (cells) and nutrient loads (organic and inorganic nutrients). When treated water moves through contaminated distribution lines and it's retained with an extensive ‘water age’, especially at the dead-end nodes, available physicochemical and microbiological contaminants can result in the deterioration of the quality of water that reaches customer's tap compared to the original water produced at the treatment plant (Proctor and Hammes, 2015).
Liu et al. (2016) identified four essential elements involved in water pollution during its distribution through pipes:
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1.
The bulk water that flows through the pipe networks;
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2.
The suspended solids which are particulate matter that is suspended in the water and transported through the network;
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3.
The pipe surface with the associated material, e.g., biofilm, extracellular polymeric substance (EPS), scaling; and
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4.
The loose deposits which are particulate matter that has accumulated and is retained in the pipes. During water distribution, suspended particles may be transported or deposited as loose deposits and then re-suspended due to flow hydraulic turbulence resulting from flow conditions and characteristics. Pipe geometry and material play a greater part in water pollution and quality with respect to energy efficiency as submitted by (Broo et al., 2001). Rabin (2008) further investigated Broo et al. (2001) submission and concluded that the release of lead in pipes poses health risks to consumers and that pipes manufactured with rubber materials promote microbial synthesis in water distribution networks, thereby increasing the microbial load of the water. Yu et al. (2004) also attributed a faulty plumbing system to the spread of SARS coronavirus in some apartment buildings in Hong Kong in 2003. It is noteworthy that materials accumulated in pipes such as biofilm, scaling and loose deposits develop over time and the significance of such an effect may not be manifested in the preliminary stage. The age of use of such a conveyance system plays a vital role in the accumulation of material in the form of pipe scales, loose deposits and biofilm material (Makris et al., 2014). Magnetic treatment of water has been reported to reduce scale formation and carbonate deposits in pipes (Lipus and Dobersek, 2007). However, it is still not a universally-proven approach to water treatment as it is marred with several controversies and divided opinions. However, human health is of global, paramount importance and a good knowledge of contaminants' effect on human health is essential, be it on the microscopic or macroscopic scale.
3. Viruses associated with water pollution
Viruses are intracellular organisms with a genome within a protein capsid and are possibly the most lethal pathogens amongst those discovered in wastewater (O'Brien et al., 2017). According to Flint et al. (2004), viruses are classified as single-stranded DNA (ssDNA), single-stranded RNA (ssRNA), double-stranded DNA (dsDNA), and double-stranded RNA (dsRNA), depending on their genome kind. Bosch et al. (2008) reported that over 100 known kinds of viruses are defecated in human feces. In contrast, about 200 high diversity of human viral pathogens are found in the environment (O'Brien et al., 2017). They are also raised in samples affected by pollution with more species discovered (Bibby, 2013). Moreover, human viral pathogens such as bacteriophages might have a severe impact on the natural watercourses that receive treated effluent containing these viruses which are specifically resistant to wastewater treatment and difficult to detect in environmental media despite the recent advances in water and wastewater treatment technologies (Shapiro et al., 2010).
Water has been recognized as a common medium for the proliferation of viruses which may allow their continued existence (Pinon and Vialette, 2019). Surface water resources like oceans, rivers, lakes, estuary, groundwater, marine water are concerned with viral pollution (Shoham et al., 2012). This is because the sewage treated effluents are not efficiently removed, containing certain amounts of viruses that are subsequently discharged into the water environment (Okoh et al., 2010). The receiving water bodies further convey these viruses downstream, where it is utilized for various purposes like irrigation of crops, recreational activities, and other anthropogenic uses. This clearly explained how humans are exposed to fecally contaminated water via different exposure routes like direct ingestion of water during recreation, improperly treated drinking water and feeding on contaminated food products (Lodder et al., 2015; Ehlers et al., 2005). Some viruses such as coxsackieviruses, echoviruses, adenoviruses, noroviruses, and hepatitis A viruses are portrayed as recreationally related waterborne microorganisms (Sinclair et al., 2009).
Pathogenic germs such as protozoa and bacteria are also transmitted via the water route and stayed in the gastrointestinal tract of their host (humans and animals) and subsequently released into the environment via feces from where surface and ground waters are polluted (Paleologos et al., 2020). It may also be released into the host's environment through urine and respiratory secretions (Ghernaout, 2020). The most common human enteric viruses include enterovirus, Hepatitis A virus, Adenoviruses, Torovirus, Hepatitis E virus, Bocaviruses and coronaviruses, which may be released into water supplies, recreational waters and crops through sewage, runoffs, solid waste landfills and septic tanks (Ghernaout, 2020). Instances are prevalent with swimming pool water where outbreaks of norovirus, hepatitis A virus and adenoviruses were recorded.
Other human viruses such as adenovirus type 40 and noroviruses genogroup I and genogroup II are widely found in wastewater through fecal excretion. Aichi virus 1 and adenovirus are likely major human enteric viruses regularly detected throughout the year (Rachmadi et al., 2016; Kitajima et al., 2014). Adenoviruses are among the most abundant human viruses in wastewater treatment plant effluent (La Rosa et al., 2010) and were previously identified in wastewater through conventional techniques (Bofill-Mas et al., 2010). Wastewater is remediated microbiologically and physicochemically in wastewater treatment plants to eliminate pollutants before the discharge of environmentally safe water. Fecal pollution of environmental water is the main health concern, given that environmental waters are utilized for the production of food and drinking water supply (Masclaux et al., 2013). Besides, viruses from the released environmental water might reach diverse food items such as vegetables, fruits and raw shellfish (Bosch et al., 2008). Moreover, a virus infecting pepper plant called pepper mild mottle virus was suggested as a new indicator for human fecal contamination in a water environment because of its moderately high occurrence in treated sewage (Kitajima et al., 2014; Hamza et al., 2011).
At the moment, the newly discovered strain from the coronavirus family has unquestionably attracted the attention of the world as some studies have reported its detection in wastewater in Netherlands, Australia, USA and Greece (Paleologos et al., 2020; Medema et al., 2020; Ahmed et al., 2020; Lodder and de Roda Husman, 2020). Meanwhile, few reports indicate whether the SARS-CoV-2 can be transmitted via contaminated water (Adelodun et al., 2020a; Arslan et al., 2020a). However, supporting evidence to monitor the dynamics of SARS-CoV-2 closely has emerged as Arslan et al. (2020a,b) posited that the virus could stay longer in the digestive tract than the respiratory tract with infected patients excreting viral nucleic acid despite testing negative after 6 and 14 days from respiratory sampling specimen. Also, the close similarity of SARS-CoV-1 and SARS-CoV-2 in chemical structures and morphological characteristics needs full-fledged attention as the outbreak of the former in 2003 was traced to a failed water seal system and poor sanitation procedures.
4. Socioeconomic inequality due to virus-associated water pollution
One of the 21st century's challenges is the continuous gap in educational and socioeconomic inequalities that have ravaged different countries around the world and consequently rendered the world economic growth and development at high risk (Anlimachie and Avoada, 2020). Generally, it has been established that there exists a wide margin of inequalities between the rich and the poor; an average rich man's income is 57 times the poorest (Katiyatiya, 2020). Socioeconomic inequality has distinctively shown the varied level of access to basic social amenities within most developing nations' homes, including essential facilities such as access to potable water and sanitation (Akoteyon, 2019; Gbemiga and Deborah, 2019; Gasana et al., 2002); . Part of the United Nations sustainable development goals (SDG) (Goal 6) stressed on the need to provide adequate and sustainable water and environmental sanitation for all (United Nations, 2018). However, adequate water supply, proper sanitation and improved hygiene are devoid of a particular location and time – it is a primary need for human survival. These are mostly not adequately provided, especially in developing nations (World Bank Group, 2017a; Gasana et al., 2002).
The lack of access to potable water, proper sanitation and proper waste management conspicuously exists in many parts of the developing nations. For instance, Nigeria recorded a decline in access to potable water from 32% to 7% from 1990 to 2015, while 90% of rural dwellers in Niger republic practices open defecation and 51% do not have access to potable water (World Bank Group, 2017b). Similarly, lower-income households in Haiti have high susceptibility factors of 2.4 in contracting enteric diseases than high-income household children; 41% of water supply sources in Bangladesh is contaminated with E. coli and 56% of the top 20% in India has access to treated water compared to 6% of the bottom 20% (World Bank Group, 2017b). Developing nations have been ravaged with high death rates due to the use of contaminated water from complications from enteric diseases, with a larger percentage of these populations from rural dwellers (Gomez et al., 2019). The socioeconomic imbalance of water supply and sanitation have rendered the low-income earners to wait for options provided by the government, which sometimes are irregular. In contrast, the high-income earners sought after personal provisions, such as borehole and premium sanitation services. Improved access to water and sanitation services will increase people's hygiene, increase work productivity, reduce susceptibility to diseases and malnourishment (Morales-Novelo et al., 2018).
Though socioeconomic indicators are crucial for assessing and mitigating the impact of waterborne viral diseases, only in the past decade or so have efforts been made to understand better their role (Ajibade et al., 2020; Beltran et al., 2011). The advent of current novel coronavirus (SARS-CoV-2) and the possible persistence in a water environment (Carducci et al., 2020) has further created more apprehension on potential socioeconomic implications of virus-associated water pollution, especially in less developed countries with a wide-gap of socioeconomic inequality (Arslan et al., 2020a,b; Adelodun et al., 2020). Waterborne viral pathogens have huge socioeconomic impacts in both developed and developing nations; however, the magnitude of the impact and the burden of viral diseases including severity and prevalence are more severe in regions of the world with highly polluted environments, majority of which are developing nations (Rodríguez-Díaz et al., 2009). There have been global reports on viral pathogens resulting from exposure to contaminated drinking and recreational waters, especially as it concerns human socioeconomic factors. This section, therefore, examines some of the socioeconomic factors and their linkage with waterborne viral diseases.
4.1. Poverty
The poor are more susceptible to waterborne diseases than the well-off (WHO and UNICEF, 2015). This is because they lack adequate supplies of safe water and proper methods of disposing of their wastes. The lack of quality water and sanitation creates ideal conditions under which viral pathogens thrive. Further, the lack of good quality and reliable water sources may drive the poor to extract water from unsafe alternative sources, thereby exposing them to waterborne viral diseases and putting their health at risk. Several studies have established linkages between poverty and virus-associated water pollution. El Zanfaly (2015) reported a clear link between poverty and water pollution, implying an association between poverty and dirtiness, and dirtiness with microbial polluted water. The author further reported that children in rural households were more prone to contaminated water sources than children who live in urban households and that effects of polluted water were compounded by the tendency of rural women to reuse the household water drawn from pumps or wells, further buttressing the significance of poverty on the use of microbially contaminated water. Also, Blaise and Dovie (2007) in their study on diarrheal diseases in the history of public health reported that poverty and environmental filth (hygiene level) were leading risk factors associated with water pollution and consequently waterborne diseases. Similarly, Parvez et al. (2019) reported a direct relationship between poverty and waterborne diseases, implying that extreme poverty levels resulted in increased waterborne diseases, especially in developing countries. Furthermore, research conducted in Latin America by Saback et al. (2001) and Struchiner et al. (1999) found waterborne viral diseases to be higher in low-income populations than high-income populations implying that poverty was a major cause of waterborne illnesses.
