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Othmane Friha, Mohamed Amine Ferrag, Lei Shu, Leandros Maglaras, and Xiaochan Wang, "Internet of Things for the Future of Smart Agriculture: A Comprehensive Survey of Emerging Technologies," vol. 8, no. 4, pp. 718-752, Apr. 2021. doi:

Othmane Friha, Mohamed Amine Ferrag, Lei Shu, Leandros Maglaras, and Xiaochan Wang, "Internet of Things for the Future of Smart Agriculture: A Comprehensive Survey of Emerging Technologies," vol. 8, no. 4, pp. 718-752, Apr. 2021. doi:

Internet of Things for the Future of Smart Agriculture: A Comprehensive Survey of Emerging Technologies

Doi:  10.1109/jas.2021.1003925.

• Othmane Friha 1 ,  , 
• Mohamed Amine Ferrag 2 ,  , 
• Lei Shu 3, 4 ,  ,  , 
• Leandros Maglaras 5 ,  , 
• Xiaochan Wang 6 , 

Networks and Systems Laboratory, University of Badji Mokhtar-Annaba, Annaba 23000, Algeria

Department of Computer Science, Guelma University, Gulema 24000, Algeria

College of Engineering, Nanjing Agricultural University, Nanjing 210095, China

School of Engineering, University of Lincoln, Lincoln LN67TS, UK

School of Computer Science and Informatics, De Montfort University, Leicester LE1 9BH, UK

Department of Electrical Engineering, Nanjing Agricultural University, Nanjing 210095, China

Othmane Friha received the master degree in computer science from Badji Mokhtar-Annaba University, Algeria, in 2018. He is currently working toward the Ph.D. degree in the University of Badji Mokhtar-Annaba, Algeria. His current research interests include network and computer security, internet of things (IoT), and applied cryptography

Mohamed Amine Ferrag received the bachelor degree (June, 2008), master degree (June, 2010), Ph.D. degree (June, 2014), HDR degree (April, 2019) from Badji Mokhtar-Annaba University, Algeria, all in computer science. Since October 2014, he is a Senior Lecturer at the Department of Computer Science, Guelma University, Algeria. Since July 2019, he is a Visiting Senior Researcher, NAULincoln Joint Research Center of Intelligent Engineering, Nanjing Agricultural University. His research interests include wireless network security, network coding security, and applied cryptography. He is featured in Stanford University’s list of the world’s Top 2% Scientists for the year 2019. He has been conducting several research projects with international collaborations on these topics. He has published more than 60 papers in international journals and conferences in the above areas. Some of his research findings are published in top-cited journals, such as the IEEE Communications Surveys and Tutorials , IEEE Internet of Things Journal , IEEE Transactions on Engineering Management , IEEE Access , Journal of Information Security and Applications (Elsevier), Transactions on Emerging Telecommunications Technologies (Wiley), Telecommunication Systems (Springer), International Journal of Communication Systems (Wiley), Sustainable Cities and Society (Elsevier), Security and Communication Networks (Wiley), and Journal of Network and Computer Applications (Elsevier). He has participated in many international conferences worldwide, and has been granted short-term research visitor internships to many renowned universities including, De Montfort University, UK, and Istanbul Technical University, Turkey. He is currently serving on various editorial positions such as Editorial Board Member in Journals (Indexed SCI and Scopus) such as, IET Networks and International Journal of Internet Technology and Secured Transactions (Inderscience Publishers)

Lei Shu (M’07–SM’15) received the B.S. degree in computer science from South Central University for Nationalities in 2002, and the M.S. degree in computer engineering from Kyung Hee University, South Korea, in 2005, and the Ph.D. degree from the Digital Enterprise Research Institute, National University of Ireland, Ireland, in 2010. Until 2012, he was a Specially Assigned Researcher with the Department of Multimedia Engineering, Graduate School of Information Science and Technology, Osaka University, Japan. He is currently a Distinguished Professor with Nanjing Agricultural University and a Lincoln Professor with the University of Lincoln, U.K. He is also the Director of the NAU-Lincoln Joint Research Center of Intelligent Engineering. He has published over 400 papers in related conferences, journals, and books in the areas of sensor networks and internet of things (IoT). His current H-index is 54 and i10-index is 197 in Google Scholar Citation. His current research interests include wireless sensor networks and IoT. He has also served as a TPC Member for more than 150 conferences, such as ICDCS, DCOSS, MASS, ICC, GLOBECOM, ICCCN, WCNC, and ISCC. He was a Recipient of the 2014 Top Level Talents in Sailing Plan of Guangdong Province, China, the 2015 Outstanding Young Professor of Guangdong Province, and the GLOBECOM 2010, ICC 2013, ComManTel 2014, WICON 2016, SigTelCom 2017 Best Paper Awards, the 2017 and 2018 IEEE Systems Journal Best Paper Awards, the 2017 Journal of Network and Computer Applications Best Research Paper Award, and the Outstanding Associate Editor Award of 2017, and the 2018 IEEE ACCESS. He has also served over 50 various Co-Chair for international conferences/workshops, such as IWCMC, ICC, ISCC, ICNC, Chinacom, especially the Symposium Co-Chair for IWCMC 2012, ICC 2012, the General Co-Chair for Chinacom 2014, Qshine 2015, Collaboratecom 2017, DependSys 2018, and SCI 2019, the TPC Chair for InisCom 2015, NCCA 2015, WICON 2016, NCCA 2016, Chinacom 2017, InisCom 2017, WMNC 2017, and NCCA 2018

Leandros Maglaras (SM’15) received the B.Sc. degree from Aristotle University of Thessaloniki, Greece, in 1998, M.Sc. in industrial production and management from University of Thessaly in 2004, and M.Sc. and Ph.D. degrees in electrical & computer engineering from University of Volos in 2008 and 2014, respectively. He is the Head of the National Cyber Security Authority of Greece and a Visiting Lecturer in the School of Computer Science and Informatics at the De Montfort University, U.K. He serves on the Editorial Board of several International peer-reviewed journals such as IEEE Access , Wiley Journal on Security & Communication Networks , EAI Transactions on e-Learning and EAI Transactions on Industrial Networks and Intelligent Systems . He is an author of more than 80 papers in scientific magazines and conferences and is a Senior Member of IEEE. His research interests include wireless sensor networks and vehicular ad hoc networks

Xiaochan Wang is currently a Professor in the Department of Electrical Engineering at Nanjing Agricultural University. His main research fields include intelligent equipment for horticulture and intelligent measurement and control. He is an ASABE Member, and the Vice Director of CSAM (Chinese Society for Agricultural Machinery), and also the Senior Member of Chinese Society of Agricultural Engineering. He was awarded the Second Prize of Science and Technology Invention by the Ministry of Education (2016) and the Advanced Worker for Chinese Society of Agricultural Engineering (2012), and he also gotten the “Blue Project” in Jiangsu province young and middle-aged academic leaders (2010)

• Corresponding author: Lei Shu, e-mail: [email protected]
• Revised Date: 2020-11-25
• Accepted Date: 2020-12-30
• Agricultural internet of things (IoT) , 
• internet of things (IoT) , 
• smart agriculture , 
• smart farming , 
• sustainable agriculture

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On-Farm Experimentation to transform global agriculture

• Myrtille Lacoste   ORCID: orcid.org/0000-0001-6557-1865 1 , 2 ,
• Simon Cook   ORCID: orcid.org/0000-0003-0902-1476 1 , 3 ,
• Matthew McNee 4 ,
• Danielle Gale   ORCID: orcid.org/0000-0003-3733-025X 1 ,
• Julie Ingram   ORCID: orcid.org/0000-0003-0712-4789 5 ,
• Véronique Bellon-Maurel 6 , 7 ,
• Tom MacMillan   ORCID: orcid.org/0000-0002-2893-6981 8 ,
• Roger Sylvester-Bradley 9 ,
• Daniel Kindred   ORCID: orcid.org/0000-0001-7910-7676 9 ,
• Rob Bramley   ORCID: orcid.org/0000-0003-0643-7409 10 ,
• Nicolas Tremblay   ORCID: orcid.org/0000-0003-1409-4442 11 ,
• Louis Longchamps   ORCID: orcid.org/0000-0002-4761-6094 12 ,
• Laura Thompson   ORCID: orcid.org/0000-0001-5751-7869 13 ,
• Julie Ruiz   ORCID: orcid.org/0000-0001-5672-2705 14 ,
• Fernando Oscar García   ORCID: orcid.org/0000-0001-6681-0135 15 , 16 ,
• Bruce Maxwell 17 ,
• Terry Griffin   ORCID: orcid.org/0000-0001-5664-484X 18 ,
• Thomas Oberthür   ORCID: orcid.org/0000-0002-6050-9832 19 , 20 ,
• Christian Huyghe 21 ,
• Weifeng Zhang 22 ,
• John McNamara 23 &
• Andrew Hall   ORCID: orcid.org/0000-0002-8580-6569 24  

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Restructuring farmer–researcher relationships and addressing complexity and uncertainty through joint exploration are at the heart of On-Farm Experimentation (OFE). OFE describes new approaches to agricultural research and innovation that are embedded in real-world farm management, and reflects new demands for decentralized and inclusive research that bridges sources of knowledge and fosters open innovation. Here we propose that OFE research could help to transform agriculture globally. We highlight the role of digitalization, which motivates and enables OFE by dramatically increasing scales and complexity when investigating agricultural challenges.

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Acknowledgements

This study was funded by the Premier’s Agriculture and Food Fellowship Program of Western Australia. This Fellowship is a collaboration between Curtin and Murdoch Universities and the State Government. The Fellowship is the centrepiece of the Science and Agribusiness Connect initiative, made possible by the State Government’s Royalties for Regions program. Additional support was provided by the MAK’IT-FIAS Fellowship programme (Montpellier Advanced Knowledge Institute on Transitions – French Institutes for Advanced Study) co-funded by the University of Montpellier and the European Union’s Horizon 2020 Marie Skłodowska-Curie Actions (co-fund grant agreement no. 945408), the Digital Agriculture Convergence Lab #DigitAg (grant no. ANR-16-CONV-0004) supported by ANR/PIA, and the Elizabeth Creak Charitable Trust. Contributions toward enabling workshops were made by the USDA (USDA AFRI FACT Los Angeles 2017), the International Society for Precision Agriculture (ICPA Montreal 2018 OFE-C, On-Farm Experimentation Community), the National Key Research and Development Program of China (2016YFD0201303) and ADAS (Cambridge 2018), the European Conference for Precision Agriculture (ECPA Montpellier 2019) and the OECD Co-operative Research Program for ‘Biological resource management for sustainable agricultural systems – Transformational technologies and innovation’ towards ‘#OFE2021, the first Conference on farmer-centric On-Farm Experimentation – Digital Tools for a Scalable Transformative Pathway’. L. Tresh assisted with the design and preparation of Figs. 2 and 3. Members of the #OFE2021 Working Groups also contributed their experiences and insights.

