Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

A One Health approach to managing the applications and implications of nanotechnologies in agriculture

Abstract

The need for appropriate science and regulation to underpin nanosafety is greater than ever as ongoing advances in nanotechnology are rapidly translated into new industrial applications and nano-enabled commercial products. Nevertheless, a disconnect persists between those examining risks to human and environmental health from nanomaterials. This disconnect is not atypical in research and risk assessment and has been perpetuated in the case of engineered nanomaterials by the relatively limited overlap in human and environmental exposure pathways. The advent of agri-nanotechnologies brings both increased need and opportunity to change this status quo as it introduces significant issues of intersectionality that cannot adequately be addressed by current discipline-specific approaches alone. Here, focusing on the specific case of nanoparticles, we propose that a transdisciplinary approach, underpinned by the One Health concept, is needed to support the sustainable development of these technologies.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Human and environmental exposure pathways not considering agri-nanotechnology.
Fig. 2
Fig. 3: A possible One Health framework for the risk assessment of agri-nanotechnologies.

Similar content being viewed by others

References

  1. Wang, J. X. et al. Translocation of inhaled TiO2 nanoparticles along olfactory nervous system to brain studied by synchrotron radiation X-ray fluorescence. High. Energy Phys. Nucl. Phys. 29, 76–79 (2005).

    CAS  Google Scholar 

  2. Sun, T. Y., Bornhöft, N. A., Hungerbühler, K. & Nowack, B. Dynamic probabilistic modeling of environmental emissions of engineered nanomaterials. Environ. Sci. Technol. 50, 4701–4711 (2016).

    CAS  Google Scholar 

  3. Bardos, P., Merly, C., Kvapil, P. & Koschitzky, H. P. Status of nanoremediation and its potential for future deployment: risk–benefit and benchmarking appraisals. Remediation 28, 43–56 (2018).

    Google Scholar 

  4. Wang, P., Lombi, E., Zhao, F. J. & Kopittke, P. M. Nanotechnology: a new opportunity in plant sciences. Trends Plant Sci. 21, 699–712 (2016).

    CAS  Google Scholar 

  5. Wickson, F., Carew, A. L. & Russell, A. W. Transdisciplinary research: characteristics, quandaries and quality. Futures 38, 1046–1059 (2006).

    Google Scholar 

  6. Future and emerging technologies. European Commission (20 February 2019); http://ec.europa.eu/programmes/horizon2020/en/h2020-section/future-and-emerging-technologies

  7. Stone, V. et al. The essential elements of a risk governance framework for current and future nanotechnologies. Risk Anal. 38, 1321–1331 (2018).

    Google Scholar 

  8. Teunenbroek, T. V., Baker, J. & Dijkzeul, A. Towards a more effective and efficient governance and regulation of nanomaterials. Part. Fibre Toxicol. 14, 54 (2017).

    Google Scholar 

  9. Kraegeloh, A., Suarez-Merino, B., Sluijters, T. & Micheletti, C. Implementation of safe-by-design for nanomaterial development and safe innovation: why we need a comprehensive approach. Nanomaterials 8, 239 (2018).

    Google Scholar 

  10. Hjorth, R., van Hove, L. & Wickson, F. What can nanosafety learn from drug development? The feasibility of “safety by design”. Nanotoxicology 11, 305–312 (2017).

    Google Scholar 

  11. Karcher, S. et al. Integration among databases and data sets to support productive nanotechnology: challenges and recommendations. NanoImpact 9, 85–101 (2018).

    Google Scholar 

  12. Risk Governance of nanotechnology (RIA). European Commission (27 October 2017); http://ec.europa.eu/research/participants/portal/desktop/en/opportunities/h2020/topics/nmbp-13-2018.html

  13. Haas, P. M. Do regimes matter? Epistemic communities and mediterranean pollution control. Int. Organ. 43, 377–403 (1989).

