Elsevier

Science of The Total Environment

Volumes 601–602, 1 December 2017, Pages 1712-1719
Science of The Total Environment

Probabilistic quantitative microbial risk assessment model of norovirus from wastewater irrigated vegetables in Ghana using genome copies and fecal indicator ratio conversion for estimating exposure dose

https://doi.org/10.1016/j.scitotenv.2017.05.168Get rights and content

Highlights

  • Study sought to improve estimates of QMRA model by using both field data and literature reported values

  • Comparison of fecal indicator ratio conversion and gene copies of virus for dose estimation

  • Fecal indicator conversion ratio underestimates the risk possess to vegetable consumers

  • Modeling methodology used for estimating dose is a form of uncertainty in risk assessment modelling

  • QMRA estimates based on virus of interest should be always encourage instead of fecal indicator measurements

Abstract

The need to replace the commonly applied fecal indicator conversions ratio (an assumption of 1:10 5 virus to fecal indicator organism) in Quantitative Microbial Risk Assessment (QMRA) with models based on quantitative data on the virus of interest has gained prominence due to the different physical and environmental factors that might influence the reliability of using indicator organisms in microbial risk assessment. The challenges facing analytical studies on virus enumeration (genome copies or particles) have contributed to the already existing lack of data in QMRA modelling. This study attempts to fit a QMRA model to genome copies of norovirus data. The model estimates the risk of norovirus infection from the intake of vegetables irrigated with wastewater from different sources. The results were compared to the results of a corresponding model using the fecal indicator conversion ratio to estimate the norovirus count. In all scenarios of using different water sources, the application of the fecal indicator conversion ratio underestimated the norovirus disease burden, measured by the Disability Adjusted Life Years (DALYs), when compared to results using the genome copies norovirus data. In some cases the difference was > 2 orders of magnitude. All scenarios using genome copies met the 10 4 DALY per person per year for consumption of vegetables irrigated with wastewater, although these results are considered to be highly conservative risk estimates. The fecal indicator conversion ratio model of stream-water and drain-water sources of wastewater achieved the 10 6 DALY per person per year threshold, which tends to indicate an underestimation of health risk when compared to using genome copies for estimating the dose.

Introduction

To secure and increase crop production, irrigation has become a principal water use in many countries, where it has traditionally been dependent on rain water (Anonymous, 2014, Jiménez, 2006). In developing countries, the increase in wastewater usage has ensured that farmers produce adequate food throughout the year, and millions of small-scale farmers in urban and peri-urban areas are dependent on irrigation to grow high-value edible crops for urban markets (Qadir et al., 2010); irrigation has also contributed to improved nutrition and employment opportunities for farmers. The use of wastewater provides nutrients needed for plant growth and reduces the costs of using fertilizer on plants (Jiménez, 2006). It permits higher crop yields, year-round production, and enlarges the range of crops that can be grown, particularly in (but not limited to) arid and semi-arid areas.

In Ghana, the use of wastewater for vegetable farming is widespread, particularly in and around the more populated cities, where safe water is scarce (Seidu et al., 2008, Keraita et al., 2013). This places Ghana among the countries with the highest volume of raw wastewater usage worldwide, and represents an appropriate study area in relation to wastewater usage in agriculture within developing countries (Amoah et al., 2005, Jiménez, 2006, Amoah et al., 2006, WHO, 2006, Amoah et al., 2007, Raschid-sally and Jayakody, 2008, Hall et al., 2009, Mara and Sleigh, 2009, Drechsel et al., 2009, Mara and Sleigh, 2010a, Mara and Sleigh, 2010b, Labite et al., 2010, Fung, 2011, Ackerson and Awuah, 2012, Tiimub et al., 2012; Lundqvist and Raschid-Sally, 2013, Mok and Hamilton, 2014).

