Abstract
Recycling sewage sludge by applying it to agricultural land is strategically important in the European Union and is regulated by Directive 86/278/EEC, aimed at protecting the soil and humans from the presence of unwanted substances. However, because of the ruminant feeding habits, there is a risk that animals grazed on pasture or fed crops grown on land treated in this way may ingest biosolids adhered to foliage and/or on the top soil. This paper describes an episode of toxicity in a dairy herd consuming silage from a field fertilized with sewage sludge produced in a wastewater treatment plant. The affected cows were recumbent, unable to rise and suffered diarrhoea. Analysis of tissues (fresh weight) from a cow that subsequently died revealed severe hepatic iron loading (6720 mg/kg) and secondary multi-trace element hepatic deficiency, particularly of copper (0.812 mg/kg) and manganese (0.436 mg/kg), but also selenium (0.164 mg/kg) and zinc (19.9 mg/kg). The study findings indicate that the use of sewage sludge in agriculture can cause secondary multi-trace element deficiencies in ruminants. Careful attention should be taken when crops are ensilaged avoiding top-soil sewage sludge contamination, since the acidification process may greatly increase Fe bioavailability.
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References
Borreani G, Tabacco E, Schmidt RJ, Holmes BJ, Muck RE (2018) Silage review: factors affecting dry matter and quality losses in silages. J Dairy Sci 101:3952–3979. https://doi.org/10.3168/jds.2017-13837
Bożym M, Siemiątkowski G (2018) Characterization of composted sewage sludge during the maturation process: a pilot scale study. Environ Sci Pollut Res 25:34332–34342. https://doi.org/10.1007/s11356-018-3335-x
Campbell AG, Coup MR, Bishop WH, Wright DE (1974) Effect of elevated iron intake on the copper status of grazing cattle. New Zeal J Agric Res 17:393–399. https://doi.org/10.1080/00288233.1974.10421023
Cherfouh R, Lucas Y, Derridj A, Merdy P (2018) Long-term, low technicality sewage sludge amendment and irrigation with treated wastewater under Mediterranean climate: impact on agronomical soil quality. Environ Sci Pollut Res 25:35571–35581. https://doi.org/10.1007/s11356-018-3463-3
Sousa IKF De, Minervino AH, Sousa RDS, et al (2012) Copper deficiency in sheep with high liver iron accumulation Vet Med Int 2012. https://doi.org/10.1155/2012/207950
Eriksson J (2001) Concentration of 61 trace elements in sewage sludge, farmyard manure, mineral fertiliser, precipitation and in soil and crops, Report 5159, Swedish Environmental Protection Agency. Stockholm 2001
European Commission (1986) 86/278/EEC. Off J Eur Commun 6–12
Fytianos K, Voudrias E, Raikos N (1998) Modelling of phosphorus removal from aqueous and wastewater samples using ferric iron. Environ Pollut 101:123–130. https://doi.org/10.1016/S0269-7491(98)00007-4
Fytili D, Zabaniotou A (2008) Utilization of sewage sludge in EU application of old and new methods-a review. Renew Sust Energ Rev 12:116–140
Gordeuk VR, Bacon BR, Brittenham GM (1987) Iron overload: causes and consequences. Annu Rev Nutr 7:485–508
Gould L, Kendall NR (2011) Role of the rumen in copper and thiomolybdate absorption. Nutr Res Rev 24:176–182
Hansen SL, Spears JW (2009) Bioaccessibility of iron from soil is increased by silage fermentation. J Dairy Sci 92:2896–2905. https://doi.org/10.3168/jds.2008-1933
Herdt TH, Hoff B (2011) The use of blood analysis to evaluate trace mineral status in ruminant livestock. Vet Clin North Am Food Anim Pract 27:255–283. https://doi.org/10.1016/J.CVFA.2011.02.004
Hillman JP, Hill J, Morgan JE, Wilkinson JM (2003) Recycling of sewage sludge to grassland: a review of the legislation to control of the localization and accumulation of potential toxic metals in grazing systems. Grass Forage Sci 58:101–111. https://doi.org/10.1046/j.1365-2494.2003.00365.x
Janas M, Zawadzka A, Cichowicz R (2018) The influence of selected factors on leaching of metals from sewage sludge. Environ Sci Pollut Res 25:33240–33248. https://doi.org/10.1007/s11356-018-3094-8
Kabata-Pendias A (2011) Trace elements in soils and plants
