Preventive Veterinary Medicine 164 (2019) 23–32

Contents lists available at ScienceDirect

Preventive Veterinary Medicine

journal homepage: www.elsevier.com/locate/prevetmed

Revealing the structure of the associations between housing system, T

facilities, management and welfare of commercial laying hens using
Additive Bayesian Networks
Arianna Comina,b, , Alexandra Jeremiassonc, Gilles Kratzerd, Linda Keelinga
⁎

a
Department of Animal Environment and Health, Unit of Animal Welfare, Swedish University of Agricultural Sciences, Box 7068, Uppsala, Sweden
b
Department of Disease Control and Epidemiology, Section of Epidemiological Methods, Swedish National Veterinary Institute, 751 89, Uppsala, Sweden
c
The Swedish Egg Association, Green Tech Park, Gråbrödragatan 11, 532 31, Skara, Sweden
d
Department of Mathematics, Unit of Applied Statistics, University of Zurich, Winterthurerstrasse 190, Zürich, Switzerland

ARTICLE INFO ABSTRACT

Keywords: After the ban of battery cages in 1988, a welfare control programme for laying hens was developed in Sweden.
Additive Bayesian Network Its goal was to monitor and ensure that animal welfare was not negatively affected by the new housing systems.
Animal welfare The present observational study provides an overview of the current welfare status of commercial layer flocks in
Poultry Sweden and explores the complexity of welfare aspects by investigating and interpreting the inter-relationships
Multivariate modelling
between housing system, production type (i.e. organic or conventional), facilities, management and animal
welfare indicators. For this purpose, a machine learning procedure referred to as structure discovery was applied
to data collected through the welfare programme during 2010–2014 in 397 flocks housed in 193 different farms.
Seventeen variables were fitted to an Additive Bayesian Network model. The optimal model was identified by an
exhaustive search of the data iterated across incremental parent limits, accounting for prior knowledge about
causality, potential over-dispersion and clustering. The resulting Directed Acyclic Graph shows the inter-re-
lationships among the variables. The animal-based welfare indicators included in this study – flock mortality,
feather condition and mite infestation – were indirectly associated with each other. Of these, severe mite in-
festations were rare (4% of inspected flocks) and mortality was below the acceptable threshold (< 0.6%).
Feather condition scored unsatisfactory in 21% of the inspected flocks; however, it seemed to be only associated
to the age of the flock, ruling out any direct connection with managerial and housing variables. The environ-
ment-based welfare indicators – lighting and air quality – were an issue in 5 and 8% of the flocks, respectively,
and showed a complex inter-relationship with several managerial and housing variables leaving room for several
options for intervention. Additive Bayesian Network modelling outlined graphically the underlying process that
generated the observed data. In contrast to ordinary regression, it aimed at accounting for conditional in-
dependency among variables, facilitating causal interpretation.

1. Introduction
In the European Union (EU), conventional battery cages were the
dominating housing system for laying hens until the official ban in
January 1st, 2012. For example, in 2008, only 27% of the laying hens
were housed in some form of alternative system in the EU, whereas by
2015, the conventional cages had been replaced, mainly by enriched
cages, representing 56% of the egg production (European Commission,
2017). In Sweden, however, housing of laying hens in battery cages was
already banned in 1988, making it one of the first countries in the world
implementing alternative housing systems. Compared to most of the
member states in the EU, trimming of the beaks of birds has always
been prohibited in Sweden. During the transition period, from con-
ventional battery cages to alternative systems, the Swedish Egg Asso-
ciation, together with representatives from the Swedish Board of
Agriculture and the Swedish University of Agricultural Sciences de-
veloped a layer welfare program, in order to monitor and ensure that
the welfare of the layers was not negatively affected. Over the years, the

Abbreviations: ABN, Additive Baysian Network; BN, Bayesian Network; DAG, directed acyclic graph; GLM, generalized linear model; GLMM, generalized linear
mixed model; MCMC, Markov chain Monte Carlo
⁎
Corresponding author at: Department of Disease Control and Epidemiology, Swedish National Veterinary Institute, 751 89 Uppsala, Sweden.
E-mail address: arianna.comin@sva.se (A. Comin).