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Centre for Digital Agriculture, Curtin University, Perth, Western Australia, Australia

Myrtille Lacoste, Simon Cook & Danielle Gale

Montpellier Advanced Knowledge Institute on Transitions (MAK’IT), University of Montpellier, Montpellier, France

Myrtille Lacoste

Centre for Digital Agriculture, Murdoch University, Perth, Western Australia, Australia

Department of Agriculture, Falkland Islands Government, Stanley, Falkland Islands

Matthew McNee

Countryside and Community Research Institute, University of Gloucestershire, Cheltenham, UK

Julie Ingram

Technologies and methods for the agricultures of tomorrow (ITAP), University of Montpellier–National Research Institute for Agriculture, Food and Environment (INRAE)–L’Institut Agro, Montpellier, France

Véronique Bellon-Maurel

Digital Agriculture Convergence Lab (#DigitAg), National Research Institute for Agriculture, Food and Environment (INRAE), Montpellier, France

Centre for Effective Innovation in Agriculture, Royal Agricultural University, Cirencester, UK

Tom MacMillan

ADAS, Cambridge, UK

Roger Sylvester-Bradley & Daniel Kindred

Commonwealth Scientific and Industrial Research Organisation (CSIRO), Adelaide, South Australia, Australia

Rob Bramley

Saint-Jean-sur-Richelieu Research and Development Centre, Agriculture and Agri-Food Canada (AAFC), St-Jean-sur-Richelieu, Quebec, Canada

Nicolas Tremblay

School of Integrative Plant Science, Cornell University, Ithaca, NY, USA

Louis Longchamps

Institute of Agriculture and Natural Resources, University of Nebraska-Lincoln, Falls City, NE, USA

Laura Thompson

Watershed and Aquatic Ecosystem Interactions Research Centre (RIVE), Université du Québec à Trois-Rivières, Trois-Rivières, Québec, Canada

Latin America Southern Cone Group, International Plant Nutrition Institute (IPNI), Buenos Aires, Argentina

Fernando Oscar García

Faculty of Agricultural Sciences, National University of Mar del Plata, Balcarce, Argentina

Montana Institute on Ecosystems, Montana State University, Bozeman, MT, USA

Bruce Maxwell

Department of Agricultural Economics, Kansas State University, Manhattan, KS, USA

Terry Griffin

Southeast Asia Group, International Plant Nutrition Institute (IPNI), Penang, Malaysia

Thomas Oberthür

Business and Partnership Development, African Plant Nutrition Institute (APNI), Benguérir, Morocco

Scientific Direction of Agriculture, National Research Institute for Agriculture, Food and Environment (INRAE), Paris, France

Christian Huyghe

College of Resources and Environmental Sciences and National Academy of Agriculture Green Development, China Agricultural University, Beijing, China

Weifeng Zhang

National Animal Nutrition Program (NANP), United States Department of Agriculture (USDA), Pullman, WA, USA

John McNamara

Commonwealth Scientific and Industrial Research Organisation (CSIRO), Canberra, Australian Capital Territory, Australia

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Contributions

M.L. and S.C. developed the study concept. M.M., D.G., J.I., V.B.-M., T.M., R.S.-B. and A.H. contributed additional concept development. M.L. and D.G. obtained the data and prepared the results. M.L., M.M., L.T., D.K., F.O.G., B.M., V.B.-M., J.R., C.H. and W.Z. contributed data. M.L. wrote the manuscript with input from all other authors.

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Correspondence to Myrtille Lacoste .

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Lacoste, M., Cook, S., McNee, M. et al. On-Farm Experimentation to transform global agriculture. Nat Food 3 , 11–18 (2022). https://doi.org/10.1038/s43016-021-00424-4

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Issue Date : January 2022

DOI : https://doi.org/10.1038/s43016-021-00424-4

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Farming for Life Quality and Sustainability: A Literature Review of Green Care Research Trends in Europe

Marina garcía-llorente.

1 Department of Applied Research and Agricultural Extension, Madrid Institute for Rural, Agricultural and Food Research and Development (IMIDRA), Finca Experimental ‘‘El Encín’’Ctra N-II, Km 38, Madrid 28800, Spain

Radha Rubio-Olivar

2 Social-Ecological Systems Laboratory, Department of Ecology, Edificio de Biología, Universidad Autónoma de Madrid, C/Darwin 2, Madrid 28049, Spain; [email protected] (R.R.O.); [email protected] (I.G.B.)

Inés Gutierrez-Briceño

Associated data.

Green care is an innovative approach that combines simultaneously caring for people and caring for land through three elements that have not been previously connected: (1) multifunctional agriculture and recognition of the plurality of agricultural system values; (2) social services and health care; and (3) the possibility of strengthening the farming sector and local communities. The current research provides a comprehensive overview of green care in Europe as a scientific discipline through a literature review ( n = 98 studies). According to our results, the Netherlands, the UK, Norway and Sweden followed by Italy have led the scientific studies published in English. Green care research comprises a wide range of perspectives and frameworks (social farming, care farming, nature-based solutions, etc.) with differences in their specificities. Green care studies have mainly focused on measuring the effectiveness of therapeutic interventions. Studies that evaluate its relevance in socio-economic and environmental terms are still limited. According to our results, the most common users studied were people suffering from psychological and mental ill health, while the most common activities were horticulture, animal husbandry and gardening. Finally, we discuss the potential of green care to reconnect people with nature and to diversify the farming sector providing new public services associated with the relational values society obtains from the contact with agricultural systems.

1. Introduction

Agriculture has been performed by our species for approximately 10,000 years [ 1 ], and practices have been altered according to human needs and preferences. The agricultural industrialization of the 20th century dramatically changed agricultural activities and relations between agriculture and our culture; for example, agriculture now focuses largely on the maximization of both production and profit [ 2 ]. This change has become even more severe over the last 50 years, during the green revolution, with the intensification of large-scale agricultural production and the abandonment of the countryside in traditionally agricultural rural areas [ 3 , 4 ].

The consequences of this transition not only has environmental impacts (i.e., loss of agricultural landscapes, water pollution, loss of genetic heritage related to local varieties and breeds), economic impacts (i.e., loss in profitability) and cultural impacts (i.e., loss of local knowledge and identity linked to agricultural management) but also affects our general nutrition, relationships, health and quality of life. The value and importance of the relation between humans and nature has been overlooked during recent decades. However, currently, it is known that contact with nature has a positive influence on quality of life in terms of both physical and psychological health [ 5 , 6 , 7 ]. Nevertheless, this disconnection (in terms of access and appreciation) with agroecosystems and the ecosystem services that agroecosystems provide is increasing in western and urbanized societies. It is argued by Pretty [ 8 ] that as urbanized societies we have become disconnected from the land that sustains us and we cultivate; thus, we are losing part of our culture and identity.

Human beings, as part of nature, have always coexisted with it; thus, the association between people and nature has always existed. This concept has been formalized in the academic world through the study of social-ecological systems [ 9 ]. Following the biophilia theory [ 10 ], this connection should be more important and integrated into our lives, but the ability to connect with and understand nature often depends on our experiences as children, and such experiences should be reinforced in our society [ 11 ]. In addition to the biophilia theory, Kaplan’s attention restoration theory [ 12 ] and Ulrich’s psycho-evolutionary theory [ 13 ] should be highlighted, as these theories defend and explain why and how our surrounding natural environment influences our lives and is important for us. In socio-cultural terms, the current individualist lifestyle in western societies has resulted in a disregard for social well-being, deriving in a disconnection from other people and lack of community [ 14 ]. According to Spain’s Millennium Ecosystem Assessment, in recent decades in urbanized societies’ good social relations have deteriorated, with a specific tendency toward the loss of social cohesion and an increase in individualistic, sedentary and isolated lifestyles [ 15 ]. These trends are reflected by various indicators such the number of people living alone and the amount of television consumption [ 3 ]. This situation affects the most vulnerable people in the system more dramatically, placing them at risk of social exclusion.

Green care is an approach that aims to combine, simultaneously, caring for people and caring for land. It promotes health and well-being for people at risk of social exclusion through the use of natural environments as the central element [ 14 , 16 ]. In green care, a series of activities are carried out in the context of agricultural and natural environments where activities and interactions with nature take place (i.e., activities performed on farms, orchards and gardens, forests, etc.) to produce physical, psychological, emotional, social, cognitive-educational, social and labor-integration benefits for people at risk of social exclusion [ 7 , 14 , 16 , 17 , 18 ]. At those interventions, diverse social groups could be involved, including elderly people, people with mental disabilities, people with various mental disorders or mental health problems (i.e., dementia, stress, anxiety, depression and schizophrenia), refugees, teenagers with problems, ex-prisoners, people with addiction or abuse problems, women suffering from male violence, people with various physical disorders (cancer, obesity, hearing impairment and other disabilities), migrants with difficulties, long-term unemployed people, persons belonging to ethnic minorities, etc.

Green care is an inclusive and umbrella term that includes a broad variety of interventions such as nature-based rehabilitation, care farming, social farming, therapeutic horticulture, animal-assisted intervention, etc. While these concepts are sometimes used as synonyms, all of them are sustained by different backgrounds and theories and have different representations in each country. In this study we will refer to the term green care in order to cover a broad area of research. Over recent decades, in many European countries, the use of agriculture as a tool of public health and social integration has been developed in different forms. Many projects and initiatives have arisen, with the existence of more than 170 care farms in the UK as of 2011 [ 19 ], nearly 600 care farms in the Netherlands as of 2005 [ 20 ], and nearly 700 social farms in Italy [ 17 ]. In this way, in many European countries, green care is a practice with a long history; however, numerous research projects and studies have been developed to formalize the concept only in the last decade. In fact, in 2007, a cost action called “COST Action 866 Green Care in Agriculture” was created as one of the first attempts to increase scientific knowledge of green care, as one of the main limitations of green care has been the lack of evidence about the effectiveness of its various practices [ 16 ].