4.2. Standard of living
A decent standard of living entails that people are able to comfortably provide health or medical facilities for the well-being of their families. Thus, the prevalence of waterborne diseases could be used as an index for measuring the level of development in a given country. Studies have shown that waterborne diseases vary widely due to a country's standard of living. Polimeni et al. (2016) reported varying degree of macro-level socioeconomic factors such as the standard of living; the unbalanced split of rural/urban population; regional inequality; the level of trade (imports of goods and services) and access to health care with an increased risk for viral waterborne illnesses and death. Also, Yongsi and Ntetu (2008) and Pande et al. (2008), whose study areas were developing countries (Cameroun and Benin Republic, respectively), reported that households with the low standard of living recorded a higher prevalence of waterborne illnesses and vice versa; implying that waterborne illnesses could be inhibited or encouraged by households standard of living. Kunasol et al. (1998), whose study was conducted in Southeast Asia, also documented that exposure to waterborne viral pathogens decreased with an improvement in living standards. Similar results were also reported by Osundare et al. (2020), Salman (2017), and Potgieter et al. (2010), who observed an increase in waterborne viral infections between populations with the low standard of living, thus recommending that prompt actions should be taken to improve the living standards in the study areas.
4.3. Level of education
Several findings show a clear inverse correlation between the level of education of a people and the rate of viral waterborne illnesses. The more people know about waterborne viral diseases, the greater the tendency to manage the diseases, and hence the lower the disease occurrence. Nearly one-third of the global population lives in developing South Asia, where waterborne diseases are high, especially in rural areas due to the inadequate awareness about these diseases (Malik et al., 2012). Arora et al. (2013) also reported that an increase in the household level of education would decrease viral waterborne disease prevalence. Martins et al. (2015) also confirmed these reports in their study on environmental sanitation and mortality associated with waterborne diseases in Brazilian children, concluding that the most significant health hazards related to water pollution were found in the rural communities characterized by a high concentration of low-income population with limited education. Furthermore, similar studies conducted in Algeria and Bangladesh by Guenifi et al. (2017) and Parvez et al. (2019), respectively, also reported a lower seroprevalence rate within households with a higher educational level, further confirming the significance of educational level to the degree of waterborne disease prevalence.
4.4. Access to healthcare
The risk of infection with waterborne viral diseases can be influenced by the level of access to healthcare, reflecting a factor of households' socioeconomic status. The tendency to easily access healthcare facilities can decrease susceptibility to waterborne viral disease complications by providing early detection and required medication to curb morbidity (Dickin and Schuster-Wallace, 2014). As reported by Polimeni et al. (2016), the level of access to healthcare would influence the risk level of waterborne viral infections. Households with low access to health facilities were at a greater risk of waterborne illnesses than households with high access, implying a negative correlation between access to healthcare and waterborne diseases. Saback et al. (2001) also gave an account of similar findings in their study on waterborne viral infections and socioeconomic status in a developing country. They observed that exposure to waterborne infections among residents decreased with an improvement in the country's healthcare status. Similarly, WHO (2009) and Hughes et al. (2014) reported that poor access to healthcare facilities was a measure of the high waterborne disease burden in developing countries of Africa and Asia.
4.5. Age
The most glaring implication of not preventing waterborne diseases is a possible high morbidity and mortality rates among children (Gleick, 2002). Waterborne viral pathogens can cause serious health challenges in children and the elderly alike. Even though several viral waterborne diseases are not age-specific, many cases of infections occur early in life, affecting mainly children between the ages of 5 and 9 (Mantovani et al., 2015b). Globally, unsafe water due to microbial contamination kills at least 1.6 million children under the age of five years, of which 84% of them live in rural areas characterized by poor socioeconomic status (Olowe et al., 2016). Hau et al. (1999) investigated a potential outbreak of enteric Hepatitis A and E viruses as a function of the vulnerable population group in the Mekong River Delta region of Vietnam, where the high risk of infection was found to be among the occupational and age-dependent group. McMichael (2019) and Rana (2010) also observed that children under the age of five were more likely to get seriously ill from waterborne pathogens compared to their adult counterparts. Similarly, Alian et al. (2011) also affirmed that viral waterborne disease infections increased with age, with the majority of infections coming from children living in rural areas. This is not surprising since rural settlements, especially developing countries, face huge sanitation problems and acute poverty, thus rendering the children from these areas vulnerable to waterborne disease infections. As El Zanfaly (2015) stated, lack of access to safe water and proper sanitation leads to the spread of waterborne diseases and has a significant impact, especially on the health of vulnerable age groups (5 years and below).
4.6. Gender
Gender differences exist in the social determinants of waterborne diseases due to the different household roles borne by each gender, which is a determining factor of waterborne infections. There is a significant contribution of women in fetching water, especially within rural household labor division in developing countries (Kher et al., 2015). The domination of women involved in fetching water invariably means that they have the most contact with water and less access to unpolluted alternatives and are thus more prone to waterborne infections than their male counterparts (World Bank Group, 2012). Similar findings were reported by Siddiqui et al. (2012), who attributed the high level of waterborne disease vulnerability of the female gender to the fact that the activities of women involve water usage in many ways, such as washing, cooking, etc. Furthermore, Pouramin et al. (2020) also affirmed that the female gender is more prone to waterborne infections.
The prevention of waterborne viral diseases is of great importance wordwide, especially in developing countries characterized by low and middle-income inhabitants. This is because the majority of the casualties from waterborne viral diseases have been reported among low and middle-income countries. Therefore to develop appropriate policies to reduce virus-associated water pollution, a complex approach to social structures and economic systems is required. In terms of socioeconomics, the literature on waterborne viral diseases finds the sources of infection to include poverty (low income and hygiene level), low level of education, low standard of living, inadequate access to healthcare, age, and gender (Fig. 2 ).
Fig. 2.
Socioeconomic factors influencing the occurrence of viral waterborne diseases.
5. Human health risk of virus-associated water pollution
Viral agents are being recognized as the leading cause of epidemic as relates to water pollution and contamination. The ingestion of virus-contaminated water or any other contaminants of such have a considerable health risk to human life. Many human viruses have been identified to cause gastroenteritis, a communicable disease that is mainly transmitted through water (Schwab, 2007). Gastroenteritis can lead to other illnesses, including headache, fever, and diarrhea, which could result in significant causes of mortality in developing nations due to its dehydration effect on infected individuals coupled with the existence of inadequate measures on rehydration therapy (Cheng et al., 2005). Some of these viruses are highly infectious and can persist, ranging from weeks to months in the water environment (Seitz et al., 2011; Shoham et al., 2012). Notably, among these viruses is the rotavirus that causes diarrhea and responsible for the majority of childhood morbidity and mortality in developing nations (Schwab, 2007). Diarrhea is singly responsible for the death of the world's youngest children (525,000 cases annually) within the bracket age of 5 years and below, with the majority of the cases occurring among the disadvantaged children in sub-Saharan Africa and South Asia (Pooi and Ng, 2018; UNICEF, 2012). Other waterborne viruses such as adenoviruses, enterovirus, hepatitis A and norovirus have also been reported to transmit various forms of infections and diseases including respiratory, ocular and urinary tract, muscle pain, pharyngitis, meningitis, conjunctivitis, paralysis, cardiomyopathy, gastroenteritis, and diarrhea which resulted in epidemics (Bonadonna and La Rosa, 2019); hence making the emergence of SARS-CoV-2 and its potential risk of COVID-19 spread through water, a serious of concern. Table 1 shows the presence of selected viruses in water environment across different countries, which indicate the potential risk of the virus transmission through this medium.
Table 1.
Detection of viruses in water environment.
| Virus type | Water Matrix | Concentration in genome (copies/L) | Country | Reference |
|---|---|---|---|---|
| Rotavirus | Wastewater treatment plant (influent and effluent) | 103 to 105 | South Africa | Osuolale and Okoh (2017) |
| Adenovirus, | Treated wastewater | 4.6 × 104 to 1.2 × 106 | Brazil | Schlindwein et al. (2010) |
| Pepper mild mottle | Municipal pond | 1.0 × 103 to 1.0 × 106 | Bolivia | Symonds et al. (2014) |
| Hepatitis E | Wastewater treatment plant (influent and effluent) | 6.1 × 102 to 5.8 × 105 | Italy | Di Profio et al. (2019) |
| SARS-CoV-2 | Sewage | Low of detection to 5.6 × 104 | Italy | La Rosa et al. (2021) |
| SARS-CoV-2 | River | 2.1 × 103 to 3.2 × 104 | Ecuador | Guerrero-Latorre et al. (2020) |
| SARS-CoV-2 | Wastewater (treated and untreated) | 105 to 106.5 | France | Wurtzer et al. (2020) |
| SARS-CoV-2 | Untreated wastewater | 2.6 × 103 to 2.2 × 106 | The Netherlands | Medema et al. (2020) |
| SARS-CoV-2 | Wastewater (treated and untreated) | 3.1 × 103 to 7.5 × 103 | USA | Sherchan et al. (2020) |
| SARS-CoV-2 | Untreated wastewater | 1.9 × 101 to 1.2 × 102 | Australia | Ahmed et al. (2020) |
| SARS-CoV-2 | Wastewater (Untreated and Secondary treated wastewater) |
1.4 × 105 to 3.4 × 105 | Spain | Randazzo et al. (2020) |
| SARS-CoV-2 | Secondary treated wastewater (before chlorination) | 2.4 × 103 | Japan | Haramoto et al. (2020) |
Developing nations with inadequate water and sanitation system are at high risk receiving end when the possible pathways of SARS-CoV-2 maybe from wastewater from hospitals and isolations centers and indiscriminate infected materials disposals with possible runoffs and underground water contamination of the nearby communities that relied mostly on wells and rivers (Adelodun et al., 2020a). The risk of exposing the vulnerable sections of the communities is a determining factor in combating the pandemic to a standstill. However, negligence of their basic needs (such as adequate wastewater treatment, provision of clean and drinkable water, and good sanitation management) will affect the fight against COVID-19.
This is evident as some of these countries lacked a working wastewater treatment plant and had to rely on discharging effluents into rivers, streams, and canals with little or no treatment (Arslan et al., 2020b). For instance, enterovirus of detectable level was confirmed in about 19% of the drinking water samples in South Africa (Ehlers et al., 2005). To curb the possibility of widespread COVID-19 amongst the vulnerable part of the community, Adelodun et al. (2020a,b) posited the following sustainable preventive measures – special treatment of hospital and isolation waste from public waste, proper monitoring within the community and frequent testing of SARS-CoV-2 in effluent water, practicing best sanitation procedure and improved water quality, provision of adequate decontaminants (such as point-of-use device) and government policy intervention.
Globally, the human health risk due to the socioeconomic inequality experienced in developing nations and felt mainly by women and girls due to exposure to contaminated water and soil has increased as against the SDG's goal 6 agenda (Pouramin et al., 2020). In the face of this coronavirus pandemic, the inadequate resources available has dramatically opened up a lot of loopholes in crisis management and decision making, inadequate and underpaid medical personnel, lack of investment in research and development for new product and services; these factors are results of decades of negligence in socioeconomic provisions for the citizens (UNDP, 2020).
In a report by Rosa et al. (2020), it was opined that SARS-CoV-2 has low stability in the environment and sensitive to chlorine, the virus survival at a temperature around 23 °C–25 °C declines and non-availability of data to claim the transmission via drinking water route. However, there is a need for continuous research on the survival of the virus in water, recovery method for Covid-19 polluted water, and capacity to provide tests for the populace and detection of the virus in waterways. The most vulnerable population will be badly hit if none of the above measures are put in place.
6. Management and mitigation strategies
The sustainable management of viral contaminated water in developing countries is paramount in preventing environmental degradation and reducing human infection (Lim et al., 2015). In this section, the issues around sustainable management in this domain are discussed, and possible mitigation strategies proffered. Improperly conducted waste management and pollution prevention practices can have negative consequences on human health and the environment (Girones et al., 2014). This risk is quite high in developing countries where water quality monitoring is not efficient, and water reuse is done for resource conservation (Toze, 2006).