Kaneko JJ, Harvey JW, Bruss ML (2008) Clinical biochemistry of domestic animals
Kent G, Bahu RM (1979) Iron overload. In: MacSween, R.N.M. A, P.P. and Schewr PJ (eds) Pathology of the Liver. Churchill Livingstone, Edinburgh, pp 148–163
Khan ZI, Safdar H, Ahmad K, et al (2019) Health risk assessment through determining bioaccumulation of iron in forages grown in soil irrigated with city effluent. Environ Sci Pollut Res 1–10. https://doi.org/10.1007/s11356-019-04721-1
Lee LH, Wu TY, Shak KPY et al (2018) Sustainable approach to biotransform industrial sludge into organic fertilizer via vermicomposting: a mini-review. J Chem Technol Biotechnol 93:925–935
Lim SL, Lee LH, Wu TY (2016) Sustainability of using composting and vermicomposting technologies for organic solid waste biotransformation: recent overview, greenhouse gases emissions and economic analysis. J Clean Prod 111:262–278
López-Alonso M (2012) Trace minerals and livestock: not too much not too little. ISRN Vet Sci 2012:1–18. https://doi.org/10.5402/2012/704825
Lu Q, He ZL, Stoffella PJ (2012) Land application of biosolids in the USA: a review. Appl Environ Soil Sci. https://doi.org/10.1155/2012/201462
Luna D, Miranda M, Minervino AHH, Piñeiro V, Herrero-Latorre C, López-Alonso M (2019) Validation of a simple sample preparation method for multielement analysis of bovine serum. PLoS One 14:e0211859. https://doi.org/10.1371/journal.pone.0211859
Minervino AHH, López-Alonso M, Barrêto Júnior RA et al (2018) Dietary zinc supplementation to prevent chronic copper poisoning in sheep. Animals 8:227. https://doi.org/10.3390/ani8120227
Mosquera-Losada R, Amador-García A, Muñóz-Ferreiro N et al (2017) Sustainable use of sewage sludge in acid soils within a circular economy perspective. CATENA 149:341–348. https://doi.org/10.1016/J.CATENA.2016.10.007
Nardis BO, Silva EB, Grazziotti PH, Alleoni LRF, Melo LCA, Farnezi MMM (2018) Availability and zinc accumulation in forage grasses grown in contaminated soil. Int J Phytoremed 20:205–213. https://doi.org/10.1080/15226514.2017.1365347
NRC (2001) Requirements of dairy cattle seventh revised edition, 2001
NRC (2005) Mineral tolerance of animals: Second Revised Edition
Orjales I, Herrero-Latorre C, Miranda M, Rey-Crespo F, Rodríguez-Bermúdez R, López-Alonso M (2018) Evaluation of trace element status of organic dairy cattle. Animal 12:1296–1305. https://doi.org/10.1017/S1751731117002890
Ottosen LM, Kirkelund GM, Jensen PE (2013) Extracting phosphorous from incinerated sewage sludge ash rich in iron or aluminum. Chemosphere 91:963–969. https://doi.org/10.1016/j.chemosphere.2013.01.101
Puls R (1994) Mineral levels in animal health, second. Clearbrook: Sherpa International, Canada
RD 1310/1990 (1990) Royal Decree 1310/1990, of 29 October 1990, concerning the correct use of sewage sludge in agriculture
Sas B (1989) Secondary copper deficiency in cattle caused by molybdenum contamination of fodder: a case history. Vet Hum Toxicol 1:29–33
Suttle NF (2010) Mineral nutrition of livestock: Fourth edition
Thornton I, Abrahams P (1983) Soil ingestion - a major pathway of heavy metals into livestock grazing contaminated land. Sci Total Environ. https://doi.org/10.1016/S0048-9697(83)80026-6
Tlustoš P, Hejcman M, Hůlka M, Patáková M, Kunzová E, Száková J (2016) Mobility and plant availability of risk elements in soil after long-term application of farmyard manure. Environ Sci Pollut Res 23:23561–23572. https://doi.org/10.1007/s11356-016-7592-2
Acknowledgments
AHHM is grateful to Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq, for his research productivity fellowship. The authors thank Lucia Casanova Iglesias and staff of RIAIDT for their technical assistance. The English grammar of the text was revised by Christine Francis.
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Miranda, M., Méndez, L., Pereira, V. et al. Iron loading and secondary multi-trace element deficiency in a dairy herd fed silage grass grown on land fertilized with sewage sludge. Environ Sci Pollut Res 26, 36978–36984 (2019). https://doi.org/10.1007/s11356-019-06828-x
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DOI: https://doi.org/10.1007/s11356-019-06828-x