key: cord-0744473-2bxcdpil
authors: van Wyk, Yazeed; Ubomba-Jaswa, Eunice; Dippenaar, Matthys Alois
title: Potential SARS-CoV-2 contamination of groundwater as a result of mass burial: A mini-review
date: 2022-04-22
journal: Sci Total Environ
DOI: 10.1016/j.scitotenv.2022.155473
sha: b6b49bfd94a7b124e177da112898d303a85d3105
doc_id: 744473
cord_uid: 2bxcdpil

The recent COVID-19 disease has highlighted the need for further research around the risk to human health and the environment because of mass burial of COVID-19 victims. Despite SARS-CoV-2 being an enveloped virus, which is highly susceptible to environmental conditions (temperature, solar/UV exposure). This review provides insight into the potential of SARS-CoV-2 to contaminate groundwater through burial sites, the impact of various types of burial practices on SARS-CoV-2 survival, and current knowledge gaps that need to be addressed to ensure that humans and ecosystems are adequately protected from SARS-CoV-2. Data available shows temperature is still likely to be the driving factor when it comes to survival and infectivity of SARS-CoV-2. Research conducted at cemetery sites globally using various bacteriophages (MS2, PRD1, faecal coliforms) and viruses (TGEV, MHV) as surrogates for pathogenic enteric viruses to study the fate and transport of these viruses showed considerable contamination of groundwater, particularly where there is a shallow vadose zone and heterogeneous structures are known to exist with very low residence times. In addition, changes in solution chemistry (e.g., decrease in ionic strength or increase in pH) during rainfall events produces large pulses of released colloids that can result in attached viruses becoming remobilised, with implications for groundwater contamination. Viruses cannot spread unaided through the unsaturated zone. Since groundwater is too deep to be in contact with the interred body and migration rates are very slow, except where preferential flow paths are known to exist, the groundwater table will not be significantly impacted by contamination from SARS-CoV-2. When burial takes place using scientifically defensible methods the possibility of infection will be highly improbable. Furthermore, the SARS-CoV-2 pandemic has helped us to prepare for other eventualities such as natural disasters where mass fatalities and subsequently burials may take place in a relatively short space of time.

than at 4 ℃). Also, there appears to be no current evidence that human coronaviruses are present in surface water or groundwater or are transmitted through contaminated drinking water (La Rosa et al., 2020) . Shakil et al. (2020) conducted a critical analysis of 57 studies on the nexus between COVID-19 and the environment. The cluster under COVID-19 and temperature indicated that the virus is highly stable at 4 °C, but sensitive to heat. At 4 °C, there was only around a 0.7 log-unit reduction of infectious titre after 2 weeks. The temperature of groundwater during the year in a temperate climate is about 8 ℃, and therefore the virus can be stable at this temperature as well. With the incubation temperature increased to 70 °C, the time for virus inactivation was reduced to 5 min. It was also found that a 1 °C increase in temperature was linked to a 4.9% decline in daily COVID-19 transmissions when the temperature was lower than 25.8 °C. However, the same study found no evidence for the reduction in COVID-19 transmissions for temperatures above 25.8 °C. Nevertheless, as with other coronaviruses, it is an enveloped virus that is not likely to persist and remain infective in the environment given their unstable nature and susceptibility to unfavourable conditions (high temperature, light exposure, and antagonistic microorganisms like Escherichia coli, Enterococcus spp., Bacillus spp., Clostridium spp.).

In contrast, other microorganisms, although not relevant to this study, are long-lived and can survive in appropriate environmental conditions in soil profiles or groundwater systems for quite some time (e.g., B. anthracis, variola virus, and Clostridium spp.) . The survival and transport rate of pathogens in soils and aquifers are controlled by climate, soil or aquifer type, pore fluid properties, and the pathogen itself (Bitton & Harvey, 1992) . Batch and column experiments have shown that viruses do not readily sorb to or are released from soil particle surfaces when suspended in low ionic strength solutions (Sasidharan et al., 2017) . Rainwater having low ionic strength can be instrumental in the redistribution and transport of viruses J o u r n a l P r e -p r o o f Journal Pre-proof within the vadose zone (Bitton & Harvey, 1992) . Changes in solution chemistry (e.g. decrease in ionic strength or increase in pH) produce large pulses of released colloids (Walshe et al., 2010) . As a result, there is growing concern that attached viruses can become remobilised with a decrease in ionic strength or divalent cation concentrations during rainfall events (Sasidharan et al., 2017) . This can have implications for groundwater contamination, particularly where the vadose zone is relatively thin and heterogeneous structures are known to exist with very low residence times.

