Microbial Risk Assessment of Mature Compost from Human Excreta, Cattle Manure, Organic Waste, and Biochar
Abstract
:1. Introduction
2. Materials and Methods
2.1. Composting Trial and Sampling
2.2. Most Probable Number Method for the Detection of E. coli and Salmonella spp.
2.3. Microscopy Count of Ascaris Lumbricoides Eggs
2.4. Statistical Analysis
3. Results
3.1. Detection of Bacterial Indicators E. coli and Salmonella spp.
3.2. Ascaris Lumbricoides Eggs Microscopy Count
4. Discussion
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- WHO and UNICEF. Progress on Drinking Water, Sanitation and Hygiene: 2017 Update and SDG Baselines; World Health Organization (WHO) United Nations Children’s Fund (UNICEF), Licence: Geneva, Switzerland, 2017. [Google Scholar]
- UN-Water. Summary Progress Update 2021: SDG 6—Water and Sanitation for All. UN-Water Integr. Monit. Initiat. 2021, 1–58. Available online: https://www.unwater.org/new-data-on-global-progress-towards-ensuring-water-and-sanitation-for-all-by-2030/ (accessed on 4 April 2022).
- Prüss-Ustün, A.; Wolf, J.; Bartram, J.; Clasen, T.; Cumming, O.; Freeman, M.C.; Gordon, B.; Hunter, P.R.; Medlicott, K.; Johnston, R. Burden of disease from inadequate water, sanitation and hygiene for selected adverse health outcomes: An updated analysis with a focus on low- and middle-income countries. Int. J. Hyg. Environ. Health 2019, 222, 765–777. [Google Scholar] [CrossRef]
- Langergraber, G.; Muellegger, E. Ecological Sanitation—A way to solve global sanitation problems? Environ. Int. 2005, 31, 433–444. [Google Scholar] [CrossRef] [PubMed]
- Asaye, Z.; Kim, D.-G.; Yimer, F.; Prost, K.; Obsa, O.; Tadesse, M.; Gebrehiwot, M.; Brüggemann, N. Effects of Combined Application of Compost and Mineral Fertilizer on Soil Carbon and Nutrient Content, Yield, and Agronomic Nitrogen Use Efficiency in Maize-Potato Cropping Systems in Southern Ethiopia. Land 2022, 11, 784. [Google Scholar] [CrossRef]
- Obsa, O.; Tadesse, M.; Kim, D.-G.; Asaye, Z.; Yimer, F.; Gebrehiwot, M.; Brüggemann, N.; Prost, K. Organic Waste Generation and Its Valorization Potential through Composting in Shashemene, Southern Ethiopia. Sustainability 2022, 14, 3660. [Google Scholar] [CrossRef]
- Carrington, E.G. Evaluation of Sludge Treatments for Pathogen Reduction—Final Report. European Commission. Report No. CO 5026/1. 2001. Available online: https://ec.europa.eu/environment/archives/waste/sludge/pdf/sludge_eval.pdf (accessed on 22 March 2022).