https://doi.org/10.1016/j.prevetmed.2019.01.004
Received 4 July 2018; Received in revised form 7 January 2019; Accepted 8 January 2019
0167-5877/ © 2019 Elsevier B.V. All rights reserved.
A. Comin et al.
program has been refined and controls are currently performed every
fourth year in each flock on a farm. However, a formal epidemiological
evaluation of the data collected in this program investigating the im-
pact of housing and management on animal welfare has not yet been
carried out.
There is a considerable body of work comparing the welfare of birds
in different housing systems, but it can be difficult to make an overall
decision, since there are advantages and disadvantages in all systems.
The most trustworthy approach therefore is to combine several dif-
ferent indicators of welfare (EFSA, 2005; Veissier et al., 2013). Early
work comparing different systems focused on health, production and
welfare-related problems such as cannibalism, eggs laid outside the nest
boxes and feather pecking, since all these affect the economy (Odén
et al., 2002; Aerni et al., 2005). There has also been an increase in basic
research to reduce these problems involving genetic selection (Leenstra
et al., 2016) and improved understanding of the causal factors, in-
cluding how the birds are reared (Brunberg et al., 2016; Lutz et al.,
2016). What is noticeable in all the studies comparing different housing
systems is the large variation between flocks, even when housed in the
same system. There are relatively few studies analysing welfare out-
comes in large number of flocks and some of these are old and not
representative of the genetic and management developments (Weeks
et al., 2016; Bestman et al., 2017).
The welfare status of individuals or group of animals likely depends
on many inter-related variables. Such complexity can be under-
estimated by traditional multivariable regression models, such as linear
or generalized linear models, where one variable is designated as a
single response variable and the remaining variables all as predictors. In
a study about potential determinants of diarrhoea in children, Lewis
and McCormick (2012) showed that relationships previously identified
using multivariable regression may no longer be supported when a full
multivariate regression model (i.e., a model with multiple dependent
variables) is considered. This provides a strong theoretical justification
for preferring a holistic – multidimensional – approach when con-
ducting exploratory data analyses (Lewis and Ward, 2013).
Additive Bayesian Network (ABN) modelling is a modern graphical
approach for analysing complex systems and it is increasingly finding
application in areas like genetics, systems biology, livestock production
(including poultry), and epidemiology (Jansen et al., 2003; Poon et al.,
2007; Lewis et al., 2011; Ward and Lewis, 2013; Firestone et al., 2014;
Felipe et al., 2015) thanks to its ability to generalize standard regres-
sion approaches. Unlike other widely used multivariate approaches,
such as principal component analysis, ABN does not involve any di-
mension reduction. ABN modelling focus is on structure discovery:
determining an optimal statistical model (i.e. graphical structure) di-
rectly from observed data, allowing all variables to be potentially re-
sponse and explanatory. This methodology is well suited to discriminate
between indirect and direct associations in complex and highly corre-
lated datasets, by estimating the optimal factorization of the joint
probability distribution of all variables, both quantitative and catego-
rical (Lewis et al., 2011).
The objectives of this study were to (i) provide an overview of the
current production practices and welfare status of commercial layer
flocks in Sweden; (ii) identify and critically interpret the associations
between housing system, rearing facilities, farm management and
welfare indicators in laying hens; and (iii) speculate about the potential
causative role of variables directly and indirectly associated with the
welfare status of the flock. The novelty of the study is the application of
a machine learning algorithm – ABN modelling – to investigate animal
welfare, using a large dataset covering over 65% of all commercial layer
farms in Sweden.
24
Preventive Veterinary Medicine 164 (2019) 23–32
2. Material and methods
2.1. The welfare control programme
The industry-based welfare control programme consists of a
checklist of 31 control points, evaluating facilities, barn, equipment and
animals. A full description of the checklist is provided in the supple-
mentary material (Table S1). The unit of observation is the flock, de-
fined as a unique group of hens of the same age, housed in the same
barn of a farm at a given time. During the welfare inspections, the
different checkpoints are scored from 0 (worse) to 4 (best) by an in-
spector from the Swedish Egg Association. The welfare control is per-
formed in each barn on a farm every fourth year, when the flock is
approximately 40–65 weeks old. This means that one control cycle of
all Swedish barns is completed every 4 years. However, if something is
changed in the barn during this period, for example a change in housing
system, a new control is required.
2.2. Data
We used data collected through the welfare control programme
from January 2010 to December 2014. All the flocks older than 25
weeks assessed during that period were included in the study. In total,
397 flocks belonging to 193 different farms affiliated with the Swedish
Egg Association (i.e. 65% of all the commercial layer farms in Sweden)
were examined. For this analysis, the checkpoint scores were dichot-
omized. Based on a conservative cutoff, scores equal to 3 or 4 were
considered satisfactory and kept as the baseline reference group. Scores
going from 0 to 2 were considered unsatisfactory and set as the outcome.
Of the 31 available, 11 checkpoints were included in the analysis,
namely: outer biosecurity; condition of the packing room; inner biose-
curity; lighting conditions; air quality; water management; furnishing
and litter; alarm; logbook; feather condition; and mites. These selected
checkpoints were either linked to animal conditions or to the Swedish
welfare legislation and had enough variation to provide some statistical
insight (i.e. a checkpoint should have been classified as unsatisfactory
in at least 2.5% of the inspected flocks). Additional information about
the flock, beyond the scored checkpoints, included whether it belonged
to organic production; flock size (i.e. number of birds); age of the flock
(in weeks); mean monthly mortality (calculated as the cumulative
proportion of dead birds in the flock at inspection divided by number
months since the onset of production cycle); and type of housing system
(i.e. enriched cage, single-tier system, multi-tier system). The latter was
subsequently coded as a set of two dummy variables to be handled by
the model. The role of season as a potential confounder or effect
modifier for the true associations between the variables of interest was
assessed and ruled out during preliminary investigations.
In total, 17 variables (i.e. 11 checkpoints and 6 additional flock
descriptors) related to housing (4), facilities and management (9), and
animals (4) were included in the analysis (Table 1). Inference about the
welfare status of the flock was based on three animal-based welfare
indicators: feather condition, presence of external parasites (mites) and
flock mortality. In addition, two environment-based welfare indicators
– lighting and air quality – were also considered, both of which are
known to have a strong impact on production as well as being tightly
linked to welfare legislation.
2.3. Bayesian network modelling
We sought to identify a robust statistical model for the selected
variables using Additive Bayesian Network modelling. ABN models are
a special type of Bayesian Network (BN) models which can be seen as
direct analogous to multivariate generalized linear regression, where
each variable in the data is modelled by an additive multivariable re-
gression model. All types of BN models comprise two reciprocally de-
pendent parts: one qualitative (the structure) and one quantitative (the
A. Comin et al. Preventive Veterinary Medicine 164 (2019) 23–32

Table 1
Descriptive summary statistics of the variables included in the Additive Bayesian Network model (n = 397). Welfare-related variables are marked in italics.
Variable Description Levels / Unit of measure Summary statisticsa

