# Advisers' perception of biosecurity implementation on large-scale poultry farms in Europe

Rozenn Souillard, Virginie Allain, Anne Christine Dufay-Lefort, Nathalie

Rousset, Arthi Amalraj, Annick Spaans, Artur Zbikowski, Alessandra

Piccirillo, Sandra Sevilla-Navarro, László Kovács, et al.

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► To cite this version:

Rozenn Souillard, Virginie Allain, Anne Christine Dufay-Lefort, Nathalie Rousset, Arthi Amalraj, et al. Advisers' perception of biosecurity implementation on large-scale poultry farms in Europe. Preventive Veterinary Medicine, 2025, 241, pp.106552. 10.1016/j.prevetmed.2025.106552. anses-05118089

HAL Id: anses-05118089

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# Advisers' perception of biosecurity implementation on large-scale poultry farms in Europe

Rozenn Souillard<sup>a,1,*</sup>, Virginie Allain<sup>a,1</sup>, Anne Christine Dufay-Lefort<sup>b</sup>, Nathalie Rousset<sup>b</sup>, Arthi Amalraj<sup>c</sup>, Annick Spaans<sup>d</sup>, Artur Zbikowski<sup>e</sup>, Alessandra Piccirillo<sup>f</sup>, Sandra Sevilla-Navarro<sup>g</sup>, László Kovács<sup>h,i</sup>, Sophie Le Bouquin<sup>a</sup>

## ARTICLE INFO

### Keywords:

Biosecurity

Adviser

Poultry

Europe

## ABSTRACT

Biosecurity is a fundamental preventive tool to control animal infectious diseases. The relationship between advisers and farmers plays a key role in determining farmers' compliance with on-farm biosecurity measures (BMs). The aims of this survey were (1) to provide an overview on the implementation of biosecurity in European poultry farms as declared by the advisers and (2) to better understand advisers' perception of the reasons why farmers do not comply with biosecurity rules and pinpoint potential obstacles to their implementation. One hundred and fifty-seven advisers working in various poultry sectors (breeders, enclosed and free-range layers, enclosed and free-range meat poultry) were interviewed to give their opinion on the implementation of 62 BMs. The advisers' replies (n = 6485) on the implementation of BMs were reported as "always" (67.6 %), "sometimes" (19.8 %) and "never" (8.1 %) implemented. The advisers from the local governmental institutions declared a significantly lower percentage of "always implemented" replies (62 %) than those from other categories (producer organisations (73.7 %), companies (73.8 %) and veterinary clinics (67 %)). Regardless of the poultry sector, the most commonly implemented BMs declared by the advisers were the "daily surveillance of birds", "flock register", "rodent control" and "feed storage protection". The BMs declared as the least commonly implemented were "visitors and personnel showering before entering the poultry house" for all the surveyed productions and "personnel hand washing" for all the production types except breeders. Some hygiene practices were also declared to be poorly implemented in most of the surveyed productions such as the "cleaning/disinfection of the rendering tank after each collection", the "presence of concrete area around the house", the "use of separate material for the poultry house" and the "restriction of domestic animals entering the site" and especially in meat poultry "the bacterial self-check of the house" and "the cleaning/disinfection of the feed silo between each flock". According to the advisers 'reports, the reasons why farmers do not comply with biosecurity on their farm were insufficient knowledge of biosecurity issues ("not enough training" 12.3 % and "not enough advice" 8.5 %), low awareness of the expected benefits ("no known advantages" 14 % and "not useful" 4.6 %), the lack of time (17.8 %), financial issues (16.8 %) and the unsuitability of the measures (17.4 %). This study highlighted, from the European advisers 'point of view, the shortcomings of the implementation of biosecurity on poultry

<footnote><sup>a</sup> Epidemiology, Health and Welfare Unit, French Agency for Food, Environmental and Occupational Health & Safety, Ploufragan, France</footnote>

<footnote><sup>b</sup> French Technical Institute of Poultry Farming, Rabbit Farming and Aquaculture, Paris, France</footnote>

<footnote><sup>c</sup> Department of Internal Medicine, Reproduction and Population Medicine, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium</footnote>

<footnote><sup>d</sup> Southern Agriculture and Horticulture Organization, 's Hertogenbosch, Netherlands</footnote>

<footnote><sup>e</sup> Department of Pathology and Veterinary Diagnostics, Institute of Veterinary Medicine, Warsaw University of Life Sciences, Warsaw, Poland</footnote>

<footnote><sup>f</sup> Department of Comparative Biomedicine and Food Science, University of Padova, Legnaro, Italy</footnote>

<footnote><sup>g</sup> Poultry Quality and Animal Nutrition Centre of the Valencia Region, Castellón, Spain</footnote>

<footnote><sup>h</sup> Department of Animal Hygiene, Herd Health and Mobile Clinic, University of Veterinary Medicine, Budapest, Hungary</footnote>

<footnote><sup>i</sup> Poultry Care Kft., Újszász, Hungary</footnote>

<footnote>* Correspondence to: ANSES (French Agency for Food, Environmental and Occupational Health & Safety), Ploufragan 22440, France.</footnote>

<footnote>E-mail addresses: rozenn.souillard@anses.fr (R. Souillard), virginie.allain@anses.fr (V. Allain), anne-christine.lefort@elancoah.com (A.C. Dufay-Lefort), rousset@itavi.asso.fr (N. Rousset), Arthi.Amalraj@UGent.be (A. Amalraj), annick.spaans@zlto.nl (A. Spaans), artur_zbikowski@sggw.edu.pl (A. Zbikowski), alessandra piccirillo@unipd.it (A. Piccirillo), s.sevilla@cecav.org (S. Sevilla-Navarro), kovacs.laszlo@univet.hu (L. Kovács), Sophie.LEBOUQUIN-LENEVEU@anses.fr (S. Le Bouquin).</footnote>

<footnote n="1">¹ Equal contributions</footnote>
farms and a room of improvement requiring adapted and tailored support measures for a better biosecurity
compliance.

# 1. Introduction

Animal health is a key issue in the European Union for ensuring public health, animal production and food safety. In recent years, European animal farming has faced devastating contagious diseases such as African swine fever, epizootic haemorrhagic disease (https://www.efsa.europa.eu/en/topics/topic/animal-health) and successive major epizootic outbreaks of highly pathogenic avian influenza (HPAI) (Fusaro et al., 2024). These health threats require stakeholders to enhance the prevention of transmissible and epizootic animal diseases. The European Union is one of the world's largest poultry meat producers with more than 13.4 million tons produced annually. Seventy-three percent of European poultry production in 2023 comes from six Member States: Poland (21 %), Spain (13 %), Germany (12 %), France (11 %), Italy (10 %) and the Netherlands (6 %) (https://agriculture.ec.europa.eu). The European poultry sector is characterised by the growth of animal and food trade between Member States. In this context of broad commercial European exchange, the spread of transmissible poultry diseases such as highly pathogenic avian influenza can result in devastating economic and social consequences for the European poultry sector. This threat requires enhanced disease control and preventive strategies throughout the European Union. Adopted in 2016 by the European Parliament, the "Animal Health Law" provides the regulatory framework and requirements for transmissible animal diseases in European Member States including their prevention, surveillance and eradication and emphasising on biosecurity as a major preventive tool (Regulation (EU) 2016/429; Council., 2019). Biosecurity is a fundamental component of preventive practices to avoid the transmission of pathogens, including measures to reduce the risk of introduction (external biosecurity) and the spread of pathogens (internal biosecurity) (Gelaude et al., 2014; OIE, 2019).

The expected benefits of BMs in preventing and controlling farmed animals infectious diseases are well known, particularly in poultry farms against the influenza virus (Ssematimba et al., 2013; Guinat et al., 2020) and food-borne zoonotic agents such as Salmonella or Campylobacter (Hald et al., 2000; Snow et al., 2010). However, many studies report a sub-optimal application of BMs. Shortcomings are commonly reported on poultry farms, for instance regarding the practices of personnel and visitors in the anteroom or vehicle flow on the farms (Dorea et al., 2010; Racicot et al., 2011; Van Limbergen et al., 2018). Improving biosecurity compliance in animal farming is challenging. A better understanding of the barriers and obstacles to the proper application of BMs on farms is needed.