Since the end of the 20th century and the beginning of the 21st century, there has been an increase in the number of scientific studies focused on green care throughout Europe. Therefore, the current paper uses Europe as a case study with the intention of better understanding the main research trends and pathways that have been taken in terms of green care development to obtain a comprehensive understanding of the progress and dimensions of this new discipline in Europe. The proposed specific objectives of this systematic review have focused on analyzing: (1) which countries have published more, within which approach and which research areas have been emphasized by studies related to green care; (2) the temporal evolution of these studies and the research objectives investigated; (3) the targeted populations of green care studies as well as the activities carried out with each population; and (4) the methods used for assessing green care interventions. Finally, we discuss how our analysis can contribute to future research and green care practices.

2. Materials and Methods

2.1. search procedure.

The methodology of this study consists of a systematic review of the existing scientific literature on green care in Europe. Specifically, we gathered and selected all studies published in peer-reviewed journals via the search engine Web of Science. To encompass the spectrum of terminology used to refer to green care, we considered this term as well as all related terms that have been used. The complete list of English keywords included “care farm”, “ecotherapy”, “farm animal-assisted”, “gardening-based intervention”, “green care”, “horticultural therapy”, “nature-based rehabilitation”, “nature-assisted therapy”, “social farm”, “therapeutic garden”, “therapeutic horticulture”, “working in nature”.

The search was restricted according to the following criteria: (1) all studies published until 2017 were included to avoid incomplete years (i.e., 2018); (2) original articles were from scientific journals to avoid double counting (and excluded short communications, letters to the editor or editorials, communications in congresses and reviews); (3) scientific articles were restricted to those published in English; and (4) scientific articles were published in European countries.

Initially, 128 scientific articles were gathered in the search. Following the application of the above selection criteria and an inspection of the abstracts, 98 valid articles were selected ( Supplementary material, Table S1 ). The remaining articles were excluded from the study because they did not meet any of the above criteria or because a read through of the publication indicated that they did not correspond to the topic in question ( Figure 1 ).

Flow diagram with the different phases of a systematic review (adapted from PRISMA, [ 21 ]).

2.2. Database Generation and Analysis

We extracted the following information from these publications: (1) publication identification (title, authors, year and journal); (2) discipline (level of disciplinary integration, i.e., uni-disciplinary or interdisciplinary, discipline area and research labels); (3) study characteristics (country studied, study type—theoretical or empirical); (4) study approach (following the terminology used in the study) and purpose; (5) target population; (6) type of activities conducted; and (7) methodological approach used to assess the intervention (when an intervention was implemented) ( Table 1 ).

List of variables extracted from the database.

Variable Type	Variable	Description	Variable Coding
Publication identification	Title	Title of the publication	Open, text.
	Authors	Author (s) of the publication
	Year	Year in which the research was published	Continuous (year).
	Journal	Name of the journal in which the article was published	Open, text.
Discipline	Interdisciplinary	Interdisciplinary team if at least two of the authors belonged to different research areas	Interdisciplinary; unidisciplinary.
	Discipline area	Based on the institution’s department and discipline where the first author works, we identified three main categories	Environmental Sciences; Science of the Health; Social Sciences.
	Research area (journal)	Based on Web of Science labels (one or more)	Categories.
Study characteristics	Study site	European country where the research was carried out	Dummy per each country.
	Type of study	Theoretical or empirical	Dummy for each category.
Study approach and purpose	Approach	Categories of existing theoretical frameworks following the terminology used in the study	Green care; nature-based rehabilitation; care farming; social farming; therapeutic horticulture; therapeutic gardening; farm animal-assisted intervention.
	Purpose	Categories of purposes pursued	Therapeutic intervention assessment; concept, development and relevance of social farming; professionals perception, needs and networks.
Users	Target population	Collective at risk of social exclusion on which the research is focus	Refugees and displaced persons; long-term unemployed persons; offenders; people suffering from addictions; people suffering for physical disabilities or illness; older population; people with learning disabilities; children and young people at risk of exclusion; people suffering from mental health illness; people suffering from psychological health illness.
Activities	Activity performed	Social agriculture activities carried out by participants benefiting from interventions	Outdoor activities (including forest walks and green exercise); agriculture (horticulture, viticulture and olive growing); gardening; therapeutic activities with animals; animal care; food processing and sale; nature exposure; relaxation; dialog with the farmer and staff.
Methodological approach	Assessment tools	Type of method used if there has been a follow up or assessment of participants of an green care intervention	Official statistics; surveys; interviews; focus groups; participant observation and participatory methods; clinical assessment; recordings.

Regarding the purpose of publications, the published studies were classified into three main categories: (1) therapeutic assessments, including all the studies from the health sector that analyzed the effectiveness of different interventions; (2) concept, development and relevance of green care, including all the studies that practically or theoretically addressed the emergence of this new approach or aimed to define concepts, hypothesize potential benefits, or consider the impacts of its implementation; and (3) publications where the professionals were the cornerstone of the article and defined their preferences, views, needs to provide this health and social service as well as their networks (i.e., how are they organized).

First, we explored the current state of knowledge of green care through a general descriptive analysis of all included studies. To do so, we analyzed the countries that have published more studies, the theoretical framework used (care farming, nature-based rehabilitation, etc.), the field-specific disciplines related to the subject, the temporal evolution of the studies that included green care as their main research goal, the activities conducted, the main stakeholders and the methods used. Then, chi-square tests were performed to detect significant associations between specific variables. Specifically, chi-square tests were used to assess the relationship between countries and theoretical frameworks used, countries and discipline areas, countries and user types, countries and activities conducted, and finally, between activities and user types.

3.1. Overview of the Scientific Studies on Green Care Carried out in Europe

A comparison of the studies published in different European countries showed that four countries led the scientific research on green care: the Netherlands (24%), the UK (22%), Norway (17%) and Sweden (16%). These top four countries were followed by Italy, which accounted for 7% of the publications, and other countries, such as Denmark, Spain, Germany, Switzerland, Belgium, Finland and France, which had low representation (approximately 1–4% each) (see Figure 2 ). The differences in the percentages of studies published in different countries may be due to the language restrictions used during the search process, as we analyzed only papers published in English.

Number of publications per country, including the approach used.

Green care research comprises a wide range of perspectives and frameworks with differences in their specificities. In this regard, we identified seven different terminologies associated with those frameworks: care farming (used at 31% of the publications), nature-based rehabilitation (which includes forest interventions and ecotherapy, used at 16% of the publications), green care (15%), therapeutic horticulture (13%), therapeutic gardening (11%), social farming (8%) and farm animal-assisted interventions (5%). We detected significant differences performing chi-squared contingency-table test showing that some countries follow specific approaches. In this regard, the Netherlands used green care concept in its broadest sense more than other terms in their research studies (χ 2 = 27.46; p < 0.05). In the UK most of the studies came from the therapeutic horticulture approach (χ 2 = 21.64; p < 0.05). In Norway we found a significantly higher number of studies using the farm animal-assisted intervention approach (χ 2 = 30.06; p < 0.05). Publications conducted in Sweden used the term nature-based rehabilitation significantly more than other terms (χ 2 = 52.87; p < 0.05). Finally, studies from Italy used mainly the term social farming (χ 2 = 35.46; p < 0.05) ( Figure 2 ).

Most of the articles (63% of the studies analyzed) were interdisciplinary in nature, which allowed for a holistic approach to assessing the field of green care. Concerning the disciplines that assessed the subject of green care, health sciences and environmental sciences were the dominant areas (45% each of them), followed by social sciences (10%). In Europe, green care has been frequently framed in the field of health sciences (including areas such as rehabilitation, geriatrics and gerontology, occupational health, public health, psychiatry, dietetic and nutrition and oncology) and has included research on the therapeutic effects of green care and its impact on indicators of health and well-being. Such research includes publications on the impacts of therapeutic landscapes for older people [ 22 ], horticulture for clinical depression [ 23 ], and farm animal-assisted interventions for people with clinical depression [ 24 ]. From the environmental perspective (including researchers from the fields of vegetal science, agriculture, ecology and forest science), examples of published studies have focused on the values of landscapes and their management [ 25 ] or on the conceptualization of terms and the capacity of green care farms to promote social-ecological sustainability and ecosystem services [ 26 ]. A lower number of authors came from social sciences backgrounds emphasizing socioeconomic aspects; such as analyzing the economic impacts of green care, including indicators of expenditure and employment [ 27 ]; or investigating the evolution of rural social cooperatives engaged in green care farm practices [ 28 ]. When we performed the chi-squared contingency table test we detected significant differences, showing that the Netherlands and the UK were specialized in specific research areas. Such specialization was specifically seen in the Netherlands, where there was a predominance of studies coming from the environmental sciences (χ 2 = 9.21; p < 0.05). In the UK most of the studies came from the health sector (χ 2 = 11.88; p < 0.05), which is consistent with the therapeutic horticulture approach used with clear health goals defined ( Figure 2 ).

3.2. Temporal Evolution of Green Care Studies and Their Research Objectives

The first study was published in the UK in 1979, and it focused on the requirements of horticultural training programs for people with mental health disabilities [ 29 ]. During the 1990s, two studies were published in relation to the concept, development and relevance of green care. These two theoretical studies were conducted in the health sector and explored the role of horticultural therapy [ 30 ] and gardens [ 31 ] in supporting people with disabilities, and they emphasized the elderly population. These types of studies had the purpose of providing confidence to caregivers regarding the use of green tools in human well-being interventions. Since 2004, a progressive increase in the number of studies has been observed, and this increase has been exponential since 2010 ( Figure 3 ). In 2004, a network was created to promote knowledge sharing in European countries; it was the community of practice (Cop) “farming for health”. Later, in 2007, a project called “COST Action 866 Green Care in Agriculture” was launched, and it aimed to further investigate the concept of green care and its development in different European countries. The COST Action 866 Green Care Initiative was born in 2007 as a network in which researchers, engineers and scientists cooperated and whose main objective was to increase knowledge within the framework of green care. This project involved researchers from 22 countries, and it aimed to promote scientific knowledge in relation to green care, develop and deepen the concept, and highlight the potential of this new discipline in different European countries [ 16 ]). Thus, COST 866 was one of the first initiatives to formalize green care as a scientific discipline. Subsequently, at the scientific level, the European SoFar (Social Farming in Multifunctional Farms) project was financed by the Sixth Framework Programme during the 2006–2009 period. More recently, the SoFab Project (Social Farming across Borders) has been approved and implemented (2014–2017) in Ireland and Northern Ireland through INTERREG IVA Cross-border Programme funding. All these academic initiatives may explain the increase in the number of published studies.