Organic The flock belongs to organic egg production 0 (no), 1 (yes) 0.19
Enriched cageb The flock is housed in enriched cages 0 (no), 1 (yes) 0.17
Single tierb The flock is housed in a single-tier barn 0 (no), 1 (yes) 0.22
Flock size Number of birds housed in the flock at the beginning of the production cycle Number of birds 14590 ± 11813
Outer biosecurity Measures to prevent rodents or wild birds from entering the barn. There should be: secured 0 (satisfactory), 1 0.16
ventilation, no holes in the walls, zone without vegetation outside the barn. (unsatisfactory)
Packing room This room must be clean and in order since eggs, which are considered food, are handled here. The 0 (satisfactory), 1 0.03
walls must be painted, so that they can be easily cleaned, and the floor in good condition. There (unsatisfactory)
must be hot/cold water and a visitor journal.
Inner biosecurity The barn must have an external biosecurity zone, with a barrier of at least 40 cm that you have to 0 (satisfactory), 1 0.06
step over after you have changed your shoes and taken off your jacket. Then there also has to be an (unsatisfactory)
internal biosecurity zone at each barn entrance, also with a barrier of at least 40 cm. Here you
must change shoes again and put on protective clothing.
Lighting The quality of the lighting conditions. Does the barn have windows? Are the windows used? How 0 (satisfactory), 1 0.05
are the windows regulated, automatically or manually? What is the quality of lamps? (unsatisfactory)
Air quality Air quality in the barn. Maximum level NH3 = 10 ppm in cages and multi-tier or maximum level 0 (satisfactory), 1 0.08
NH3 = 25 ppm in single-tier. Maximum CO2 = 3000 ppm. (unsatisfactory)
Water management Are there enough drinking places? Has the water been tested yearly? Are the drinking lines 0 (satisfactory), 1 0.03
regularly flushed (unsatisfactory)
Furnishing and litter The amount of floor eggs in single-or multi-tier systems. The quality of the litter on the floor in 0 (satisfactory), 1 0.05
single- or multi-tier systems. The litter must be dry and friable, not wet and hard. In enriched cages (unsatisfactory)
there must be enough litter in the litter bath.
Alarm If the barn houses more than 2000 birds, it is required by law to have an alarm system. The alarm 0 (satisfactory), 1 0.04
should be connected to ventilation, electricity, temperature and water. (unsatisfactory)
Logbook The farmer should note amount of collected eggs, number of culled birds and vaccination routines. 0 (satisfactory), 1 0.29
The barn should be approved in both the voluntary Salmonella control programme and the round (unsatisfactory)
worm control programme.
Feather condition Quality of plumage. No featherless areas. 0 (satisfactory), 1 0.21
(unsatisfactory)
Mites Occurrence of red mite infestations and management routines 0 (satisfactory), 1 0.04
(unsatisfactory)
Age of the flock Age of the flock since the onset of production cycle Weeks 53.8 ± 11.8
Mean monthly mortality Cumulative proportion of dead birds in the flock at inspection divided by number months since the Percentage 0.35% ± 0.25%
onset of production cycle

a
This column reports the proportion of outcomes (i.e. value of 1) for qualitative variables and the mean ± standard deviation for quantitative variables.
b
When both enriched cages and single-tier equal to 0, it means that animals are housed in a multi-tier barn (which represents the reference category in the original
multinomial variable). 61% of the flocks were housed in such barns.

parameters). The model structure is defined by a directed acyclic graph
(DAG), which is the graphical representation of the factorization of the
joint probability distribution of all random variables. Each node re-
presents a random variable, while arrows represent probabilistic de-
pendencies between them. Analogous to the classical regression fra-
mework, the direction of the arrows represents the flow of the
information in a prediction perspective. Indeed, incoming arrows to a
node and regression coefficients encode the way the index node is
predicted based on its parent set (i.e. which distribution to use to model
the error term). However, this indicates only a statistical relationship
and not a causal statement, exactly as in classical regression. The model
applied in this study uses a Bayesian approach for both structure dis-
covery and parameter learning, and as such it relies on prior informa-
tion. We used a uniform structural prior (i.e. all eligible DAG structures
were equally supported in the absence of any data) and uninformative
priors for all the parameters at each arrow (i.e. all values were equally
possible in the absence of any data).
The modelling was carried out using the open source software R (R
Core Team, 2017) and JAGS (Plummer, 2003), and involved four
consecutive steps: (1) setting the input values, (2) identifying a globally
optimal DAG, (3) adjusting the chosen model for over-fitting, and (4)
adjusting the marginal posterior densities for potential data clustering.
2.3.1. Input values
All the variables in the ABN model were modelled by specific
probability distributions according to their type: binomial distribution
for binary variables and gaussian distribution for quantitative ones. The
variable housing system had three levels (i.e. enriched cages, single-tier
and multi-tier) and was therefore coerced into two binary variables
(enriched cages: yes/no; single tier: yes/no) with the third level (multi-
tier) being the reference group. The variables age of the flock and
monthly mortality were highly skewed and were therefore transformed
(by taking the binary logarithm and the square root, respectively) to
facilitate the Bayesian estimation of the marginal distributions.
Furthermore, quantitative variables were standardized (by subtracting
the mean and dividing by the standard deviation) to avoid numerical
accuracy issues (Gelman and Pardoe, 2007).
Prior knowledge about data structure, that could guide the search
for the optimal model, was included by banning some specific arcs from
being considered in the final DAG. This was done by providing a ban
matrix (Table 2), where rows and columns represent children and
parents, respectively, and 1 and 0 indicates whether the arc is banned
or allowed. For example, all the arcs going to the variable age of the
flock (i.e. fourth row) were banned (i.e. all 1 s) under the reasonable
assumption that none of the considered variable was expected to in-
fluence the process of ageing. Similarly, the nodes organic production
and enriched cage housing system were set to be only parents in the
graphical model, since it was known that such variables were not going
to be affected by any other variable. Inner biosecurity and alarm system
were set to be potentially affected only by flock size, which in turn
could only be affected by organic production and housing system. The
last knowledge-based constraint was that the single-tier housing system
could only be affected by organic production. All other bidirectional
links were allowed (i.e. zeros in the ban matrix). The information en-
coded in the ban matrix was subjectively chosen by the authors to re-
flect their belief about data structure, which in turn was derived from
knowledge of field practice (e.g. the alarm system is compulsory for all
barns housing more than 2000 birds (The Swedish Board of Agriculture,

