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34 SUMMER 2012 | THE ENRICHMENT RECORD
Article
The provision of environmental
enrichment, whilst good for animal
welfare, can sometimes be a
contentious issue with regard to
scientific data. Some argue that
the inclusion of enrichment
increases the number of experi-
mental variables and therefore has
a negative impact on the science,
whilst others argue that only those
results achieved in an appropri-
ately enriched environment, when
the animal is displaying a range of
natural behaviours, can be said to
present the ‘true’ nature of any
effect. Whichever of these opinions
is closest to your own, in my view,
a good way to inform the debate is
to ensure that all published research
includes details of any environmen-
tal enrichment that the experimen-
tal animals have experienced.
But is this happening? Following an
in-depth, but unlikely to be com-
prehensive PubMed search using 53
different ‘animal model’ and ‘envi-
ronmental enrichment’ search term
variations, I have in my hand a list
of 126 references from 64 differ-
ent journals. Not a lot, when you
consider that I didn’t include any
time frame limits, and less still when
reading of the abstracts reduces
this number to just 87 references,
in 46 journals, that actually provide
details and data on environmental
enrichments for a range of species;
primarily mice and rats. The vast
majority of these papers report the
effect of environmental enrichments
(not including social housing/enrich-
ment) on specific phenotypic effects
or behaviours, with a few including
details of environmental enrich-
ments, when discussing current
best practice in housing and care. I
am, of course, aware that this quick
search will not have picked up any
papers that include details of en-
richments within the materials and
methods sections, as these are not
indexed, but it does illustrate how
difficult it can be to find the limited
amount of research published in
this field. On a brighter note, The
Enrichment Record does a fantastic
job of filling what is clearly a very
big hole in this regard, but we really
need to get the majority of authors
including enrichment details within
all published research in order to
accumulate a sufficient body of data
with which to analyse and address
the many questions surrounding
the use, mis-use, pros and cons of
environmental enrichment. So how
can this be achieved?
The RSPCA’s approach has been to
see whether journals have publica-
tion policies on the use of animals
in the research that they publish,
and if so, whether they included any
reference to the 3Rs, enrichment,
or other animal welfare related
issues. Most of the headline results
from our surveys have already been
published, but to summarise...
the publication policies of a total
of 868 different English language
peer-reviewed journals publish-
ing primary research involving the
use of animals were surveyed from
January 2007-2010. This figure
is equivalent to 40% of the
total number of relevant journals
(3,000+) in 2010 (Osborne et
al. 2010). Of these 868 journals,
over 57% had no meaningful
policies relating to the use of
animals in the research they
published, meaning that we con-
firmed that they didn’t have
a policy or that it only included
the word ‘animal’ at some point.
Most relevant to The Enrichment
Record readers is the fact that
only 18 out of 868 journal
policies gave any mention to the
3Rs, either with or without using
the term specifically. Of these,
8 policies referred to all 3Rs,
5 mentioned 2 of the 3Rs
(either replacement & reduction,
or reduction & refinement) and
5 policies mentioned 1 of the
3Rs. None of the policies included
environmental enrichment and
only 2 policies mentioned
disseminating best practice by
publishing improvements. Armed
with this data, we have gone on
to produce, with input from
some journal editors and publish-
ing societies, some simple
‘Publication Policy Principles’ and
a ‘Good Practice Model:
Instructions to Authors’ (Osborne
et al. 2010). These are aimed at
providing journal editors with a
short list of points relating to the
publication of research involving
animals that they can consider
when next updating their
editorial/publication policies.
Or, for those currently without a
policy, we provide an instruction
to authors that can be copied,
Nikki Osborne, Research Animals Department, RSPCA, Southwater, West Sussex, UK
Reporting Enrichment in Research Papers
SUMMER 2012 | THE ENRICHMENT RECORD 35
pasted and edited to cater to an
individual journal’s needs.
We believe that journal editors
are well placed to influence the
content of the papers submitted
to them for publication, because
authors will ensure that the paper
they submit is prepared in a jour-
nal’s preferred style and format.
So, why not also stipulate required
content? An argument against this
approach is that the author of the
paper, not journal editor, is best
placed to know what details are
pertinent to include within the
description of the study. Where
this argument falls flat is revealed
by a number of studies that have
analysed what information is
included within published research
papers (Smith et al. 1997, Gomez
& Conlee 2007, Kilkenny et al.