Even in very low concentrations, the presence of viruses is an indicator of overall poor water quality (Lin and Ganesh, 2013). Viruses in the environment and drinking water treatment plants were previously confirmed (Albinana-Gimenez et al., 2006, Verbyla and Mihelcic, 2015; Ehlers et al., 2005). In the environment, it has been identified in rivers (Phanuwan et al., 2006), source water dams (Chigor et al., 2014), water basins (De Paula et al., 2007) and groundwater (Hunt et al., 2010). These viruses include polyomaviruses (Albinana-Gimenez et al., 2006), adenoviruses (Rames et al., 2016), hepatitis virus (De Paula et al., 2007), acanthamoeba polyphaga mimivirus (Ashbolt, 2015), rotavirus (Sano et al., 2016), enterovirus (Chigor et al., 2014), norovirus (Seitz et al., 2011), pepper mild mottle virus (Kitajima et al., 2018; Haramoto et al., 2013), human picobirnaviruses, torque teno virus (Hamza et al., 2011), poliovirus (Robeck et al., 1962) and caliciviruses (Xagoraraki et al., 2014).
These viruses bear grave consequences on human health in the case of infection. Besides the risk to humans (Masclaux et al., 2013), virus contamination also bears significant cost implications from its mitigation (Adelman et al., 1998). For the conventional treatment of polluted water by treatment plants, virus removal efficiency can be affected by meteorological and physicochemical factors (Carducci and Verani, 2013). This suggests that more intricate and integrated processes are needed to treat virus-contaminated water to achieve sustainable management. Processes generally used for the mitigation of viral pollution in water is membrane processes (Antony et al., 2012; Madaeni et al., 1995), reverse osmosis (Pype et al., 2016), activated sludge (Sano et al., 2016) and chlorination (Yang et al., 2011).
Researchers have investigated a variety of novel techniques for the mitigation of virus contamination of water in recent times. Asami et al. (2016) compared coagulation-sedimentation and rapid sand filtration to mitigate the spread of pepper mild mottle virus and JC polyomavirus through water. Coagulation-sedimentation was observed to be less efficient for pepper mild mottle virus in comparison to JC polyomavirus. The study furthermore observed that the reverse was the case for rapid sand filtration. Chlorination is effective for the mitigation of noroviruses, rotaviruses, and hepatitis E virus contamination of water (El-Senousy et al., 2014a, 2014b; Nasser, 1994). At a 4 mg/L dosage of chlorine, Log 10 reduction value of ≥6 was achieved for all three viruses. Positive results have also been achieved using a similar process, albeit for adenovirus (Girones et al., 2014). Cold atmospheric-pressure plasma (in argon) mixed with air and plasma-activated water have also been evaluated as potential techniques for the mitigation of viral contamination of water (Guo et al., 2018). The key focus of Guo et al. (2018) investigation was to elucidate how singlet oxygen inactivated the bacteriophages T4, ɸ174, and MS2 by damaging their nucleic acid.
The mechanism of virus inactivation by the iron electro-coagulation process has been recently investigated (Heffron et al., 2019a). For adenovirus, echovirus, and feline calicivirus and bacteriophage surrogates, coagulation is quite efficient in de-contaminating the water. However, the performance of ferrous ions in deactivating the virus was observed to depend on the electrostatic interactions between the ions and the viruses (Heffron et al., 2019a). These, in turn, are controlled by the solution chemistry of the process. Having established the suitability of electro-coagulation, it has also been shown that adding a secondary electro-oxidation stage does not give a significant performance advantage, especially in light of the added costs (Heffron et al., 2019b). A hybrid process of ozonation, coagulation, and ceramic membrane separation has been shown to reduce bacteriophage MS2 in water effectively (Im et al., 2018). The utilization of ozonation in the process was observed to reduce both reversible and irreversible fouling of the experimental apparatus, which enhanced overall performance. However, this came at the cost of a slight reduction in the coagulation of MS2, especially at high ozone input.
These are but a few of the studies considered in recent times. Table 2 presents a more detailed catalog of mitigation strategies for virus contamination of water conducted in recent times alongside the key findings. Most studies implement a hybrid technique where two or more processes are integrated to improve performance and efficiency. Besides those already discussed, other recent mitigation techniques studied for virus decontamination include ceramic water filter (Farrow et al., 2014; Van der Laan et al., 2014), coagulation – microfiltration (Matsushita et al., 2013a; Zhu et al., 2005) and solar and UV irradiation (Mayer et al., 2015; Polo et al., 2015). Furthermore, it is also observed that the most common target species investigated in recent times was Bacteriophage MS2. Most of these studies indicated positive findings for virus removal. This bodes well for the general environmental sustainability effort and affords more options for tackling the problem.
Table 2.
Summary of mitigation strategies for virus contamination of water.
| Process | Target viruses | Key findings | Reference |
|---|---|---|---|
| Coagulation-sedimentation | Pepper mild mottle virus and JC polyomavirus | The process was able to achieve a Log 10 reduction value of 0.41 and 1.91 for Pepper mild mottle virus and JC polyomavirus (wet season). | Asami et al. (2016) |
| Rapid sand filtration | Pepper mild mottle virus and JC polyomavirus | The process was able to achieve a Log 10 reduction value of 1.26 and 0.49 for Pepper mild mottle virus and JC polyomavirus (wet season). | Asami et al. (2016) |
| Chlorination | Noroviruses, rotaviruses and hepatitis E virus | At a 4 mg/L dosage of chlorine, Log 10 reduction value of ≥6 was achieved for all three viruses. | El-Senousy et al. (2014a, 2014b) |
| Ceramic water filter | Enteric virus | Though the process was efficient, increasing the turbidity of the influent water using bentonite helped to improve the viral decontamination efficiency. | Farrow et al. (2014) |
| Chlorination | Hepatitis E virus and human adenovirus 2 | A Log reduction of value of 0.41 was achieved. | Girones et al. (2014) |
| Cold atmospheric-pressure plasma and plasma-activated water | Bacteriophages T4, ɸ174 and MS2 | The mechanism of virus deactivation was a singlet oxygen attack on the nucleic acid and other proteins. | Guo et al. (2018) |
| Iron electrocoagulation | Adenovirus, echovirus, and feline calicivirus and bacteriophage surrogates (Fr, MS2, P22 and ɸ174) | The viruses were effectively removed by the physical coagulation process but less susceptible to iron inactivation. | Heffron et al. (2019a) |
| Sequential electrocoagulation-electrooxidation by boron-doped diamond electrodes | Bacteriophages ɸ174 and MS2 | The results were not that positive as the sequential process alone did not give any major advantage in comparison with using the only electrocoagulation. | Heffron et al. (2019b) |
| Combined ozonation, coagulation and ceramic membrane | Bacteriophage MS2 | Introducing ozonation to the process improves the performance of the process. | Im et al. (2018) |
| Ceramic pot filter with silver | Bacteriophage MS2 | Pot characteristics were observed not to affect the virus decontamination process nor the contact time in the filtration phase. The important effect of silver came at contact time with silver during storage. | Van der Laan et al. (2014) |
| Silver-doped titanium oxide photocatalytic degradation | Bacteriophage MS2 | The higher silver content in the photocatalytic adsorbent improved the inactivation efficiency of the virus. | Liga et al. (2011) |
| Silica-modified titanium oxide photocatalytic degradation | Bacteriophage MS2 | Modification improved viral deactivation by about 270%. | Liga et al. (2013) |
| Micro-filtration membrane | Foot-and-mouth disease (type O) and Infectious bovine respiratory disease | The fuzzy inference system was successfully used to model the experimental data to predict virus removal based on operational parameters. | Madaeni and Kurdian (2011) |
| Aluminum-based coagulation | Bacteriophages T4, Qβ and MS2 | The viruses were effectively decontaminated due to interactions with the coagulant. | Matsushita et al. (2011) |
| Adsorption by super-powdered activated carbon | Bacteriophages Qβ and MS2 | In contrast with the ordinary activated carbon (AC), the super-powdered AC was more effective in virus removal due to its higher hydrophobicity, the greater portion of nano-pores and lesser electrophoretic repulsion. | Matsushita et al. (2013b) |
| Microfiltration | Norovirus | It was unsuitable for virus removal (pore size 0.1 μm). | Matsushita et al. (2013a) |
| Ultrafiltration | Norovirus | The process was able to achieve a virus reduction value in the Log 4 region. | Matsushita et al. (2013a) |
| Hybrid pre-coagulation – microfiltration process | Norovirus | A first-stage coagulation process helped to improve the efficiency of the microfiltration. | Matsushita et al. (2013a) |
| Ultraviolet (UV) irradiation | Adenovirus, feline calicivirus, coxsackievirus, echovirus, poliovirus and bacteriophage | The process was more efficient in the decontamination of adenoviruses than for the others. | Mayer et al. (2015) |
| Titanium oxide photocatalytic degradation | Adenovirus, feline calicivirus, coxsackievirus, echovirus, poliovirus and bacteriophage | The process was more efficient in the decontamination of bacteriophages than for the others. | Mayer et al. (2015) |
| Ferric chloride coagulation | Adenovirus, feline calicivirus, coxsackievirus, echovirus, poliovirus and bacteriophage | The process was more efficient in the decontamination of coxsackievirus, bacteriophage MS2 and adenovirus than for the others. | Mayer et al. (2015) |
| Nano-filtration by carbon nanotubes | Bacteriophage MS2 | At an 8–11 bar pressure, virus removal was effectively achieved. | Mostafavi et al. (2009) |
| Solar water disinfection | Hepatitis A virus, norovirus surrogate and murine norovirus | UV from solar irradiation was effective for virus inactivation albeit to a greater extent than the temperature of the process. | Polo et al. (2015) |
| Polysulfone membrane coated with magnetite | Bacteriophage MS2 | Coating with magnetite improves treatment performance up to 99.99% in the Log 4 region. | Raciny et al. (2011) |
| Advanced bardenpho as a secondary treatment in a water plant | Pepper mild mottle virus, Aichi virus, noroviruses, enterovirus, sapovirus, rotavirus, adenovirus and polyomaviruses | When the advanced bardenpho was used as a secondary treatment in a water treatment plant, most pathogenic viruses were removed and it compared better to the conventional process. | Schmitz et al. (2016) |
| Activated carbon modified with silver and copper oxide nanoparticles | Bacteriophage T4 | The modified porous media was able to achieve virus reduction in the region of Log 3. | Shimabuku et al. (2017) |
| Iron electrocoagulation – microfiltration | Bacteriophage MS2 | The primary mechanism was by sweep flocculation which was assisted by charge neutralization. | Tanneru and Chellam (2012) |
| Nano-Titanium oxide membrane adsorption | Bacteriophage F2 | PAN (0.05 μm) membrane had higher removal efficiency than PVDF (0.20 μm) membrane. | Zheng et al. (2013) |
| Photocatalytic membrane separation process | Bacteriophage F2 | At an optimum condition of 40 L/(m2h) intermittent suction mode, virus removal of over 5 log was achieved in 24 h. | Zheng et al. (2015) |
| Iron coagulation – microfiltration | Bacteriophage MS2 | The process was able to achieve over 4-log virus removal at optimum conditions. | Zhu et al. (2005) |
Based on the discussions in this section, several recommendations are herein presented in light of the need for the mitigation of viral contamination of water sources in developing countries. Most of the studies have implemented hybrid processes using a combination of two or more techniques for virus mitigation. Such techniques can be employed in treatment at the plant scale. These are only relevant to larger cities where such treatment plants are in place. Though studies have shown that the utilization of silver in the virus de-contamination of water is of advantage like for photocatalytic degradation (Liga et al., 2011), adsorption column (Shimabuku et al., 2017) and ceramic pot filtration (Van der Laan et al., 2014), these would be rather expensive solutions for developing countries especially when implementation is on a large scale.