25
A. Comin et al.
Table 2
Ban matrix to guide the search of the optimal DAG accounting for existing knowledge about data structure. Rows
are children and columns are parents. Zeros denote allowed arcs and ones banned arcs.
2017)), legislation constraints (e.g. organic farms cannot have caged
birds (European Commission, 1999 2008)) and thorough reasoning
(e.g. it is reasonable to assume that age cannot be affected by any
variable).
2.3.2. Identification of the globally optimal model
The optimal model was identified by an exhaustive search of the
data using the exact order based method (Koivisto and Sood, 2004)
iterated across incremental parent limits, that is by increasing subse-
quently the number of allowed parents per node from one to five. The
maximal goodness-of-fit was reached when the network score (Lewis
et al., 2011) did not improve further even when more parents were
allowed. The R package abn (version 1.0.2) (Kratzer et al., 2016) was
used for the purpose.
2.3.3. Adjustment for overfitting
ABN modelling is known to be prone to overfitting (Burnham and
Anderson, 2002; Babyak, 2004), i.e. it may identify more parameters
than can be actually justified by the data. Therefore, a parametric
bootstrapping approach using Markov chain Monte Carlo (MCMC) si-
mulations was used to address this issue, as described in Lewis and
McCormick (2012). Briefly, the model chosen from the exact search
(outcome of step 2) was used to generate 10 000 bootstrap datasets of
equal size to the original dataset. These simulations were computed
using JAGS. Each bootstrap dataset was then treated as if it were the
original data, and a globally optimal DAG was identified exactly as
described before (i.e. exact search with incremental parent limit). This
bootstrapping process generated 10 000 different DAGs. To address
over-fitting, any arcs in the DAG from the original data which were not
recovered in > 50% of the bootstrap DAGs were deemed to have in-
sufficient statistical support to be considered robust (Lewis et al., 2011).
These arcs were therefore removed, obtaining a final pruned DAG.
26
Preventive Veterinary Medicine 164 (2019) 23–32
2.3.4. Correction for clustered data
Flocks of hens from the same farm are potentially correlated as they
share the same farm environment and are likely subjected to the same
management procedures. Not explicitly accounting for such within-
group clustering might result in an underestimation of the variance, and
therefore unreliable parameter estimates. The usual solution to over-
come this problem is to move from generalized linear models (GLM) to
generalized linear mixed models (GLMM), which include random ef-
fects at group level to incorporate additional variance into the sampling
distributions. However, doing it for each node of the DAG within the
ABN model search introduces considerable additional numerical com-
plexity, making it vastly computationally demanding.
An alternative approach to deal with potential clustering in ABN
was first described and applied by McCormick et al. (2013), who ig-
nored it during the model searching and then applied an appropriate
adjustment to the final chosen model to compensate for the potential
over-fitting due to ignoring correlation effects. We adopted the same
method and fitted the final pruned DAG (outcome of step 3) to the
observed data including a random effect at farm level for each node by
means of MCMC simulations (in JAGS). We followed the usual good
practice measures (Congdon, 2007) such as running multiple chains,
visual inspection and use of Gelman-Rubin convergence diagnostics,
along with a relatively large effective sample size and a proper sam-
pling lag to avoid autocorrelation. The resulting new marginal densities
were then compared to those previously obtained ignoring clustering,
to see whether the parameters (fixed effects) in the model were still
statistically significant when additional correlation structure via
random effects was included (i.e. to adjust for correlated residuals or
non-constant variance). Arcs whose 95% credible intervals of the
marginals crossed the origin were removed to produce a final DAG
adjusted for clustering effect. The marginal densities obtained from this
last step were those considered for final inference. The parameters had
A. Comin et al.
the interpretation as posterior marginal log odds ratios for binary
variables and correlations for continuous ones. Log odds ratios were
exponentiated to obtain the odds ratios.
2.4. Strength of associations
The concept of link strength in a discrete Bayesian network was
already developed in 1992 and good overviews are given in Ebert-
Uphoff (2009) and Oniśko and Druzdzel (2014). This approach is par-
ticularly useful as the classical metric in frequentist statistics to account
for significance, the p-value, is essentially not applicable in this setup.
Link strength is useful for both visualization and approximate inference.
In addition, the strength of the edges is as important as the existence of
the edges and it is a complementary metric to regression coefficients.
We used a link strength metric called true average link strength per-
centage (LS%) (Ebert-Uphoff, 2009), which expresses by how many
percentage points the uncertainty in variable Y is reduced by knowing
the state of its parent X, if the states of all other parent variables are
known (averaged over the parent states using their actual joint prob-
ability).
3. Results
3.1. Data description
The majority of flocks (n = 189/397) were housed in multi-tier
barns in a conventional production system (Fig. 1). Enriched cages were
not represented in the organic production, as this is forbidden by the EU
legislation (European Commission, 2008).
Flock size ranged from 720 to 111,600 birds and was smaller in
single-tier housing systems and in organic production (Fig. 1). A large
variability in flock size was observed in multi-tier systems, especially in
conventional egg production.
The mean monthly mortality was higher and more variable in loose
housing systems (i.e. single- and multi-tier) and it also increased with
the aging of the hens (Fig. 2).
The absolute number and the relative proportion of flocks with
checkpoints classified as unsatisfactory within each housing system is
reported in Table 3. Poor feather condition and lack of records (i.e. no
logbook) were reported in all three housing systems. In general, only a
small proportion of the inspected flocks had checkpoints that were
classified as unsatisfactory.
3.2. Model outcome
The optimal DAG had a parent limit of 3, 17 nodes and 23 arcs. After
adjustment for overfitting, two arcs were pruned resulting in a final
Fig. 1. Distribution of the flock size by housing system and type of production in the 397 investigated flocks.
27
Preventive Veterinary Medicine 164 (2019) 23–32
DAG with 17 nodes and 21 arcs (Fig. 3). The parameters estimated from
the final pruned DAG after accounting for potential clustering within
farm are reported in Table 4 together with the estimated link strength
for all the arcs. Adjustment for farm clustering did not suggest any
further need for arc pruning, but it produced slightly wider credibility
intervals for some of the estimates of the marginal posterior densities.
Fig. 3 shows that organic production was positively associated to
poor outer biosecurity and inadequate logbook (i.e. solid arrows going
from organic production to outer biosecurity and logbook), meaning
that outer biosecurity and record keeping are more likely to be classi-
fied as unsatisfactory (as the checkpoint variables indicate un-
satisfactory conditions) in organic production compared to conven-
tional production. Organic production was also negatively associated
(i.e. dashed arrows) to unsatisfactory furnishing and litter and to flock
size, meaning that organic production had more satisfactory furnishing
and litter and smaller flock sizes compared to conventional production.
Enriched cages were associated with a higher presence of external
parasites (i.e. solid arrow going to mites), as they were 8.1 times more
likely to house birds with moderate to high mite infestations compared
to multi-tier systems (ORmites | enriched_cage = 8.06, Table 4). On the
other hand, enriched cages were associated with a better water man-
agement and air quality compared to multi-tier systems, although the
binomial regression failed to provide an odds ratio due to data se-
paration (i.e. there were no flocks housed in enriched cages having
these two checkpoints classified as unsatisfactory). Finally, housing
animals in enriched cages was directly negatively associated with flock
mortality.
Another factor affecting mortality, although the relation was quite
weak (link strength = 2.7%), was the age of the flock. For every week
increase in age, there was a non- linear increase in mortality (correla-
tion√mortality | age = 0.21). In addition, age was the only factor asso-
ciated with feather condition, which was worse in older hens.
According to the estimated parameters, the odds of having un-
satisfactory feather condition increased by 68% for every week increase
in age (ORfeather_condition | age = 1.68).
Single-tier housing systems were directly linked to smaller flock
sizes (correlationlog2(flock size) | single tier = -0.89) and more satisfactory
lighting conditions in the barn (ORlighting | single_tier = 0.02) compared to
multi-tier systems.
An inadequate alarm system was positively associated with un-
satisfactory lighting conditions in the barn (ORlighting | alarm = 55.39),
which in turn was associated with unsatisfactory furnishing and litter
(ORfurnishing&litter | lighting = 12.7).
Poor inner biosecurity measures were strongly associated (link
strength = 51%) to unsatisfactory conditions in the packing room
(ORpacking_room | inner_biosecurity = 265). This relation had by far the
highest link strength percentage found in this study, with inner
A. Comin et al. Preventive Veterinary Medicine 164 (2019) 23–32