Temporal trends in published research by the study purpose.

Considering the general purposes of these publications, articles assessing health interventions have a long tradition, while studies exploring the concept, development and implementation of this discipline have been present but to a much lesser extent. During recent years, articles from the perspective of green care providers and how they are organized have become more visible ( Figure 3 ). In our sample, we found that 58% of the studies were assessments on therapeutic intervention. Specifically, these studies from the health sector analyze the effectiveness of different treatments with different user types. Währborg et al. conducted a study comparing the effects of therapeutic gardening with the effects of conventional therapy on the rehabilitation of people suffering from depression or stress [ 32 ]. The results obtained after therapy concluded that people who had been treated in nature required less medical help than the other group. The study carried out by [ 33 ] aimed to evaluate whether the results of therapy that used activities in boreal forests could be utilized for the rehabilitation of patients suffering from exhaustion disorder. One of the results obtained suggested that the effect of this therapy is transitory, indicating that activities in nature should not be temporary in our lives; rather, these activities should be incorporated into our daily lives. The influence of contact with nature on children with attention deficit hyperactivity disorder was examined by [ 34 ]. The way in which women with stress-related illnesses experienced rehabilitation in a therapeutic garden was described by [ 35 ].

Then, 27% of the studies emphasized the concept, development and relevance of green care and included practical or theoretical publications that addressed the emergence of this novel approach; these studies aimed to identify the concepts and potential benefits, implementation possibilities and legislative frames that supported its implementation. These aspects differed by country, and many of these studies analyzed the evolution of green care in different countries that had their own particularities and trends, as seen by the evolution in the Netherlands [ 36 , 37 ], Flanders [ 36 ], Italy [ 28 ], and Switzerland [ 38 ]. Finally, in 15% of the publications, professionals were the cornerstone of the research, and they defined their preferences, views, need to provide this social service and health care, as well as their networks and organizational strategies and the benefits that they could obtain by including green care (mainly care and social farms) in their enterprises [ 39 , 40 , 41 ].

3.3. Target Population and Greem Care Activities

Green care research covers a wide range of users who benefit from the interventions in which they participate. Following our sample, 10 categories of users have been identified, and two of these categories stand out ( Figure 4 ): people suffering from psychological health illnesses such as depression, burnout and/or stress (e.g., [ 35 , 42 ]; in 30% of the studies), and people suffering from mental health illnesses, such as cases of dementia, schizophrenia, personality and behavioral disorders and other mental health problems (e.g., [ 43 , 44 ]; in 21% of the studies). Other publications focused on children and young people at risk of exclusion (e.g., those with behavioral problems or with dysfunctional family backgrounds; such as [ 11 ]; in 8% of the studies), on people with learning disabilities (e.g., [ 45 ]; in 7% of the studies), on elderly populations (e.g., [ 22 ]; in 7% of the studies), and on people suffering from physical disabilities or physical health illnesses (e.g., people with chronic muscle pain, coronary and pulmonary diseases or cancer; [ 46 ]; in 6% of the studies). Finally, a more limited number of studies focused on people suffering from addictions (4%), offenders (e.g., [ 47 ]; in 3% of the studies), people experiencing long-term unemployment (e.g., [ 48 ]; in 1% of the studies), and refugees and displaced people (e.g., [ 49 ]; in 1% of the studies).

Type of users involved in green care programs.

Most of the studies were concentrated on a particular type of user (in 90% of the studies). We found a higher number of studies on people suffering from mental health illnesses in the Netherlands than in other countries (χ 2 = 4.71; p < 0.05). We found a significantly higher number of studies focused on people suffering from psychological health illnesses in Sweden than in other countries (χ 2 = 23.67; p < 0.001). Finally, we found a significantly higher number of studies focused on people with learning disabilities in the UK than in other countries (χ 2 = 7.74; p < 0.05).

A wide variety of activities and tasks have been analyzed in the literature review conducted. Horticulture stands out as the most widely performed activity (32%), followed by animal husbandry by feeding and taking care of farm animals and working in stables (27%), gardening (26%), and outdoor activities, such as forest walks and other physical activities in green spaces (24%; Figure 5 ). Other types of activities that were carried out included being in contact with nature (e.g., passive exposure to vegetated environments) and contemplation (12%); food processing, cooking and preparing meals from farm products for sale (9%); agriculture production, including viticulture and olive orchards (9%); relaxation (6%); conversation with the farmers, other staff and the farm community (7%); firewood collection (2%) and equine-assisted therapy (2%). There were also mentions of training and educational activities through combined workshops (e.g., textile, carpentry, ceramics and art) focused on agricultural education and user training for labor market integration.

Green care activities carried out during interventions.

In 60% of the publications analyzed, a unique principal activity was studied, with 27% of the studies having two or three activities and 13% of the publications describing more than four activities. The typology of activities also differed from country to country in some cases, and we found a higher number of studies on engaging in outdoor activities (χ 2 = 6.73; p < 0.05), relaxation activities in nature (χ 2 = 18.38; p < 0.001) and gardening (χ 2 = 6.03; p < 0.001) in Sweden than in other countries. Gardening was significantly more studied in the UK than in other countries (χ 2 = 5.11; p < 0.05). In addition, Norway and the Netherlands produced more studies related to animal-assisted interventions, including activities such as animal husbandry (χ 2 = 7.36 and χ 2 = 5.25, respectively; p < 0.05). Finally, we tested associations between activities and user types. Following chi-square tests, we found that research publications studied the impact of relaxation activities on people suffering from psychological health illness (χ 2 = 7.00; p < 0.05).

3.4. Methodological Tools for Assessing Green Care Interventions

The most common methods used to evaluate green care interventions were interviews (43%) and surveys (41%; Figure 6 ). Interviews involved semi-structured guides and open-ended questions to explore users’ experiences with green care practices. This was the case in the work conducted by [ 50 ], who analyzed forest-based rehabilitation through semi-structured interviews and analyzed the results from the perspective of the grounded theory. Interviews were carried out by [ 51 ] with care farmer professionals to explore the characteristics of diverse types of care farms in the Netherlands. Interviews were conducted by [ 52 ] with therapeutic garden users who had stress-related disorders to explore how they experienced the rehabilitation process.

Methodological tools to assess intervention effectiveness.

Other studies have used quantitative data collected from questionnaires using experimental or quasi-experimental designs at clinical assesments. How a woodland program improved the psychological well-being of members of deprived urban communities was assessed by [ 53 ] using the perceived stress scale. Horticultural therapy as a physical health, mental health and social interaction with patients with chronic musculoskeletal pain was used by [ 54 ]. They used an experimental design and assessed indicators measured by the West Haven-Yale multidimensional pain inventory or the hospital anxiety and depression scale. A lower number of other studies gathered information from participant observations (8%), official statistics (7%), focal groups (7%), participatory methods (2%) and recordings (2%).

4. Discussion

4.1. overview of green care discipline across europe.

This study builds on previous literature reviews of green care interventions. A literature review was completed by [ 55 ] ( n = 38 studies) on nature-assisted therapy that used controlled and observational studies to evaluate the scientific evidence, while five other publications were dedicated to specific user groups. The impacts on military veterans of sport and physical activity, including nature-based physical activities, were analyzed by [ 56 ] , ( n = 11 studies). In the same way, [ 57 ] focused their literature review ( n = 20 studies) on military veterans suffering traumatic experiences after active service and their participation in nature-assisted therapies. The evidence on the effectiveness of farm-based interventions for people with mental health disorders was reviewed by [ 58 ] ( n = 11 studies). The benefits of gardening-based mental health interventions was evaluated by [ 59 ] ( n = 10). Regarding dementia care, Whear et al. used qualitative and qualitative studies to examine the impacts of gardens and outdoor spaces on people with dementia ([ 60 ]; n = 17 studies), while González et al. evaluated the benefits of sensory gardens and horticultural activities ([ 61 ]; n = 16). Those reviews aimed to evaluate evidence that supported the effectiveness of green care interventions to significantly improve public health, mainly the health of specific users. Finally, a descriptive review was conducted by [ 62 ] of research on care farms for adults with mental health problems in Norway.

This research provides the first attempt to complete a comprehensive review of green care as a scientific discipline and includes studies assessing not only the effectiveness of interventions from the perspective of health but also other key aspects that require scientific attention, such as the concept, development and relevance of green care, as well as publications where professionals’ preferences, views, needs and networks were explored. Here, we analyzed trends in green care research using 98 publications that were conducted in different European countries. Although this study covered all Europe, we specifically reviewed scientific articles published in English. This limit provided a systematic method of searching for publications and avoided duplication; simultaneously, there was a limitation imposed by not collecting works published in other languages. For instance, there is evidence concerning the situation of green care under the approach of social farming in Catalonia in studies written in Spanish [ 63 ] or Catalan [ 64 ]. Much research conducted in Italy, mainly within the framework of social farming, has been published in Italian [ 17 ]; thus, such research has been underrepresented in the current study. In addition, Pawelczyk et al. attributed the lack of knowledge and research in Poland to the lack of knowledge about the usefulness of farming activities as a tool for tackling socio-health problems [ 65 ].