    Google Scholar 

  14. Haas, P. M. Introduction: epistemic communities and international policy coordination. Int. Organ. 46, 1–35 (1992).

    Google Scholar 

  15. Bos, P. M. J. et al. The MARINA risk assessment strategy: a flexible strategy for efficient information collection and risk assessment of nanomaterials. Int. J. Environ. Res. Public Health 12, 15007–15021 (2015).

    Google Scholar 

  16. Owen, R. & Handy, R. Formulating the problems for environmental risk assessment of nanomaterials. Environ. Sci. Technol. 41, 5582–5588 (2007).

    Google Scholar 

  17. Silva, T. et al. Particle size, surface charge and concentration dependent ecotoxicity of three organo-coated silver nanoparticles: comparison between general linear model-predicted and observed toxicity. Sci. Total Environ. 468–469, 968–976 (2014).

    Google Scholar 

  18. Espinasse, B. P. et al. Comparative persistence of engineered nanoparticles in a complex aquatic ecosystem. Environ. Sci. Technol. 52, 4072–4078 (2018).

    CAS  Google Scholar 

  19. Malysheva, A., Voelcker, N., Holm, P. E. & Lombi, E. Unraveling the complex behavior of AgNPs driving NP-cell interactions and toxicity to algal cells. Environ. Sci. Technol. 50, 12455–12463 (2016).

    CAS  Google Scholar 

  20. Levard, C. et al. Sulfidation of silver nanoparticles: natural antidote to their toxicity. Environ. Sci. Technol. 47, 13440–13448 (2013).

    CAS  Google Scholar 

  21. Lombi, E. et al. Transformation of four silver/silver chloride nanoparticles during anaerobic treatment of wastewater and post-processing of sewage sludge. Environ. Pollut. 176, 193–197 (2013).

    CAS  Google Scholar 

  22. Pulido-Reyes, G., Leganes, F., Fernández-Piñas, F. & Rosal, R. Bio-nano interface and environment: a critical review. Environ. Toxicol. Chem. 36, 3181–3193 (2017).

    CAS  Google Scholar 

  23. Gottschalk, F., Sonderer, T., Scholz, R. W. & Nowack, B. Modeled environmental concentrations of engineered nanomaterials (TiO2, ZnO, Ag, CNT, fullerenes) for different regions. Environ. Sci. Technol. 43, 9216–9222 (2009).

    CAS  Google Scholar 

  24. Maynard, A. D. Old materials, new challenges? Nat. Nanotechnol. 9, 658–659 (2014).

    CAS  Google Scholar 

  25. Nowack, B. et al. Progress towards the validation of modeled environmental concentrations of engineered nanomaterials by analytical measurements. Environ. Sci. Nano 2, 421–428 (2015).

    CAS  Google Scholar 

  26. Gondikas, A. et al. Where is the nano? Analytical approaches for the detection and quantification of TiO2 engineered nanoparticles in surface waters. Environ. Sci. Nano 5, 313–326 (2018).

    CAS  Google Scholar 

  27. Kühnel, D. & Nickel, C. The OECD expert meeting on ecotoxicology and environmental fate: towards the development of improved OECD guidelines for the testing of nanomaterials. Sci. Total Environ. 472, 347–353 (2014).

    Google Scholar 

  28. Miller, G. & Wickson, F. Risk analysis of nanomaterials: exposing nanotechnology’s naked emperor. Rev. Pol. Res. 32, 485–512 (2015).

    Google Scholar 

  29. Dusinska, M. et al. Towards an alternative testing strategy for nanomaterials used in nanomedicine: lessons from NanoTEST. Nanotoxicology 9, 118–132 (2015).

    CAS  Google Scholar 

  30. Dusinska, M. et al. Immunotoxicity, genotoxicity and epigenetic toxicity of nanomaterials: new strategies for toxicity testing? Food Chem. Toxicol. 109, 797–811 (2017).