2009). Fifteen years ago, Smith
et al. (1997) looked at the
information authors included
within the methods sections of
149 biomedical science papers
taken from eight journals. This
may not be a statistically signifi-
cant sample, but their conclusion
was that ‘Our study points to
the need for journals to estab-
lish more rigorous guidelines and
editorial procedures, in order
to ensure adequate reporting.’
These comments were reiterated
by Kilkenny et al. (2009) who
analysed the quality of report-
ing in 271 publications and again
concluded that ‘we believe there
is a need to develop reporting
standards specifically for research
using animals, with the aim of
enhancing the transparency of
reporting and encouraging both
researchers, and those journals
responsible for publishing this
research, to adopt and adhere to
them.’
So what reporting standards are
there and do they include a refer-
ence to environmental enrichment?
In 1985, the GV-SOLAS Working
Committee for the Biological
Characterization of Laboratory
Animals published ‘Guidelines for
specification of animals and
husbandry methods when reporting
the results of animal experiments’
(GV-SOLAS 1985). Perhaps,
unsurprisingly, these do not
include reference to environmental
enrichment; however, the guidelines
published by Festing & van Zutphen
in 1997 definitely do (Festing & van
Zutphen 1997). More recently,
several groups have revisited
reporting standards publishing ‘the
ARRIVE guidelines’ for bioscience
research reporting (Kilkenny et al.
2010) and the ‘gold standard
publication checklist’ for animal
studies (Hooijmans et al. 2010).
Similarly, ILAR (2011) published
‘Guidelines for the description
of animal research in scientific
publications’, with all of these
specifying the need to report on the
presence and type of environmental
enrichment. Likewise, the provision
of environmental enrichment has
been included as part and parcel of
contemporary good practice within
the guidance associated with the
new revised European Directive
on the use of animals in scientific
procedures.
I am therefore hopeful that this
will prove to be an important turn-
ing point, when the provision and
reporting of environmental enrich-
ment for laboratory animals hits the
scientific mainstream. If authors
don’t report it because journals ask
them to, then maybe they will do
so to demonstrate that their
research conforms to the good
practice standards set out in both
the Directive and ILAR Guide—and
that they recognise better welfare
and better science go hand in hand.
References
Osborne, N.J., Phillips, B.J. and Westwood, K.
(2010). Journal editorial polices as a driver
for change—animal welfare and the Three Rs.
Proceedings of the Eleventh FELASA
Symposium and the 40th Scand-LAS
Symposium, 14-17 June 2010, Helsinki,
Finland. FELASA, http://www.felasa.eu
Festing, M.F.W. and van Zutphen, L.F.M.
(1997). Guidelines for reviewing manuscripts
on studies involving live animals. In L.F.M. van
Zutphen and M. Balls (Eds), Animal Alterna-
tives, Welfare and Ethics (pp. 405-410).
Amsterdam: Elsevier.
Gomez, L.M. and Conlee, K.M. (2007).
An analysis of reporting pain and distress
recognition and alleviation in scientific journal
publications. AATEX 14, Special Issue:
171-177.
GV-SOLAS Working Committee for the
Biological Characterisation of Laboratory
Animals (1985). Guidelines for specification
of animals and husbandry methods when
reporting the results of animal experiments.
Laboratory Animals 19: 106-108.
Hooijmans, C.R., Leenaars, M. and
Ritskes-Hoitinga, M. (2010). A gold standard
publication checklist to improve the quality of
animal studies, to fully integrate the Three Rs,
and to make systematic reviews more feasible.
ATLA 38: 167-182.
ILAR (Institute for Laboratory Animal
Resources). (2011). Guidance for the
Description of Animal Research in Scientific
Publications. National Research Council
Institute for Laboratory Animal Research.
Washington, DC: The National Academies
Press.
Kilkenny, C., Parsons, N., Kadyszewski, E.,
Festing, M.F.W., Cuthill, I.C. et al. (2009).
Survey of the quality of experimental design,
statistical analysis and reporting of research
using animals. PLoS ONE 4(11): e7824.
Kilkenny, C., Browne, W.J., Cuthill, I.C.,
Emerson, M. and Altman, D.G. (2010).
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research. PLoS Biology 8(6): e1000412.
Smith, J., Birke, L. and Sadler, D. (1997).
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