- Dumontet, S.; Scopa, A.; Kerje, S.; Krovacek, K. The importance of pathogenic organisms in sewage and sewage sludge. J. Air Waste Manag. Assoc. 2001, 51, 848–860. [Google Scholar] [CrossRef] [Green Version]
- WHO. WHO Guidelines for the Afe Use of Wastewater, Excreta and Greywater; Excret; World Health Organization (WHO): Geneva, Switzerland, 2006; Volume IV. [Google Scholar]
- Sidhu, J.P.S.; Toze, S.G. Human pathogens and their indicators in biosolids: A literature review. Environ. Int. 2009, 35, 187–201. [Google Scholar] [CrossRef] [PubMed]
- Black, Z.; Balta, I.; Black, L.; Naughton, P.J.; Dooley, J.S.G.; Corcionivoschi, N. The Fate of Foodborne Pathogens in Manure Treated Soil. Front. Microbiol. 2021, 12, 3873. [Google Scholar] [CrossRef]
- Teplitski, M.; de Moraes, M. Of Mice and Men....and Plants: Comparative Genomics of the Dual Lifestyles of Enteric Pathogens. Trends Microbiol. 2018, 26, 748–754. [Google Scholar] [CrossRef]
- Jechalke, S.; Schierstaedt, J.; Becker, M.; Flemer, B.; Grosch, R.; Smalla, K.; Schikora, A. Salmonella establishment in agricultural soil and colonization of crop plants depend on soil type and plant species. Front. Microbiol. 2019, 10, 967. [Google Scholar] [CrossRef] [Green Version]
- Schierstaedt, J.; Grosch, R.; Schikora, A. Agricultural production systems can serve as reservoir for human pathogens. FEMS Microbiol. Lett. 2019, 366, fnaa016. [Google Scholar] [CrossRef] [PubMed]
- Seymour, I.; Appleton, H. Foodborne viruses and fresh produce. J. Appl. Microbiol. 2001, 91, 759–773. [Google Scholar] [CrossRef]
- Nasser, A.M. Transmission of Cryptosporidium by Fresh Vegetables. J. Food Prot. 2022, 85, 1737–1744. [Google Scholar] [CrossRef]
- Ng-Nguyen, D.; Stevenson, M.A.; Traub, R.J. A systematic review of taeniasis, cysticercosis and trichinellosis in Vietnam. Parasites Vectors 2017, 10, 150. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wei, Z.; Mohamed, T.A.; Zhao, L.; Zhu, Z.; Zhao, Y.; Wu, J. Microhabitat drive microbial anabolism to promote carbon sequestration during composting. Bioresour. Technol. 2022, 346, 126577. [Google Scholar] [CrossRef]
- Gurtler, J.B.; Doyle, M.P.; Erickson, M.C.; Jiang, X.; Millner, P.; Sharma, M. Composting to inactivate foodborne pathogens for crop soil application: A review. J. Food Prot. 2018, 81, 1821–1837. [Google Scholar] [CrossRef]
- Greff, B.; Szigeti, J.; Nagy, E.; Lakatos, E.; Varga, L. Influence of microbial inoculants on co-composting of lignocellulosic crop residues with farm animal manure: A review. J. Environ. Manag. 2021, 302, 114088. [Google Scholar] [CrossRef] [PubMed]
- Godlewska, P.; Schmidt, H.P.; Ok, Y.S.; Oleszczuk, P. Biochar for composting improvement and contaminants reduction. A review. Bioresour. Technol. 2017, 246, 193–202. [Google Scholar] [CrossRef] [PubMed]
- Sanchez-Monedero, M.A.; Cayuela, M.L.; Roig, A.; Jindo, K.; Mondini, C.; Bolan, N.J.B.T. Role of biochar as an additive in organic waste composting. Bioresour. Technol. 2018, 247, 1155–1164. [Google Scholar] [CrossRef]
- Bond, T.; Roma, E.; Foxon, K.M.; Templeton, M.R.; Buckley, C. Ancient water and sanitation systems—Applicability for the contemporary urban developing world. Water Sci. Technol. 2013, 67, 935–941. [Google Scholar] [CrossRef]