In this study we decided to use the broadest framework (green care) in order to cover the larger number of studies developed in Europe. However, as presented in our findings and also pointed out by other authors, there is a diversity of terms associated with different interpretations of the synergy between being in contact with natural and agricultural landscapes and the promotion of health together with other quality of life dimensions (e.g., employment, good social relationships, equity, education) [ 14 , 48 , 66 ]. Here, we identified seven terms used in research publications, the most popular being care farming. Nevertheless there were differences among countries, for example the green care term was used more in the Netherlands research, therapeutic horticulture approach in UK, farm animal-assisted intervention in Norway, the concept of nature-based rehabilitation in Sweden, and studies from Italy mainly used the term social farming. Some of the differences between those approaches are in the level of care and therapy provided [ 16 ]. Those interventions done within structured rehabilitation or health programs with clearly defined patient-orientated goals are commonly defined with the terms therapy or care such as therapeutic horticulture, therapeutic gardening or care farming [ 67 ]. In care farming and social farming the objectives are more related to conducting meaningful occupational activities and achieving employment goals at real production and commercial farms [ 40 ] and especially within social farming the therapeutic intent is not so explicit, with the aim being to promote innovation and collaboration pathways between sectors in local communities following social and employment inclusion and integration principles [ 68 ]. Other studies differ by the key element or tool used during the intervention, such as being in contact with nature at outdoor surroundings (at nature-based rehabilitation, [ 50 ]) or farm animal-assisted therapy being essential to the interactions established with animals (such as empathy, expression emotions or not being judged; [ 69 ]). In this way, green care is an umbrella term that represents a complex interaction between nature–people with different goals and specificities that determines the formalization of the approach. Green care is a dynamic concept, that has developed rapidly during the last 10 years and that will continue in progress as it represents a mirror of the different European countries and societies in terms of its culture, path dependence, needs and future expectations. This study reflects the green care research trends, giving the opportunity to offer an overview of the recent years and present time and to draw conclusions for the future. As presented by Di Iacovo et al., in Europe there are two models derived from two welfare systems: the northern European specialized model and the Mediterranean communitarian one. While in the first (followed by countries such as Sweden and the Netherlands), green care farms provide a health service (delivered by specialized facilities and skills) in private farms they receive direct payments (from the state or from the market being directly paid by users) for those services [ 70 ]. In the Mediterranean model (e.g., Italy or Spain) usually farmers do not receive a direct payment but receive other benefits more related with enhancing their reputation and expanding their networks. In this model, the goals pursued are more linked to social inclusion and justice than therapy. This situation may also explain the larger number of studies found in northern countries compared with those in the Mediterranean area; the number of studies being higher when the green care activities are more explicitly defined and where it is essential to measure the therapeutic effectiveness of the interventions conducted. In fact, there are small cooperatives or enterprises operating at the agrifood sector sustained by social economy and following agroecological principles (e.g., community supported agriculture) which are closely connected with social farming (e.g., justice, inclusion, solidarity, promotion of rural economies) but this is not explicitly stated, and it would be interesting to study the association between both approaches.

4.2. Target Population and Green Care Activities

It has increasingly been seen that green care responds to the needs of diverse groups, such as the training and working skills required by people who have experienced long-term unemployment or low employability, and the social integration of marginalized communities or spaces for community dialogue and interaction [ 71 ]. It improves not only their health but also their physical, psychological and emotional well-being (e.g., [ 55 ]). Green care provides opportunities to allow people to actively participate in society and agricultural landscape conservation. Green care has the potential to stress the relationships established between people and nature, uncovering the relational values obtained from agricultural landscapes. In an increasingly urban society, spending time in more natural, greener and more rural environments can help to meet new food, labor and social needs [ 72 ]. It has been proposed that to go beyond the classical duality to sustain landscape conservation based on intrinsic vs. instrumental values, policies should take into consideration relational values derived from the relationships establish between people and nature (e.g., cultural identity, stewardship principles), including relationships that are between people but involve natural surroundings (e.g., social cohesion) [ 73 ]. Active exposure to nature can promote a healthier lifestyle in the long term, which can help people cope with the effects of rapid lifestyles experienced in cities (e.g., stress, depression, fatigue) and address problems (quality food or lack of physical activity) facing people with increasingly sedentary futures [ 74 ].

Regarding green care activities, according to our findings, the most researched activities are horticulture, feeding and taking care of farm animals, gardening activities and outdoor activities, such as forest walks and green exercise. We found some significant associations between users and activities. In this regard, [ 75 ] analyzed different green care farming activities in terms of their suitability for different type of users taking into account aspects such as previous knowledge needed, need of support, risk due to the use of tools, etc. It would be a step forward to carry out further research to connect practices and specific well-being objectives to reach different users.

5. Conclusions

Some of the difficulties that a new science, movement and practice such as green care can face include gaining scientific, political and social credibility. Despite the advances in research publications, the potential of green care is still poorly understood [ 19 , 38 ]. As shown, in the last decade, researchers have started to study the effectiveness of green care compared to other therapeutic processes. However, since green care (mainly its orientation through social farming) contributes to rural revitalization—and the conservation of the agricultural landscape—it requires more scientific research that evaluates its relevance in socio-economic and environmental terms. It has been stressed that there is a need to recognize the complexity of views required to evaluate green care and to go beyond health indicators, since the mainstream measures of those indicators could mask and underestimate key components necessary to assess the development of green care practices (e.g., management procedures, networks of actors involved, certifications, consumer knowledge and acceptance of green care farms products, private or public policies to support them, etc.) [ 76 ]. Further research that proposes indicators and measures to analyses it as an innovative practice to diversify the farming sector, conserve agricultural landscapes and improve human well-being is required to ensure its establishment. In this regard, green care farming can be a major source of income for farmers [ 19 , 20 ] and a way to increase their visibility and reputation [ 26 ], which can stimulate the economy of the sector. It is necessary to determine which strategies farmers use, whether they are sufficiently innovative and whether they favor economic development [ 77 ]. It is also important to analyze the key factors that contribute to the success of green care projects by focusing on the point of view of producers and their willingness to innovate [ 40 ]. According to our findings, during recent years, the number of publications from the perspective of green care providers has been increasing ( Figure 3 ). A shift in production models on farms can attract new types of workers by offering diversified activities through other approaches, skills, interests, benefits and resources that break with traditional farming and livestock activities. The diversification of agricultural activities can offer farm owners opportunities to provide new services. Green care, together with agro-tourism, has also been seen as motivation for women to diversify farming activities and promote female succession in farm properties in Norway, helping to counterbalance the masculinization of rural areas [ 78 ]. This can provide an incentive to significantly halt population declines in rural areas and could stimulate an increase in the number of women owners at the head of green care activities that occur on farms.

Green care activities can play a key role in enhancing life quality and sustainability in rural areas by providing economic and social benefits, as seen by recent cases of rural social cooperatives that have emerged in Italy [ 28 ]. Such cooperatives create a new relationship between urban and rural areas, as urban people are attracted to local markets in which they can find organic and ethical products with added social value. As was shown by [ 79 ], people were willing to support a green care initiative in the UK and were willing to contribute their money and voluntary time. Similarly, Carbone, A. et al. found that consumers’ buying groups in short food supply chains in Italy hold a strong concern for ethical issues when purchasing products and had an interest in supporting social farming products [ 80 ]. Unlike other economic sectors, agricultural activity can be understood as a transversal field with the capacity to influence a diversity of well-being components, not only in terms of production but also in terms of nutritional, educational, social and relational components as well as a new way of understanding the food system and our relationship with natural environments. This viewpoint aims to intensify social capital over intensive technological capital. From this perspective, farmers are essential actors since they can provide new services to society.

Acknowledgments

We would like to thank the two anonymous referees for providing thoughtful and valuable comments and suggestions.

Supplementary Materials

The following are available online at http://www.mdpi.com/1660-4601/15/6/1282/s1 , Table S1: Publications included in the systematic review.

Author Contributions

M.G.L. conceived and designed the study; R.R.O. and I.G.B. conducted the literature review and data extraction; M.G.L. provided conceptual and analytical advice; R.R.O., I.G.B. and M.G.L. conducted the data analysis, M.G.L. wrote most of the paper.

This research was funded by a grant from the Spanish National Institute for Agriculture and Food Research and Technology, co-funded by the Social European Fund (Doc-INIA CCAA); and the IMIDRA research projects: Social Farming viability at the Madrid Region (FP16 VAS) and Assessment of Ecosystem Services provided by Agroecosystems (FP16 ECO).

Conflicts of Interest

The authors declare no conflict of interest.

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Title: rag vs fine-tuning: pipelines, tradeoffs, and a case study on agriculture.

Abstract: There are two common ways in which developers are incorporating proprietary and domain-specific data when building applications of Large Language Models (LLMs): Retrieval-Augmented Generation (RAG) and Fine-Tuning. RAG augments the prompt with the external data, while fine-Tuning incorporates the additional knowledge into the model itself. However, the pros and cons of both approaches are not well understood. In this paper, we propose a pipeline for fine-tuning and RAG, and present the tradeoffs of both for multiple popular LLMs, including Llama2-13B, GPT-3.5, and GPT-4. Our pipeline consists of multiple stages, including extracting information from PDFs, generating questions and answers, using them for fine-tuning, and leveraging GPT-4 for evaluating the results. We propose metrics to assess the performance of different stages of the RAG and fine-Tuning pipeline. We conduct an in-depth study on an agricultural dataset. Agriculture as an industry has not seen much penetration of AI, and we study a potentially disruptive application - what if we could provide location-specific insights to a farmer? Our results show the effectiveness of our dataset generation pipeline in capturing geographic-specific knowledge, and the quantitative and qualitative benefits of RAG and fine-tuning. We see an accuracy increase of over 6 p.p. when fine-tuning the model and this is cumulative with RAG, which increases accuracy by 5 p.p. further. In one particular experiment, we also demonstrate that the fine-tuned model leverages information from across geographies to answer specific questions, increasing answer similarity from 47% to 72%. Overall, the results point to how systems built using LLMs can be adapted to respond and incorporate knowledge across a dimension that is critical for a specific industry, paving the way for further applications of LLMs in other industrial domains.

Subjects:	Computation and Language (cs.CL); Machine Learning (cs.LG)
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Better farming through nanotechnology

An argument for applying medical insights to agriculture

Advanced technologies enable the controlled release of medicine to specific cells in the body. Scientists argue these same technologies must be applied to agriculture if growers are to meet increasing global food demands. 

In a new Nature journal review paper , scientists from UC Riverside and Carnegie Mellon University highlight some of the best-known strategies for improving agriculture with nanotechnology.

Nanotechnology is an umbrella term for the study and design of microscopically small things. How small? A nanometer is one billionth of a meter, or about 100,000 times smaller than the width of a human hair. Using nanotechnology, drugs can now be delivered where they’re most needed. But these insights have yet to be applied to plant science on a large scale.

“There are studies predicting we will need to increase food production by up to 60% in 2050 relative to 2020 levels. Right now, we are trying to do that through inefficient agrochemical delivery,” said Juan Pablo Giraldo, UCR associate professor and paper co-corresponding author.

“Half of all the fertilizer applied on farms is lost in the environment and pollutes the groundwater. In the case of commonly used pesticides, it’s even worse. Only 5% reach their intended targets. The rest ends up contaminating the environment. There is a lot of room for improvement,” Giraldo said.

Currently, agriculture accounts for up to 28% of global greenhouse gas emissions. This, in addition to a range of other factors from extreme weather events to rampant crop pests and rapidly degrading soil, underlines the need for new agricultural practices and technologies. 