The use of raw wastewater for irrigation is, however, not without public health risks. Quantitative Microbial Risk Assessment (QMRA) has over the years become a powerful tool for estimating health risk through the use of probabilistic modelling. Recent studies estimating the risks of gastroenteritis applied the QMRA methodology to determine the disease burden associated with the consumption of vegetables irrigated with wastewater (Barker et al., 2014; Barker et al., 2013a, Barker et al., 2013b, Mok et al., 2014). Barker (2014) has indicated that the common challenge to conduct such QMRA has been the limited availability of input data on an actual pathogen, in particular virus concentrations as well as virus dose response models. To establish virus concentration, a fecal indicator conversion ratio has therefore been used to express the relationship between the occurrence of fecal indicators (typically E. coli) and the virus. This approach is also used in the current WHO guidelines (WHO, 2006), and has been adopted by subsequent QMRA studies (Barker et al., 2014, Barker et al., 2013a, Barker et al., 2013b, Mara and Hamilton, 2010, Mara and Sleigh, 2010a, Mara and Sleigh, 2010b, Travis et al., 2010, Mok and Hamilton, 2014, Ackerson and Awuah, 2012).

In this study, QMRA model is developed that uses the conversion ratio based on E. coli and norovirus genome copies data that was measured in wastewater to estimate final dose. The model employs a parametric approach to characterize the distribution of norovirus genomic copies to estimate the dose. The study further assesses the impact and likelihood of underestimating or overestimating the health risk (DALY) as a result of using the fecal indicator conversion ratio to estimate the dose of norovirus for risk assessment, when compared to using the genome copies data.

Section snippets

Exposure assessment model

The objective of the exposure assessment model was to estimate the dose of norovirus that consumers are exposed to through the consumption of wastewater-irrigated lettuce and cabbage. Lettuce and cabbage were selected as the main vegetables to represent crops commonly consumed raw in Ghana and other African countries as main ingredients in street foods (Fung, 2011). Water types used for irrigation in developing countries typically include wastewater from streams, drain-water and partially

Estimation of annual probability of infection and illness of norovirus gastroenteritis

The annual probability of norovirus infection ranged from 9.2 × 10 1 to 9.4 × 10 1 for all norovirus genome copies while the ratio conversion method provided a similar range from 8.8 × 10 1 to 9.1 × 10 1. These findings are supported by the estimation of the annual probability of diseases at a given infection that ranged from 8.6 × 10 1 to 9.0 × 10 1 for the norovirus genome copies and 8.1 × 10 1 to 8.3 × 10 1 for E. coli ratio conversion (Table 4). Using the USEPA's threshold of 1 × 10 4 annual probability of

Discussion

The disease burden of the different model scenarios was found to be acceptable under different thresholds of DALY. Nevertheless, it should be noted that the DALY figures are conservative estimates and might in reality be a few orders higher due to the challenges of recovering and enumerating norovirus from sample material as discussed in Papafragkou et al., 2013, Schrader et al., 2012, Laverick et al., 2004. This means, the true disease burden (DALY) from stream wastewater and drain wastewater

Conclusion

We estimated the risk of illness and the disease burden expressed in DALYs with the use of fecal indicator ratio conversion or genome copies of norovirus for the consumption of vegetables irrigated with wastewater in Ghana. A QMRA model was developed to estimate the differences in diseases burden, and the results showed that:

  • 1.

    All model scenarios for consuming vegetables irrigated with wastewater (stream or drain) met the 1 × 10 4 DALY pppy threshold for norovirus. However, models using genome

Acknowledgement

We want to appreciate the help of the following people and their contribution, Rejoice Ametepey, Prof Anders Permin (Technical Univ. of Denmark), Dr Torben Schou (DHI Denmark) and also to faculty members of National Food Institute Soborg, Technical Univ. of Denmark for their critique. This work was supported by DANIDA project Safe Water for Food (11-058DHI).

References (70)

  • T.Z. Mitakakis et al.

    Food safety in family homes in Melbourne, Australia

    J. Food Prot.

    (2004)
  • H.-F. Mok et al.