    CAS  Google Scholar 

  31. Smolkova, B., Dusinska, M. & Gabelova, A. Nanomedicine and epigenome. Possible health risks. Food Chem. Toxicol. 109, 780–796 (2017).

    CAS  Google Scholar 

  32. Zhou, G. & Hu, W. Public acceptance of and willingness-to-pay for nanofoods in the U. S. Food Control 89, 219–226 (2018).

    Google Scholar 

  33. Sohal, I. S., O’Fallon, K. S., Gaines, P., Demokritou, P. & Bello, D. Ingested engineered nanomaterials: state of science in nanotoxicity testing and future research needs. Part. Fibre Toxicol. 15, 29 (2018).

    Google Scholar 

  34. Bettini, S. et al. Food-grade TiO2 impairs intestinal and systemic immune homeostasis, initiates preneoplastic lesions and promotes aberrant crypt development in the rat colon. Sci. Rep. 7, 40373 (2017).

    CAS  Google Scholar 

  35. France Plans to ban Titanium Dioxide in Food Products (USDA, 2018).

  36. Missaoui, W. N., Arnold, R. D. & Cummings, B. S. Toxicological status of nanoparticles: what we know and what we don’t know. Chem.-Biol. Interact. 295, 1–12 (2018).

    CAS  Google Scholar 

  37. Patzelt, A. et al. Do nanoparticles have a future in dermal drug delivery? J. Control. Release 246, 174–182 (2017).

    CAS  Google Scholar 

  38. Bakand, S. & Hayes, A. Toxicological considerations, toxicity assessment, and risk management of inhaled nanoparticles. Int. J. Mol. Sci. 17, 929 (2016).

    Google Scholar 

  39. Fröhlich, E. & Roblegg, E. Oral uptake of nanoparticles: human relevance and the role of in vitro systems. Arch. Toxicol. 90, 2297–2314 (2016).

    Google Scholar 

  40. Sun, T. Y. et al. Probabilistic modelling of engineered nanomaterial emissions to the environment: a spatio-temporal approach. Environ. Sci. Nano 2, 340–351 (2015).

    CAS  Google Scholar 

  41. Malysheva, A., Lombi, E. & Voelcker, N. H. Bridging the divide between human and environmental nanotoxicology. Nat. Nanotechnol. 10, 835–844 (2015).

    CAS  Google Scholar 

  42. Huggett, D. B., Cook, J. C., Ericson, J. F. & Williams, R. T. A theoretical model for utilizing mammalian pharmacology and safety data to prioritize potential impacts of human pharmaceuticals to fish. Hum. Ecol. Risk Assess. 9, 1789–1799 (2003).

    CAS  Google Scholar 

  43. Williams, M., Saison, C. L. A., Williams, D. B. & Kookana, R. S. Can aquatic distribution of human pharmaceuticals be related to pharmacological data? Chemosphere 65, 2253–2259 (2006).

    CAS  Google Scholar 

  44. Scott-Fordsmand, J. J. et al. Environmental risk assessment strategy for nanomaterials. Int. J. Environ. Res. Public Health 14, 1251 (2017).

    Google Scholar 

  45. One Health: A New Professional Imperative (American Veterinary Medical Association, 2015).

  46. Global Action Plan on Antimicrobial Resistance (WHO, 2015).

  47. McEwen, S. A. & Collignon, P. J. Antimicrobial resistance: a One Health perspective. Microbiol. Spectr. https://doi.org/10.1128/microbiolspec.ARBA-0009-2017 (2018).

    Article  Google Scholar 

  48. Antibiotic Resistance Threats in the United States (Centers for Disease Control and Prevention, US Department of Health and Human Services, 2013).

  49. Lammie, S. L. & Hughes, J. M. Antimicrobial resistance, food safety, and One Health: the need for convergence. Annu. Rev. Food Sci. Technol. 7, 287–312 (2016).