There are other quite simple technologies for virus decontamination like the ceramic water filter (Farrow et al., 2014; Van der Laan et al., 2014) shown in Fig. 3 . The ceramic water filter shown in Fig. 3 Was used in the removal of human enteric viruses from water (using MS2 ad a surrogate phage). The device was able to achieve optimum removal efficiency values of 1.5–2.5 log using 100 NTU turbid influent water and no cleaning between trials. Though the process was efficient, increasing the turbidity of the influent water using bentonite helped to improve the viral decontamination efficiency. This specific system is elaborated due to its simplicity, ease-of-use, low-cost and usability even in rural areas. Such simple techniques can be re-designed and improved for domestic and local applications in developing countries (albeit at low cost). Putting all these into consideration, the onus is on the government agencies to develop regulations for the water co-operations to ensure the viral decontamination of water being processed for commercial use. Furthermore, entrepreneurial insight is needed to develop low-cost technologies for virus decontamination that would be amenable to remote and rural locations in developing countries.
Fig. 3.
Schematic of a ceramic water filter (Farrow et al., 2014).
7. Future scope and recommended policies
In line with the observations of this review, interesting areas of work are hereby discussed that could form the foundations of novel investigations. As observed by Ighalo and Adeniyi (2020), water quality monitoring and assessment in developing countries have been more focused on the conventional physico-chemical parameters. There is a need for future studies to direct their efforts towards the analysis of viral contamination too. In light of these, policy adjustments would also be needed to develop guideline limits of viral contamination in water sources. The COVID-19 pandemic has changed so many areas in contemporary societies and important adjustments will need to be made in line with the prevailing peculiarities. IoT-enables systems will also be an interesting technology for water monitoring systems and mitigation technologies. These are fast, reliable and can produce results in real-time. In the area of mitigation, entrepreneurial insight is needed to develop low-cost technologies for virus decontamination that would be amenable to remote and rural locations in developing countries. The following specific recommendation policies are therefore proposed.
-
i.
The regulatory guidelines for pathogen removal in water for various reuse calls for thorough evaluation for stricter requirements with the recent detection of the SARS-CoV-2 in wastewater.
-
ii.
In water distribution systems, appropriate chlorine residual should be applied in the piping system to decontaminate any viruses that can easily recolonize or provide protection from entry of pollution to the pipes during the process of unintended cross-connection between non-potable and potable lines.
-
iii.
A comprehensive understanding of the efficiency of evolving disinfection treatment techniques (Ozonation, activated carbon, UV based advanced oxidation processes) for virus and other pathogenic organisms deactivation specifically procedural steps that are incorporated into safe water reuse is a vital research necessity.
-
iv.
The development of new or improved existing water and wastewater treatment facilities for critical areas that receives coronavirus from hospitals, isolation centers, clinics and swine pen should be the focal point of all researchers.
-
v.
At the point of use, specifically for drinking purpose in homes, handy disinfection devices should be provided to reduce the waterborne viral diseases and secondary transmission
-
vi.
Detailed appraisal and usage of new and promising sustainable methodologies for viral and other pathogenic/infectious disease surveillance.
-
vii.
An enhanced understanding of the fate and behavior of these viruses in water environment will pave way for routine implementation for water quality monitoring and for viral risk evaluation. There is therefore, a need for the synergy between the public health experts, scientists (Chemists, virologist, and Microbiologist), engineers to team up and proffer pragmatic solutions for potable water and healthy environs to address this issue of virus and other pathogen contamination in water especially developing a simple operating process for the detection of viruses in water.
8. Conclusion
In this review, socioeconomic inequality based on virus-contaminated water usage in developing countries was assessed and discussed. Possible mitigation strategies were proffered based on the existing literature that can be adopted for the developing countries, especially those characterized by low level social and economic development. The recent global COVID-19 pandemic has changed the paradigm by reawakening the importance of water quality and sanitation and focusing more attention on the deleterious effect of contaminated water. As discussed in the review, the socioeconomic factors attributed to the various waterborne diseases due to the use of virus-contaminated water in many developing countries are poverty, the standard of living, access to health care facilities, age, gender, and level of education. Some mitigation strategies to address the viral contamination of water sources are therefore proposed, while future scope and recommendations on tackling the essential issues related to socioeconomic inequality in developing nations are highlighted.
Credit author statement
Bashir Adelodun: Conceptualization, Investigation, Visualization, Writing –Original draft, Writing – Reviewing and Editing. Fidelis Odedishemi Ajibade: Investigation, Visualization, Writing –Original draft, Writing – Reviewing and Editing. Joshua O. Ighalo Investigation, Visualization, Writing –Original draft, Writing – Reviewing and Editing. Golden Odey: Investigation, Visualization, Writing –Original draft, Writing – Reviewing and Editing. Rahmat Gbemisola Ibrahim: Investigation, Visualization, Writing – Reviewing and Editing. Kola Yusuff Kareem: Investigation, Visualization, Writing –Original draft, Writing – Reviewing and Editing. Hashim Olalekan Bakare: Investigation, Visualization, Writing – Reviewing and Editing. AbdulGafar Olatunji Tiamiyu: Investigation, Visualization, Writing –Original draft, Writing – Reviewing and Editing. Temitope F. Ajibade: Investigation, Visualization, Writing – Reviewing and Editing. Taofeeq Sholagberu Abdulkadir: Investigation, Visualization, Writing – Reviewing and Editing. Kamoru Akanni Adeniran: Investigation, Visualization, Writing – Reviewing and Editing. Kyung Sook Choi: Visualization, Resources, Supervision, Project administration.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgments
We gratefully acknowledge the assistance of Pankaj Kumar of Agro-ecology and Pollution Research Laboratory, Department of Zoology and Environmental Science, Gurukula Kangri Vishwavidyalaya, Haridwar-249404 (Uttarakhand), India, who thoroughly read the manuscript and offered brilliant suggestions to improve the manuscript.
References
- Adelman D.D., Stansbury J., Tabidian M.A. A risk/cost analysis to manage viral contamination of groundwater. Water Sci. Technol. 1998;38:1–6. doi: 10.2166/wst.1998.0485. [DOI] [Google Scholar]
- Adelodun B., Ajibade F.O., Ibrahim R.G., Bakare H.O., Choi K.-S. Snowballing transmission of COVID-19 (SARS-CoV-2) through wastewater: any sustainable preventive measures to curtail the scourge in low-income countries? Sci. Total Environ. 2020;742:108334. doi: 10.1016/j.scitotenv.2020.140680. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Adelodun B., Ajibade F.O., Ogunshina M.S., Choi K.-S. Dosage and settling time course optimization of Moringa oleifera in municipal wastewater treatment using response surface methodology. Desalin. Water Treat. 2019;167:45–56. doi: 10.5004/dwt.2019.24616. [DOI] [Google Scholar]
- Adelodun B., Ogunshina M.S., Ajibade F.O., Abdulkadir T.S., Bakare H.O., Choi K.S. Kinetic and prediction modeling studies of organic pollutants removal from municipal wastewater using moringa oleifera biomass as a coagulant. Water. 2020;12:1–14. doi: 10.3390/w12072052. [DOI] [Google Scholar]
- Ahmed W., Angel N., Edson J., Bibby K., Bivins A., O'Brien J.W., Choi P.M., Kitajima M., Simpson S.L., Li J., Tscharke B., Verhagen R., Smith W.J.M., Zaugg J., Dierens L., Hugenholtz P., Thomas K.V., Mueller J.F. First confirmed detection of SARS-CoV-2 in untreated wastewater in Australia: a proof of concept for the wastewater surveillance of COVID-19 in the community. Sci. Total Environ. 2020;728:138764. doi: 10.1016/j.scitotenv.2020.138764. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ajibade F.O., Adelodun B., Lasisi K.H., Fadare O.O., Ajibade T.F., Nwogwu N.A., Sulaymon I.D., Ugya A.Y., Wang H.C., Wang A. In: Microbe Mediated Remediation of Environmental Contaminants. Kumar A., Singh V.K., Singh P., Mishra V.K., editors. Woodhead Publishing, Elsevier; 2020. Environmental pollution and their socioeconomic impacts. [DOI] [Google Scholar]
- Akoteyon I.S. Inequalities in access to water and sanitation in rural settlements in parts of southwest Nigeria. Ghana J. Geogr. 2019;11:158–184. [Google Scholar]
- Albinana-Gimenez N., Clemente-Casares P., Bofill-Mas S., Hundesa A., Ribas F., Girones R. Distribution of human polyomaviruses, adenoviruses, and hepatitis E virus in the environment and in a drinking-water treatment plant. Environ. Sci. Technol. 2006;40:7416–7422. doi: 10.1021/es060343i. [DOI] [PubMed] [Google Scholar]
- Alian S., Ajami A., Ghasemian R., Yadegarinia D. Age-specific seroprevalence of hepatitis A in Sari, northern Islamic Republic of Iran. East. Mediterr. Health J. 2011;17:754–758. doi: 10.26719/2011.17.10.754. [DOI] [PubMed] [Google Scholar]
- Anlimachie M.A., Avoada C. Socio-economic impact of closing the rural-urban gap in pre-tertiary education in Ghana: context and strategies. Int. J. Educ. Dev. 2020;77:102236. doi: 10.1016/j.ijedudev.2020.102236. [DOI] [Google Scholar]
- Antony A., Blackbeard J., Leslie G. Removal efficiency and integrity monitoring techniques for virus removal by membrane processes. Crit. Rev. Environ. Sci. Technol. 2012;42:891–933. doi: 10.1080/10643389.2011.556539. [DOI] [Google Scholar]