Most studies on SARS-CoV-2, Coronaviruses, influenza viruses, transmissible gastroenteritis virus (TGEV) and mouse hepatitis virus (MHV) have been conducted on a laboratory scale as shown in the previous section; however, the extent to which these results are reproducible in field-scale situations is an area that needs more attention to further enhance the understanding of pathogen interactions in the environment. Gundy et al. (2009) investigated the survival of a human coronavirus (HCoV-229E) and of an animal coronavirus (FIPV, feline infectious peritonitis virus) in tap water (filtered and nonfiltered) and wastewater (primary and activated sludge effluents), comparing results with those of Poliovirus-1 (PV-1, Sabin attenuated strain LSc-2ab). In wastewater, the tested HCoV died off quite rapidly, with a T99.9 of 2.77-3.54 days at 23 ℃. Significantly, the PV-1 lasted 2 to 3 times longer than CoV did, requiring 10.9 days for a comparable reduction in unfiltered tap water, confirming the observation that non-enveloped viruses display higher resistance in water environments compared to enveloped viruses. The study conducted by Gundy et al. (2009) further showed that CoV inactivation was faster in filtered tap water than in unfiltered tap water, suggesting that suspended solids in water can provide protection for viruses adsorbed to these particles.

Wang and co-workers studied the persistence of SARS-CoV in various water types (hospital wastewater, domestic wastewater, and dechlorinated tap water) and in faeces and urine (Wang et al., 2005) . In the study, the performance of sodium hypochlorite and chlorine dioxide in inactivating SARS-CoV, Escherichia coli, and the Enterobacteria phage f2 spiked in wastewater was evaluated. The SARS-CoV virus was detected in hospital wastewater, domestic wastewater, and tap water for 2 days at 20 ℃ and for up to 14 days at 4 ℃, thus demonstrating once again that temperature strongly influences viral persistence. Indeed, it has been universally demonstrated that higher temperatures are associated with rapid inactivation of enteric viruses, and temperature is recognised as the main factor affecting virus survival in the environment, through protein denaturation, damage to nucleic acid, or capsid dissociation (Pinon & Vialette, 2018) .

As indicated, it is well documented that SARS-CoV-2 is susceptible to various environmental factors; however, some uncertainty still remains as to whether or not and through which mechanisms the SARS-CoV-2 virus could potentially contaminate groundwater systems.

Research carried out by Zhang et al. (2022) on the evaluation of pathogen migration capacity using an assessment algorithm on five key physiological indices gave a migration ability for SARS-CoV-2 (size 60-140 nm) of 0.70. This shows that SARS-CoV-2 has a strong migration potential in the vadose zone. Given that groundwater is not exposed to sunlight as most J o u r n a l P r e -p r o o f Journal Pre-proof surface water streams are, and the fact that the spatial distribution of groundwater temperature is mainly affected by geographical latitude, air temperature and local topographic elevations, the groundwater temperature usually stays within a narrow range year-round (Smith, 1982) . As a result, the likelihood of SARS-CoV-2 surviving in groundwater remains a possibility. Preliminary results using a simulation-based approach to better understand the transport mechanisms of coronavirus through soil media, show that viruses can move through porous soil media and eventually contaminate groundwater systems (Petrosino et al., 2021) .

In a limited area of the selected soil section, the contamination was seen to be limited to a maximum of 0.1 PFU/mL after just 20 days of contaminated water drainage.