    A probabilistic quantitative microbial risk assessment model of norovirus disease burden from wastewater irrigation of vegetables in Shepparton, Australia

    Water Res.

    (2014)
  • M. Qadir et al.

    The challenges of wastewater irrigation in developing countries

    Agric. Water Manag.

    (2010)
  • M. Rygaard et al.

    Holistic assessment of a secondary water supply for a new development in Copenhagen, Denmark

    Sci. Total Environ.

    (2014)
  • H. Shuval et al.

    Development of a risk assessment approach for evaluating wastewater reuse standards for agriculture

    Water Sci. Technol.

    (1997)
  • E. Sokolova et al.

    Microbial risk assessment of drinking water based on hydrodynamic modelling of pathogen concentrations in source water

    Sci. Total Environ.

    (2015)
  • N. Ackerson et al.

    Microbial risk assessment of urban agricultural farming: a case study on Kwame Nkrumah University of Science and Technology campus, Kumasi, Ghana

    Technology

    (2012)
  • P. Amoah et al.

    Effectiveness of common and improved sanitary washing methods in selected cities of West Africa for the reduction of coliform bacteria and helminth eggs on

    Tropical Med. Int. Health

    (2007)
  • P. Amoah et al.

    Irrigated urban vegetable production in Ghana: sources of pathogen contamination and health risk elimination

    Irrig. Drain.

    (2005)
  • P. Amoah et al.

    Pesticide and pathogen contamination of vegetables in Ghana's urban markets

    Arch. Environ. Contam. Toxicol.

    (2006)
  • P. Amoah et al.

    Irrigated urban vegetable production in Ghana: microbiological contamination in farms and markets and associated consumer risk groups

    J. Water Health

    (2007)
  • Anonymous

    Water for Agriculture

    (2014)
  • P. Antwi-Agyei

    Wastewater Use in Urban Agriculture: An Exposure and Risk Assessment in Accra, Ghana

    (2015)
  • R.L. Atmar et al.

    Determination of the 50% human infectious dose for Norwalk virus

    J. Infect. Dis.

    (2014)
  • L. Baert et al.

    Survival and transfer of murine norovirus 1, a surrogate for human noroviruses, during the production process of deep-frozen onions and spinach

    J. Food Prot.

    (2008)
  • S.F. Barker

    Risk of norovirus gastroenteritis from consumption of vegetables irrigated with highly treated municipal wastewater-evaluation of methods to estimate sewage quality

    Risk Anal.

    (2014)
  • S.F. Barker et al.

    A probabilistic model of norovirus disease burden associated with greywater irrigation of home-produced lettuce in Melbourne, Australia

    Water Res.

    (2013)
  • S.F. Barker

    Risk of norovirus gastroenteritis from consumption of vegetables irrigated with highly treated municipal wastewater. Evaluation of methods to estimate sewage quality

    Risk Analysis

    (2014)
  • S. Begg et al.

    The burden of disease and injury in Australia 2003. PHE 82

    (2007)
  • P. Drechsel et al.

    Wastewater Irrigation and Health

    (2009)
  • FAO, Meat processing technology for small- to medium-scale producers. FAO Corporate Document Repository. 2007....
  • J. Fung

    Microbiological quality of urban-vended salad and its association with gastrointestinal diseases in Kumasi, Ghana

    Int. J. Food Saf., Nutr. Publ. Health

    (2011)
  • J.A. Haagsma et al.

    Disability adjusted life years and minimal disease: application of a preference-based relevance criterion to rank enteric pathogens

    Popul. Health Metrics

    (2008)
  • J.N. Hall et al.

    Global variability in fruit and vegetable consumption

    Am. J. Prev. Med.

    (2009)
  • A.J. Hamilton et al.

    Quantitative microbial risk assessment models for consumption of raw vegetables irrigated with reclaimed water quantitative microbial risk assessment models for consumption of raw vegetables irrigated with reclaimed water

    Appl. Environ. Microbiol.

    (2006)
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