- Arora D., Jindal N., Shukla R.K., Bansal R. Water borne hepatitis A and hepatitis E in malwa region of Punjab, India. J. Clin. Diagn. Res. 2013;7:2163–2166. doi: 10.7860/JCDR/2013/5966.3459. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arslan M., Xu B., Gamal El-Din M. Transmission of SARS-CoV-2 via fecal-oral and aerosols–borne routes: environmental dynamics and implications for wastewater management in underprivileged societies. Sci. Total Environ. 2020;743:140709. doi: 10.1016/j.scitotenv.2020.140709. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Arslan M., Xu B., Gamal El-Din M. Transmission of SARS-CoV-2 via fecal-oral and aerosols–borne routes: environmental dynamics and implications for wastewater management in underprivileged societies. Sci. Total Environ. 2020;743:140709. doi: 10.1016/j.scitotenv.2020.140709. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Asami T., Katayama H., Torrey J.R., Visvanathan C., Furumai H. Evaluation of virus removal efficiency of coagulation-sedimentation and rapid sand filtration processes in a drinking water treatment plant in Bangkok, Thailand. Water Res. 2016;101:84–94. doi: 10.1016/j.watres.2016.05.012. [DOI] [PubMed] [Google Scholar]
- Ashbolt N.J. Microbial contamination of drinking water and human health from community water systems. Curr. Environ. Heal. reports. 2015;2:95–106. doi: 10.1007/s40572-014-0037-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Awoke A., Beyene A., Kloos H., Goethals P.L.M., Triest L. river water pollution status and water policy scenario in Ethiopia: raising awareness for better implementation in developing countries. Environ. Manag. 2016;58:694–706. doi: 10.1007/s00267-016-0734-y. [DOI] [PubMed] [Google Scholar]
- Beltran V.M., Harrison K.M.D., Irene Hall H., Dean H.D. Collection of social determinant of health measures in U.S. national surveillance systems for HIV, viral hepatitis, STDs, and TB. Publ. Health Rep. 2011;126:41–53. doi: 10.1177/00333549111260s309. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Beyene A., Kassahun Y., Addis T., Assefa F., Amsalu A., Legesse W., Kloos H., Triest L. The impact of traditional coffee processing on river water quality in Ethiopia and the urgency of adopting sound environmental practices. Environ. Monit. Assess. 2012;184:7053–7063. doi: 10.1007/s10661-011-2479-7. [DOI] [PubMed] [Google Scholar]
- Bibby K. Metagenomic identification of viral pathogens. Trends Biotechnol. 2013;31:275–279. doi: 10.1016/j.tibtech.2013.01.016. [DOI] [PubMed] [Google Scholar]
- Blaise H.N.Y., Dovie D.B.K. Diarrheal diseases in the history of public health. Arch. Med. Res. 2007;38:159–163. doi: 10.1016/j.arcmed.2006.11.001. [DOI] [PubMed] [Google Scholar]
- Bofill-Mas S., Rodriguez-Manzano J., Calgua B., Carratala A., Girones R. Newly described human polyomaviruses Merkel Cell, KI and Wu are present in urban sewage and may represent potential environmental contaminants. Virol. J. 2010;7:1–5. doi: 10.1186/1743-422X-7-141. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bonadonna L., La Rosa G. A review and update on waterborne viral diseases associated with swimming pools. Int. J. Environ. Res. Publ. Health. 2019;16:1–11. doi: 10.3390/ijerph16020166. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bosch A., Guix S., Sano D., Pintó R.M. New tools for the study and direct surveillance of viral pathogens in water. Curr. Opin. Biotechnol. 2008;19:295–301. doi: 10.1016/j.copbio.2008.04.006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bougnom B.P., Zongo C., McNally A., Ricci V., Etoa F.X., Thiele-Bruhn S., Piddock L.J.V. Wastewater used for urban agriculture in West Africa as a reservoir for antibacterial resistance dissemination. Environ. Res. 2019;168:14–24. doi: 10.1016/j.envres.2018.09.022. [DOI] [PubMed] [Google Scholar]
- Broo A.E., Berghult B., Hedberg T. Pipe material selection in drinking water systems - a conference summary. Water Sci. Technol. Water Supply. 2001;1:117–125. doi: 10.2166/ws.2001.0059. [DOI] [Google Scholar]
- Cannon M.J., Hyde T.B., Schmid D.S. Review of cytomegalovirus shedding in bodily fluids and relevance to congenital cytomegalovirus infection. Rev. Med. Virol. 2011;21:240–255. doi: 10.1002/rmv.695. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carducci A., Federigi I., Liu D., Thompson J.R., Verani M. Making waves: coronavirus detection, presence and persistence in the water environment: state of the art and knowledge needs for public health. Water Res. 2020;179:115907. doi: 10.1016/j.watres.2020.115907. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Carducci A., Verani M. Effects of bacterial, chemical, physical and meteorological variables on virus removal by a wastewater treatment plant. Food Environ. Virol. 2013;5:69–76. doi: 10.1007/s12560-013-9105-5. [DOI] [PubMed] [Google Scholar]
- Célia da Silva Lanna M., Viancelli A., Michelon W., Castro Carvalho S.V., de Almeida dos Reis D., Fernandez de Salles L.A., Sant'Anna I.H., Resende L.T., de Souza Ferreira C., Aparecido das Chagas I., Hernández M., Treichel H., Rodríguez-Lázaro D., Fongaro G. Household-based biodigesters promote reduction of enteric virus and bacteria in vulnerable and poverty rural area. Environ. Pollut. 2019;252:8–13. doi: 10.1016/j.envpol.2019.05.104. [DOI] [PubMed] [Google Scholar]
- Cheng A.C., McDonald J.R., Thielman N.M. Infectious diarrhea in developed and developing countries. J. Clin. Gastroenterol. 2005;39:757–773. doi: 10.1097/01.mcg.0000177231.13770.07. [DOI] [PubMed] [Google Scholar]
- Chigor V.N., Sibanda T., Okoh A.I. Assessment of the risks for human health of adenoviruses, hepatitis A virus, rotaviruses and enteroviruses in the buffalo river and three source water dams in the eastern cape. Food Environ. Virol. 2014;6:87–98. doi: 10.1007/s12560-014-9138-4. [DOI] [PubMed] [Google Scholar]
- De Paula V.S., Diniz-Mendes L., Villar L.M., Luz S.L.B., Silva L.A., Jesus M.S., da Silva N.M.V.S., Gaspar A.M.C. Hepatitis A virus in environmental water samples from the Amazon Basin. Water Res. 2007;41:1169–1176. doi: 10.1016/j.watres.2006.11.029. [DOI] [PubMed] [Google Scholar]
- Di Profio F., Melegari I., Palombieri A., Sarchese V., Arbuatti A., Fruci P., Marsilio F., Martella V., Di Martino B. High prevalence of hepatitis E virus in raw sewage in Southern Italy. Virus Res. 2019;272 doi: 10.1016/j.virusres.2019.197710. [DOI] [PubMed] [Google Scholar]
- Dickin S.K., Schuster-Wallace C.J. Assessing changing vulnerability to dengue in northeastern Brazil using a water-associated disease index approach. Global Environ. Change. 2014;29:155–164. doi: 10.1016/j.gloenvcha.2014.09.007. [DOI] [Google Scholar]
- Ehlers M.M., Grabow W.O.K., Pavlov D.N. Detection of enteroviruses in untreated and treated drinking water supplies in South Africa. Water Res. 2005;39:2253–2258. doi: 10.1016/j.watres.2005.04.014. [DOI] [PubMed] [Google Scholar]
- El-Senousy M.W., El-Gamal M.S., Mousa A.A.E.-B., El-Hawary S.E.-S., Kamel M.M., Fathi M.N., El-Mahdy E.-M.M. Effect of chlorine on noroviruses, rotaviruses and hepatitis E virus in drinking water. World Appl. Sci. J. 2014;32:2206–2212. doi: 10.5829/idosi.wasj.2014.32.11.91114. [DOI] [Google Scholar]
- El-Senousy W.M., Osman G.A., Melegy A.A. Survival of adenovirus, rotavirus, Hepatitis A virus, pathogenic bacteria and bacterial indicators in ground water. World Appl. Sci. J. 2014;29:337–348. doi: 10.5829/idosi.wasj.2014.29.03.13849. [DOI] [Google Scholar]
- El Zanfaly H.T. Water quality and health in Egyptian rural areas. J. Environ. Prot. Sustain. Dev. 2015;1:203–210. [Google Scholar]
- Farrow C., McBean E., Salsali H. Virus removal efficiency of ceramic water filters: effects of bentonite turbidity. Water Sci. Technol. Water Supply. 2014;14:304–311. doi: 10.2166/ws.2013.206. [DOI] [Google Scholar]
- Flint S., Enquist L., Racaniello V., Skalka A. Principles of Virology. 2004. Molecular biology, pathogenesis, and control of animal viruses. [Google Scholar]
- Gall A.M., Mariñas B.J., Lu Y., Shisler J.L. Waterborne viruses: a barrier to safe drinking water. PLoS Pathog. 2015;11:1–7. doi: 10.1371/journal.ppat.1004867. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gallego-Schmid A., Tarpani R.R.Z. Life cycle assessment of wastewater treatment in developing countries: a review. Water Res. 2019 doi: 10.1016/j.watres.2019.01.010. [DOI] [PubMed] [Google Scholar]
- Ganesh A., Lin J., Singh M. Detecting virus-like particles from the Umgeni River, South Africa. Clean. 2014;42:393–407. doi: 10.1002/clen.201200564. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gasana J., Morin J., Ndikuyeze A., Kamoso P. Impact of water supply and sanitation on diarrheal morbidity among young children in the socioeconomic and cultural context of Rwanda (Africa) Environ. Res. 2002;90:76–88. doi: 10.1006/enrs.2002.4394. [DOI] [PubMed] [Google Scholar]
- Gbemiga F., Deborah O. In: The Relevance of Hygiene to Health in Developing Countries. Potgieter N., Hoffman A.N.T., editors. 2019. Inequalities in households' environmental sanitation practices in a developing nation's city: the example of ile-ife, Nigeria; p. 13. [DOI] [Google Scholar]
- Gerba C.P. Applied and theoretical aspects of virus adsorption to surfaces. Adv. Appl. Microbiol. 1984 doi: 10.1016/S0065-2164(08)70054-6. [DOI] [PubMed] [Google Scholar]
- Gerba C.P., Betancourt W.Q., Kitajima M., Rock C.M. Reducing uncertainty in estimating virus reduction by advanced water treatment processes. Water Res. 2018;133:282–288. doi: 10.1016/j.watres.2018.01.044. [DOI] [PubMed] [Google Scholar]
- Ghernaout D. Water treatment challenges towards viruses removal. OALib. 2020;7:1–22. doi: 10.4236/oalib.1106408. [DOI] [Google Scholar]
- Girones R., Carratalà A., Calgua B., Calvo M., Rodriguez-Manzano J., Emerson S. Chlorine inactivation of hepatitis e virus and human adenovirus 2 in water. J. Water Health. 2014;12:436–442. doi: 10.2166/wh.2014.027. [DOI] [PubMed] [Google Scholar]
- Gleick P.H. 2002. Dirty-water: Estimated Deaths from Water-Related Diseases 2000-2020. [Google Scholar]
- Gomez M., Perdiguero J., Sanz àlex. Socioeconomic factors affecting water access in rural areas of low and middle income countries. Water. 2019;11 doi: 10.3390/w11020202. [DOI] [Google Scholar]
- Guenifi W., Laouamri S., Lacheheb A. Changes in prevalence of hepatitis A and associated factors in Setif-Algeria. Rev. Epidemiol. Sante Publique. 2017;65:437–442. doi: 10.1016/j.respe.2017.05.009. [DOI] [PubMed] [Google Scholar]
- Guerrero-Latorre L., Ballesteros I., Villacrés-Granda I., Granda M.G., Freire-Paspuel B., Ríos-Touma B. SARS-CoV-2 in river water: implications in low sanitation countries. Sci. Total Environ. 2020;743:140832. doi: 10.1016/j.scitotenv.2020.140832. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Guo L., Xu R., Gou L., Liu Z., Zhao Y., Liu D., Zhang L., Chen H., Kong M.G. Mechanism of virus inactivation by cold atmospheric-pressure plasma and plasma-activated water. Appl. Environ. Microbiol. 2018;84 doi: 10.1128/AEM.00726-18. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hamza I.A., Jurzik L., Überla K., Wilhelm M. Evaluation of pepper mild mottle virus, human picobirnavirus and Torque teno virus as indicators of fecal contamination in river water. Water Res. 2011;45:1358–1368. doi: 10.1016/j.watres.2010.10.021. [DOI] [PubMed] [Google Scholar]