In their review, the researchers highlight specific approaches borrowed from nanomedicine that could be used to deliver pesticides, herbicides, and fungicides to specific biological targets. 

“We are pioneering targeted delivery technologies based on coating nanomaterials with sugars or peptides that recognize specific proteins on plant cells and organelles,” Giraldo said. “This allows us to take the existing molecular machinery of the plant and guide desired chemicals to where the plant needs it, for example the plant vasculature, organelles, or sites of plant pathogen infections.”

Doing this could make plants more resilient to disease and harmful environmental factors like extreme heat or high salt content in soil. This type of delivery would also be a much greener approach, with fewer off-target effects in the environment.

Another strategy discussed in the paper is using artificial intelligence and machine learning to create a “digital twin.” Medical researchers use computational models or “digital patients” to simulate how medicines interact with and move within the body. Plant researchers can do the same to design nanocarrier molecules that deliver nutrients or other agrochemicals to plant organs where they’re most needed.

“It’s like J.A.R.V.I.S. (Just A Rather Very Intelligent System) from the film Iron Man. Essentially an artificial intelligence guide to help design nanoparticles with controlled delivery properties for agriculture,” Giraldo said. “We can follow up these twin simulations with real-life plant experiments for feedback on the models.”

“Nano-enabled precision delivery of active agents in plants will transform agriculture, but there are critical technical challenges that we must first overcome to realize the full range of its benefits,” said Greg Lowry, Carnegie Mellon engineering professor and co-corresponding author of the review paper. 

“I’m optimistic about the future of plant nanobiotechnology approaches and the beneficial impacts it will have on our ability to sustainably produce food.”

(Cover image: ipopba/iStock/Getty)

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Molecular basis of energy crops functioning in bioremediation of heavy metal pollution, 1. introduction, 2. mechanisms of heavy metal tolerance in energy crops, 3. remediation mechanisms of heavy metals by energy crops, 3.1. uptake, 3.2. translocation, 3.3. chelation, 3.4. immobilization and sequestration, 4. the application of post-harvest energy crop biomass which remediated heavy metals, 5. the challenges of remediating heavy metal pollution by energy crops, 5.1. limitations of energy crops, 5.2. more environmental influencing factors, 5.3. difficulties in energy crop transformation, 5.4. less research on unpopular energy crops, 5.5. few sources of biofuel, 5.6. commercialization difficulties, 6. conclusions, 7. future prospects, author contributions, data availability statement, acknowledgments, conflicts of interest.

Energy Crop Types	Latin Name	Introduction	Main Mechanism	Biomass Application	Related Heavy Metals	Related Literature
Sugar beet	Beta vulgaris L.	Biennial herbs of the genus Beet in Amaranthaceae	Tolerance, uptake, translocation, immobilization, and sequestration	Biochar, biofuel	Cd, Pb, Zn, Cu, Ni, Fe, Mn	[ , , , , , ]
Sugarcane	Saccharum officinarum	Perennial herbs of the Sugarcane in Gramineae	Uptake, immobilization, and sequestration	Biochar, biofuel	Zn, Cu, Cd, Pb, As	[ , , ]
Maize	Zea mays L.	Annual herbs of the Zea in Gramineae	Uptake, chelation, immobilization, and sequestration	Biofuel	Cu, Cd, Co, Pb, Cr, Zn	[ , , , ]
Sweet sorghum	Sorghum dochna L.	Annual plants of the Sorghum in Gramineae	Tolerance, uptake, translocation, immobilization, and sequestration	Biochar, biofuel	Pb, Zn, Cd, Cu, As, Cr, Ni	[ , , , ]
Wheat	Triticum aestivum L.	Annual or perennial herbs of the Wheat in Gramineae	Uptake, translocation, chelation, immobilization, and sequestration	Biofuel	Cd, Zn, Cr, Pb, As, Hg	[ , , , , ]
Yam	Dioscorea esculenta (Lour.) Burkill	Twisted herbaceous vine of the Dioscorea in Dioscoreaceae	Uptake, chelation, immobilization, and sequestration	Biochar	Cd, Cu	[ , , ]
Cassava	Manihot esculenta Crantz	Cassava plants of the Euphorbiaceae	Uptake, immobilization, and sequestration	Biochar, biofuel	Zn, Pb, Mn, Cu, Co, Ni, Cd, Cr	[ , , ]
Mustard	Brassica campestris L.	Annual or biennial herbs of the Brassica in Cruciferae	Tolerance, translocation, immobilization, and sequestration	Biofuel	Cd, Cr, Cu, Hg, Ni, Pb, Zn	[ , , ]
Rubber tree	Hevea brasiliensis (Willd. ex A. Juss.) Muell. Arg.	Hevea of the Euphorbiaceae	Uptake, immobilization, and sequestration	Biochar, biofuel	Cd, Na, Ni, Zn	[ , , ]
Willow	Salix babylonica L.	Salix plants of the Chrysopoda in Salicaceae	Tolerance, uptake, translocation, chelation, immobilization, and sequestration	Biochar	Cd, Hg, Zn, Ni, Pb, Cu	[ , , , ]
Reed	Phragmites australis (Cav.) Trin. ex Steud.	Reed plants of the Gramineae	Uptake, translocation, immobilization, and sequestration	Biochar, biofuel	Cu, Zn, Pb, As, Cd	[ , , , ]
Miscanthus sinensis	Miscanthus	Plants of the Miscanthus in Gramineae	Tolerance, uptake, immobilization, and sequestration	Biochar, biofuel	Cd, Cu, Ni, Pb, Zn, Cr	[ , , , ]

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Huang, S.; Lu, Z.; Zhao, X.; Tan, W.; Wang, H.; Liu, D.; Xing, W. Molecular Basis of Energy Crops Functioning in Bioremediation of Heavy Metal Pollution. Agriculture 2024 , 14 , 914. https://doi.org/10.3390/agriculture14060914

Huang S, Lu Z, Zhao X, Tan W, Wang H, Liu D, Xing W. Molecular Basis of Energy Crops Functioning in Bioremediation of Heavy Metal Pollution. Agriculture . 2024; 14(6):914. https://doi.org/10.3390/agriculture14060914

Huang, Shuoqi, Zhenqiang Lu, Xiaoxin Zhao, Wenbo Tan, Hao Wang, Dali Liu, and Wang Xing. 2024. "Molecular Basis of Energy Crops Functioning in Bioremediation of Heavy Metal Pollution" Agriculture 14, no. 6: 914. https://doi.org/10.3390/agriculture14060914

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Climate change is the single biggest health threat facing humanity. Climate impacts are already harming health, through air pollution, disease, extreme weather events, forced displacement, pressures on mental health, and increased hunger and poor nutrition in places where people cannot grow or find sufficient food. Every year, environmental factors take the lives of around 13 million people. Changing weather patterns are expanding diseases, and extreme weather events increase deaths and make it difficult for health care systems to keep up.

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Volume 30, Number 7—July 2024

Highly Pathogenic Avian Influenza A(H5N1) Clade 2.3.4.4b Virus Infection in Domestic Dairy Cattle and Cats, United States, 2024

Suggested citation for this article

We report highly pathogenic avian influenza A(H5N1) virus in dairy cattle and cats in Kansas and Texas, United States, which reflects the continued spread of clade 2.3.4.4b viruses that entered the country in late 2021. Infected cattle experienced nonspecific illness, reduced feed intake and rumination, and an abrupt drop in milk production, but fatal systemic influenza infection developed in domestic cats fed raw (unpasteurized) colostrum and milk from affected cows. Cow-to-cow transmission appears to have occurred because infections were observed in cattle on Michigan, Idaho, and Ohio farms where avian influenza virus–infected cows were transported. Although the US Food and Drug Administration has indicated the commercial milk supply remains safe, the detection of influenza virus in unpasteurized bovine milk is a concern because of potential cross-species transmission. Continued surveillance of highly pathogenic avian influenza viruses in domestic production animals is needed to prevent cross-species and mammal-to-mammal transmission.

Highly pathogenic avian influenza (HPAI) viruses pose a threat to wild birds and poultry globally, and HPAI H5N1 viruses are of even greater concern because of their frequent spillover into mammals. In late 2021, the Eurasian strain of H5N1 (clade 2.3.4.4b) was detected in North America ( 1 , 2 ) and initiated an outbreak that continued into 2024. Spillover detections and deaths from this clade have been reported in both terrestrial and marine mammals in the United States ( 3 , 4 ). The detection of HPAI H5N1 clade 2.3.4.4b virus in severe cases of human disease in Ecuador ( 5 ) and Chile ( 6 ) raises further concerns regarding the pandemic potential of specific HPAI viruses.

In February 2024, veterinarians were alerted to a syndrome occurring in lactating dairy cattle in the panhandle region of northern Texas. Nonspecific illness accompanied by reduced feed intake and rumination and an abrupt drop in milk production developed in affected animals. The milk from most affected cows had a thickened, creamy yellow appearance similar to colostrum. On affected farms, incidence appeared to peak 4–6 days after the first animals were affected and then tapered off within 10–14 days; afterward, most animals were slowly returned to regular milking. Clinical signs were commonly reported in multiparous cows during middle to late lactation; ≈10%–15% illness and minimal death of cattle were observed on affected farms. Initial submissions of blood, urine, feces, milk, and nasal swab samples and postmortem tissues to regional diagnostic laboratories did not reveal a consistent, specific cause for reduced milk production. Milk cultures were often negative, and serum chemistry testing showed mildly increased aspartate aminotransferase, gamma-glutamyl transferase, creatinine kinase, and bilirubin values, whereas complete blood counts showed variable anemia and leukocytopenia.

In early March 2024, similar clinical cases were reported in dairy cattle in southwestern Kansas and northeastern New Mexico; deaths of wild birds and domestic cats were also observed within affected sites in the Texas panhandle. In > 1 dairy farms in Texas, deaths occurred in domestic cats fed raw colostrum and milk from sick cows that were in the hospital parlor. Antemortem clinical signs in affected cats were depressed mental state, stiff body movements, ataxia, blindness, circling, and copious oculonasal discharge. Neurologic exams of affected cats revealed the absence of menace reflexes and pupillary light responses with a weak blink response.