    CAS  Google Scholar 

  50. CVM Updates: CVM Reports on Antimicrobials Sold or Distributed for Food-Producing Animals (FDA, 2010).

  51. Van Boeckel, T. P. et al. Global trends in antimicrobial use in food animals. Proc. Natl Acad. Sci. USA 112, 5649–5654 (2015).

    Google Scholar 

  52. Zhu, Y. G. et al. Continental-scale pollution of estuaries with antibiotic resistance genes. Nat. Microbiol. 2, 16270 (2017).

    CAS  Google Scholar 

  53. Gillings, M. R. Evolutionary consequences of antibiotic use for the resistome, mobilome, and microbial pangenome. Front. Microbiol. https://doi.org/10.3389/fmicb.2013.00004 (2013).

  54. Shepon, A., Eshel, G., Noor, E. & Milo, R. The opportunity cost of animal based diets exceeds all food losses. Proc. Natl Acad. Sci. USA 115, 3804–3809 (2018).

    CAS  Google Scholar 

  55. Mission Statement. One Health Initiative (2016); http://www.onehealthinitiative.com/mission.php

  56. Boqvist, S., Söderqvist, K. & Vågsholm, I. Food safety challenges and One Health within Europe. Acta Vet. Scand. 60, 1 (2018).

    Google Scholar 

  57. Wegener, H. in Improving Food Safaety Through a One Health Approach (eds Relman, D. A. et al.) 331–349 (National Academies Press, 2012).

  58. Lebov, J. et al. A framework for One Health research. One Health 3, 44–50 (2017).

    CAS  Google Scholar 

  59. Choi, B. C. K. & Pak, A. W. P. Multidisciplinarity, interdisciplinarity and transdisciplinarity in health research, services, education and policy: 1. Definitions, objectives, and evidence of effectiveness. Clin. Investig. Med. 29, 351–364 (2006).

    Google Scholar 

  60. Wickson, F. & Carew, A. L. Quality criteria and indicators for responsible research and innovation: learning from transdisciplinarity. J. Respons. Innov. 1, 254–273 (2014).

    Google Scholar 

  61. Joffe, M., Gambhir, M., Chadeau-Hyam, M. & Vineis, P. Causal diagrams in systems epidemiology. Emerg. Themes Epidemiol. 9, 1 (2012).

    Google Scholar 

  62. Rezaei, A. Food safety: the farmer first health paradigm. One Health 5, 69–73 (2018).

    Google Scholar 

  63. Owen, R., Bessant, J. & Heintz, M. Responsible Innovation: Managing the Responsible Emergence of Science and Innovation in Society (Wiley, 2013).

  64. Stilgoe, J., Owen, R. & Macnaghten, P. Developing a framework for responsible innovation. Res. Pol. 42, 1568–1580 (2013).

    Google Scholar 

  65. Burgess, J. et al. Deliberative mapping: a novel analytic-deliberative methodology to support contested science-policy decisions. Public Underst. Sci. 16, 299–322 (2007).

    Google Scholar 

  66. Grieger, K. D., Linkov, I., Hansen, S. F. & Baun, A. Environmental risk analysis for nanomaterials: review and evaluation of frameworks. Nanotoxicology 6, 196–212 (2012).

    Google Scholar 

  67. Kuzma, J., Romanchek, J. & Kokotovich, A. Upstream oversight assessment for agrifood nanotechnology: a case studies approach. Risk Anal. 28, 1081–1098 (2008).

    Google Scholar 

  68. Renn, O. A model for an analytic–deliberative process in risk management. Environ. Sci. Technol. 33, 3049–3055 (1999).

    CAS  Google Scholar 

  69. Gubala, V. et al. Engineered nanomaterials and human health: Part 2. Applications and nanotoxicology (IUPAC Technical Report). Pure Appl. Chem. 90, 1325–1356 (2018).

    CAS  Google Scholar 

  70. Ivask, A., Mitchell, A. J., Malysheva, A., Voelcker, N. H. & Lombi, E. Methodologies and approaches for the analysis of cell–nanoparticle interactions. Wiley Inter. Rev. Nanomed. Nanobiotechnol. 10, e1486 (2018).