Many factors are reported to influence the implementation of BMs on farms, such as the age, level of knowledge, attitudes, personality traits and access to information of the farm workers (Racicot et al., 2012b; Cui and Liu, 2016; Delpont et al., 2021b). Training in biosecurity practices and personalised coaching have been shown to improve biosecurity compliance on farms (Van Limbergen et al., 2018; Amalraj et al., 2024a; Delpont et al., 2024). Veterinarians are often considered the farmers' main contacts and interlocutors regarding biosecurity advice and support. The relationship between veterinarians and farmers has already been reported to influence the implementation of biosecurity measures due to several factors that include the degree of trust placed in the veterinarian, the time spent discussing biosecurity, their mutual knowledge, a demonstration of the cost-benefit of BMs and finally the level of communication and cooperation (Chomyn et al., 2023; Grant et al., 2023).

Despite the importance of biosecurity measures as a preventive tool in the European poultry sector and the key role of advisers in determining farmers' compliance with on-farm biosecurity measures, there is

little data on the European advisers' point of view regarding biosecurity adherence on poultry farms and the potential difficulties encountered by farmers. Most studies investigating advisers' perceptions of biosecurity have had a limited number of participants and very few have included poultry advisers (Moya et al., 2021; Grant et al., 2023; Laconi et al., 2023). Biosecurity implementation in poultry farms is commonly assessed through studies with farmers (Van Steenwinkel et al., 2011; Gelaude et al., 2014; Van Limbergen et al., 2018). As part of the NETPOULSAFE project, a large interview study was recently conducted with 192 poultry farmers in seven European countries (Belgium, France, Hungary, Italy, the Netherlands, Poland and Spain). The NETPOULSAFE project - Networking European poultry actors for enhancing the compliance of biosecurity measures for a sustainable production - is a EU thematic network designed to stimulate knowledge exchange between European poultry actors to improve biosecurity compliance in poultry farming. The interview study revealed that farmers declared an overall good level of biosecurity, while showing deficiencies in areas such as personnel and vehicle entry into farms, the presence of other animals and certain hygiene practices (Souillard et al., 2024). It thus showed that there was room for improvement, requiring support measures to help farmers improve biosecurity compliance on their farms. Given the fundamental relationship between advisers and farmers in the implementation of biosecurity, it was necessary to supplement the farmers' point of view by investigating how European advisers perceived the implementation of BMs. Indeed, the advisers provide a broad overview of biosecurity implementation on poultry production in Europe while the farmers' view focuses on their own farm (Souillard et al., 2024). This interview study of 157 European poultry advisers aimed 1) to provide an overview of the implementation of BMs on poultry farms as expressed by the advisers and (2) to understand what the advisers thought were the reasons for, and potential obstacles to non-compliance.

# 2. Materials and methods

## 2.1. Adviser sample selection

In each participating country (Belgium, France, Hungary, Italy, the Netherlands, Poland and Spain), the Network Facilitator (NF) (national coordinator of the NETPOULSAFE Network), with experience and knowledge of the national poultry productions, selected the advisers in a two-step process using the same approach in each country. This study was designed to acquire a broad picture of advisers' views on the implementation of BMs on farms while taking into account the wide diversity of poultry production types and farming systems at European level, without being representative of national poultry productions. Consequently, a minimum of four poultry productions in each participating country were chosen by the NF: enclosed broiler and enclosed layer productions were required, then the choice of the other production types (breeders, free-range layers, enclosed ducks, enclosed turkeys and free-range meat poultry) was dependent on the national specificities, as well as the business model (i.e. independent or under contract with a company). Within each country and production, the NF identified four specialist advisers willing to participate in the study, based on their broad experience and on the close and frequent contact with poultry farms in a given type of production. The advisers could be employed in producer organisations (interprofessional body/quality label/other organisation), poultry production companies, veterinary clinics or local governmental institutions.
## 2.2. Data collection

Data were collected in each country between April and September 2021 by the NF using a survey questionnaire. The questionnaire was developed by a working group including the 7 NFs from each country. The questions were written in English and each NF was free to translate it into their own language for the interviews. Previous tests on farms ensured the standardisation of the data collected and proper understanding of each question/reply option by each NF. The questionnaire used to survey the advisers contained 62 BMs (36 internal and 26 external measures). The first section was common to all the poultry production types and included 26 external BMs under the items "Animal production on the site", "Structure and circulation on the site", "Personnel, visitors or teams", "Poultry at arrival", "Feed and drinking water", "Biological vector control", "Management of poultry manure", "Management of dead animals" and 12 Internal BMs under the items "Structure and circulation in the poultry house", "Management of material or litter in the poultry house", "Cleaning and disinfection of the house and material" and "Management of poultry". Additional specific sections were added for the following types of poultry production, free-range (nine Internal BMs under the item "Management of the free-range area"), breeders (eight internal BMs under the item "Management of hatching eggs") and layers (seven internal BMs under the item "Management of laying eggs"). For each BM, the advisers were asked the following three questions: (1) their opinion on the implementation (Would you say this measure is implemented on the farms? Always, sometimes, never, other frequency, unknown) (2) the reasons for non-compliance with these measures (When a measure is not always implemented on the farms, could you explain the reasons? Takes too much time, too expensive, not suited to the farm, no known advantages, not useful, not enough training, not enough advice, other reason or unknown) and (3) their opinion on the effectiveness of the BMs they declared were not implemented (When a measure is not always implemented on the farms, do you think this biosecurity measure would be effective for the farms and why? Effective, moderately effective, ineffective, other opinion, unknown). In addition to their professional category (producer organisation, companies, veterinary clinics or local governmental institutions), the gender and age of the advisers were also collected. The farming systems (independent for direct sale or under contract with a company) about which the advisers were interviewed was recorded. The adviser questionnaire is available in Supplementary data 1. Seventy percent of the interviews were conducted by the NF by telephone/online meetings and the others during a physical meeting.

## 2.3. Data analysis

The data were entered into the Sphynx® software tool by each national NF. The whole database was exported into Excel 2016 and analysed with R-4.0.2 software (R foundation, Vienna, Austria). Verifications were made to check for missing or potentially incoherent data. We carried out an overall descriptive analysis of all the answers collected from the advisers (e.g. implementation, reason and efficiency), with a focus on both the 10 most commonly implemented BMs (the 10 highest percentages of "always implemented" replies in each poultry production type) and the 10 least commonly implemented BMs (the 10 lowest percentages of "always implemented" replies in each poultry production type). The associated reasons for non-implementation reported by the advisers and their opinion on effectiveness were also studied. An analysis of statistical association was performed using Pearson's Chi-squared test or Student's t-test, with *p* < 0.05 considered to be a significant difference.

# 3. Results

## 3.1. Advisers interviews

A total of 157 adviser interviews were completed in the following production types: 28 breeders, 39 enclosed broilers, 9 enclosed ducks, 32 enclosed layers, 21 enclosed turkeys, 22 free-range layers, and six free-range meat poultry (Table 1). Between 16 and 37 advisers were interviewed in each country. Regarding the farming system, 37.1 % (n = 52) of the advisers were interviewed for independent farms vs. 62.8 % (n = 88) for farms under contract with a company. Both farming systems were found in the seven production types and in each country except Italy (all interviews were for farms under contract with a company). The advisers' characteristics are shown in Table 2. Most of the interviewed advisers were men (74 %). Overall, advisers were between 35 and 55 years of age (54 %) and slightly over half were from veterinary clinics (55 %).

## 3.2. Implementation of biosecurity measures

The 157 interviewed advisers gave a total of 6 485 replies on the implementation of biosecurity measures. Most of the advisers (136/157) answered to the expected number of BMs required for a given poultry production type (21 advisers transmitted incomplete questionnaire with missing data). The analysis of all the advisers' responses (n = 6485) regarding the implementation of BMs revealed the following: "always" accounted for 67.6 %, "sometimes" for 19.8 % and "never" for 8.1 % (Fig. 1a). A statistically significant difference was found between the replies of the advisers interviewed in the 'breeder' poultry production sector with the highest percentage of "always implemented" replies (81 %) compared with all the other production sectors (*p* < 0.001). The farming system was also significantly associated (*p* < 0.001) with the biosecurity level reported by advisers, with a higher percentage of "always implemented" answers for farms under contract with a company (71.5 % vs. 66.2 % for independent farms). The gender of the advisers was significantly associated with the replies on the implementation of BMs, with a percentage of "always implemented" answers reported in 71.1 % of all the replies from women versus 66.5 % from men (*p* < 0.001). The age of advisers was also significantly linked to the responses, with a lower percentage of "always implemented" replies in the category < 35 years of age compared with the 35–55 years and > 55 years age groups, respectively 64.7 %, 69.5 % and 68.6 % (*p* < 0.001). Regarding the advisers' categories, those from local governmental institutions declared a lower percentage of "always implemented" replies (62 %) than advisers in the other categories (producer organisation (73.7 %), companies (73.8 %), veterinary clinics (67 %)) (*p* < 0.001).