Fig. 2. Box-plots of the mean monthly mortality by age group and housing system in the 397 investigated flocks.

biosecurity status accounting for more than half the belief of packing
room status. In turn, unsatisfactory conditions in the packing room
were positively associated with poor air quality, both directly (ORair
quality | packing_room = 25.8) and indirectly through its connection with
unsatisfactory lightning (ORlighting | packing_room = 33.5) and un-
satisfactory furnishing and litter (ORair quality | furnishing & litter = 9.4).
4. Discussion
This study explored the complexity of welfare aspects in laying hens
by means of a machine learning procedure referred to as structure
discovery. To the authors’ knowledge, this is the first attempt to use a
multivariate approach to explore the inter-relationships between input
factors and welfare outcomes in laying hens using field data system-
atically collected over time in a fairly large number of flocks.
4.1. Biological interpretation
As already mentioned, the result of this ABN only provided evidence
of statistical associations among the considered variables, as the data
came from an observational study (i.e. without randomized controlled
setting) and the model structure was not specified a priori but learned
from the data itself (i.e. data-driven as opposed to theory-driven).
Nevertheless, causal interpretation of some of the discovered associa-
tions can still be speculated upon, because (i) the structure discovery
was guided by including available knowledge on causality and data
structure (influencing the directionality of some arcs), (ii) observational
studies can carry information beyond mere statistical association (Rosa
and Valente, 2013) and (iii) causality can be inferred, or at least hy-
pothesized, from empirically observed covariation by applying other
form of judgement, such as the Bradford Hill criteria (Fedak et al.,
2015).
Most of the resulting associations matched the personal views de-
rived from field experience. However, while some of the associations
truly reflect expected relations between managerial and welfare as-
pects, some others are more likely to be a consequence of the welfare
program itself or of the specific requirements for that particular pro-
duction system. For example, in order to achieve the highest score in
the checkpoint outer biosecurity, the farm must be approved in the
voluntarily Salmonella control and fulfil all the biosecurity require-
ments in that program. If not, the score will be downgraded to 2 points
(i.e. unsatisfactory) no matter the appearance of the buildings. Since it
is more difficult for the organic farms to be approved in the voluntarily
Salmonella control program (because of their outdoor access), these
farms will usually have a lower score in the checkpoint outer biosecurity.
In addition, flock sizes in organic production are usually smaller. The
European regulation (European Commission, 2008) states that the
maximum stocking density of open-air runs must not be greater than
one hen per 4 m2 at all times, which therefore requires large pastures.
The Swedish organic standards, KRAV, also do not allow more than
18 000 organic layers per building (KRAV association, 2017), which
puts an upper limit to organic flock size.
Red mites were found to be a problem (i.e. high to moderate in-
festation – scores 0 to 2) in only 4% of the inspected flocks (Table 1).