On March 21, 2024, milk, serum, and fresh and fixed tissue samples from cattle located in affected dairies in Texas and 2 deceased cats from an affected Texas dairy farm were received at the Iowa State University Veterinary Diagnostic Laboratory (ISUVDL; Ames, IA, USA). The next day, similar sets of samples were received from cattle located in affected dairies in Kansas. Milk and tissue samples from cattle and tissue samples from the cats tested positive for influenza A virus (IAV) by screening PCR, which was confirmed and characterized as HPAI H5N1 virus by the US Department of Agriculture National Veterinary Services Laboratory. Detection led to an initial press release by the US Department of Agriculture Animal and Plant Health Inspection Service on March 25, 2024, confirming HPAI virus in dairy cattle ( 7 ). We report the characterizations performed at the ISUVDL for HPAI H5N1 viruses infecting cattle and cats in Kansas and Texas.

Materials and Methods

Milk samples (cases 2–5) and fresh and formalin-fixed tissues (cases 1, 3–5) from dairy cattle were received at the ISUVDL from Texas on March 21 and from Kansas on March 22, 2024. The cattle exhibited nonspecific illness and reduced lactation, as described previously. The tissue samples for diagnostic testing came from 3 cows that were euthanized and 3 that died naturally; all postmortem examinations were performed on the premises of affected farms.

The bodies of 2 adult domestic shorthaired cats from a north Texas dairy farm were received at the ISUVDL for a complete postmortem examination on March 21, 2024. The cats were found dead with no apparent signs of injury and were from a resident population of ≈24 domestic cats that had been fed milk from sick cows. Clinical disease in cows on that farm was first noted on March 16; the cats became sick on March 17, and several cats died in a cluster during March 19–20. In total, >50% of the cats at that dairy became ill and died. We collected cerebrum, cerebellum, eye, lung, heart, spleen, liver, lymph node, and kidney tissue samples from the cats and placed them in 10% neutral-buffered formalin for histopathology.

At ISUVDL, we trimmed, embedded in paraffin, and processed formalin-fixed tissues from affected cattle and cats for hematoxylin/eosin staining and histologic evaluation. For immunohistochemistry (IHC), we prepared 4-µm–thick sections from paraffin-embedded tissues, placed them on Superfrost Plus slides (VWR, https://www.vwr.com ), and dried them for 20 minutes at 60°C. We used a Ventana Discovery Ultra IHC/ISH research platform (Roche, https://www.roche.com ) for deparaffinization until and including counterstaining. We obtained all products except the primary antibody from Roche. Automated deparaffination was followed by enzymatic digestion with protease 1 for 8 minutes at 37°C and endogenous peroxidase blocking. We obtained the primary influenza A virus antibody from the hybridoma cell line H16-L10–4R5 (ATCC, https://www.atcc.org ) and diluted at 1:100 in Discovery PSS diluent; we incubated sections with antibody for 32 minutes at room temperature. Next, we incubated the sections with a hapten-labeled conjugate, Discovery anti-mouse HQ, for 16 minutes at 37°C followed by a 16-minute incubation with the horse radish peroxidase conjugate, Discovery anti-HQ HRP. We used a ChromoMap DAB kit for antigen visualization, followed by counterstaining with hematoxylin and then bluing. Positive controls were sections of IAV-positive swine lung. Negative controls were sections of brain, lung, and eyes from cats not infected with IAV.

We diluted milk samples 1:3 vol/vol in phosphate buffered saline, pH 7.4 (Gibco/Thermo Fisher Scientific, https://www.thermofisher.com ) by mixing 1 unit volume of milk and 3 unit volumes of phosphate buffered saline. We prepared 10% homogenates of mammary glands, brains, lungs, spleens, and lymph nodes in Earle’s balanced salt solution (Sigma-Aldrich, https://www.sigmaaldrich.com ). Processing was not necessary for ocular fluid, rumen content, or serum samples. After processing, we extracted samples according to a National Animal Health Laboratory Network (NAHLN) protocol that had 2 NAHLN-approved deviations for ISUVDL consisting of the MagMax Viral RNA Isolation Kit for 100 µL sample volumes and a Kingfisher Flex instrument (both Thermo Fisher Scientific).

We performed real-time reverse transcription PCR (rRT-PCR) by using an NAHLN-approved assay with 1 deviation, which was the VetMAX-Gold SIV Detection kit (Thermo Fisher Scientific), to screen for the presence of IAV RNA. We tested samples along with the VetMAX XENO Internal Positive Control to monitor the possible presence of PCR inhibitors. Each rRT-PCR 96-well plate had 2 positive amplification controls, 2 negative amplification controls, 1 positive extraction control, and 1 negative extraction control. We ran the rRT-PCR on an ABI 7500 Fast thermocycler and analyzed data with Design and Analysis Software 2.7.0 (both Thermo Fisher Scientific). We considered samples with cycle threshold (Ct) values <40.0 to be positive for virus.

After the screening rRT-PCR, we analyzed IAV RNA–positive samples for the H5 subtype and H5 clade 2.3.4.4b by using the same RNA extraction and NAHLN-approved rRT-PCR protocols as described previously, according to standard operating procedures. We performed PCR on the ABI 7500 Fast thermocycler by using appropriate controls to detect H5-specific IAV. We considered samples with Ct values <40.0 to be positive for the IAV H5 subtype.

We conducted genomic sequencing of 2 milk samples from infected dairy cattle from Texas and 2 tissue samples (lung and brain) from cats that died at a different Texas dairy. We subjected the whole-genome sequencing data to bioinformatics analysis to assemble the 8 different IAV segment sequences according to previously described methods ( 8 ). We used the hemagglutinin (HA) and neuraminidase (NA) sequences for phylogenetic analysis. We obtained reference sequences for the HA and NA segments of IAV H5 clade 2.3.4.4 from publicly available databases, including GISAID ( https://www.gisaid.org ) and GenBank. We aligned the sequences by using MAFFT version 7.520 software ( https://mafft.cbrc.jp/alignment/server/index.html ) to create multiple sequence alignments for subsequent phylogenetic analysis. We used IQTree2 ( https://github.com/iqtree/iqtree2 ) to construct the phylogenetic tree from the aligned sequences. The software was configured to automatically identify the optimal substitution model by using the ModelFinder Plus option, ensuring the selection of the most suitable model for the dataset and, thereby, improving the accuracy of the reconstructed tree. We visualized the resulting phylogenetic tree by using iTOL ( https://itol.embl.de ), a web-based platform for interactive tree exploration and annotation.

Gross Lesions in Cows and Cats

All cows were in good body condition with adequate rumen fill and no external indications of disease. Postmortem examinations of the affected dairy cows revealed firm mammary glands typical of mastitis; however, mammary gland lesions were not consistent. Two cows that were acutely ill before postmortem examination had grossly normal milk and no abnormal mammary gland lesions. The gastrointestinal tract of some cows had small abomasal ulcers and shallow linear erosions of the intestines, but those observations were also not consistent in all animals. The colon contents were brown and sticky, suggesting moderate dehydration. The feces contained feed particles that appeared to have undergone minimal ruminal fermentation. The rumen contents had normal color and appearance but appeared to have undergone minimal fermentation.

The 2 adult cats (1 intact male, 1 intact female) received at the ISUVDL were in adequate body and postmortem condition. External examination was unremarkable. Mild hemorrhages were observed in the subcutaneous tissues over the dorsal skull, and multifocal meningeal hemorrhages were observed in the cerebrums of both cats. The gastrointestinal tracts were empty, and no other gross lesions were observed.

Microscopic Lesions in Cows and Cats

Figure 1 . Mammary gland lesions in cattle in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. A, B) Mammary gland...

The chief microscopic lesion observed in affected cows was moderate acute multifocal neutrophilic mastitis ( Figure 1 ); however, mammary glands were not received from every cow. Three cows had mild neutrophilic or lymphocytic hepatitis. Because they were adult cattle, other observed microscopic lesions (e.g., mild lymphoplasmacytic interstitial nephritis and mild to moderate lymphocytic abomasitis) were presumed to be nonspecific, age-related changes. We did not observe major lesions in the other evaluated tissues. We performed IHC for IAV antigen on all evaluated tissues; the only tissues with positive immunoreactivity were mastitic mammary glands from 2 cows that showed nuclear and cytoplasmic labeling of alveolar epithelial cells and cells within lumina ( Figure 1 ) and multifocal germinal centers within a lymph node from 1 cow ( Table 1 ).

Figure 2 . Lesions in cat tissues in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. Tissue sections were stained with...

Both cats had microscopic lesions consistent with severe systemic virus infection, including severe subacute multifocal necrotizing and lymphocytic meningoencephalitis with vasculitis and neuronal necrosis, moderate subacute multifocal necrotizing and lymphocytic interstitial pneumonia, moderate to severe subacute multifocal necrotizing and lymphohistiocytic myocarditis, and moderate subacute multifocal lymphoplasmacytic chorioretinitis with ganglion cell necrosis and attenuation of the internal plexiform and nuclear layers ( Table 2 ; Figure 2 ). We performed IHC for IAV antigen on multiple tissues (brain, eye, lung, heart, spleen, liver, and kidney). We detected positive IAV immunoreactivity in brain (intracytoplasmic, intranuclear, and axonal immunolabeling of neurons), lung, and heart, and multifocal and segmental immunoreactivity within all layers of the retina ( Figure 2 ).

PCR Data from Cows and Cats

We tested various samples from 8 clinically affected mature dairy cows by IAV screening and H5 subtype-specific PCR ( Table 3 ). Milk and mammary gland homogenates consistently showed low Ct values: 12.3–16.9 by IAV screening PCR, 17.6–23.1 by H5 subtype PCR, and 14.7–20.0 by H5 2.3.4.4 clade PCR (case 1, cow 1; case 2, cows 1 and 2; case 3, cow 1; and case 4, cow 1). We forwarded the samples to the National Veterinary Services Laboratory, which confirmed the virus was an HPAI H5N1 virus strain.

When available, we also tested tissue homogenates (e.g., lung, spleen, and lymph nodes), ocular fluid, and rumen contents from 6 cows by IAV and H5 subtype-specific PCR ( Table 3 ). However, the PCR findings were not consistent. For example, the tissue homogenates and ocular fluid tested positive in some but not all cows. In case 5, cow 1, the milk sample tested negative by IAV screening PCR, but the spleen homogenate tested positive by IAV screening, H5 subtype, and H5 2.3.4.4 PCR. For 2 cows (case 3, cow 1; and case 4, cow 1) that had both milk and rumen contents available, both samples tested positive for IAV. Nevertheless, all IAV-positive nonmammary gland tissue homogenates, ocular fluid, and rumen contents had markedly elevated Ct values in contrast to the low Ct values for milk and mammary gland homogenate samples.