## 3.3. The biosecurity measures declared as being most commonly implemented

Table 3 shows the BMs most frequently declared as being implemented by the advisers (with the 10 highest percentages of "always implemented" replies in each poultry production type). Four BMs related to poultry surveillance ("flock register" and "daily surveillance") and to standard hygiene practices ("feed storage protected" and "rodent control") were declared by the advisers as being the most commonly implemented for all the surveyed poultry productions. Other BMs were reported in the top 10 most implemented BMs for more than half of the production types, such as the "presence of a closed and protected rendering tank", "cleaning and disinfection of the poultry house and material between each flock", "register for visitors and teams" and "vaccination protocol for each poultry flock". Regarding the specificities of the free-range and eggs production farms, two BMs ("traceability of the eggs" and "specific egg sorting and storage rooms") in the three surveyed egg productions (breeders, enclosed and free-range layers), along with the "period of sanitary downtime in the free-range area" in
<table><caption>**Table 1**
Distribution of advisers interviewed by poultry production type and country (n = 157).</caption><thead><tr><th>Production</th><th>Belgium</th><th>Spain</th><th>France</th><th>Hungary</th><th>Italy</th><th>Netherlands</th><th>Poland</th><th>Total</th></tr></thead><tbody><tr><td><strong>Breeders</strong></td><td><strong>3</strong></td><td><strong>3</strong></td><td><strong>4</strong></td><td><strong>6</strong></td><td><strong>4</strong></td><td><strong>4</strong></td><td><strong>4</strong></td><td><strong>28</strong></td></tr><tr><td>Independent for direct sales</td><td>1</td><td></td><td></td><td>6</td><td></td><td>4</td><td>3</td><td>14</td></tr><tr><td>Under contract with a company for product sales</td><td></td><td>3</td><td>4</td><td></td><td>4</td><td></td><td>1</td><td>12</td></tr><tr><td>NA*</td><td>2</td><td></td><td></td><td></td><td></td><td></td><td></td><td>2</td></tr><tr><td><strong>Enclosed layers</strong></td><td><strong>5</strong></td><td><strong>4</strong></td><td><strong>4</strong></td><td><strong>4</strong></td><td><strong>7</strong></td><td><strong>4</strong></td><td><strong>4</strong></td><td><strong>32</strong></td></tr><tr><td>Independent for direct sales</td><td>3</td><td>4</td><td></td><td>4</td><td></td><td>4</td><td>1</td><td>16</td></tr><tr><td>Under contract with a company for product sales</td><td>1</td><td></td><td>4</td><td></td><td>6</td><td></td><td>3</td><td>14</td></tr><tr><td>NA</td><td>1</td><td></td><td></td><td></td><td>1</td><td></td><td></td><td>2</td></tr><tr><td><strong>Free-range layers</strong></td><td><strong>3</strong></td><td><strong>4</strong></td><td><strong>4</strong></td><td></td><td><strong>7</strong></td><td><strong>4</strong></td><td></td><td><strong>22</strong></td></tr><tr><td>Independent for direct sales</td><td>1</td><td>4</td><td>2</td><td></td><td></td><td>3</td><td></td><td>10</td></tr><tr><td>Under contract with a company for product sales</td><td>1</td><td></td><td>2</td><td></td><td>6</td><td></td><td></td><td>9</td></tr><tr><td>NA</td><td>1</td><td></td><td></td><td></td><td>1</td><td>1</td><td></td><td>3</td></tr><tr><td><strong>Enclosed broilers</strong></td><td><strong>4</strong></td><td><strong>4</strong></td><td><strong>6</strong></td><td><strong>1</strong></td><td><strong>8</strong></td><td><strong>5</strong></td><td><strong>11</strong></td><td><strong>39</strong></td></tr><tr><td>Independent for direct sales</td><td>2</td><td></td><td></td><td></td><td></td><td>3</td><td>3</td><td>8</td></tr><tr><td>Under contract with a company for product sales</td><td></td><td>4</td><td>6</td><td>1</td><td>6</td><td></td><td>5</td><td>22</td></tr><tr><td>NA</td><td>2</td><td></td><td></td><td></td><td>2</td><td>2</td><td>3</td><td>9</td></tr><tr><td><strong>Enclosed ducks</strong></td><td></td><td><strong>1</strong></td><td><strong>4</strong></td><td><strong>3</strong></td><td></td><td><strong>1</strong></td><td></td><td><strong>9</strong></td></tr><tr><td>Independent for direct sales</td><td></td><td></td><td>1</td><td>1</td><td></td><td></td><td></td><td>2</td></tr><tr><td>Under contract with a company for product sales</td><td></td><td>1</td><td>3</td><td>2</td><td></td><td>1</td><td></td><td>7</td></tr><tr><td><strong>Enclosed turkeys</strong></td><td><strong>1</strong></td><td><strong>3</strong></td><td><strong>4</strong></td><td><strong>3</strong></td><td><strong>6</strong></td><td></td><td><strong>4</strong></td><td><strong>21</strong></td></tr><tr><td>Independent for direct sales</td><td>1</td><td></td><td></td><td></td><td></td><td></td><td></td><td>1</td></tr><tr><td>Under contract with a company for product sales</td><td></td><td>3</td><td>4</td><td>3</td><td>6</td><td></td><td>4</td><td>20</td></tr><tr><td><strong>Free-range meat poultry</strong></td><td></td><td></td><td></td><td></td><td>5</td><td>1</td><td></td><td><strong>6</strong></td></tr><tr><td>Independent for direct sales</td><td></td><td></td><td></td><td></td><td></td><td>1</td><td></td><td>1</td></tr><tr><td>Under contract with a company for product sales</td><td></td><td></td><td></td><td></td><td>4</td><td></td><td></td><td>4</td></tr><tr><td>NA</td><td></td><td></td><td></td><td></td><td>1</td><td></td><td></td><td>1</td></tr><tr><td><strong>All poultry</strong></td><td><strong>16</strong></td><td><strong>19</strong></td><td><strong>26</strong></td><td><strong>17</strong></td><td><strong>37</strong></td><td><strong>19</strong></td><td><strong>23</strong></td><td><strong>157</strong></td></tr><tr><td>Independent for direct sales</td><td>8</td><td>8</td><td>3</td><td>11</td><td>0</td><td>15</td><td>7</td><td>52</td></tr><tr><td>Under contract with a company for product sales</td><td>2</td><td>11</td><td>23</td><td>6</td><td>32</td><td>1</td><td>13</td><td>88</td></tr><tr><td>NA</td><td>6</td><td>0</td><td>0</td><td>0</td><td>5</td><td>3</td><td>3</td><td>17</td></tr></tbody></table>

<table><caption>**Table 2**
Characteristics (gender, age and category) of the advisers interviewed by poultry production type (n = 157).</caption><thead><tr><th rowspan="2"></th><th colspan="2">Gender*</th><th colspan="2">Age*</th><th colspan="2">Category*</th><th rowspan="2">Producer<br>organisation<br>% (n)</th><th rowspan="2">Veterinary<br>clinic<br>% (n)</th><th rowspan="2">Other<br>category<br>% (n)</th></tr><tr><th>Woman</th><th>Man</th><th>&lt; 35</th><th>35-55</th><th>&gt; 55</th><th>Companies</th><th>Local governmental<br>institutions</th></tr></thead><tbody><tr><td><strong>Breeders (n = 28)</strong></td><td>% (n)</td><td>% (n)</td><td>% (n)</td><td>% (n)</td><td>% (n)</td><td>% (n)</td><td>7 (2)</td><td>61 (17)</td><td></td></tr><tr><td></td><td>25 (7)</td><td>75 (21)</td><td>18 (5)</td><td>54<br>(15)</td><td>21 (6)</td><td>21 (6)</td><td>11 (3)</td><td></td><td></td></tr><tr><td><strong>Enclosed layers (n = 32)</strong></td><td>28 (9)</td><td>72 (23)</td><td>31<br>(10)</td><td>47<br>(15)</td><td>22 (7)</td><td>13 (4)</td><td>13 (4)</td><td>19 (6)</td><td>56 (18)</td></tr><tr><td><strong>Free-range layers (n = 22)</strong></td><td>36 (8)</td><td>64 (14)</td><td>23 (5)</td><td>59<br>(13)</td><td>14 (3)</td><td>18 (4)</td><td>18 (4)</td><td>9 (2)</td><td>41 (9)</td><td>14 (3)</td></tr><tr><td><strong>Enclosed broilers (n = 39)</strong></td><td>23 (9)</td><td>74 (29)</td><td>28<br>(11)</td><td>46<br>(18)</td><td>26<br>(10)</td><td>10 (4)</td><td>10 (4)</td><td>5 (2)</td><td>67 (26)</td><td>5 (2)</td></tr><tr><td><strong>Enclosed ducks (n = 9)</strong></td><td>11 (1)</td><td>89 (8)</td><td>22 (2)</td><td>78 (7)</td><td>22 (2)</td><td>11 (1)</td><td></td><td>11 (1)</td><td>56 (5)</td><td></td></tr><tr><td><strong>Enclosed turkeys (n = 21)</strong></td><td>24 (5)</td><td>76 (16)</td><td>24 (5)</td><td>67<br>(14)</td><td>10 (2)</td><td>19 (4)</td><td>10 (2)</td><td>14 (3)</td><td>52 (11)</td><td>5 (1)</td></tr><tr><td><strong>Free-range meat poultry<br>(n = 6)</strong></td><td>17 (1)</td><td>83 (5)</td><td>17 (1)</td><td>50 (3)</td><td>33 (2)</td><td>33 (2)</td><td></td><td>33 (2)</td><td></td><td></td></tr><tr><td><strong>All poultry (n = 157)</strong></td><td>25 (40)</td><td>74<br>(116)</td><td>25<br>(39)</td><td>54<br>(85)</td><td>19<br>(30)</td><td>17 (26)</td><td>13 (20)</td><td>11 (18)</td><td>55 (86)</td><td>4 (6)</td></tr></tbody></table>

the two free-range productions surveyed (layers and meat poultry) were mentioned by the advisers as most commonly applied in these production types.

### 3.4. The biosecurity measures declared as being the least commonly implemented

Table 4 shows the BMs declared by the advisers as being the least commonly implemented based on the 10 BMs with the lowest percentage of “always implemented” replies in each poultry production type. The main BMs declared by the advisers as being the least implemented concern the entry of personnel or visitors to the farms, with “personnel and visitor shower before entering the poultry house” reported in the top

10 least implemented BMs in all the surveyed production types and “personnel wash hands before entering the poultry house” in all the surveyed productions except breeders. Some hygiene practices were also mentioned as least implemented in more than half of the production types, such as “cleaning and disinfection of the rendering tank after each collection”, “no domestic animals on the site”, the presence of “a concrete area around the poultry house” and “recognisable separate material only for the poultry house”, and particularly in meat poultry production “cleaning and disinfection of the feed silo between each flock” and “bacterial self-check of the cleaning and disinfection of the poultry house between each flock”. Regarding the specificities of the free-range and egg production farms, “different personnel in the poultry room and the egg sorting and storage room” in the three surveyed egg productions

<footnote>* NA: missing data.</footnote>

<footnote>* Missing data (gender: n = 1, age: n = 3, category: n = 1).</footnote>
<figure><img src="image_4.png" /><figcaption>**Fig. 1.** Distribution of all the replies given by advisers (n = 157) on implementation of the 62 BMs (1a), the adviser's opinion on the reasons for not implementing the measures (1b), and the adviser's opinion on the effectiveness of those measures that are not implemented (1c) by poultry production type.</figcaption></figure>
<caption>**Table 3**</caption>

Distribution of the 10 biosecurity measures declared by the advisers to be the most commonly implemented by production type with the highest % of “always implemented” replies highlighted in grey.*.

<table><thead><tr><th>Item</th><th>BM</th><th>Description of BM</th><th>Breeders</th><th>Enclosed layers</th><th>Free range layers</th><th>Enclosed broilers</th><th>Enclosed ducks</th><th>Enclosed turkeys</th><th>Free range meat poultry</th></tr><tr><th></th><th></th><th></th><th>% (n)</th><th>% (n)</th><th>% (n)</th><th>% (n)</th><th>% (n)</th><th>% (n)</th><th>% (n)</th></tr></thead><tbody><tr><td>E1</td><td>BM02</td><td>No backyard poultry on the site</td><td>92.9 (28)</td><td>84.4 (32)</td><td>90.9 (22)</td><td>74.4 (39)</td><td>75.0 (8)</td><td>100.0 (21)</td><td>100.0 (6)</td></tr><tr><td rowspan="3">E3</td><td>BM10</td><td>Register for visitors and teams</td><td>92.9 (28)</td><td>87.5 (32)</td><td>81.8 (22)</td><td>84.6 (39)</td><td>88.9 (9)</td><td>95.2 (21)</td><td>100.0 (6)</td></tr><tr><td>BM11</td><td>Specific clothes for visitors before entering the poultry house</td><td>85.7 (28)</td><td>87.5 (32)</td><td>77.3 (22)</td><td>81.6 (38)</td><td>100.0 (9)</td><td>66.7 (21)</td><td>66.7 (6)</td></tr><tr><td>BM12</td><td>Specific shoes for visitors before entering the poultry house</td><td>96.3 (27)</td><td>96.8 (31)</td><td>85.0 (20)</td><td>84.2 (38)</td><td>100.0 (9)</td><td>81.0 (21)</td><td>100.0 (6)</td></tr><tr><td rowspan="2">E4</td><td>BM15</td><td>Flock register</td><td>100.0 (28)</td><td>100.0 (32)</td><td>95.2 (21)</td><td>94.7 (38)</td><td>100.0 (9)</td><td>95.2 (21)</td><td>100.0 (6)</td></tr><tr><td>BM16</td><td>If the chick deliverer enters the poultry house: specific clothes and shoes</td><td>90.0 (20)</td><td>69.0 (29)</td><td>70.6 (17)</td><td>74.1 (27)</td><td>42.9 (7)</td><td>91.7 (12)</td><td>100.0 (2)</td></tr><tr><td>E5</td><td>BM17</td><td>Feed storage protected</td><td>100.0 (28)</td><td>96.9 (32)</td><td>86.4 (22)</td><td>94.9 (39)</td><td>77.8 (9)</td><td>95.2 (21)</td><td>100.0 (6)</td></tr><tr><td>E6</td><td>BM19</td><td>Rodent control</td><td>100.0 (28)</td><td>90.6 (32)</td><td>90.9 (22)</td><td>92.3 (39)</td><td>88.9 (9)</td><td>95.2 (21)</td><td>100.0 (6)</td></tr><tr><td>E8</td><td>BM24</td><td>Presence of a closed and protected rendering tank</td><td>89.3 (28)</td><td>93.8 (32)</td><td>76.2 (21)</td><td>92.1 (39)</td><td>88.9 (9)</td><td>90.0 (20)</td><td>100.0 (6)</td></tr><tr><td>I1</td><td>BM28</td><td>Changing room with two separate zones</td><td>82.1 (28)</td><td>65.6 (32)</td><td>61.9 (21)</td><td>65.8 (38)</td><td>77.8 (9)</td><td>76.2 (21)</td><td>50.0 (6)</td></tr><tr><td rowspan="3">I3</td><td>BM31</td><td>Cleaning and disinfection of the poultry house between each flock</td><td>100.0 (28)</td><td>84.4 (32)</td><td>72.7 (22)</td><td>94.9 (38)</td><td>87.5 (8)</td><td>100.0 (21)</td><td>100.0 (6)</td></tr><tr><td>BM32</td><td>Cleaning and disinfection of the material between each flock</td><td>100.0 (28)</td><td>87.5 (32)</td><td>86.4 (22)</td><td>97.4 (38)</td><td>87.5 (8)</td><td>100.0 (21)</td><td>100.0 (6)</td></tr><tr><td>BM36</td><td>Period of the sanitary downtime > 15 days between each flock</td><td>96.4 (28)</td><td>73.3 (30)</td><td>84.2 (19)</td><td>35.1 (37)</td><td>50.0 (8)</td><td>85.7 (21)</td><td>50.0 (6)</td></tr><tr><td rowspan="2">I5</td><td>BM37</td><td>Vaccination protocol for each poultry flock</td><td>100.0 (25)</td><td>96.6 (29)</td><td>85.7 (21)</td><td>89.5 (38)</td><td>75.0 (8)</td><td>100.0 (21)</td><td>50.0 (6)</td></tr><tr><td>BM38</td><td>Daily surveillance with clinical alert criteria</td><td>100.0 (28)</td><td>93.8 (32)</td><td>95.2 (21)</td><td>94.7 (38)</td><td>88.9 (9)</td><td>100.0 (21)</td><td>100.0 (6)</td></tr><tr><td>I4</td><td>BM47</td><td>Period of sanitary downtime in the free-range area</td><td></td><td></td><td>86.4 (22)</td><td></td><td></td><td></td><td>100.0 (5)</td></tr><tr><td rowspan="3">I5</td><td>BM48-BM56</td><td>Automatic egg collection system</td><td>92.3 (26)</td><td>93.8 (32)</td><td>70.6 (17)</td><td></td><td></td><td></td><td></td></tr><tr><td>BM49-BM57</td><td>Traceability of the eggs</td><td>100.0 (26)</td><td>100.0 (32)</td><td>93.3 (15)</td><td></td><td></td><td></td><td></td></tr><tr><td>BM51-BM58</td><td>Specific egg sorting and storage rooms</td><td>100.0 (24)</td><td>89.3 (28)</td><td>92.3 (13)</td><td></td><td></td><td></td><td></td></tr></tbody></table>

BM: Biosecurity Measure; External items: E1 - Animal production on the site, E3 - Personnel, visitors or teams, E4 - The poultry at arrival, E5 - Feed and drinking water E6 - Biological vector control, E8 - Management of dead animals; Internal items: I1 - Structure and circulation in the poultry house, I3 - Cleaning and disinfection of the house and material, I4 - Management of the free-range area, I5 - Management of poultry or eggs.

<caption>**Table 4**</caption>

Distribution of the 10 biosecurity measures declared by the advisers to be the least commonly implemented by production type with the lowest % of “always implemented” replies highlighted in grey*.

<table><thead><tr><th>Item</th><th>BM</th><th>Description of BM</th><th>Breeders</th><th>Enclosed layers</th><th>Free-range layers</th><th>Enclosed broilers</th><th>Enclosed ducks</th><th>Enclosed turkeys</th><th>Free-range meat poultry</th></tr><tr><th></th><th></th><th></th><th>% (n)</th><th>% (n)</th><th>% (n)</th><th>% (n)</th><th>% (n)</th><th>% (n)</th><th>% (n)</th></tr></thead><tbody><tr><td>E1</td><td>BM01</td><td>All-in/all-out poultry production on the site</td><td>85.7 (28)</td><td>46.9 (32)</td><td>36.4 (22)</td><td>79.5 (39)</td><td>33.3 (9)</td><td>90.5 (21)</td><td>100.0 (6)</td></tr><tr><td rowspan="2">E2</td><td>BM04</td><td>Delimitation with a barrier or secured professional area with access only to necessary vehicles</td><td>67.9 (28)</td><td>51.6 (31)</td><td>36.4 (22)</td><td>56.4 (39)</td><td>44.4 (9)</td><td>85.7 (21)</td><td>83.3 (6)</td></tr><tr><td>BM05</td><td>Wheel dips to disinfect the vehicles or pulverisation before entering the site</td><td>66.7 (27)</td><td>50.0 (32)</td><td>54.5 (22)</td><td>39.5 (38)</td><td>44.4 (9)</td><td>52.4 (21)</td><td>100.0 (4)</td></tr><tr><td rowspan="4">E3</td><td>BM06</td><td>Specific clothes for personnel before entering the poultry house</td><td>75.0 (28)</td><td>56.2 (32)</td><td>45.5 (22)</td><td>43.6 (39)</td><td>44.4 (9)</td><td>47.6 (21)</td><td>50.0 (6)</td></tr><tr><td>BM08</td><td>Personnel wash hands before entering the poultry house</td><td>78.6 (28)</td><td>34.4 (32)</td><td>27.3 (22)</td><td>30.8 (39)</td><td>22.2 (9)</td><td>23.8 (21)</td><td>16.7 (6)</td></tr><tr><td>BM09</td><td>Personnel shower before entering the poultry house</td><td>46.4 (28)</td><td>3.1 (32)</td><td>4.6 (22)</td><td>2.6 (39)</td><td>11.1 (9)</td><td>9.5 (21)</td><td>0.0 (6)</td></tr><tr><td>BM14</td><td>Visitors shower before entering the poultry house</td><td>60.7 (28)</td><td>6.2 (32)</td><td>9.5 (21)</td><td>0.0 (38)</td><td>22.2 (9)</td><td>0.0 (21)</td><td>0.0 (6)</td></tr><tr><td>E4</td><td>BM16</td><td>If the chick deliverer enters the poultry house: specific clothes and shoes</td><td>90.0 (20)</td><td>69.0 (29)</td><td>70.6 (17)</td><td>74.1 (27)</td><td>42.9 (7)</td><td>91.7 (12)</td><td>100.0 (2)</td></tr><tr><td>E6</td><td>BM21</td><td>No domestic animals on the site</td><td>75.0 (28)</td><td>43.8 (32)</td><td>36.4 (22)</td><td>30.8 (39)</td><td>66.7 (9)</td><td>52.4 (21)</td><td>50.0 (6)</td></tr><tr><td>E8</td><td>BM26</td><td>Cleaning and disinfection of the rendering tank after each collection</td><td>60.7 (28)</td><td>37.5 (32)</td><td>28.6 (21)</td><td>31.6 (38)</td><td>22.2 (9)</td><td>60.0 (20)</td><td>66.7 (6)</td></tr><tr><td rowspan="2">I1</td><td>BM27</td><td>Concrete area around the poultry house</td><td>64.3 (28)</td><td>62.5 (32)</td><td>33.3 (21)</td><td>34.2 (38)</td><td>33.3 (9)</td><td>38.1 (21)</td><td>16.7 (6)</td></tr><tr><td>BM28</td><td>Changing room with two separate zones</td><td>82.1 (28)</td><td>65.6 (32)</td><td>61.9 (21)</td><td>65.8 (38)</td><td>77.8 (9)</td><td>76.2 (21)</td><td>50.0 (6)</td></tr><tr><td rowspan="2">I2</td><td>BM29</td><td>Recognisable separate material only for the poultry house</td><td>53.6 (28)</td><td>37.5 (32)</td><td>33.3 (21)</td><td>42.1 (38)</td><td>22.2 (9)</td><td>47.6 (21)</td><td>66.7 (6)</td></tr><tr><td>BM34</td><td>Cleaning and disinfection of the feed silo between each flock</td><td>67.9 (28)</td><td>45.2 (31)</td><td>38.1 (21)</td><td>35.9 (39)</td><td>12.5 (8)</td><td>57.1 (21)</td><td>50.0 (6)</td></tr><tr><td rowspan="2">I3</td><td>BM35</td><td>Bacterial self-check of the cleaning and disinfection of the poultry house between each flock</td><td>78.6 (28)</td><td>56.2 (32)</td><td>45.5 (22)</td><td>28.2 (39)</td><td>0.0 (8)</td><td>33.3 (21)</td><td>0.0 (6)</td></tr><tr><td>BM36</td><td>Period of the sanitary downtime > 15 days between each flock</td><td>96.4 (28)</td><td>73.3 (30)</td><td>84.2 (19)</td><td>35.1 (37)</td><td>50.0 (8)</td><td>85.7 (21)</td><td>50.0 (6)</td></tr><tr><td>I4</td><td>BM44</td><td>Protective net over the free-range area</td><td></td><td></td><td>9.1 (22)</td><td></td><td></td><td></td><td>40.0 (5)</td></tr><tr><td rowspan="4">I5</td><td>BM50</td><td>Hatching eggs disinfected on the farm</td><td>53.9 (26)</td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>BM52-BM59</td><td>Specific entrance for drivers collecting eggs</td><td>61.5 (26)</td><td>37.0 (27)</td><td>54.5 (11)</td><td></td><td></td><td></td><td></td></tr><tr><td>BM53-BM60</td><td>If the driver enters storage rooms to collect eggs: specific clothes and shoes</td><td>75.0 (20)</td><td>40.0 (25)</td><td>44.4 (9)</td><td></td><td></td><td></td><td></td></tr><tr><td>BM54-BM61</td><td>Cleaning and disinfection of the storage room after each collection</td><td>53.9 (26)</td><td>29.6 (27)</td><td>72.7 (11)</td><td></td><td></td><td></td><td></td></tr><tr><td></td><td>BM55-BM62</td><td>Different personnel in the poultry room and the egg sorting and storage rooms</td><td>0.0 (26)</td><td>3.6 (28)</td><td>0.0 (13)</td><td></td><td></td><td></td><td></td></tr></tbody></table>

BM: Biosecurity Measure; External items: E1 - Animal production on the site, E2 - Structure and circulation on the site, E3 - Personnel, visitors or teams, E4 - The poultry at arrival, E6 - Biological vector control, E8 - Management of dead animals; Internal items: I1 - Structure and circulation in the poultry house, I2 - Management of the material or litter in the poultry house, I3 - Cleaning and disinfection of the house and material, I4 - Management of the free-range area, I5 - Management of poultry or eggs.

(breeders, enclosed and free-range layers), along with “protective net over the free range area” in the two free-range productions surveyed (layers and meat poultry) were mentioned by the advisers as the least commonly applied in these production types.

### 3.5. Reasons for non-compliance with biosecurity measures and opinion on effectiveness

Considering all the replies collected, the reasons reported by advisers

for not always implementing measures (n = 2895) varied (Fig. 1b): “takes too much time” (17.8 %), “not suited to the farm” (17.4 %) “too expensive” (16.8 %), “no known advantages” (14 %), “not enough training” (12.3 %) “not enough advice” (8.5 %) and “not useful” (4.6 %). About 70 % of BMs reported least implemented were considered effective, with only 13.6 % being judged ineffective (Fig. 1c).

Fig. 2 shows the specific reasons of non-implementation mentioned by the advisers for each BM they reported in the top 10 “least implemented” measures. Fig. 3 describes the opinion of the advisers on the

<footnote>* It is possible to have more than 10 BMs in the event of similar percentages</footnote>

<footnote>* It is possible to have more than 10 BMs in the event of similar percentages</footnote>
<figure><img src="image_5.png" /><figcaption>**Fig. 2.** Distribution of the reasons reported by advisers for non-implementation of the biosecurity measures declared to be least commonly implemented. * n = total number of replies, the question about reasons for non-implementation was only asked when the BM was declared not to be implemented. BM: Biosecurity Measure; External items: E1 - Animal production on the site, E2 - Structure and circulation on the site, E3 - Personnel, visitors or teams, E4 - The poultry at arrival, E6 - Biological vector control, E8 - Management of dead animals; Internal items: I1 - Structure and circulation in the poultry house, I2 - Management of the material or litter in the poultry house; I3 - Cleaning and disinfection of the house and material, I4 - Management of the free-range area, I5 - Management of poultry or eggs.</figcaption></figure>

<figure><img src="image_6.png" /><figcaption>**Fig. 3.** Distribution of the adviser's opinion on the effectiveness of the biosecurity measures declared least commonly implemented. * n = total number of replies, the question about the effectiveness was only asked when the BM was declared not to be implemented. BM: Biosecurity Measure; External items: E1 - Animal production on the site, E2 - Structure and circulation on the site, E3 - Personnel, visitors or teams, E4 - The poultry at arrival, E6 - Biological vector control, E8 - Management of dead animals; Internal items: I1 - Structure and circulation in the poultry house, I2 - Management of the material or litter in the poultry house; I3 - Cleaning and disinfection of the house and material, I4 - Management of the free-range area, I5 - Management of poultry or eggs.</figcaption></figure>
effectiveness of these measures declared not-implemented. According to the advisers, the poor implementation of the practices related to the entry of personnel/visitors to the house was mainly due to a “lack of time”. For the “personnel wash hands before entering the poultry house”, the following reasons were mentioned: “lack of time”, “No known advantages” and “Not enough training and advice”. The reason for the non-application of “personnel and visitors shower before entering the poultry house” was mainly reported as “Too time consuming” or “Not suited to the farm”. The practices related to the entry of personnel/visitors were deemed by the advisers to be widely effective for the farms (in over 80 % of replies), except the showering (about 50 % of the replies). It was mentioned by the advisers that showering would be an excessive practice and that farm specific clothes/ shoes and hand washing could be sufficient particularly in meat poultry farms.

The “lack of time” reason was also mentioned by the advisers for the hygiene practices of cleaning and disinfection, along with the reason “No known advantages” frequently reported for the “cleaning and disinfection of the rendering tank after each collection” and the reasons “Too expensive”, “No known advantage” and “Not enough training and advice” for “cleaning and disinfection of the feed silo between each flock”. Regarding the advisers' opinion on the effectiveness of these practices, “the cleaning/disinfection of the rendering tank after each collection” was deemed by the advisers to be widely effective for the farms (in over 80 % of replies), whereas the “cleaning/disinfection of the feed silo between each flock” was declared less effective (about 50 % of the replies). It was mentioned by the advisers that the cleaning/ disinfection of the silo could be applied periodically or only in cases of health problems (salmonella or mycotoxins), especially in meat poultry, given the moisture risks and the difficulty of implementation. Consider- ing “no domestic animals on the site”, the main reasons reported for not implementing this measure on the farms were “No known advan- tages” and “Not enough training and advices”. The advisers also re- ported that the farmers usually consider domestic animals as pest control, guards for their farms and as cultural or habit practice. The banning of domestic animals on site was largely considered by the ad- visers as an effective biosecurity practice for the farms (in nearly 75 % of the replies).

Regarding measures related to the management of the farms (“all-in/ all-out poultry production on the site” and “period of sanitary downtime between each flock”) and to the structural characteristics of the farms (“specific entrance for drivers collecting eggs” and “different personnel in the poultry room and the egg sorting and storage rooms”), the ad- visers mainly explained their poor implementation as “Not suited to the farm”. Among these management characteristics, “all-in/all-out poultry production on the site” was reported by the advisers to be the most effective measure for the farms (88 % of the replies).

It is also worth noting that the advisers more frequently replied that “the cost” was the reason for not implementing measures related to equipment of the farms, such as “concrete area around the poultry house”, “recognisable separate material only for the poultry house” or “protective net over the free-range area” as well as “bacterial self-check of the cleaning and disinfection of the poultry house between each flock”. The advisers deemed the concrete area and the recognisable separate material efficient in more than two thirds of the replies, whereas the net was reported as much less efficient. The “bacterial self-check of the cleaning and disinfection of the house between each flock” was declared as efficient in slightly more than half of the replies (57 %). It was reported by advisers that a standardised protocol of cleaning/ disinfection along with a periodic bacteriological checks could be suf- ficient especially in the meat poultry sector.

## 4. Discussion

Given the key relationship between advisers and farmers in improving biosecurity compliance on farms, this study provides a broad

overview of advisers' perceptions of the implementation of BMs on poultry farms in Europe, highlighting, from their point of view, the difficulties encountered by farmers. In order to consider the great diversity of poultry productions in Europe, the national NFs were free to choose the surveyed productions (except enclosed broilers and layers, the two main type of productions in Europe) and the business model (under contract or independent) according to the specificities of each country. For each production type, the advisers were chosen by the NF for their broad expertise and experience in poultry management. Consequently, it is necessary to take into account the potential selection bias of the interviewed advisers, related both to the subjectivity of the NFs in their sampling choice and to the likely diversity of adviser profiles. However, our study was not designed to be representative of the national poultry production sectors in each country, but rather to highlight the broad field-level views of European advisers with regard to the implementation of BMs on farms, considering the full diversity of poultry production in Europe. Moreover, to limit a potential data collection bias, the questionnaires were administered only by the NF in each country, trained to standardise the way the questions were posed to the advisers and to ensure the proper understanding of each question and reply option. It is worth noting that the reply options “not enough training”/“not enough advice” and “no known advantages”/“not useful” had relatively similar meanings and respectively refer to the notions “low awareness of the expected benefits” and “lack of biosecurity knowledge”. Aside from these limitations, this study provides a broad overview of advisers' perception of the implementation of biosecurity in poultry and the potential difficulties encountered by farmers throughout Europe. With more time and resources, the study could have been more original with the inclusion of the social relationship between farmers and advisers or actual behaviours on farms. However, this is the first large-scale study on the advisers' opinion regarding biosecurity implementation in poultry that considers the full diversity of poultry farming in Europe.