- Carlton, E.J.; Liu, Y.; Zhong, B.; Hubbard, A.; Spear, R.C. Associations between Schistosomiasis and the Use of Human Waste as an Agricultural Fertilizer in China. PLoS Negl. Trop. Dis. 2015, 9, e0003444. [Google Scholar] [CrossRef]
- Phuc, P.D.; Konradsen, F.; Phuong, P.T.; Cam, P.D.; Dalsgaard, A. Practice of using human excreta as fertilizer and implications for health in Nghean Province, Vietnam. Southeast Asian J. Trop. Med. Public Health 2006, 37, 222–229. [Google Scholar] [PubMed]
- Diener, S.; Semiyaga, S.; Niwagaba, C.B.; Muspratt, A.M.; Gning, J.B.; Mbéguéré, M.; Ennin, J.E.; Zurbrugg, C.; Strande, L. A value proposition: Resource recovery from faecal sludge—Can it be the driver for improved sanitation? Resour. Conserv. Recycl. 2014, 88, 32–38. [Google Scholar] [CrossRef] [Green Version]
- Kanteraki, A.; Isari, E.; Svarnas, P.; Kalavrouziotis, I. Biosolids: The Trojan horse or the beautiful Helen for soil fertilization? Sci. Total Environ. 2022, 839, 156270. [Google Scholar] [CrossRef] [PubMed]
- Moya, B.; Parker, A.; Sakrabani, R. Challenges to the use of fertilisers derived from human excreta: The case of vegetable exports from Kenya to Europe and influence of certification systems. Food Policy 2019, 85, 72–78. [Google Scholar] [CrossRef]
- Council of the European Union. Council Directive 86/278/EEC of 12 June 1986 on the protection of the environment, and in particular of the soil, when sewage sludge is used in agriculture. Off. J. Eur. Communities 1986, 181, 6–12. [Google Scholar]
- Collivignarelli, M.C.; Abbà, A.; Frattarola, A.; Carnevale Miino, M.; Padovani, S.; Katsoyiannis, I.; Torretta, V. Legislation for the Reuse of Biosolids on Agricultural Land in Europe: Overview. Sustainability 2019, 11, 6015. [Google Scholar] [CrossRef] [Green Version]
- Jones, E.R.; van Vliet, M.T.H.; Qadir, M.; Bierkens, M.F.P. Country-level and gridded estimates of wastewater production, collection, treatment and reuse. Earth Syst. Sci. Data 2021, 13, 237–254. [Google Scholar] [CrossRef]
- Pietsch, M.; Schleusner, Y.; Müller, P.; Eling, R.; Philipp, W.; Hoelzle, L.E. Risikoanalyse der bodenbezogenen Verwertung kommunaler Klärschlämme unter Hygieneaspekten. Umweltbundesamt 2014, 96, 156. Available online: http://www.umweltbundesamt.de/publikationen/risikoanalyse-der-bodenbezogenen-verwertung (accessed on 24 October 2019).
- DüMV. Düngemittelverordnung vom 5. Dezember 2012 (BGBl. I S. 2482), die zuletzt durch Artikel 3 der Verordnung vom 26. Mai 2017 (BGBl. I S. 1305) geändert worden ist. Germany. 2012. Available online: https://www.gesetze-im-internet.de/d_mv_2012/DüMV.pdf (accessed on 22 December 2020).
- AbfKlärV. Klärschlammverordnung vom 27. September 2017 (BGBl. I S. 3465), die zuletzt durch Artikel 137 der Verordnung vom 19. Juni 2020 (BGBl. I S. 1328) geändert worden ist. Germany. 2017. Available online: https://www.gesetze-im-internet.de/abfkl_rv_2017/AbfKl%C3%A4rV.pdf (accessed on 21 July 2022).
- BioAbfV. Bioabfallverordnung in der Fassung der Bekanntmachung vom 4. April 2013 (BGBl. I S. 658), die Zuletzt durch Artikel 3 Absatz 2 der Verordnung vom 27. September 2017 (BGBl. I S. 3465) geändert worden ist; Federal Ministry for the Environment, Nature Conservation, Nuclear Safety and Consumer Protection: Bonn, Germany, 1998.