We tested brain and lung samples from the 2 cats (case 6, cats 1 and 2) by IAV screening and H5 subtype-specific PCR ( Table 3 ). Both sample types were positive by IAV screening PCR; Ct values were 9.9–13.5 for brain and 17.4–24.4 for lung samples, indicating high amounts of virus nucleic acid in those samples. The H5 subtype and H5 2.3.4.4 PCR results were also positive for the brain and lung samples; Ct values were consistent with the IAV screening PCR ( Table 3 ).

Phylogenetic Analyses

We assembled the sequences of all 8 segments of the HPAI viruses from both cow milk and cat tissue samples. We used the hemagglutinin (HA) and neuraminidase (NA) sequences specifically for phylogenetic analysis to delineate the clade of the HA gene and subtype of the NA gene.

Figure 3 . Phylogenetic analysis of hemagglutinin gene sequences in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. Colors indicate different...

For HA gene analysis, both HA sequences derived from cow milk samples exhibited a high degree of similarity, sharing 99.88% nucleotide identity, whereas the 2 HA sequences from cat tissue samples showed complete identity at 100%. The HA sequences from the milk samples had 99.94% nucleotide identities with HA sequences from the cat tissues, resulting in a distinct subcluster comprising all 4 HA sequences, which clustered together with other H5N1 viruses belonging to clade 2.3.4.4b ( Figure 3 ). The HA sequences were deposited in GenBank (accession nos. PP599465 [case 2, cow 1], PP599473 [case 2, cow 2], PP692142 [case 6, cat 1], and PP692195 [case 6, cat 2]).

Figure 4 . Phylogenetic analysis of neuraminidase gene sequences in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. Colors indicate different...

For NA gene analysis, the 2 NA sequences obtained from cow milk samples showed 99.93% nucleotide identity. Moreover, the NA sequences derived from the milk samples exhibited complete nucleotide identities (100%) with those from the cat tissues. The 4 NA sequences were grouped within the N1 subtype of HPAI viruses ( Figure 4 ). The NA sequences were deposited in GenBank (accession nos. PP599467 [case 2, cow 1], PP599475 [case 2, cow 2], PP692144 [case 6, cat 1], and PP692197 [case 6, cat 2]).

This case series differs from most previous reports of IAV infection in bovids, which indicated cattle were inapparently infected or resistant to infection ( 9 ). We describe an H5N1 strain of IAV in dairy cattle that resulted in apparent systemic illness, reduced milk production, and abundant virus shedding in milk. The magnitude of this finding is further emphasized by the high death rate (≈50%) of cats on farm premises that were fed raw colostrum and milk from affected cows; clinical disease and lesions developed that were consistent with previous reports of H5N1 infection in cats presumably derived from consuming infected wild birds ( 10 – 12 ). Although exposure to and consumption of dead wild birds cannot be completely ruled out for the cats described in this report, the known consumption of unpasteurized milk and colostrum from infected cows and the high amount of virus nucleic acid within the milk make milk and colostrum consumption a likely route of exposure. Therefore, our findings suggest cross-species mammal-to-mammal transmission of HPAI H5N1 virus and raise new concerns regarding the potential for virus spread within mammal populations. Horizontal transmission of HPAI H5N1 virus has been previously demonstrated in experimentally infected cats ( 13 ) and ferrets ( 14 ) and is suspected to account for large dieoffs observed during natural outbreaks in mink ( 15 ) and sea lions ( 16 ). Future experimental studies of HPAI H5N1 virus in dairy cattle should seek to confirm cross-species transmission to cats and potentially other mammals.

Clinical IAV infection in cattle has been infrequently reported in the published literature. The first report occurred in Japan in 1949, where a short course of disease with pyrexia, anorexia, nasal discharge, pneumonia, and decreased lactation developed in cattle ( 17 ). In 1997, a similar condition occurred in dairy cows in southwest England leading to a sporadic drop in milk production ( 18 ), and IAV seroconversion was later associated with reduced milk yield and respiratory disease ( 19 – 21 ). Rising antibody titers against human-origin influenza A viruses (H1N1 and H3N2) were later again reported in dairy cattle in England, which led to an acute fall in milk production during October 2005–March 2006 ( 22 ). Limited reports of IAV isolation from cattle exist; most reports occurred during the 1960s and 1970s in Hungary and in the former Soviet Union, where H3N2 was recovered from cattle experiencing respiratory disease ( 9 , 23 ). Direct detection of IAV in milk and the potential transmission from cattle to cats through feeding of unpasteurized milk has not been previously reported.

An IAV-associated drop in milk production in dairy cattle appears to have occurred during > 4 distinct periods and within 3 widely separated geographic areas: 1949 in Japan ( 17 ), 1997–1998 and 2005–2006 in Europe ( 19 , 21 ), and 2024 in the United States (this report). The sporadic occurrence of clinical disease in dairy cattle worldwide might be the result of changes in subclinical infection rates and the presence or absence of sufficient baseline IAV antibodies in cattle to prevent infection. Milk IgG, lactoferrin, and conglutinin have also been suggested as host factors that might reduce susceptibility of bovids to IAV infection ( 9 ). Contemporary estimates of the seroprevalence of IAV antibodies in US cattle are not well described in the published literature. One retrospective serologic survey in the United States in the late 1990s showed 27% of serum samples had positive antibody titers and 31% had low-positive titers for IAV H1 subtype-specific antigen in cattle with no evidence of clinical infections ( 24 ). Antibody titers for H5 subtype-specific antigen have not been reported in US cattle.

The susceptibility of domestic cats to HPAI H5N1 is well-documented globally ( 10 – 12 , 25 – 28 ), and infection often results in neurologic signs in affected felids and other terrestrial mammals ( 4 ). Most cases in cats result from consuming infected wild birds or contaminated poultry products ( 12 , 27 ). The incubation period in cats is short; clinical disease is often observed 2–3 days after infection ( 28 ). Brain tissue has been suggested as the best diagnostic sample to confirm HPAI virus infection in cats ( 10 ), and our results support that finding. One unique finding in the cats from this report is the presence of blindness and microscopic lesions of chorioretinitis. Those results suggest that further investigation into potential ocular manifestations of HPAI H5N1 virus infection in cats might be warranted.

The genomic sequencing and subsequent analysis of clinical samples from both bovine and feline sources provided considerable insights. The HA and NA sequences derived from both bovine milk and cat tissue samples from different Texas farms had a notable degree of similarity. Those findings strongly suggest a shared origin for the viruses detected in the dairy cattle and cat tissues. Further research, case series investigations, and surveillance data are needed to better understand and inform measures to curtail the clinical effects, shedding, and spread of HPAI viruses among mammals. Although pasteurization of commercial milk mitigates risks for transmission to humans, a 2019 US consumer study showed that 4.4% of adults consumed raw milk > 1 time during the previous year ( 29 ), indicating a need for public awareness of the potential presence of HPAI H5N1 viruses in raw milk.

Ingestion of feed contaminated with feces from wild birds infected with HPAI virus is presumed to be the most likely initial source of infection in the dairy farms. Although the exact source of the virus is unknown, migratory birds (Anseriformes and Charadriiformes) are likely sources because the Texas panhandle region lies in the Central Flyway, and those birds are the main natural reservoir for avian influenza viruses ( 30 ). HPAI H5N1 viruses are well adapted to domestic ducks and geese, and ducks appear to be a major reservoir ( 31 ); however, terns have also emerged as an important source of virus spread ( 32 ). The mode of transmission among infected cattle is also unknown; however, horizontal transmission has been suggested because disease developed in resident cattle herds in Michigan, Idaho, and Ohio farms that received infected cattle from the affected regions, and those cattle tested positive for HPAI H5N1 ( 33 ). Experimental studies are needed to decipher the transmission routes and pathogenesis (e.g., replication sites and movement) of the virus within infected cattle.

In conclusion, we showed that dairy cattle are susceptible to infection with HPAI H5N1 virus and can shed virus in milk and, therefore, might potentially transmit infection to other mammals via unpasteurized milk. A reduction in milk production and vague systemic illness were the most commonly reported clinical signs in affected cows, but neurologic signs and death rapidly developed in affected domestic cats. HPAI virus infection should be considered in dairy cattle when an unexpected and unexplained abrupt drop in feed intake and milk production occurs and for cats when rapid onset of neurologic signs and blindness develop. The recurring nature of global HPAI H5N1 virus outbreaks and detection of spillover events in a broad host range is concerning and suggests increasing virus adaptation in mammals. Surveillance of HPAI viruses in domestic production animals, including cattle, is needed to elucidate influenza virus evolution and ecology and prevent cross-species transmission.

Dr. Burrough is a professor and diagnostic pathologist at the Iowa State University College of Veterinary Medicine and Veterinary Diagnostic Laboratory. His research focuses on infectious diseases of livestock with an emphasis on swine.

Acknowledgment

We thank the faculty and staff at the ISUVDL who contributed to the processing and analysis of clinical samples in this investigation, the veterinarians involved with clinical assessments at affected dairies and various conference calls in the days before diagnostic submissions that ultimately led to the detection of HPAI virus in the cattle, and the US Department of Agriculture National Veterinary Services Laboratory and NAHLN for their roles and assistance in providing their expertise, confirmatory diagnostic support, and communications surrounding the HPAI virus cases impacting lactating dairy cattle.

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• Figure 1 . Mammary gland lesions in cattle in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. A, B) Mammary...
• Figure 2 . Lesions in cat tissues in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. Tissue sections were stained...
• Figure 3 . Phylogenetic analysis of hemagglutinin gene sequences in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. Colors indicate...
• Figure 4 . Phylogenetic analysis of neuraminidase gene sequences in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. Colors indicate...
• Table 1 . Microscopic lesions observed in cattle in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024
• Table 2 . Microscopic lesions observed in cats in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024
• Table 3 . PCR results from various specimens in study of highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024

Suggested citation for this article : Burrough ER, Magstadt DR, Petersen B, Timmermans SJ, Gauger PC, Zhang J, et al. Highly pathogenic avian influenza A(H5N1) clade 2.3.4.4b virus infection in domestic dairy cattle and cats, United States, 2024. Emerg Infect Dis. 2024 Jul [ date cited ]. https://doi.org/10.3201/eid3007.240508

DOI: 10.3201/eid3007.240508

Original Publication Date: April 29, 2024

Table of Contents – Volume 30, Number 7—July 2024

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