- Haramoto E., Kitajima M., Kishida N., Konno Y., Katayama H., Asami M., Akiba M. Occurrence of pepper mild mottle virus in drinking water sources in Japan. Appl. Environ. Microbiol. 2013;79:7413–7418. doi: 10.1128/AEM.02354-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Haramoto E., Malla B., Thakali O., Kitajima M. First environmental surveillance for the presence of SARS-CoV-2 RNA in wastewater and river water in Japan. Sci. Total Environ. 2020;737:140405. doi: 10.1016/j.scitotenv.2020.140405. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hau C.H., Hien T.T., Tien N.T.K., Khiem H.B., Sac P.K., Nhung V.T., Larasati R.P., Laras K., Putri M.P., Doss R., Hyams K.C., Corwin A.L. Prevalence of enteric hepatitis A and E viruses in the Mekong River delta region of Vietnam. Am. J. Trop. Med. Hyg. 1999;60:277–280. doi: 10.4269/ajtmh.1999.60.277. [DOI] [PubMed] [Google Scholar]
- Heffron J., McDermid B., Maher E., McNamara P.J., Mayer B.K. Mechanisms of virus mitigation and suitability of bacteriophages as surrogates in drinking water treatment by iron electrocoagulation. Water Res. 2019;163:114877. doi: 10.1016/j.watres.2019.114877. [DOI] [PubMed] [Google Scholar]
- Heffron J., Ryan D.R., Mayer B.K. Sequential electrocoagulation-electrooxidation for virus mitigation in drinking water. Water Res. 2019;160:435–444. doi: 10.1016/j.watres.2019.05.078. [DOI] [PubMed] [Google Scholar]
- Hughes C., Naik V.S., Sengupta R., Saxena D. Proceedings of the 3rd ACM SIGSPATIAL International Workshop on the Use of GIS in Public Health, HealthGIS 2014 - in Conjuncture with the 22nd ACM SIGSPATIAL International Conference on Advances in Geographic Information Systems, ACM GIS 2014. 2014. Geovisualization for cluster detection of Hepatitis A & E outbreaks in Ahmedabad, Gujarat, India. [DOI] [Google Scholar]
- Hunt R.J., Borchardt M.A., Richards K.D., Spencer S.K. Assessment of sewer source contamination of drinking water wells using tracers and human enteric viruses. Environ. Sci. Technol. 2010;44:7956–7963. doi: 10.1021/es100698m. [DOI] [PubMed] [Google Scholar]
- Ighalo J.O., Adeniyi A.G. Elsevier Ltd; 2020. A Comprehensive Review of Water Quality Monitoring and Assessment in Nigeria, Chemosphere. [DOI] [PubMed] [Google Scholar]
- Im D., Nakada N., Fukuma Y., Kato Y., Tanaka H. Performance of combined ozonation, coagulation and ceramic membrane process for water reclamation: effects and mechanism of ozonation on virus coagulation. Separ. Purif. Technol. 2018;192:429–434. doi: 10.1016/j.seppur.2017.10.044. [DOI] [Google Scholar]
- Karn S.K., Harada H. Surface water pollution in three urban territories of Nepal, India, and Bangladesh. Environ. Manag. 2001;28:483–496. doi: 10.1007/s002670010238. [DOI] [PubMed] [Google Scholar]
- Katiyatiya L.M. Part a: socio-economic inequality in South Africa and the continual plight for social protection in the future world of work. J. Poverty. 2020;24:203–221. doi: 10.1080/10875549.2019.1678552. [DOI] [Google Scholar]
- Kher J., Aggarwal S., Punhani G. Vulnerability of poor urban women to climate-linked water insecurities at the household level: a case study of slums in Delhi. Indian J. Gend. Stud. 2015;22:15–40. doi: 10.1177/0971521514556943. [DOI] [Google Scholar]
- Kitajima M., Iker B.C., Pepper I.L., Gerba C.P. Relative abundance and treatment reduction of viruses during wastewater treatment processes - identification of potential viral indicators. Sci. Total Environ. 2014;488–489:290–296. doi: 10.1016/j.scitotenv.2014.04.087. [DOI] [PubMed] [Google Scholar]
- Kitajima M., Sassi H.P., Torrey J.R. 2018. Pepper Mild Mottle Virus as a Water Quality Indicator. Npj Clean Water 1. [DOI] [Google Scholar]
- Kiulia N.M., Netshikweta R., Page N.A., Van Zyl W.B., Kiraithe M.M., Nyachieo A., Mwenda J.M., Taylor M.B. The detection of enteric viruses in selected urban and rural river water and sewage in Kenya, with special reference to rotaviruses. J. Appl. Microbiol. 2010;109:818–828. doi: 10.1111/j.1365-2672.2010.04710.x. [DOI] [PubMed] [Google Scholar]
- Kunasol P., Cooksley G., Chan V.F., Isahak I., John J., Loleka S., Villar E.P., Poovorawan Y., Seong N.H., Sulaiman H.A., Wah L.B. Hepatitis A virus: declining seroprevalence in children and adolescents in Southeast Asia. Southeast Asian J. Trop. Med. Publ. Health. 1998 [PubMed] [Google Scholar]
- La Rosa G., Mancini P., Bonanno Ferraro G., Veneri C., Iaconelli M., Bonadonna L., Lucentini L., Suffredini E. SARS-CoV-2 has been circulating in northern Italy since December 2019: evidence from environmental monitoring. Sci. Total Environ. 2021;750:141711. doi: 10.1016/j.scitotenv.2020.141711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liga M.V., Bryant E.L., Colvin V.L., Li Q. Virus inactivation by silver doped titanium dioxide nanoparticles for drinking water treatment. Water Res. 2011;45:535–544. doi: 10.1016/j.watres.2010.09.012. [DOI] [PubMed] [Google Scholar]
- Liga M.V., Maguire-Boyle S.J., Jafry H.R., Barron A.R., Li Q. Silica decorated TiO2 for virus inactivation in drinking water -simple synthesis method and mechanisms of enhanced inactivation kinetics. Environ. Sci. Technol. 2013;47:6463–6470. doi: 10.1021/es400196p. [DOI] [PubMed] [Google Scholar]
- Lim K.Y., Hamilton A.J., Jiang S.C. Assessment of public health risk associated with viral contamination in harvested urban stormwater for domestic applications. Sci. Total Environ. 2015;523:95–108. doi: 10.1016/j.scitotenv.2015.03.077. [DOI] [PubMed] [Google Scholar]
- Lin J., Ganesh A. Water quality indicators: bacteria, coliphages, enteric viruses. Int. J. Environ. Health Res. 2013;23:484–506. doi: 10.1080/09603123.2013.769201. [DOI] [PubMed] [Google Scholar]
- Lipus L.C., Dobersek D. Influence of magnetic field on the aragonite precipitation. Chem. Eng. Sci. 2007;62:2089–2095. doi: 10.1016/j.ces.2006.12.051. [DOI] [Google Scholar]
- Liu G., Ling F.Q., Van Der Mark E.J., Zhang X.D., Knezev A., Verberk J.Q.J.C., Van Der Meer W.G.J., Medema G.J., Liu W.T., Van Dijk J.C. Comparison of particle-associated bacteria from a drinking water treatment plant and distribution reservoirs with different water sources. Sci. Rep. 2016;6:1–8. doi: 10.1038/srep20367. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lodder W., de Roda Husman A.M. SARS-CoV-2 in wastewater: potential health risk, but also data source. lancet. Gastroenterol. Hepatol. 2020;1253:30087. doi: 10.1016/S2468-1253(20)30087-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lodder W.J., Schijven J.F., Rutjes S.A., de Roda Husman A.M., Teunis P.F.M. Entero- and parechovirus distributions in surface water and probabilities of exposure to these viruses during water recreation. Water Res. 2015;75:25–32. doi: 10.1016/j.watres.2015.02.024. [DOI] [PubMed] [Google Scholar]
- Madaeni S.S., Fane A.G., Grohmann G.S. Virus removal from water and wastewater using membranes. J. Membr. Sci. 1995;102:65–75. doi: 10.1016/0376-7388(94)00252-T. [DOI] [Google Scholar]
- Madaeni S.S., Kurdian A.R. Fuzzy modeling and hybrid genetic algorithm optimization of virus removal from water using microfiltration membrane. Chem. Eng. Res. Des. 2011;89:456–470. doi: 10.1016/j.cherd.2010.07.009. [DOI] [Google Scholar]
- Makris K.C., Andra S.S., Botsaris G. Pipe scales and biofilms in drinking-water distribution systems: undermining finished water quality. Crit. Rev. Environ. Sci. Technol. 2014;44:1477–1523. doi: 10.1080/10643389.2013.790746. [DOI] [Google Scholar]
- Malik A., Yasar A., Tabinda A.B., Abubakar M. Water-borne diseases, cost of illness and willingness to pay for diseases interventions in rural communities of developing countries. Iran. J. Public Health. 2012;41:39–49. [PMC free article] [PubMed] [Google Scholar]
- Mantovani S.A.S., Delfino B.M., Martins A.C., Oliart-Guzmán H., Pereira T.M., Branco F.L.C.C., Braña A.M., Filgueira-Júnior J.A., Santos A.P., Arruda R.A., Guimarães A.S., Ramalho A.A., Oliveira C.S. de M., Araújo T.S., Arróspide N., Estrada C.H.M.L., Codeço C.T., Da Silva-Nunes M. Socioeconomic inequities and hepatitis A virus infection in Western Brazilian Amazonian children: spatial distribution and associated factors. BMC Infect. Dis. 2015;15:1–12. doi: 10.1186/s12879-015-1164-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mantovani S.A.S., Delfino B.M., Martins A.C., Oliart-Guzmán H., Pereira T.M., Branco F.L.C.C., Braña A.M., Filgueira-Júnior J.A., Santos A.P., Arruda R.A., Guimarães A.S., Ramalho A.A., Oliveira C.S. de M., Araújo T.S., Arróspide N., Estrada C.H.M.L., Codeço C.T., Da Silva-Nunes M. Socioeconomic inequities and hepatitis A virus infection in Western Brazilian Amazonian children: spatial distribution and associated factors. BMC Infect. Dis. 2015;15:1–12. doi: 10.1186/s12879-015-1164-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marie V., Lin J. Viruses in the environment - presence and diversity of bacteriophage and enteric virus populations in the Umhlangane River, Durban, South Africa. J. Water Health. 2017;15:966–981. doi: 10.2166/wh.2017.066. [DOI] [PubMed] [Google Scholar]
- Martins M., Lacerda M.V.G., Monteiro W.M., Moura M.A.S., Santos E.C.S., Saraceni V., Saraiva M.G.G. Progression of the load of waterborne and intestinal parasitic diseases in the state of amazonas. Rev. Soc. Bras. Med. Trop. 2015;48:42–54. doi: 10.1590/0037-8682-0162-2014. [DOI] [PubMed] [Google Scholar]
- Masclaux F.G., Hotz P., Friedli D., Savova-Bianchi D., Oppliger A. High occurrence of hepatitis E virus in samples from wastewater treatment plants in Switzerland and comparison with other enteric viruses. Water Res. 2013;47:5101–5109. doi: 10.1016/j.watres.2013.05.050. [DOI] [PubMed] [Google Scholar]
- Matsushita T., Shirasaki N., Matsui Y., Ohno K. Virus inactivation during coagulation with aluminum coagulants. Chemosphere. 2011;85:571–576. doi: 10.1016/j.chemosphere.2011.06.083. [DOI] [PubMed] [Google Scholar]
- Matsushita T., Shirasaki N., Tatsuki Y., Matsui Y. Investigating norovirus removal by microfiltration, ultrafiltration, and precoagulation-microfiltration processes using recombinant norovirus virus-like particles and real-time immuno-PCR. Water Res. 2013;47:5819–5827. doi: 10.1016/j.watres.2013.07.004. [DOI] [PubMed] [Google Scholar]
- Matsushita T., Suzuki H., Shirasaki N., Matsui Y., Ohno K. Adsorptive virus removal with super-powdered activated carbon. Separ. Purif. Technol. 2013;107:79–84. doi: 10.1016/j.seppur.2013.01.017. [DOI] [Google Scholar]