- Liyih, M.; Damtie, D.; Tegen, D. Prevalence and Associated Risk Factors of Human Intestinal Helminths Parasitic Infections in Ethiopia: A Systematic Review and Meta-Analysis. Sci. World J. 2022, 2022, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Aemiro, A.; Menkir, S.; Tegen, D.; Tola, G. Prevalence of Soil-Transmitted Helminthes and Associated Risk Factors Among People of Ethiopia: A Systematic Review and Meta-Analysis. Infect. Dis. Res. Treat. 2022, 15, 11786337211055437. [Google Scholar] [CrossRef]
- Castro-Herrera, D.; Prost, K.; Schäfer, Y.; Kim, D.G.; Yimer, F.; Tadesse, M.; Gebrehiwot, M.; Brüggemann, N. Nutrient dynamics during composting of human excreta, cattle manure, and organic waste affected by biochar. J. Environ. Qual. 2021, 51, 19–32. [Google Scholar] [CrossRef]
- Jenkins, J. The humanure handbook. In A guide to Composting Human Manure, 3rd ed.; Joseph Jenkins: Grove City, PA, USA, 2005. [Google Scholar]
- De Man, J.C. MPN Tables, Corrected. Eur. J. Appl. Microbiol. Biotechnol. 1983, 331, 301–305. [Google Scholar] [CrossRef]
- Cringoli, G.; Maurelli, M.P.; Levecke, B.; Bosco, A.; Vercruysse, J.; Utzinger, J.; Rinaldi, L. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat. Protoc. 2017, 12, 1723–1732. [Google Scholar] [CrossRef]
- Boelow, H.; Krücken, J.; Thomas, E.; Mirams, G.; von Samson-Himmelstjerna, G. Comparison of FECPAKG2, a modified Mini-FLOTAC technique and combined sedimentation and flotation for the coproscopic examination of helminth eggs in horses. Parasites Vectors 2022, 15, 166. [Google Scholar] [CrossRef] [PubMed]
- Pommerville, J.C. Chapter 5: Microbial growth and nutrition. In Fundamentals of Microbiology, 11th ed.; Jones & Bartlett Learning: Burlington, MA, USA, 2018; p. 149. [Google Scholar]
- Guo, Y.; Sivakumar, M.; Jiang, G. Decay of four enteric pathogens and implications to wastewater-based epidemiology: Effects of temperature and wastewater dilutions. Sci. Total Environ. 2022, 819, 152000. [Google Scholar] [CrossRef]
- Pourcher, A.-M.; Morand, P.; Picard-Bonnaud, F.; Billaudel, S.; Monpoeho, S.; Federighi, M.; Ferre, V.; Moguedet, G. Decrease of enteric micro-organisms from rural sewage sludge during their composting in straw mixture. J. Appl. Microbiol. 2005, 99, 528–539. [Google Scholar] [CrossRef] [PubMed]
- Berendes, D.; Levy, K.; Knee, J.; Handzel, T.; Hill, V.R. Ascaris and escherichia coli inactivation in an ecological sanitation system in Port-au-Prince, Haiti. PLoS ONE 2015, 10, e0125336. [Google Scholar] [CrossRef] [PubMed]
- Kelova, M.E.; Ali, A.M.; Eich-Greatorex, S.; Dörsch, P.; Kallenborn, R.; Jenssen, P.D. Correction to: Small-scale on-site treatment of fecal matter: Comparison of treatments for resource recovery and sanitization. Environ. Sci. Pollut. Res. 2021, 28, 63965–63967. [Google Scholar] [CrossRef]
- Hashemi, S.; Boudaghpour, S.; Han, M. Evaluation of different natural additives effects on the composting process of source separated feces in resource-oriented sanitation systems. Ecotoxicol. Environ. Saf. 2019, 185, 109667. [Google Scholar] [CrossRef] [PubMed]