The study shows that most of the advisers' replies (67.6 %) on BM implementation were declared as “always implemented”. The evaluation of biosecurity levels is often complex and challenging when based on declarative statements in contrast to methods capturing what is truly implemented on the farm. Farmers tended to declare higher biosecurity levels when they were interviewed about their own farms (81 % of replies “always implemented”) (Souillard et al., 2024). Racicot et al.'s work suggests that the percentage of “always implemented” could be an over-estimation of reality (Racicot et al., 2011). One difference was already shown between what farmers declared about their own farms and what the managers of these farms thought was happening (Nespeca et al., 1997). There is likely a gap between the statements made by the poultry farmers and what is actually applied on the farms, requiring for example the use of video surveillance in the anteroom to actually assess compliance with these practices (Racicot et al., 2011). The biosecurity level was reported as significantly lower among advisers employed in local governmental institutions compared with advisers from other categories (producer organisations, companies and veterinary clinics). One possible explanation could be more stringent requirements for advisers employed by government authorities, who are highly experienced and skilled in animal health and biosecurity legislation and used to carrying out inspections. A lower level of biosecurity implementation was also reported by advisers from veterinary clinics. A possible explanation could be due to their perception of biosecurity as an essential tool in preventing animal diseases, one of the main priorities of the profession. This has also been investigated by Gröndal et al. who reported that better awareness of biosecurity aspects could be one reason for a more critical assessment of biosecurity applied on farms (Gröndal et al., 2023). A lower level of biosecurity implementation was also reported by advisers aged < 35 years, which perhaps could be explained by the stricter requirements of younger advisers, may be more aware of more recent concepts of biosecurity and guidelines. Regarding the poultry production types, a statistically higher level of biosecurity
was reported by the advisers in the “breeder” farms as compared to the other poultry productions. This perception of better biosecurity levels among breeders could be due to more stringent health requirements in this production stage, including a strict *Salmonella* regulation programme (Regulation (EC) No 2160/2003). The financial consequences of infectious diseases on breeders could also explain why biosecurity measures may be more implemented on these farms. Moreover, a lower level of biosecurity was reported by the advisers on independent farms than on farms under contract with a company (66.2 % vs 71.5 %). This finding supports a previously reported perception of lower biosecurity implementation levels on independent farms (Van Steenwinkel et al., 2011; Delpont et al., 2021a), which is probably due to poorer guidance and technical support on biosecurity implementation for farmers in these farms. This higher biosecurity level in breeders compared to the other poultry productions and for farms under contract with a company compared to independent farms was also previously reported by European farmers interviewed on their own farm (Souillard et al., 2024).

Our findings show that several BMs were declared by the advisers to be most frequently implemented irrespective of the surveyed poultry production types. These BMs are related to the surveillance of poultry (flock register, daily surveillance, traceability of eggs) and basic hygiene practices (feed storage protected and rodent control). The presence of a closed rendering tank and the cleaning/disinfection of the poultry house and material between each flock were also reported by the advisers as most commonly implemented. The high implementation of these practices on the farms as declared by the advisers could be explained by the regulatory status of these biosecurity measures as required in the European “Animal Health Law” (Regulation (EU) 2016/429). Indeed, the European regulation requires of the EU Members States the surveillance of animals (health, behaviour and abnormal mortalities), record-keeping obligations (species, number of animals, date and place of origin and destination) and the implementation of appropriate biosecurity measures on farms, such as the cleaning and disinfection, rodent control, the procedures for the entrance of personnel and vehicles onto the farms and a system for the safe disposal of dead animals. The daily monitoring of birds and the traceability of poultry and eggs are key components of poultry management and the basic hygiene measures are generally reported to be correctly applied on farms (Van Limbergen et al., 2018; Tilli et al., 2022). The recent interview study with European farmers also showed that daily surveillance, rodent control and feed storage protection, were the measures the farmers declared as being the most commonly implemented on their own farms regardless the production type (Souillard et al., 2024).

However, some specific hygiene shortcomings were reported by the advisers in several poultry productions. The secured protection of feed is reported by the advisers to be correctly implemented in all the surveyed productions, while the cleaning/disinfection of the silo between each flock is declared poorly implemented. It is well known that unprotected feed can become contaminated by various pathogens from the feces of rodents or wild birds, especially by *Salmonella*, one of the most common biological hazards in feed (Colett and Smith, 2020; Obe et al., 2023). This could explain why the secured protection of feed, a proven and usefulness practice, is reported by the advisers to be widely applied on the farms. However, one biosecurity point is the cleaning/disinfection of the feed chain, such as feeders and external silos. From the advisers' point of view, the cleaning/disinfection of the silo between each flock was reported as poorly implemented on the farms, especially in meat poultry with better implementation in breeder and egg-layer farms. It is worth noting that the lifespan of broilers is much shorter than breeders or layers. Hence, the short cycle leads to more frequent decontamination periods. The cleaning/disinfection of the silo was also declared as the least regularly applied by farmers on their own farms. Farmers mainly reported that they did not perceive the expected benefits of this measure (Souillard et al., 2024). It was reported both by the farmers and advisers the difficulty in reaching the silos and the fear of moisture retention and mould. The contamination of feed can occur during the unsecured

storage on the farms, but also during the production or the transport of the feed (Gelaude et al., 2014). Without cleaning/disinfection of the silo, dirt or feed residues from the previous cycle could promote the development of moulds or micro-organisms. Breeder and layer farms are included in high-level of *Salmonella* regulation programmes (Regulation (EC) No 2160/2003), which could explain why this measure would be more commonly implemented in these productions.

The bacterial self-check of the poultry house between each flock is also declared to be less implemented by the advisers especially in meat poultry farms, in their opinion mainly due to the cost of this measure. The poor application of this practice was also reported by European meat poultry farmers interviewed on their own farm in our previous study (Souillard et al., 2024). The farmers had reported costs as the reason for non-implementation along with the lack of usefulness and awareness of the expected benefits of this measure (Souillard et al., 2024). A bacterial self-check of the poultry house provides verification of cleaning/disinfection effectiveness and could serve as a warning signal (Racicot and Vaillancourt, 2015). This practice is more commonly implemented to check cleaning/disinfection before the arrival of new flocks on breeder and layer farms probably due to the higher monetary value of these farms and a better perception of the cost-benefit.

Regarding the disposal of dead animals, according to the advisers the presence of a closed rendering tank seems to be well implemented on the farms, but the cleaning/disinfection after each collection of carcasses is reported to be poorly applied in several poultry productions. It is well known that carcasses are a source of contamination in case of infectious diseases on the farms, but also in flocks that may be healthy carriers of pathogens, such as *C botulinum* already detected in carcasses tank in broiler healthy farms (Souillard et al., 2021). Carcasses as a decaying organic matter harboring high amounts of protein substrates and anaerobic conditions are known to support the growth of *C. botulinum* (Annihalli et al., 2013). Consequently, safe disposal of dead animals in a closed tank is needed to avoid the proliferation of insects and vermin that could become vectors of pathogens (Regulation (EU) 2016/429; Racicot and Vaillancourt, 2015). Removal of carcasses by the rendering truck also represents a high risk for the farms (Van Limbergen et al., 2018), requiring specific biosecurity measures to prevent contamination during the truck's movements (protection of containers and isolation from the poultry houses). The rendering truck could also contaminate the tank when collecting the carcasses. However, the cleaning/disinfection of the rendering tank after each collection of carcasses is a rarely emphasised point. Although specific data proving the expected benefit of this practice is lacking, this measure should not be neglected. An uncleaned tank could remain a source of contamination for the farm, because the insects or vermin could be attracted despite that the tank is closed and become potential vectors of pathogens. According to the advisers' perception, this shortcoming could be mainly due to a lack of time and low awareness by farmers of expected benefits. In addition, a lack of training/advice was also declared by European farmers as a reason for not applying this measure on their own farms (Souillard et al., 2024). The advisers widely considered that the cleaning/disinfection of the rendering tank after each collection would be efficient for the farms where this practice was not applied. Providing specific explanations to the farmers on the potential risks of an uncleaned rendering tank on their farm could improve compliance with this biosecurity practice.