- Mayer B.K., Yang Y., Gerrity D.W., Abbaszadegan M. The impact of capsid proteins on virus removal and inactivation during water treatment processes. Microbiol. Insights. 2015;8s2 doi: 10.4137/mbi.s31441. MBI.S31441. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McMichael C. Water, sanitation and hygiene (WASH) in schools in low-income countries: a review of evidence of impact. Int. J. Environ. Res. Publ. Health. 2019;16:1–21. doi: 10.3390/ijerph16030359. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Medema G., Heijnen L., Elsinga G., Italiaander R., Brouwer A. Presence of SARS-coronavirus-2 RNA in sewage and correlation with reported COVID-19 prevalence in the early stage of the epidemic in The Netherlands. Environ. Sci. Technol. Lett. 2020 doi: 10.1021/acs.estlett.0c00357. [DOI] [PubMed] [Google Scholar]
- Montgomery M.A., Elimelech M. Water and sanitation in developing countries: including health in the equation - millions suffer from preventable illnesses and die every year. Environ. Sci. Technol. 2007;41:17–24. doi: 10.1021/es072435t. [DOI] [PubMed] [Google Scholar]
- Morales-Novelo J.A., Rodríguez-Tapia L., Revollo-Fernández D.A. Inequality in access to drinkingwater and subsidies between low and high income households in Mexico City. Water. 2018;10:1–16. doi: 10.3390/w10081023. [DOI] [Google Scholar]
- Morrison C.M., Betancourt W.Q., Quintanar D.R., Lopez G.U., Pepper I.L., Gerba C.P. Potential indicators of virus transport and removal during soil aquifer treatment of treated wastewater effluent. Water Res. 2020;177:115812. doi: 10.1016/j.watres.2020.115812. [DOI] [PubMed] [Google Scholar]
- Mostafavi S.T., Mehrnia M.R., Rashidi A.M. Preparation of nanofilter from carbon nanotubes for application in virus removal from water. Desalination. 2009;238:271–280. doi: 10.1016/j.desal.2008.02.018. [DOI] [Google Scholar]
- Mukate S., Wagh V., Panaskar D., Jacobs J.A., Sawant A. Development of new integrated water quality index (IWQI) model to evaluate the drinking suitability of water. Ecol. Indicat. 2019;101:348–354. doi: 10.1016/j.ecolind.2019.01.034. [DOI] [Google Scholar]
- Murphy H.M., Prioleau M.D., Borchardt M.A., Hynds P.D. Review: epidemiological evidence of groundwater contribution to global enteric disease, 1948–201. Hydrogeol. J. 2017;25:981–1001. doi: 10.1007/s10040-017-1543-y. [DOI] [Google Scholar]
- Nasser A. Prevalence and fate of hepatitis A virus in water. Crit. Rev. Environ. Sci. Technol. 1994 doi: 10.1080/10643389409388470. [DOI] [Google Scholar]
- Nhamo G., Nhemachena C., Nhamo S. Is 2030 too soon for Africa to achieve the water and sanitation sustainable development goal? Sci. Total Environ. 2019;669:129–139. doi: 10.1016/j.scitotenv.2019.03.109. [DOI] [PubMed] [Google Scholar]
- O'Brien E., Munir M., Marsh T., Heran M., Lesage G., Tarabara V.V., Xagoraraki I. Diversity of DNA viruses in effluents of membrane bioreactors in traverse city, MI (USA) and La grande motte (France) Water Res. 2017;111:338–345. doi: 10.1016/j.watres.2017.01.014. [DOI] [PubMed] [Google Scholar]
- Okoh A.I., Sibanda T., Gusha S.S. Inadequately treated wastewater as a source of human enteric viruses in the environment. Int. J. Environ. Res. Publ. Health. 2010;7:2620–2637. doi: 10.3390/ijerph7062620. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Olowe B., Oluyege J., Famurewa O. Prevalence of waterborne diseases and microbial assessment of drinking water quality in ado-ekiti and its environs, southwestern, Nigeria. Br. Microbiol. Res. J. 2016;12:1–13. doi: 10.9734/bmrj/2016/22444. [DOI] [Google Scholar]
- Opere W.M., John M., Ombori O. Occurrence of enteric viruses in surface water and the relationship with changes in season and physical water quality dynamics. Adv. Virol. 2020;2020 doi: 10.1155/2020/9062041. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Osundare F.A., Klink P., Majer C., Akanbi O.A., Wang B., Faber M., Harms D., Bock C.T., Opaleye O.O. Hepatitis e virus seroprevalence and associated risk factors in apparently healthy individuals from Osun state, Nigeria. Pathogens. 2020;9:1–14. doi: 10.3390/pathogens9050392. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Osuolale O., Okoh A. Human enteric bacteria and viruses in five wastewater treatment plants in the Eastern Cape, South Africa. J. Infect. Public Health. 2017;10:541–547. doi: 10.1016/j.jiph.2016.11.012. [DOI] [PubMed] [Google Scholar]
- Paleologos E.K., O'Kelly B.C., Tang C.-S., Cornell K., Rodríguez-Chueca J., Abuel-Naga H., Koda E., Farid A., Vaverková M.D., Kostarelos K., Goli V.S.N.S., Guerra-Rodríguez S., Leong E.-C., Jayanthi P., Shashank B.S., Sharma S., Shreedhar S., Mohammad A., Jha B., Kuntikana G., Bo M.W., Mohamed A.-M.O., Singh D.N. Post COVID-19 water and wastewater management to protect public health and geoenvironment. Environ. Geotech. 2020:1–14. doi: 10.1680/jenge.20.00067. [DOI] [Google Scholar]
- Pande S., Keyzer M.A., Arouna A., Sonneveld B.G.J.S. Addressing diarrhea prevalence in the West African Middle Belt: social and geographic dimensions in a case study for Benin. Int. J. Health Geogr. 2008;7:1–17. doi: 10.1186/1476-072X-7-17. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Parvez A., Rahman M.M., Sultana S., Shaheen S.M. Prevalence of water-borne disease in farmgate slum of dhaka city: a case study of disease propagation in Bangladesh. Pharmacologyonline. 2019;1:55–63. [Google Scholar]
- Phanuwan C., Takizawa S., Oguma K., Katayama H., Yunika A., Ohgaki S. Monitoring of human enteric viruses and coliform bacteria in waters after urban flood in Jakarta, Indonesia. Water Sci. Technol. 2006;54:203–210. doi: 10.2166/wst.2006.470. [DOI] [PubMed] [Google Scholar]
- Pinon A., Vialette M. Survival of viruses in water. Intervirology. 2019;61:214–222. doi: 10.1159/000484899. [DOI] [PubMed] [Google Scholar]
- Polimeni J.M., Almalki A., Iorgulescu R.I., Albu L.L., Parker W.M., Chandrasekara R. Assessment of macro-level socioeconomic factors that impact waterborne diseases: the case of Jordan. Int. J. Environ. Res. Publ. Health. 2016;13:1–15. doi: 10.3390/ijerph13121181. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Polo D., García-Fernández I., Fernández-Ibáñez P., Romalde J.L. Solar water disinfection (SODIS): impact on hepatitis A virus and on a human norovirus surrogate under natural solar conditions. Int. Microbiol. 2015;18:41–49. doi: 10.2436/20.1501.01.233. [DOI] [PubMed] [Google Scholar]
- Pooi C.K., Ng H.Y. 2018. Review of Low-Cost Point-Of-Use Water Treatment Systems for Developing Communities. Npj Clean Water 1. [DOI] [Google Scholar]
- Potgieter N., De Beer M.C., Taylor M.B., Steele A.D. Prevalence and diversity of rotavirus strains in children with acute diarrhea from rural communities in the Limpopo Province, South Africa, from 1998 to 2000. J. Infect. Dis. 2010;202 doi: 10.1086/653561. [DOI] [PubMed] [Google Scholar]
- Pouramin P., Nagabhatla N., Miletto M. A systematic review of water and gender interlinkages: assessing the intersection with health. Front. Water. 2020;2 doi: 10.3389/frwa.2020.00006. [DOI] [Google Scholar]
- Prest E.I., Hammes F., van Loosdrecht M.C.M., Vrouwenvelder J.S. Biological stability of drinking water: controlling factors, methods, and challenges. Front. Microbiol. 2016;7:1–24. doi: 10.3389/fmicb.2016.00045. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Proctor C.R., Hammes F. Drinking water microbiology-from measurement to management. Curr. Opin. Biotechnol. 2015;33:87–94. doi: 10.1016/j.copbio.2014.12.014. [DOI] [PubMed] [Google Scholar]
- Pype M.L., Lawrence M.G., Keller J., Gernjak W. Reverse osmosis integrity monitoring in water reuse: the challenge to verify virus removal - a review. Water Res. 2016;98:384–395. doi: 10.1016/j.watres.2016.04.040. [DOI] [PubMed] [Google Scholar]
- Qiu Y., Lee B.E., Neumann N., Ashbolt N., Craik S., Pang X.L. Assessment of human virus removal during municipal wastewater treatment in Edmonton, Canada. J. Appl. Microbiol. 2015;119:1729–1739. doi: 10.1111/jam.12971. [DOI] [PubMed] [Google Scholar]
- Rabeh S.A. In: The Nile. Monographiae Biologicae. Dumont H.J., editor. Springer; Dordrecht: 2009. Bacteria and viruses in the nile; pp. 407–429. [DOI] [Google Scholar]
- Rabin R. The lead industry and lead water pipes “A modest campaign. Am. J. Publ. Health. 2008;98:1584–1592. doi: 10.2105/AJPH.2007.113555. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rachmadi A.T., Kitajima M., Pepper I.L., Gerba C.P. Enteric and indicator virus removal by surface flow wetlands. Sci. Total Environ. 2016;542:976–982. doi: 10.1016/j.scitotenv.2015.11.001. [DOI] [PubMed] [Google Scholar]
- Raciny I., Zodrow K.R., Li D., Li Q., Alvarez P.J.J. Addition of a magnetite layer onto a polysulfone water treatment membrane to enhance virus removal. Water Sci. Technol. 2011;63:2346–2352. doi: 10.2166/wst.2011.551. [DOI] [PubMed] [Google Scholar]
- Rames E., Roiko A., Stratton H., Macdonald J. Technical aspects of using human adenovirus as a viral water quality indicator. Water Res. 2016;96:308–326. doi: 10.1016/j.watres.2016.03.042. [DOI] [PubMed] [Google Scholar]
- Rana A.M. Effect of water , sanitation and hygiene intervention in reducing self-reported waterborne diseases in rural Bangladesh. RED Res. Rep. 2010 [Google Scholar]
- Randazzo W., Truchado P., Cuevas-Ferrando E., Simón P., Allende A., Sánchez G. SARS-CoV-2 RNA in wastewater anticipated COVID-19 occurrence in a low prevalence area. Water Res. 2020;181:115942. doi: 10.1016/j.watres.2020.115942. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rijsberman F.R. Water scarcity: fact or fiction? Agric. Water Manag. 2006;80:5–22. doi: 10.1016/j.agwat.2005.07.001. [DOI] [Google Scholar]
- Robeck G.G., Clarke N.A., Dostal K.A., Hartung H.O. Effectiveness of water treatment processes in virus removal. J. Am. Water Works Assoc. 1962;54:1275–1292. http://www.jstor.org/stable/41256904 [Google Scholar]
- Rodríguez-Díaz J., Querales L., Caraballo L., Vizzi E., Liprandi F., Takiff H., Betancourt W.Q. Detection and characterization of waterborne gastroenteritis viruses in urban sewage and sewage-polluted river waters in Caracas. Venezuela. Appl. Environ. Microbiol. 2009;75:387–394. doi: 10.1128/AEM.02045-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rosa G. La, Bonadonna L., Lucentini L., Kenmoe S., Suffredini E. Coronavirus in water environments: occurrence, persistence and concentration methods - a scoping review. Water Res. 2020;179:115899. doi: 10.1016/j.watres.2020.115899. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saback F.L., Palmer T.E., Sabino R.R., Carvalho S.M.F., Amorim L.M., Gaspar A.M.C., Oliveira M.L.A., Yoshida C.F.T., Niel C. Infection with hepatitis A and TT viruses and socioeconomic status in Rio de Janeiro, Brazil. Scand. J. Infect. Dis. 2001;33:121–125. doi: 10.1080/003655401750065508. [DOI] [PubMed] [Google Scholar]