    Google Scholar 

  71. Du, J. et al. ZnO nanoparticles: recent advances in ecotoxicity and risk assessment. Drug Chem. Toxicol. https://doi.org/10.1080/01480545.2018.1508218 (2018).

  72. Du, J. et al. A review on silver nanoparticles-induced ecotoxicity and the underlying toxicity mechanisms. Regul. Toxicol. Pharmacol. 98, 231–239 (2018).

    CAS  Google Scholar 

  73. Bondarenko, O. et al. Toxicity of Ag, CuO and ZnO nanoparticles to selected environmentally relevant test organisms and mammalian cells in vitro: A critical review. Arch. Toxicol. 87, 1181–1200 (2013).

    CAS  Google Scholar 

  74. Guadagnini, R. et al. Toxicity screenings of nanomaterials: challenges due to interference with assay processes and components of classic in vitro tests. Nanotoxicology 9, 13–24 (2015).

    CAS  Google Scholar 

  75. Ivask, A. et al. Complete transformation of ZnO and CuO nanoparticles in culture medium and lymphocyte cells during toxicity testing. Nanotoxicology 11, 150–156 (2017).

    CAS  Google Scholar 

  76. Sekine, R., Khurana, K., Vasilev, K., Lombi, E. & Donner, E. Quantifying the adsorption of ionic silver and functionalized nanoparticles during ecotoxicity testing: test container effects and recommendations. Nanotoxicology 9, 1005–1012 (2015).

    Google Scholar 

  77. Malta Initiative Workshop Brussels. Nanosafety Cluster (11 December 2018); https://www.nanosafetycluster.eu/calendar/318/162-Malta-Initiative-Workshop.html

  78. Le, T. C. et al. An experimental and computational approach to the development of ZnO nanoparticles that are safe by design. Small 12, 3568–3577 (2016).

    CAS  Google Scholar 

  79. Lynch, I. European NanoSafety Cluster Compendium. NanoSafety Cluster (2016); http://www.nanosafetycluster.eu/www.nanosafetycluster.eu/home/european-nanosafety-cluster-compendium.html

  80. Singh, R. & Lillard, J. W. Jr Nanoparticle-based targeted drug delivery. Exp. Mol. Pathol. 86, 215–223 (2009).

    CAS  Google Scholar 

  81. Mitter, N. et al. Clay nanosheets for topical delivery of RNAi for sustained protection against plant viruses. Nat. Plants 3, 16207 (2017).

    CAS  Google Scholar 

  82. Kah, M., Kookana, R. S., Gogos, A. & Bucheli, T. D. A critical evaluation of nanopesticides and nanofertilizers against their conventional analogues. Nat. Nanotechnol. 13, 677–684 (2018).

    CAS  Google Scholar 

  83. White, J. G.-T. J. Achieving food security through the very small. Nat. Nanotechnol. 13, 627–629 (2018).

    CAS  Google Scholar 

  84. Wickson, F., Delgado, A. & Kjølberg, K. L. Who or what is ‘the public’? Nat. Nanotechnol. 5, 757–758 (2010).

    CAS  Google Scholar 

  85. Lyons, K. & Whelan, J. Community engagement to facilitate, legitimize and accelerate the advancement of nanotechnologies in Australia. NanoEthics 4, 53–66 (2010).

    Google Scholar 

  86. Delgado, A., Kjølberg, K. L. & Wickson, F. Public engagement coming of age: from theory to practice in STS encounters with nanotechnology. Public Underst. Sci. 20, 826–845 (2011).

    Google Scholar 

  87. Kearnes, M., Grove-White, R., Macnaghten, P., Wilsdon, J. & Wynne, B. From bio to nano: learning lessons from the UK agricultural biotechnology controversy. Sci. Cult. 15, 291–307 (2006).