Table 3
Number and proportion of checkpoints classified as unsatisfactory, by production type in the 397 investigated flocks. Proportions of unsatisfactory scores within
production type were calculated using the total number of flocks per production type (i.e. 257 and 150 for conventional and organic, respectively) as denominators.
checkpoint Conventional production Organic production

Number of flocks with Proportion of unsatisfactory scores Number of flocks with Proportion of unsatisfactory scores
unsatisfactory scores within type of production unsatisfactory scores within type of production

logbook 61 24% 56 37%

feather condition 57 22% 25 17%
outer biosecurity 27 11% 39 26%
air quality 21 8% 10 7%
furnishing and litter 21 8% 0 0%
lighting 18 7% 2 1%
mites 16 6% 1 1%
inner biosecurity 12 5% 3 2%
alarm 10 4% 6 4%
packing room 7 3% 3 2%
water management 7 3% 5 3%
total 257 100% 150 100%

28
A. Comin et al. Preventive Veterinary Medicine 164 (2019) 23–32

Fig. 3. Final globally optimal DAG (after bootstrapping to prune structural detail unsupported by the data) to describe the interrelationships between housing
facilities, farm management and welfare indicators in laying hens (n = 397). Rectangles indicate binary nodes and ovals continuous nodes. Solid arrows represent a
positive association and dashed arrows a negative association. The width of the arrows reflects the strength of the association between two nodes. Animal-related
variables are coloured in black. Housing-related variables are given in grey. Variables related to facilities and management are coloured in white. Welfare indicators
are written in italics. To make it easier to interpret the checkpoint variables, the name is modified to make it clear that it is the unsatisfactory condition that is been
considered as outcome.

Table 4
Estimates of the marginal posterior densities (median and 95% credible interval) and link strength for the parameters included in the model accounting for herd
clustering. Posterior marginal densities are the result of 20 000 MCMC samples from two chains with different starting value, after a burn-in of 5000 iterations per
chain and a sampling lag of 50 to avoid autocorrelation.
Parameter Posterior median 95% credible interval Interpretation Link strength

√mortality | enriched cage −0.62 [-0.89; -0.35] correlation 5.2%

√mortality | age 0.21 [0.12; 0.29] correlation 2.7%
log2(flock size) | single tier −0.89 [-1.09; -0.68] correlation 8.2%
log2(flock size) | organic production −0.54 [-0.79; -0.28] correlation 5.1%
outer biosecurity | organic 13.29 [7.17; 25.47] odds ratio 21.4%
outer biosecurity | packing room 40.81 [8.2; 336] odds ratio 8.9%
packing room | inner biosecurity 264.69 [50.68; 2219] odds ratio 51.0%
lighting | single tier 0.02 [0.00; 0.16] odds ratio 11.0%
lighting | packing room 33.46 [3.39; 401] odds ratio 7.1%
lighting | alarm 55.39 [9.23; 493] odds ratio 11.8%
air quality | enriched cage NA* NA odds ratio 8.1%
air quality | packing room 25.78 [5.90; 139] odds ratio 9.0%
air quality | furnishing & litter 9.36 [2.27; 35.84] odds ratio 5.0%
water management | enriched cage NA NA odds ratio 4.6%
water management | packing room 32.11 [6.50; 157] odds ratio 15.4%
furnishing & litter | organic production NA NA odds ratio 5.5%
furnishing & litter | lighting 12.70 [3.10; 517] odds ratio 8.2%
logbook | organic 7.80 [4.22; 14.67] odds ratio 11.6%
logbook | outer biosecurity 4.27 [2.18; 8.52] odds ratio 6.0%
feather condition | age 1.68 [1.30; 2.21] odds ratio 4.3%
mites | enriched cage 8.06 [2.94; 23.52] odds ratio 11.3%

* NA = Estimate not available, due to complete separation of data point.

Red mites are a serious concern in Europe, with high infestation and
increasing prevalence in all production systems after the transition from
battery cages to alternative systems (Flochlay et al., 2017). Compared
to conventional battery cages, enriched cages and single- and multi-tier
systems contain more hiding places for the red mites to escape effective
treatments. This was also confirmed by a prevalence study of mites in
different housing systems in Sweden conducted in 1994, which showed
that red mites were less prevalent among layers housed in battery cages
compared to layers housed in alternative systems (Höglund et al.,
1995). In the present study, the occurrence of red mites appeared to be
significantly greater in enriched cages compared to the loose housing
systems, showing an odds eight time higher for moderate to high in-
festations. To our knowledge, this is the first study comparing the
occurrence of red mites in enriched cage and loose housing systems.
Enriched cages were also associated with satisfactory conditions of
water management and air quality. The better air quality (i.e. ≤ 10
ppm ammonia) was expected, due to the absence of deep litter. In
general, the concentrations of ammonia and dust are higher in loose
housing systems (with litter and manure on the floor) compared to
enriched cages (Nimmermark et al., 2009), since ammonia is produced
from uric acid by microbial enzymes and degradation in the manure
(David et al., 2015). In addition, a positive association between poor
litter quality (i.e. checkpoint furnishing and litter) and unsatisfactory
air quality was shown by the model (Fig. 3 and Table 4), indicating an
odds for poor air quality nine time higher when the furnishing and litter
checkpoint was unsatisfactory. The satisfactory conditions for the

29
A. Comin et al.
checkpoint water management in enriched cages was nevertheless un-
expected, since this checkpoint mainly covers the routines for taking a
yearly water sample and flushing the drinking lines, and it should
therefore not differ between the different housing systems. However,
the present analysis does not take in account the age of the buildings
and the related equipment. Most enriched cage systems are relatively
new and equipped with automatic flushing systems, making it easy to
flush the water lines regularly. This is also the case for the new multi-
tier systems, but it is less common for the older multi-tier systems. This
probably makes it more complicated to flush the water lines and so it is
performed less often, on average, in multi-tier systems. This could be a
possible explanation to the better score achieved in farms with enriched
cages.
Flock mortality was evaluated as the mean monthly mortality in-
stead of the more usual cumulative mortality, to promote a fair com-
parison among flocks, given that the welfare control is potentially
performed at different ages. According to the Swedish Egg association,
a mean monthly mortality lower than 0.6% is considered a desirable
result. This requirement was largely satisfied in all housing systems,
with average values of 0.25% in enriched cages, 0.42% in single-tier
and 0.31% in multi-tier systems. The significantly lower flock mortality
observed in the enriched cages could be due to lower bacterial and
parasitic pressure compared to the loose housing systems. In fact, it has
been earlier reported that the occurrence of bacterial and parasitic
diseases is higher in Swedish loose housing systems both with and
without outdoor access (Fossum et al., 2009). Our study showed that
the mean monthly mortality increased with the age of the flock in all
housing systems, albeit the relation was quite weak. Nevertheless, the
mortality was still low and therefore considered a satisfactory outcome
compared to what has been found in other studies. For comparison, the
average mortality for laying hens in Sweden between 2010 and 2014 in
61–70 weeks old flocks was 0.23% (corresponding to a cumulative
mortality of 2.88% at 66 weeks) in enriched cages, 0.48% (6.10% cu-
mulative mortality) in single-tier systems, and 0.37% (4.70% cumula-
tive mortality) in multi-tier systems. In the literature, a cumulative
mortality of 6.25% has been reported in 66 weeks old flocks housed in
enriched cages (Dikmen et al., 2016). For multi-tier systems, a cumu-
lative mortality of approximately 11.5% was reported for flocks be-
tween 20 and 77 weeks of age (Karcher et al., 2015) and of 4.1% in 66
weeks old flocks (Heerkens et al., 2015). The lower mortality levels
reported in our study were achieved despite the fact that birds are not
beak trimmed in Sweden, while those in the other studies were beak
trimmed. Thus, there seems to be no support for the concern that im-
plementing a more widespread ban on beak trimming would lead to
increased mortality, especially in loose housing systems.
Besides affecting mortality, age was the only factor affecting feather
condition. This may not be so surprising itself, since plumage is likely to
become more worn as the hen gets older and feathers only grow back
when birds moult, not while they are still laying eggs. What was in-
teresting, however, was the lack of further associations between feather
condition and any other variable. This differs from the knowledge re-
ported in the literature where, for example, flocks without red mite
infestation have been shown to have a better feather condition than
flocks with a mild or a severe infestation (Heerkens et al., 2015) and
there are often clear differences in feather condition between housing
systems (Brantsæter et al., 2017; Pichová and Bilčík, 2017). Further-
more, flocks with better feather condition have also shown to have a
lower mortality (Heerkens et al., 2015). The holistic approach offered
by ABN takes account of the potential dependency among all the
variables included in the model. It showed, for this particular set of
variables and data, that mortality was conditionally independent from
feather condition given age (i.e. edges going from age to feather con-
dition and to mortality d-separating them, implying that the informa-
tion between the two nodes mortality and feather condition is
“blocked” by some evidence about the intermediate node age, Fig. 3).
This means that once the age of the flock is known, then knowing the
30
Preventive Veterinary Medicine 164 (2019) 23–32
status of feather condition will not change the belief about flock mor-
tality; or, in more epidemiological terms, age is a confounder for the
relation between feather condition and mortality and once accounted
for, then the association among the two disappears.
Other resulting associations suggested that poor inner biosecurity
measures were strongly associated to unsatisfactory conditions of the
packing room, which in turn were positively associated to poor air
quality, improper lighting conditions, unsatisfactory water manage-
ment and poor outer biosecurity. These chains are likely to be affected
by the farm management routines. In fact, to fulfil the requirement for
the checkpoints inner biosecurity and packing room, the farmer has to
demonstrate good routines for changing clothes and shoes before en-
tering the buildings, provide a hygiene barrier, and the packing room
should be clean and in order. A farm with an unsatisfactory score for
management routines regarding inner biosecurity may also be more
likely to have less order in the packing room and have poor routines for
removal of litter material (resulting in a higher level of ammonia and
therefore unsatisfactory air quality), for flushing the drinking lines
(resulting in a unsatisfactory score for water management), for pre-
venting rodents or birds to enter the buildings (resulting in a un-
satisfactory score for outer biosecurity) and for using the daylight inlets
(resulting in a unsatisfactory score for lighting). The importance of the
quality of the management in livestock farming has been previously
highlighted in a study about welfare of dairy cattle (Sandgren et al.,
2009).
4.2. Welfare implications
In animal welfare research, the focus is usually on animal-based
indicators. However, these can be time consuming to collect in practice.
Environment-based indicators, that is the say the resource and man-
agement risk factors for poor animal welfare outcomes, are therefore
also of interest, especially when it comes to identifying interventions
that can improve welfare (Mollenhorst et al., 2005; Brantsæter et al.,
2017).
The animal-based welfare indicators included in this study (i.e.,
flock mortality, feather condition and mites) were all indirectly linked
together (Fig. 3). Of these, only feather condition potentially represents
a concern for Swedish farmers, since severe mite infestations were rare,
and mortality was far below the acceptable threshold. On the other
hand, feather condition seemed to be only linked to the ageing of the
flock and there were no issues with injurious pecking in the inspected
flocks (i.e. the two checkpoints related pecking injuries − at comb and
body level − were left out of the model because none of the flocks
scored unsatisfactory for them). Thus, overall welfare seems to be good
and better than the results from earlier studies in Sweden in the 1990′s
(Gunnarsson et al., 1995), but it is still relevant to speculate on how the
situation can be improved further.
Both flock mortality and occurrence of mites were directly linked to
enriched cages only, and they showed a positive and a negative asso-
ciation, respectively. This suggests that none of the variables related to
facilities and management included in the model are likely to be useful
targets for intervention to improve the three considered animal-based
welfare indicators. It may also indicate that the current animal-based
welfare indicators are already at the best they can be and cannot be
improved by intervening in any of the farm management variables
considered in the analysis or, alternatively, that the scales used at
present need to be modified to differentiate between the overall higher
scores.
On the other hand, environment-based welfare indicators – lighting
and air quality – showed a complex inter-relationship with several
managerial and housing variables (Fig. 3). Besides being conditionally
independent, they were indirectly linked to each other through multiple
pathways. For example, one path went from lighting to air quality
through the intermediate node furnishing and litter, indicating that air
quality in the barn was negatively associated with poor litter quality,
A. Comin et al.
which in turn was directly related to improper lighting conditions,
probably reflecting older barns with poor housing facilities. Another
interesting chain connecting air quality and lighting was through their
common ancestors: packing room and inner biosecurity. As already
speculated, this might suggest that less meticulous management rou-
tines are more likely perpetuated within the farm, producing un-
satisfactory environmental conditions for the welfare of the layers. As a
consequence, improving the facilities (e.g. newer barns with better
lighting) and the management routines (e.g. careful removal of litter
and manure) have the potential to positively impact the environmental-
based welfare indicators. An interesting follow-up of this study could
therefore be the formal evaluation of which of the alternative paths
(facilities or management) represents the most cost-effective target for
intervention to improve animal welfare.
Finally, none of the five considered welfare indicators was directly
affected by the production type, suggesting that animal welfare did not
differ between conventional and organic egg production for the flocks
included in this study. This was in line with findings from previous
studies conducted both in Sweden (Berg, 2002) and elsewhere in
Europe (Hovi et al., 2003; Hegelund et al., 2006).
4.3. Advantages and limitations of ABN modelling
ABN modelling outlines graphically the underlying (but unknown)
process that most likely generated the observed data. It compactly re-
presents the joint probability distribution for a multivariate domain by
using a DAG to encode conditional independences. It also offers a richer
tool for statistical inference than other regression-based modelling, as it
represents a direct generalization of GLM/GLMM to multiple dimen-
sions. Its multivariate approach allows to account for non-in-
dependence between explanatory variables, which is a key considera-
tion when analysing observational study data (Lewis and Ward, 2013).
The output of ABN – the optimal DAG – is a graphical representation
of the statistical dependency between the variables, and arcs present in
such a model do not imply any causal relationship (in direct analogy to
statistically significant coefficients in traditional regression). However,
incorporating additional expert knowledge, not present in the data, to
guide the search of the optimal model is a step towards the conclusion
of causal mechanisms. Incorporating additional knowledge about
causality in the form of network restrictions – as we did by banning the
arcs that were known to be unrealistic from a biological point of view –
has also been demonstrated to enhance the search strategy, leading to
improved network structures in less time (De Campos and Castellano,
2005). On the other hand, the use of directional constraints to provide
causal insights alters the model search space, and so may introduce
subjectivity to the final results. A more theoretically sounding alter-
native to insert causality in the learning process could be to incorporate
in the observed data some synthetic data reflecting causal associations,
as proposed by Heckerman et al., (1995). Unfortunately, this approach
requires a vast computational power, and algorithms to efficiently im-
plement this method are still under development.
Along with many advantages, ABN also has some limitations, first of
all computational demand. For now, exact structure discovery with
bootstrapping for minimizing overfitting is only feasible for around 20
variables (in the current implementation within R following the ap-
proach of Koivisto and Sood, 2004). Heuristic searches (Heckerman
et al., 1995) and inexact order-based searches (Friedman and Koller,
2003) for globally optimal DAGs offer alternative, although less ideal,
approaches to handle up to 40 variables (Lewis and Ward, 2013).
Computational demand also affects the possibility of fitting GLMMs
within ABN, which was not feasible with our settings. Nevertheless, we
overcame the problem by searching the structure using a simpler GLM
setting. Subsequently, we refined the estimates of the marginals by
applying a GLMM to the optimal DAG only. In time, advances in either
technology or statistical methods will make larger more computation-
ally intensive analyses feasible.
31
Preventive Veterinary Medicine 164 (2019) 23–32
Another potential limitation of our approach lies in the limited type
of variables allowed in the model, namely binary and normally-dis-
tributed continuous. This can be easily overcome by (i) converting
multinomial variables into sets of n-1 binary predictors (as we did for
housing system) and by (ii) applying an appropriate transformation to
continuous variables to approximate normal distribution (as we did for
mortality and flock size). However, these workarounds have the
drawback of (i) increasing the number of variables in the model and (ii)
making harder the interpretation of the posterior marginal density in
the transformed scale. Work is currently in progress in the R package
abn to allow more data distributions (e.g. multinomial distribution).
5. Conclusions
In this study, we provided an application of Additive Bayesian
Networks to outline the inter-relationship between housing, facilities,
management and welfare of laying hens. The resulting Directed Acyclic
Graph helped to identify that enriched cages, as housing factor, and
farm tidiness and routines for manure removal, as management factors,
were directly associated with animal welfare, and could potentially
become targets for intervention. The main advantage of the Additive
Bayesian Network approach was the holistic view provided, which al-
lowed us to identify also alternative indirect pathways to reach the
same welfare targets. This opens a whole range of future work, which
could, for instance, explore which of the available pathways represents
the most cost-effective intervention option.
Acknowledgements
This study has been founded by the Swedish Research Council
FORMAS with grant nr. 2013-11900-24964-53.
We would like to thank Prof. Reinhard Furrer for his help in the
development of the R package ‘abn’, for the valuable discussions about
the methodology, and for facilitating the cooperation between SLU and
UZH.
Appendix A. Supplementary data
Supplementary material related to this article can be found, in the
online version, at doi:https://doi.org/10.1016/j.prevetmed.2019.01.
004.
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