The World Health Organization (WHO) has released an interim guidance document aimed at faith-based communities and religious leaders to consider the practical considerations and recommendations in the context of COVID-19 (WHO, 2020a). The guidance document states that it is important to safely plan and perform funeral rituals and services by having appropriate funeral and burial practices in place. The establishment of burial grounds according to the best environmental options should take into account the sensitivity to social, religious and cultural practices, as burial sites are not only places for the disposal of dead bodies, but also places where people visit and mourn.

The burial of a large number of bodies in a particular area within 24 hours, as opposed to a body that has to lie in a morgue for two weeks before burial, can potentially aid in the survival of pathogens and as a result pose a risk to the receiving environment. This need for rapid disposal has contributed to the current crisis and will have implications on how to safely handle various burial practices as the pandemic worsens.

In the process of decomposition, a human body can produce in the range of 0.4-0.6 L of cemetery leachate per 1 kg of body weight that can contain pathogenic bacteria and viruses that may possibly contaminate surface water and groundwater systems (Żychowski & Bryndal, 2015; Leong et al., 2021) . Organic nitrogen compounds typically found in cemetery leachate are biogenic amines such as cadaverine (1,5-pentanediamine) and putrescine (1,4diaminobutane) that are produced by decarboxylation of amino acids through enzymatic processes. These amines are highly toxic due to their high solubility in water and generate, when degraded, ammonium ions (NH 4 + ) in the environment (Gonçalves et al., 2022) .

Depending on certain environmental conditions, it can take approximately 10-12 years for a corpse to decompose excluding the bone, with a decline in the number of substances leaching into the soil and groundwater each year (Vaezihir & Mohammadi, 2016) . After 10 years, less than 0.1% of the original loading will remain. Decomposition of the human corpse results in a necroleachate containing salts, water, and some organic substances, followed by the final remains composed essentially of hydroxyapatite, which accounts for approximately 5% of the original body that is considered inert. Previous studies (Jonker & Olivier, 2012; Neckel et al., 2021) have shown significant exceedances of the content of ions from decomposition and these can be considered a threat to human health and life. The rate of degradation is promoted by high nutrients in the subsurface, neutral soil pH, warm temperatures, well-drained soils, and burial practices promoting accessibility of the corpse to decay by invertebrates and vertebrates (Trick et al., 1999; Dent et al., 2004; da Costa Silva & Malagutti Filho, 2012; Fiedler et al., 2012; Żychowski & Bryndal, 2015) .

For a long time, groundwater has been thought of as being entirely free of microbial contaminants and viruses, assuming that vertical transport is slow enough and microbial J o u r n a l P r e -p r o o f survival too short to reach the underlying aquifer system. However, the risks of water contamination are emphasised considering the many small and huge endemic outbreaks from pathogenic microbes and viruses during the past 200 years, all linked to contaminated groundwater (Dent, 1998; Ucisik et al., 1998; Liang et al., 2006; Theng-Theng et al., 2007; Yoder et al., 2008) .

There can be no doubt that groundwater has been and continues to be contaminated by In the Geheina cemetery in Sohag, Egypt it was found that there is appreciable leaching from the dead bodies in graves that might contaminate the underlying aquifer (Mohammed & Abudeif, 2020) . This cemetery was selected as two burial methods are practised here, namely there is a possibility that the underlying groundwater, surface water and soil can also become contaminated as movement of these contaminants is mainly by underground water or by surface water (Hunt & Johnson, 2017) . Generic guidelines exist for cemeteries, mainly addressing sanitary and geotechnical risks. These have been compiled cognisant of typical contaminants emanating from cemeteries, including a variety of metals, nutrients, organics, and pathogens (Kaczmarek, 2019; Neckel et al., 2021) . From the studies above, it can be seen J o u r n a l P r e -p r o o f Journal Pre-proof that cemeteries can pose a groundwater contamination risk under certain conditions; however, the human risk cannot be discounted if the groundwater is consumed.

Various bacteriophages (MS2, PRD1, and ϕX174) were used as surrogates for pathogenic viruses to better understand the fate and transport of viral pathogens in UK aquifers (Collins et al., 2006) . It was shown that MS2 bacteriophage and poliovirus displayed rapid initial dieoff rates followed by a reduced die-off rate to approximately 50% of the initial concentration over a 77-day period. Similarly, poliovirus also exhibited similar initial die-off rates over the 77-day period when subjected to four different solution types. These findings indicate long survival times for poliovirus and MS2 in four water types emphasising the threat they pose to groundwater quality. Long survival rates for both groundwater and UV-sterilised groundwater indicate that microbial activity, at 12 °C, has little effect on the viruses (Gordon & Toze, 2003) . Hence, at typical UK groundwater temperatures, viruses can survive for several months. This is further shown by the slow inactivation coefficient rates (μ) for both poliovirus and MS2. Even-though the study was done at laboratory scale, there is enough evidence to suggest that the groundwater can become contaminated and can be considered as a potential threat to the public if it is consumed.

The WHO guidelines clearly stipulate that to date, there has been no evidence to suggest that individuals become infected through exposure to bodies of persons deceased due to COVID-19 (WHO, 2020) . If conducted according to normal best practice, choosing to bury or cremate a person who has passed away from COVID-19 should pose no additional risk to J o u r n a l P r e -p r o o f Journal Pre-proof persons alive or the environment, as was affirmed by Ubomba-Jaswa et al. (2020) . However, in many other places worldwide, including South Africa, due to very diverse religious and cultural practices around death often requiring burial, as well as the lack of sufficient crematoria, COVID-19 victims are highly likely to be buried in cemeteries. These countries also often have serious issues with access to land in metropolitan areas given the economic benefit of alternative developments, and in rural areas where agriculture, conservation, and residential developments take precedence.

Poorly located and incorrectly managed burial grounds pose a severe pollution potential. The geotechnical design adopted for mass burial should guarantee minimum rainwater infiltration into the burial site to reduce the amount of necroleachate. In addition, it should also provide an opportunity to maximise virus retention by adsorption process (Leong et al., 2021) .

Leachate produced from burial grounds (cemeteries, churchyards, park cemeteries, and green cemeteries) is of a highly pathogenic nature and can pollute the soil zone and groundwater representing a public health hazard (Oliveira et al., 2013) . Pollution problems generally occur in areas with vulnerable aquifers and climate conditions, which favour rapid seepage of decay products. It becomes vital that when establishing meaningful cemetery site selection criteria, adequate measures should be taken to ensure environmental protection and to promote rapid aerobic decomposition. Therefore, a sustainable development approach and the best environmental options should be adopted. excavations. The excavation of graves itself generates a bucket system where infiltrated water will most likely move towards less-compacted backfill or coffin voids. This changes the redox conditions, while also increasing moisture content to levels which can induce further vertical percolation or lateral flow of water. This is enhanced through compacting backfill or allowing depressions in backfilled soil, while the converse is true for mounded backfill whereby surface runoff and resulting erosion is more pronounced (Dent et al., 2004) .

Microbiological Analysis of Necrosols Collected from Urban Cemeteries in Poland

Survival of surrogate coronaviruses in water

Institute of Occupational Medicine

Guidelines for Cemetery Site Selection. Council for Geoscience

Groundwater contamination related to Peace and Saudade cemeteries in the municipality of Belo Horizonte

Fate and transport of bacteriophage in UK aquifers as surrogates for pathogenic viruses

Geoelectrical mapping of contamination in the cemeteries: the case study in Piracicaba

Review of human decomposition processes in

Bacterial sampling of monitoring bores -case notes

Department of Health/National Institute of Communicable Diseases

Disease: Infection Prevention and Control Guidelines Version 1

Towards a multi-faceted Vadose Zone Assessment Protocol: cemetery guidelines and application to a burial site located near a seasonal wetland

Environmental Risk Assessment, Monitoring and Management of Cemeteries

Vadose zone characterisation for hydrogeological and geotechnical applications

An assessment of health aspect on the impact of domestic and industrial waste disposal activities on groundwater resources

Euro surveillance: bulletin Europeen sur les maladies transmissibles = Eur

Graveyards-special landfills

Do cemeteries emit drugs? A case study from southern Germany

Another casualty of the SARS-CoV-2 pandemic-the environmental impact

Influence of groundwater characteristics on the survival of enteric viruses

Survival of coronaviruses in water and wastewater

Some geotechnical considerations in the selection of cemetery sites

Autopsy in suspected COVID-19 cases

F-specific RNA bacteriophages are adequate model organisms for enteric viruses in fresh water

Pathogen transport in groundwater systems: contrasts with traditional solute transport

Mineral contamination from cemetery soils: case study of Zandfontein Cemetery, South Africa

The heavy metal hazard of undiscovered World War I and II graves in Poland

Sustainability of waste and groundwater management systems

Coronavirus in water environments: Occurrence, persistence and concentration methods-A scoping review

Design of mass burial sites for safe and dignified disposal of pandemic fatalities

Surveillance for Waterborne Disease and Outbreaks Associated with Drinking Water and Water not Intended for Drinking -United States

Surface water-groundwater interaction using tritium and stable water isotopes: A case study of Middelburg, South Africa

Evaluation of the occurrence and transport of micro-organisms in the freatic aquifer of Vila Nova Cachoeirinha cemetery, municipality of SÃO PAULO

Use of the geophysical approaches for studying the environmental impact assessment of the human burying techniques to the soil and groundwater: A case study of Geheina cemeteries

Review: Epidemiological evidence of groundwater contribution to global enteric disease

Editorial Perspectives: 2019 novel coronavirus (SARS-COV-2): what is its fate in urban water cycle and how can the water research community respond?

Environmental damage and public health threat caused by cemeteries: a proposal of ideal cemeteries for the growing urban sprawl. urbe. Revista Brasileira de Gestão Urbana

Metals in the soil of urban cemeteries in Carazinho (South Brazil) in view of the increase in deaths from COVID-19: projects for cemeteries to mitigate

World Health Organization Water, Sanitation and Health Team, Protecting Groundwater for Health: Managing the Quality of Drinking-water Sources

Transmission of SARS-COV-2 and other enveloped viruses to the environment through protective gear: a brief review

Cemeteriesa potential risk to groundwater

Attenuation and transport of human enteric viruses and bacteriophage MS2 in alluvial sand and gravel aquifer media-laboratory studies

Survival of viruses in water

Groundwater contamination from cemeteries cases of study

Guidelines for the preparation of mass burials and cremation of COVID-19 victims

COVID-19 and the environment: A critical review and research agenda

Ground water hydrology for water well contractors

Emergence and rapid spread of a new severe acute respiratory syndrome-related coronavirus 2 (SARS-COV-2) lineage with multiple spike mutations in South Africa

Massive microbiological groundwater contamination associated with a waterborne outbreak in Lake Erie

Pollution potential of cemeteries: impact of the 19th century Carter Gate Cemetery

Burial practice and its effect on groundwater pollution in Maiduguri

COVID-19 Series Fact Sheet 4. Death and Burial in the Time of COVID-19: Environmental and Health Risks. Water Ucisik and Philip Rushbrook

Movement of faecal bacteria through the vadose zone

Groundwater contamination sourced from the main cemetery of Tabriz

Effects of pH, ionic strength, dissolved organic matter, and flow rate on the co-transport of MS2 bacteriophages with kaolinite in gravel aquifer media

Study on the resistance of severe acute respiratory syndrome-associated coronavirus

Physicochemical Factors Influencing the Preferential Transport of in Soils

WHO Guidelines for Drinking-Water Quality. Retrieved from Geneva: World Health Organization

WHO. 2020. Practical considerations and recommendations for religious leaders and faithbased communities in the context of COVID-19: interim guidance

Emerging investigators series: the source and fate of pandemic viruses in the urban water cycle

Modeling microbial fate in the subsurface environment

Surveillance for waterborne disease and outbreaks associated with recreational water use and other aquatic facility-associated health events --United States

Pollution potential of cemeteries, draft guidance

Physiological characteristics, geochemical properties and hydrological variables influencing pathogen migration in subsurface system: What we know or not? Geosci

Impact of cemeteries on groundwater contamination by bacteria and viruses -a review

Eunice Ubomba-Jaswa -Conceptualising -Review and editing of original draft

Matthys Alois Dippenaar -Securing funding -Review and editing of original draft