    Google Scholar 

  88. Petersen, A. & Bowman, D. Engaging whom and for what ends? Australian stakeholders’ constructions of public engagement in relation to nanotechnologies. Ethics Sci. Environ. Polit. 12, 67–79 (2012).

    Google Scholar 

  89. Toumey, C. Rules of engagement. Nat. Nanotechnol. 2, 386–387 (2007).

    CAS  Google Scholar 

  90. Akin, H. et al. Are attitudes toward labeling nano products linked to attitudes toward GMO? Exploring a potential ‘spillover’ effect for attitudes toward controversial technologies. J. Respons. Innov. 6, 50–74 (2018).

    Google Scholar 

  91. Dudo, A., Choi, D. H. & Scheufele, D. A. Food nanotechnology in the news. Coverage patterns and thematic emphases during the last decade. Appetite 56, 78–89 (2011).

    Google Scholar 

  92. Felt, U., Schumann, S. & Schwarz, C. G. (Re)assembling natures, cultures, and (nano)technologies in public engagement. Sci. Cult. 24, 458–483 (2015).

    Google Scholar 

  93. Siegrist, M., Stampfli, N., Kastenholz, H. & Keller, C. Perceived risks and perceived benefits of different nanotechnology foods and nanotechnology food packaging. Appetite 51, 283–290 (2008).

    Google Scholar 

  94. Sozer, N. & Kokini, J. L. Nanotechnology and its applications in the food sector. Trends Biotechnol. 27, 82–89 (2009).

    CAS  Google Scholar 

  95. Ganesh Pillai, R. & Bezbaruah, A. N. Perceptions and attitude effects on nanotechnology acceptance: an exploratory framework. J. Nanopart. Res. 19, 41 (2017).

    Google Scholar 

  96. Sodano, V., Gorgitano, M. T., Verneau, F. & Vitale, C. D. Consumer acceptance of food nanotechnology in Italy. Brit. Food J. 118, 714–733 (2016).

    Google Scholar 

  97. Frewer, L. J. Consumer acceptance and rejection of emerging agrifood technologies and their applications. Eur. Rev. Agric. Econ. 44, 683–704 (2017).

    Google Scholar 

  98. Sodano, V. Food nanotechnologies and policy challenges. Environ. Chem. Lett. 16, 5–10 (2018).

    CAS  Google Scholar 

  99. Lyons, K. & Smith, N. Governing with Ignorance: understanding the Australian Food Regulator’s response to nano food. NanoEthics 12, 27–38 (2018).

    Google Scholar 

  100. Beketov, M. A., Kefford, B. J., Schäfer, R. B. & Liess, M. Pesticides reduce regional biodiversity of stream invertebrates. Proc. Natl Acad. Sci. USA 110, 11039–11043 (2013).

    CAS  Google Scholar 

  101. Destoumieux-Garzón, D. et al. The one health concept: 10 years old and a long road ahead. Front. Vet. Sci. https://doi.org/10.3389/fvets.2018.00014 (2018).

Download references

Acknowledgements

M.D. is grateful for support from the Horizon 2020 NANoREG2 projects (H2020-NMP-2014-2015- 646221) and RiskGONE (H2020-NMBP-TO-IND-2018-814425). F.W. acknowledges support from the European Union’s Horizon 2020 research and innovation programme for the New HoRRIzon project under grant agreement no. 741402. E.D. gratefully acknowledges support from the Australian Research Council through the ARC Future Fellowship Scheme (FT130101003). We thank M. Cicera for refining the figures.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Enzo Lombi.

Additional information

Journal peer review information: Nature Nanotechnology thanks Kristen Lyons and the other anonymous reviewer(s) for their contribution to the peer review of this work.

Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lombi, E., Donner, E., Dusinska, M. et al. A One Health approach to managing the applications and implications of nanotechnologies in agriculture. Nat. Nanotechnol. 14, 523–531 (2019). https://doi.org/10.1038/s41565-019-0460-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41565-019-0460-8

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing