The correlation between on-farm biosecurity and animal welfare indices in large-scale turkey production

Abstract

This research aimed to determine the association between biosecurity and animal welfare measures in large-scale fattening turkey farms in Hungary. Large-scale farms raising male fattening turkeys across Hungary were contacted, with 24 agreeing to participate. The Biocheck.UGent questionnaire was used to evaluate biosecurity measures, and Animal Welfare Indicators (AWIN) protocol was used for welfare assessment. The association between biosecurity and welfare indicators was investigated by correlation testing and prediction accuracy using random forest classification. The areas of biosecurity that were shown to be closely linked to the welfare index were the organization of the farm (farm management, supply of materials), the control and hygienic measures implemented between farm structures, cleaning and disinfection measures on the farm, and control and hygienic measures implemented in the case of farm workers and visitors upon entrance and exit. 

Keywords

Biosecurity; Animal welfare; Turkey flocks

Introduction

Turkey meat provides high-quality lean protein with essential amino acids and low saturated fat levels, with clear health benefits for consumers . Additionally, turkey meat production is economical due to the efficient feed conversion rate and low production costs . Because of the above, turkey meat has become popular for maintaining a healthy weight and reducing the risk of chronic diseases such as heart problems, obesity, and diabetes . Turkey breeders seek options to increase productivity and fulfill growing demands. However, selective breeding for traits like rapid growth and large muscles has led to significant welfare problems for turkeys, including skeletal and muscular issues and painful leg disorders. Moreover, commercially raised turkeys often live in overcrowded conditions, restricting natural behaviors . Catching, transporting, and slaughtering them also can induce stress and suffering . The growing consumer consciousness about the origin of feedstuffs emphasizes the importance of biosecurity practices and animal welfare assessments in ensuring the ethical and safe production of meat

Biosecurity, initially linked to biological weapons and bioterrorism, has expanded to various sectors such as agriculture, laboratory safety, and public health. The Food and Agricultural Organization (FAO) defines biosecurity as a strategic and integrated approach encompassing policies and regulatory frameworks to manage risks to human, animal, and plant health and associated environmental risks. It also includes food safety, management of animal and plant diseases, use of living-modified organisms (LMOs) and genetically modified organisms (GMOs), and invasive species management . Biosecurity is divided into external and internal main components . In general, external biosecurity involves measures to prevent the introduction of disease-causing agents from outside the farm. Practices include controlling visitor and personnel movement, using personal protective equipment and decontamination procedures, limiting traffic, regulating animal and product imports, disinfecting incoming materials, and preventing contamination through feed, water, vermin, or birds. Internal biosecurity measures aim to minimize the spread of diseases within a controlled environment. Key practices include cleaning and disinfecting facilities, barn-specific personal protective equipment (PPE), managing stocking densities, following all-in-all-out procedures, and separating susceptible or diseased individuals. Biosecurity is crucial in reducing the use of antimicrobial drugs and minimizing the need for veterinary interventions. A study on global antibiotic consumption from 2000-2010 showed a significant increase in antibiotic use, highlighting the importance of biosecurity in managing antibiotic resistance . Implementing biosecurity measures has economic benefits, as they are associated with better economic outcomes in dairy or poultry farms.

Animal welfare is just as crucial as biosecurity in production efficiency. Like in other livestock production sectors, the welfare of turkeys throughout their growth and development is essential for producing quality meat while upholding ethically sustainable practices. Animal welfare is defined as the state of an animal as it copes with its environment, with failures or difficulties in coping indicating poor welfare. Suffering, involving negative emotions like fear and pain, is an essential aspect of welfare . When evaluating welfare using animal-based indicators, modern assessments consider physical and mental states. Assessing turkey welfare involves animal-based indicators, as the Animal Welfare Indicators (AWIN) protocol recommends, along with management and resource-based indicators. This approach provides a comprehensive view of welfare at the farm level, covering aspects like immobility, size, wound types, and some management strategies. Animal-based indicators are considered most relevant and appropriate for evaluating animal welfare.

Materials and methods

Farms and animals investigated

Farms raising male fattening turkeys across Hungary were contacted, with 24 agreeing to participate. Data protection regulations ensure that the name and location of farms are not published. The inspections focused on male turkey flocks nearing slaughter, averaging 132 days old (range: 98-145 days). Assessments were conducted in half of the turkey barns randomly chosen, averaging 3.7 out of 8.6 buildings per farm. The selected barns had an average floor space of 972 m² (min.: 360; max.: 2000). Farm sizes ranged from 3,000 to over 40,000 turkeys, raised in intensive enclosed buildings with windows on the side The turkeys had ad libitum access to feeders and drinkers.

The structure of the transect walks in the assessed flocks. The numbers refer to the order of transect walks. During the walk, the flock inspection should be carried out in the barn in ascending order of figure numbers.

Data of the farms involved in the study.

Farm	No of barns	Farm capacity (birds)	Density (bird/m2)	No. of birds at the time of the visit	Age of birds at the time of the visit (days)	Biosecurity score (%)	External biosec. (%)	Internal biosec. (%)	Welfare index
1	8	29000	4.0	7 250	134	77	74	83	4.5
2	6	23760	4.0	7 920	145	68	66	73	5.9
3	14	51100	3.7	7 300	120	66	64	70	8.5
4	6	31800	3.5	14 914	98	62	58	70	2.6
5	15	57000	4.4	26 819	119	54	51	62	5.0
6	12	30000	2.4	13 183	145	74	72	79	3.7
7	10	39500	4.0	18 802	139	64	62	70	2.1
8	6	27960	4.7	13 393	137	65	63	70	3.0
9	11	29700	3.2	13 825	142	39	36	47	14.0
10	6	21960	3.6	10 343	125	51	51	52	9.4
11	6	25980	4.4	12 353	131	52	52	51	4.3
12	7	18970	3.3	8 812	128	40	38	44	9.7
13	15	18990	3.5	8 897	128	40	36	50	6.0
14	6	21000	3.6	9 881	132	43	41	49	6.8
15	10	21000	5.2	9 923	138	46	45	48	5.9
16	10	53000	5.0	13 400	140	51	52	47	5.9
17	8	40000	4.8	10 600	140	51	52	48	7.6
18	10	21000	5.1	9 713	140	41	39	46	7.4
19	10	55000	5.8	25 080	135	48	47	50	8.2
20	4	28000	4.0	13 286	126	46	46	46	7.8
21	8	23000	3.1	7 608	131	61	60	63	6.3
22	3	10000	3.7	4 725	127	46	47	42	11.0
23	3	10000	4.5	4 705	137	45	46	42	14.2
24	1	6000	3.0	2 883	131	49	47	54	5.9

The biosecurity protocol

It generates scores reflecting biosecurity status through multiple-choice questions. The questionnaire covers basic farm characteristics, seven external biosecurity measures subdivisions, and three internal biosecurity subdivisions. External biosecurity subdivisions assess the biosecurity aspects of infrastructure, organization of farm management, access control, poult purchase, depopulation of barns, feeding and water supply, and waste management. Internal biosecurity subdivisions include questions about disease management, measures between compartments, and cleaning protocols. The questionnaire was completed together with the farm representatives during the visits.

 The biosecurity measures and their definitions, according to the Biocheck.UGent assessment protocol 

Name of the measures	Definition	Number of questions
External biosecurity	It consists of all the farm’s preventive measures to prevent pathogens from entering or leaving the farm.
Infrastructure	Infrastructure, location, and housing are all the structural elements (tools) necessary for biosecurity housing and farm management operations.	16
Organization	Organization of the farm and supply of materials essential for farm management.	10
Visitors and workers	Control and hygienic measures implemented in case of farm workers and visitors upon entrance and exit.	12
Purchase	Protocol of poult purchase and population of barns with livestock.	7
Depopulation	Protocol of depopulation of barns (e.g. transport of adult animals to the slaughterhouse or other poultry holding premises.)	7
Feed and water	Feed and water provision in the barns.	9
Removal	Manure and carcass removal from the barns of the farm.	13
Internal biosecurity	It encompasses all measures implemented to prevent the spread of pathogens within a farm.
Disease management	Measures of prevention and control of diseases on the farm.	10
Compartments	Measures implemented between each farm structure.	11
Cleaning	Cleaning and disinfection measures on the farm.	11

The animal welfare assessment protocol

The AWIN protocol for turkey evaluates welfare conditions using animal-based indicators and was used to assess the animal welfare status of the farms. The AWIN protocol defines four animal welfare principles: good housing, good feeding, good health, and appropriate behavior. Within these principles, twelve distinct but complementary animal welfare criteria are highlighted . The assessments were conducted by two trained individuals (the first and the second author) who filled out the questionnaire with the farm manager and performed transect walks in randomly selected barns on each farm. Their assessment scores showed good agreement during the training. The assessed barns’ width was divided into 2-3m wide transects, with an average of five transect walks per building.

Statistical analysis

Welfare indices, external, internal, and total biosecurity scores were calculated and recorded for each farm. Subscores for each biosecurity measure (within external and internal biosecurity, respectively) were also recorded. The relationship between the welfare index and total, external, and internal subtotal biosecurity scores and categorical subscores was studied by graphical exploration of the data. Having observed linearity, ‘Pearson’s product-moment correlation was chosen as a proper measure of association between the studied parameters. Pearson’s correlation coefficients between 1 (strong positive association) and -1 (strong negative association). In conditions of applicability and the interpretation of the correlation coefficient, the review of was followed. A p-value below 0.05 was set as a significance level for the obtained correlation coefficients. Correlation coefficients inform about the weak, moderate, or strong association between the welfare index and the other numerical measures but do not say much about the predictive value of these numerical measures. Moreover, pairwise correlation coefficients between the welfare index and individual biosecurity measures do not provide information about the possible collinearity between them. To overcome these statistical issues and to be able to understand better the influence each biosecurity has on the final welfare index of a given farm, the random forest classification and regression algorithm were used. The random forest algorithm works by fitting numerous decision trees to a subset of the data (training set) and tests the predictive efficiency of decision trees on the remaining part of the dataset (test set).

Results

The average welfare index was 6.9 (min.: 2.1; max.: 14.2) on the farms enrolled, while the average total, external and internal biosecurity scores were 53.3 (min.: 39; max.: 77), 51.9 (min.: 36; max.: 74), 56.5 (min.: 42; max.: 83), respectively. The explorative analysis revealed a pattern of inverse proportionality between the welfare index and total biosecurity scores (Fig. 3). It was further explored by correlation testing, including the correlation of the welfare index with external and internal biosecurity subtotals, too (Fig. 4). Besides the expected strong correlation between total biosecurity scores and subtotals (0.95-0.99), there was a significant moderate negative correlation between the welfare index and the total biosecurity score of the farms (r = -0.597 (95 %CI: -0.256; -0.806; p = 0.0021)).

 Point estimates of the correlation between the welfare index and total biosecurity score of the farms enrolled. The least-squares line is displayed for descriptive purposes only.

Point estimates of correlation coefficients between the welfare index and the biosecurity subfolders

 Point estimates of correlation coefficients of statistically significant Pearson’s product-moment correlation between the welfare index and the biosecurity category subscores.

Ranking of variable importance in the prediction of welfare index based on the random variable forest algorithm. The height of the bars is proportional to the increase in the error of the prediction of the welfare index (value of the loss function) due to the permutation of the values of the given predictor variable.