- Ceustermans, A.; De Clercq, D.; Aertsen, A.; Michiels, C.; Coosemans, J.; Ryckeboer, J. Inactivation of Salmonella Senftenberg strain W 775 during composting of biowastes and garden wastes. J. Appl. Microbiol. 2007, 103, 53–64. [Google Scholar] [CrossRef]
- Germer, J.; Boh, M.Y.; Schoeffler, M.; Amoah, P. Temperature and deactivation of microbial faecal indicators during small scale co-composting of faecal matter. Waste Manag. 2010, 30, 185–191. [Google Scholar] [CrossRef]
- Gerba, C.P.; Huber, M.; Naranjo, J.; Rose, J.; Bradford, S. Occurrence of enteric pathogens in composted domestic solid waste containing disposable diapers. Waste Manag. Res. 1995, 13, 315–324. [Google Scholar] [CrossRef]
- Chung, W.J.; Chang, S.W.; Chaudhary, D.K.; Shin, J.; Kim, H.; Karmegam, N.; Govarthanan, M.; Chandrasekaran, M.; Ravindran, B. Effect of biochar amendment on compost quality, gaseous emissions and pathogen reduction during in-vessel composting of chicken manure. Chemosphere 2021, 283, 131129. [Google Scholar] [CrossRef] [PubMed]
- Maya, C.; Torner-Morales, F.; Lucario, E.; Hernández, E.; Jiménez, B. Viability of six species of larval and non-larval helminth eggs for different conditions of temperature, pH and dryness. Water Res. 2012, 46, 4770–4782. [Google Scholar] [CrossRef]
- Erko, B.; Medhin, G. Human helminthiasis in Wondo Genet, southern Ethiopia, with emphasis on geohelminthiasis. Ethiop. Med. J. 2003, 41, 333–344. [Google Scholar]
- Sahiledengle, B.; Beker, S.; Girum, Y.; Haji, G.; Merewo, S.; Anberbir, W. Prevalence and risk factors of intestinal parasites among primary school children in Shashamane town, southern Ethiopia. MOJ Public Health 2020, 9, 55–61. [Google Scholar] [CrossRef]
- Koné, D.; Cofie, O.; Zurbrügg, C.; Gallizzi, K.; Moser, D.; Drescher, S.; Strauss, M. Helminth eggs inactivation efficiency by faecal sludge dewatering and co-composting in tropical climates. Water Res. 2007, 41, 4397–4402. [Google Scholar] [CrossRef]
- Hafidi, M.; El Fels, L.; El Asli, A.; Ouhdouch, Y. Effect of co-composting on helminth eggs removal. Environ. Eng. Manag. J. 2018, 17, 459–465. [Google Scholar] [CrossRef]
- Pecson, B.M.; Barrios, J.A.; Jiménez, B.E.; Nelson, K.L. The effects of temperature, pH, and ammonia concentration on the inactivation of Ascaris eggs in sewage sludge. Water Res. 2007, 41, 2893–2902. [Google Scholar] [CrossRef] [PubMed]
- Pecson, B.M.; Nelson, K.L. Inactivation of Ascaris suum Eggs by Ammonia. Environ. Sci. Technol. 2005, 39, 7909–7914. [Google Scholar] [CrossRef] [PubMed]
- Darimani, H.S.; Ito, R.; Maïga, Y.; Sou, M.; Funamizu, N.; Maiga, A.H. Effect of post-treatment conditions on the inactivation of helminth eggs (Ascaris suum) after the composting process. Environ. Technol. 2015, 37, 920–928. [Google Scholar] [CrossRef] [PubMed]