- Salman A.D. Prevalence of rota virus detection by reverse TranscriptasePolymerase chain reaction in stool from children fewer than five age with acute diarrhea in diyala province in Iraq. IOSR J. Pharm. Biol. Sci. 2017;12:94–99. doi: 10.9790/3008-1201039499. [DOI] [Google Scholar]
- Sambu D. Impact of global initiatives on drinking water access in Africa. African Geogr. Rev. 2016;35:151–167. doi: 10.1080/19376812.2015.1133312. [DOI] [Google Scholar]
- Sano D., Amarasiri M., Hata A., Watanabe T., Katayama H. Risk management of viral infectious diseases in wastewater reclamation and reuse: Review. Environ. Int. 2016;91:220–229. doi: 10.1016/j.envint.2016.03.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Santos S. Dos, Adams E.A., Neville G., Wada Y., Sherbinin A. De, Bernhardt E.M., Adamo S.B. Urban growth and water access in sub-Saharan Africa: progress, challenges, and emerging research directions. Sci. Total Environ. 2017;607–608:497–508. doi: 10.1016/j.scitotenv.2017.06.157. [DOI] [PubMed] [Google Scholar]
- Schlindwein A.D., Rigotto C., Simões C.M.O., Barardi C.R.M. Detection of enteric viruses in sewage sludge and treated wastewater effluent. Water Sci. Technol. 2010;61:537–544. doi: 10.2166/wst.2010.845. [DOI] [PubMed] [Google Scholar]
- Schmitz B.W., Kitajima M., Campillo M.E., Gerba C.P., Pepper I.L. Virus reduction during advanced bardenpho and conventional wastewater treatment processes. Environ. Sci. Technol. 2016;50:9524–9532. doi: 10.1021/acs.est.6b01384. [DOI] [PubMed] [Google Scholar]
- Schwab K. In: Perspectives in Medical Virology. Bosch A., editor. 2007. Waterborne gastroenteritis viruses; pp. 27–38. [DOI] [Google Scholar]
- Seitz S.R., Leon J.S., Schwab K.J., Lyon G.M., Dowd M., McDaniels M., Abdulhafid G., Fernandez M.L., Lindesmith L.C., Baric R.S., Moe C.L. Norovirus infectivity in humans and persistence in water. Appl. Environ. Microbiol. 2011;77:6884–6888. doi: 10.1128/AEM.05806-11. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sekwadi P.G., Ravhuhali K.G., Mosam A., Essel V., Ntshoe G.M., Shonhiwa A.M., Mccarthy K., Mans J., Taylor M.B., Page N.A., Govender N. Waterborne outbreak of gastroenteritis on the KwaZulu-natal coast, South Africa, december 2016/january 2017. Epidemiol. Infect. 2018;146:1318–1325. doi: 10.1017/S095026881800122X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shapiro O.H., Kushmaro A., Brenner A. Bacteriophage predation regulates microbial abundance and diversity in a full-scale bioreactor treating industrial wastewater. ISME J. 2010;4:327–336. doi: 10.1038/ismej.2009.118. [DOI] [PubMed] [Google Scholar]
- Sherchan S.P., Shahin S., Ward L.M., Tandukar S., Aw T.G., Schmitz B., Ahmed W., Kitajima M. First detection of SARS-CoV-2 RNA in wastewater in North America: a study in Louisiana, USA. Sci. Total Environ. 2020;743:140621. doi: 10.1016/j.scitotenv.2020.140621. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shimabuku Q.L., Arakawa F.S., Fernandes Silva M., Ferri Coldebella P., Ueda-Nakamura T., Fagundes-Klen M.R., Bergamasco R. Water treatment with exceptional virus inactivation using activated carbon modified with silver (Ag) and copper oxide (CuO) nanoparticles. Environ. Technol. 2017;38 doi: 10.1080/09593330.2016.1245361. 2058–2069. [DOI] [PubMed] [Google Scholar]
- Shoham D., Jahangir A., Ruenphet S., Takehara K. Persistence of avian influenza viruses in various artificially frozen environmental water types. Influenza Res. Treat. 2012;2012:1–11. doi: 10.1155/2012/912326. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Siddiqui M.S., Amin M., Amber M., Abbas M., Sherwani S.K., Malik M.W., Husaain M. Association of socio-economic features, hygienic status, age groups and gender with prevalence of waterborne diseases in rawalpindi and islamabad. Sci. Technol. Dev. 2012;31:219–226. [Google Scholar]
- Sinclair R.G., Jones E.L., Gerba C.P. Viruses in recreational water-borne disease outbreaks: a review. J. Appl. Microbiol. 2009;107:1769–1780. doi: 10.1111/j.1365-2672.2009.04367.x. [DOI] [PubMed] [Google Scholar]
- Soja R., Wiejaczka L. The impact of a reservoir on the physicochemical properties of water in a Mountain river. Water Environ. J. 2014;28:473–482. doi: 10.1111/wej.12059. [DOI] [Google Scholar]
- Struchiner C.J., De Almeida L.M., De Azevedo R.S., Massad E. Hepatitis A incidence rate estimates from a pilot seroprevalence survey in Rio de Janeiro, Brazil. Int. J. Epidemiol. 1999;28:776–781. doi: 10.1093/ije/28.4.776. [DOI] [PubMed] [Google Scholar]
- Symonds E.M., Verbyla M.E., Lukasik J.O., Kafle R.C., Breitbart M., Mihelcic J.R. A case study of enteric virus removal and insights into the associated risk of water reuse for two wastewater treatment pond systems in Bolivia. Water Res. 2014;65:257–270. doi: 10.1016/j.watres.2014.07.032. [DOI] [PubMed] [Google Scholar]
- Tandukar S., Sherchan S.P., Haramoto E. Applicability of crAssphage, pepper mild mottle virus, and tobacco mosaic virus as indicators of reduction of enteric viruses during wastewater treatment. Sci. Rep. 2020;10:1–8. doi: 10.1038/s41598-020-60547-9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tanneru C.T., Chellam S. Mechanisms of virus control during iron electrocoagulation - microfiltration of surface water. Water Res. 2012;46:2111–2120. doi: 10.1016/j.watres.2012.01.032. [DOI] [PubMed] [Google Scholar]
- Toze S. Reuse of effluent water - benefits and risks. Agric. Water Manag. 2006;80:147–159. doi: 10.1016/j.agwat.2005.07.010. [DOI] [Google Scholar]
- UN-Water . UNESCO; Paris: 2017. The United Nations World Water Development Report 2017. Wastewater: the Untapped Resource. Paris, UNESCO, the United Nations World Water Development Report 2017. Wastewater: the Untapped Resource. [DOI] [Google Scholar]
- UNDP . 2020. Covid-19 and Human Development: Assessing theCrisi, Envisioning the Recovery. 1 UN Plaza, New York, NY 10017 USA. [Google Scholar]
- UNICEF . UNICEF Publications | UNICEF; 2012. Pneumonia and Diarrhoea: Tackling the Deadliest Diseases for the World's Poorest Children.https://www.unicef.org/publications/index_65491.html WWW Document] 7.10.20. [DOI] [PubMed] [Google Scholar]
- United Nations . 2018. #Envision 2030 Goal 6: Clean Water and Sanitation | United Nations Enable [WWW Document]https://www.un.org/development/desa/disabilities/envision2030-goal6.html 7.16.20. [Google Scholar]
- Van der Laan H., van Halem D., Smeets P.W.M.H., Soppe A.I.A., Kroesbergen J., Wubbels G., Nederstigt J., Gensburger I., Heijman S.G.J. Bacteria and virus removal effectiveness of ceramic pot filters with different silver applications in a long term experiment. Water Res. 2014;51:47–54. doi: 10.1016/j.watres.2013.11.010. [DOI] [PubMed] [Google Scholar]
- Verbyla M.E., Mihelcic J.R. A review of virus removal in wastewater treatment pond systems Supplementary. Water Res. 2015 doi: 10.1016/j.watres.2014.12.031. [DOI] [PubMed] [Google Scholar]
- Verheyen J., Timmen-Wego M., Laudien R., Boussaad I., Sen S., Koc A., Uesbeck A., Mazou F., Pfister H. Detection of adenoviruses and rotaviruses in drinking water sources used in rural areas of Benin, west africa. Appl. Environ. Microbiol. 2009;75:2798–2801. doi: 10.1128/AEM.01807-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
- WHO . 2017. Diarrhoeal Disease. Fact Sheets; pp. 1–4.https://www.who.int/en/news-room/fact-sheets/detail/diarrhoeal-disease [WWW Document] 7.12.20. [Google Scholar]
- WHO . 2017. Guidelines for Drinking-Water Quality: Fourth Edition Incorporating the First Addendum. Geneva, Switzerland. [PubMed] [Google Scholar]
- WHO Global Health Risks: mortality and burden of disease attributable to selected major risks. Bull. World Health Organ. 2009 doi: 10.2471/BLT.09.070565. [DOI] [Google Scholar]
- WHO and UNICEF . 2015. Progress on Sanitation and Drinking Water: 2015 Update and MDG Assessment. [Google Scholar]
- World Bank . 2012. World Development Report 2012: Gender Equality and Development. [Google Scholar]
- World Bank Group . World Bank Group; 2017. Reducing Inequalities in Water Supply, Sanitation, and Hygiene in the Era of the Sustainable Development Goals. Synthesis Report of the WASH Poverty Diagnostic Initiative. [DOI] [Google Scholar]
- World Bank Group . World Bank Group; 2017. Reducing Inequalities in Water Supply, Sanitation, and Hygiene in the Era of the Sustainable Development Goals. Synthesis Report of the WASH Poverty Diagnostic Initiative. [DOI] [Google Scholar]
- Wurtzer S., Marechal V., Jm M., Moulin L., Université S., Metis U.M.R., Atelier Z. Time course quantitative detection of SARS-CoV-2 in Parisian wastewaters correlates with COVID-19 confirmed cases Eau de Paris , R & D Laboratory , DRDQE 11 Avenue Jean Jaurès 94200 Ivry/Seine , France . Corresponding authors * laurent.moulin@eaudeparis. medRxiv. 2020:10–13. [Google Scholar]
- Xagoraraki I., Yin Z., Svambayev Z. Fate of viruses in water systems. J. Environ. Eng. 2014;140:1–18. doi: 10.1061/(ASCE)EE.1943-7870.0000827. [DOI] [Google Scholar]
- Yang D., He Y., Wu B., Deng Y., Li M., Yang Q., Huang L., Cao Y., Liu Y. Drinking water and sanitation conditions are associated with the risk of malaria among children under five years old in sub-Saharan Africa: a logistic regression model analysis of national survey data. J. Adv. Res. 2020 doi: 10.1016/j.jare.2019.09.001. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang J., LeChevallier M.W., Teunis P.F.M., Xu M. Managing risks from virus intrusion into water distribution systems due to pressure transients. J. Water Health. 2011;9:291–305. doi: 10.2166/wh.2011.102. [DOI] [PubMed] [Google Scholar]
- Yongsi H.B.N., Ntetu A.L. Household standard of living and children's health in Cameroon. J. Develop. Area. 2008;42:251–259. [Google Scholar]
- Yu I.T.S., Li Y., Wong T.W., Tam W., Chan A.T., Lee J.H.W., Leung D.Y.C., Ho T. Evidence of airborne transmission of the severe acute respiratory syndrome virus. N. Engl. J. Med. 2004;350:1731–1739. doi: 10.1056/NEJMoa032867. [DOI] [PubMed] [Google Scholar]
- Zheng X., Chen D., Wang Z., Lei Y., Cheng R. Nano-TiO2 membrane adsorption reactor (MAR) for virus removal in drinking water. Chem. Eng. J. 2013;230:180–187. doi: 10.1016/j.cej.2013.06.069. [DOI] [Google Scholar]
- Zheng X., Wang Q., Chen L., Wang J., Cheng R. Photocatalytic membrane reactor (PMR) for virus removal in water: performance and mechanisms. Chem. Eng. J. 2015;277:124–129. doi: 10.1016/j.cej.2015.04.117. [DOI] [Google Scholar]
- Zhu B., Clifford D.A., Chellam S. Virus removal by iron coagulation-microfiltration. Water Res. 2005;39:5153–5161. doi: 10.1016/j.watres.2005.09.035. [DOI] [PubMed] [Google Scholar]