Other biosecurity measures were declared by the advisers as least implemented on several poultry productions, such as “the concrete area around the poultry house”, “separate materiel for the poultry house” and “domestic animals on the site”. Costs are the main reason given by the advisers to explain the absence of a concrete area around the house and separate materiel for the poultry house, as was previously reported by the farmers interviewed on their own farms (Souillard et al., 2024). The concrete area, particularly at the entrance is a cleaner more easily washable area (Colett and Smith, 2020) and allows a better rodent control. Even if the cost-benefit of this measure is difficult to demonstrate, this measure could increase the overall biosecurity level of farms
and was mentioned as relatively efficient by the advisers. However, a graveled area could also be an acceptable alternative for clean surrounding. In the same way, it is difficult to prove the cost-benefit of dedicated poultry material, but this practice is probably more reliable than the cleaning/disinfection, that can be easily forgotten. Regarding the banning of domestic animals on site (dogs and cats), the advisers consider that the farmers are not aware of the advantages of this measure. This is confirmed by opinions of European farmers interviewed about their own farms (Souillard et al., 2024). It was reported both by the farmers and advisers that the presence of domestic animals was considered useful as guard and pest control. However, it is known that domestic animals can be mechanical or biological carriers of various pathogens, such as Salmonella (Racicot and Vaillancourt, 2015). Their restriction on farms was deemed highly efficient by the advisers. For better compliance with this measure, it is necessary to explain to the farmers the risks of this practice and the expected benefits for their farms.

Finally, two biosecurity measures related to the entry of personnel or visitors on the farms were reported by the advisers as being least implemented in almost all productions: showering (visitors and personnel) was reported to be the least implemented in all the surveyed productions and hand washing by personnel for all the productions except breeders. Showering before entering the poultry house has already been reported as poorly implemented on European broiler farms (Van Limbergen et al., 2018). This measure was also declared least implemented in all the productions by the European farmers interviewed on their own farms (Souillard et al., 2024). According to the advisers, the main reason for not implementing this practice are “a lack of time” and “not suited to the farm”, as it was also declared by the farmers (Souillard et al., 2024). The advisers did not deem the practice highly efficient, reporting it as “excessive”, especially for the meat production. Although we did not specifically collect this data, showers are probably not available on most meat poultry farms. Showering is a measure more commonly applied in in hatcheries and breeder farms, given the higher biosecurity levels as previously shown in Italian poultry farms (Laconi et al., 2023). The advisers also mentioned that “personnel hands washing” was infrequently implemented in all the surveyed poultry productions (except breeders). In our previous survey, the farmers interviewed on their own farm did not declare this practice as one of the least implemented measures (Souillard et al., 2024). This could be explained by the potential gap between their declaration and what they actually applied on their farms. Racicot et al. have investigated the compliance with biosecurity routines by using video and shown many errors in the anteroom; these include hand washing which was not systematic (Racicot et al., 2011). To explain the shortcoming of personnel hand washing, the advisers frequently gave the reason “no known advantages”, “not enough training/advice” and “lack of time”, as reported by the farmers themselves (Souillard et al., 2024). The infrequent application of this BM could be due to a lack of awareness of the risks, requiring a better explanation of its benefits and usefulness. Personnel entering the poultry house poses high biosecurity risk, particularly the non-implementation of hands washing (Racicot et al., 2011, 2013). This practice was declared highly efficient by the advisers. A study using ultraviolet light to expose microbiological contamination showed the effectiveness of the BMs in the anteroom, including hands washing, and confirmed the great importance of training and tailored support to improve biosecurity compliance (Delpont et al., 2024).

The advisers interviewed in our study emphasised the importance of training/advice to improve biosecurity compliance. The farmers frequently mentioned the reason “not useful” for not implementing BMs on their farms (Souillard et al., 2024). These findings highlight the necessity of enhanced support in order to improve their knowledge and understanding of the usefulness of BMs. The lack of knowledge is a key factor associated with poor biosecurity compliance (Laanen et al., 2014). In addition of the knowledge, enhancing biosecurity level on the farms requires lasting changes in farmers’ attitude and willingness to

make changes. The behavioral model ADKAR® for the 5 key elements to successful change such as the Awareness, Desire, Knowledge, Ability and Reinforcement, was successfully used to better understand the farmers behaviours toward changes, for example with regard to antibiotics use or adoption of biosecurity practices, emphasizing the need of an adapted and tailored support (Houben et al., 2020; Amalraj et al., 2024b). It has been shown that training programmes and audits could be efficient but decline over time (Racicot et al., 2012a; Amalraj et al., 2024a). The long-term effects of biosecurity training programs are variable, but certain tools, such as online tools, videos or e-learning modules may be more effective in maintaining farmers’ attention and engagement (Madsen and Tablante, 2013; Tilli et al., 2024). Coaching based on personalised advice and tailored support to help farmers find long term solutions has been shown to be successful in enhancing poultry farm biosecurity in Belgium (Amalraj et al., 2024a). Several support measures were also studied in Italy, where it was shown that virtual tours and coaching encouraged farmers to improve biosecurity implementation (Tilli et al., 2024). Providing appropriate support measures is therefore crucial to compliance.

## 5. Conclusion

The European poultry sector is characterised by broad trade and biosecurity is crucial as a tool for preventing transmissible animal diseases such as highly pathogenic avian influenza. This large-scale interview study across seven European countries provides a wide overview of advisers' perceptions of biosecurity implementation in poultry farming. From the advisers' point of view, deficiencies were highlighted, such as hand washing before entering the poultry house as well as other hygiene practices, which were deemed particularly efficient to improve biosecurity levels on farms. The lack of knowledge and time, the low awareness of the expected benefits and the financial aspects were reported by the advisers to explain the poor implementation of biosecurity on the farms. This study enable us to better target the needs in terms of farmer guidance, and technical and financial support, in order to adopt the best solutions for improving farmer awareness and willingness to implement biosecurity measures. There is room for improvement and it certainly can be achieved with appropriate cooperation between advisers and farmers.

## Funding

The NetPoulsafe project has received funding from the European Union's Horizon 2020 research and innovation programme under grant agreement "No 101000728". This output reflects only the authors' view, and the European Union cannot be held responsible for any use that may be made of the information contained therein. For the purpose of open access, the author has applied a Creative Commons Attribution (CC BY) license to any Author Accepted Manuscript version arising from this submission.

## CRediT authorship contribution statement

**Spaans Annick:** Writing – review & editing, Validation, Methodology, Investigation, Conceptualization.
**Piccirillo Alessandra:** Writing – review & editing, Validation, Methodology, Investigation, Conceptualization.
**Zbikowski Artur:** Writing – review & editing, Validation, Methodology, Investigation, Conceptualization.
**Souillard Rozenn:** Writing – review & editing, Writing – original draft, Validation, Methodology, Conceptualization.
**Le Bouquin Sophie:** Writing – review & editing, Validation, Supervision, Methodology, Conceptualization.
**Kovács László:** Writing – review & editing, Validation, Methodology, Investigation, Conceptualization.
**Sevilla-Navarro Sandra:** Writing – review & editing, Validation, Methodology, Investigation, Conceptualization.
**Amalraj Arthi:** Writing – review & editing, Validation, Methodology, Investigation, Conceptualization.
**Rousset Nathalie:** Writing –
Tilli, G., Laconi, A., Galuppo, F., Grilli, G., Zbikowski, A., Amalraj, A., Piccirillo, A., 2024. Supporting measures to improve biosecurity within Italian Poultry Production. Animals 14, 1734.

Van Limbergen, T., Dewulf, J., Klinkenberg, M., Ducatelle, R., Gelaude, P., Méndez, J., Heinola, K., Papasolomontos, S., Szeleszczuk, P., Maes, D., 2018. Scoring biosecurity in European conventional broiler production. Poult. Sci. 97, 74–83.

Van Steenwinkel, S., Ribbens, S., Ducheyne, E., Goossens, E., Dewulf, J., 2011. Assessing biosecurity practices, movements and densities of poultry sites across Belgium, resulting in different farm risk-groups for infectious disease introduction and spread. Prev. Vet. Med. 98, 259–270.