- El Hayany, B.; Glaoui, G.E.M.E.; Rihanni, M.; Ezzariai, A.; El Faiz, A.; El Gharous, M.; Hafidi, M.; El Fels, L. Effect of dewatering and composting on helminth eggs removal from lagooning sludge under semi-arid climate. Environ. Sci. Pollut. Res. 2018, 25, 10988–10996. [Google Scholar] [CrossRef] [PubMed]
- Szabová, E.; Juriš, P.; Papajová, I. Sanitation composting process in different seasons. Ascaris suum as model. Waste Manag. 2010, 30, 426–432. [Google Scholar] [CrossRef] [PubMed]
Replicates * | Treatments | Start | Combining Replicates # | Sampling # | Composting Duration # | |
---|---|---|---|---|---|---|
Block 1 | HM HM+BC CM CM+BC | 02/04/2019 | 15/09/2019 | 14/12/2019 | Block 1 | 256 d |
Block 2 | HM HM+BC CM CM+BC | 19/04/2019 | Block 2 | 239 d | ||
Block 3 | HM HM+BC CM CM+BC | 08/05/2019 | Block 3 | 220 d | ||
Block 4 | HM HM+BC CM CM+BC | 24/05/2019 | Block 4 | 204 d |
Treatment | Replicate * | E. coli [CFU g−1] | Salmonella [CFU g−1] |
---|---|---|---|
HM | HM_1 | <30 | <30 |
HM_2 | <30 | <30 | |
HM_3 | <30 | <30 | |
HM_4 | <30 | <30 | |
HM_5 | <30 | <30 | |
HM_6 | <30 | <30 | |
HM | Mean | <30 | <30 |
HM+BC | HM+BC_1 | <30 | <30 |
HM+BC_2 | <30 | <30 | |
HM+BC_3 | <30 | <30 | |
HM+BC_4 | <30 | <30 | |
HM+BC_5 | <30 | <30 | |
HM+BC_6 | 36 | <30 | |
HM+BC | Mean | <31 | <30 |
CM | CM_1 | 61 | <30 |
CM_2 | <30 | <30 | |
CM_3 | <30 | <30 | |
CM_4 | <30 | <30 | |
CM_5 | 92 | <30 | |
CM_6 | <30 | <30 | |
CM | Mean | <45.5 | <30 |
CM+BC | CM+BC_1 | <30 | <30 |
CM+BC_2 | <30 | <30 | |
CM+BC_3 | <30 | <30 | |
CM+BC_4 | <30 | <30 | |
CM+BC_5 | 150 | <30 | |
CM+BC_6 | 210 | <30 | |
CM+BC | Mean | <80 | <30 |
Treatment | Replicate * | Ascaris Egg Count/g Compost |
---|---|---|
HM | HM_1 | 0 |
HM_2 | 0 | |
HM_3 | 0 | |
HM_4 | 0 | |
HM_5 | 0 | |
HM_6 | 0 | |
HM | Mean | 0 |
HM+BC | HM+BC_1 | 0 |
HM+BC_2 | 0 | |
HM+BC_3 | 0 | |
HM+BC_4 | 0 | |
HM+BC_5 | 0 | |
HM+BC_6 | 0 | |
HM+BC | Mean | 0 |
CM | CM_1 | 0 |
CM_2 | 0 | |
CM_3 | 0 | |
CM_4 | 0 | |
CM_5 | 0 | |
CM_6 | 0 | |
CM | Mean | 0 |
CM+BC | CM+BC_1 | 0 |
CM+BC_2 | 0 | |
CM+BC_3 | 0 | |
CM+BC_4 | 0 | |
CM+BC_5 | 0 | |
CM+BC_6 | 0 | |
CM+BC | Mean | 0 |
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Werner, K.A.; Castro-Herrera, D.; Yimer, F.; Tadesse, M.; Kim, D.-G.; Prost, K.; Brüggemann, N.; Grohmann, E. Microbial Risk Assessment of Mature Compost from Human Excreta, Cattle Manure, Organic Waste, and Biochar. Sustainability 2023, 15, 4624. https://doi.org/10.3390/su15054624
Werner KA, Castro-Herrera D, Yimer F, Tadesse M, Kim D-G, Prost K, Brüggemann N, Grohmann E. Microbial Risk Assessment of Mature Compost from Human Excreta, Cattle Manure, Organic Waste, and Biochar. Sustainability. 2023; 15(5):4624. https://doi.org/10.3390/su15054624
Chicago/Turabian StyleWerner, Katharina A., Daniela Castro-Herrera, Fantaw Yimer, Menfese Tadesse, Dong-Gill Kim, Katharina Prost, Nicolas Brüggemann, and Elisabeth Grohmann. 2023. "Microbial Risk Assessment of Mature Compost from Human Excreta, Cattle Manure, Organic Waste, and Biochar" Sustainability 15, no. 5: 4624. https://doi.org/10.3390/su15054624