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A critically appraised topic (CAT) to compare the effects of single and multi-cat housing on physiological and behavioural measures of stress in domestic cats in confined environments Finka et al. Finka et al. BMC Veterinary Research 2014, 10:73 http://www.biomedcentral.com/1746-6148/10/73

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Page 1: A critically appraised topic (CAT) to compare the effects of ... Clinical scenario Many cats are kept in captive environments such as re-homing centres (also referred to as rescues/shelters),

A critically appraised topic (CAT) to comparethe effects of single and multi-cat housing onphysiological and behavioural measures of stressin domestic cats in confined environmentsFinka et al.

Finka et al. BMC Veterinary Research 2014, 10:73http://www.biomedcentral.com/1746-6148/10/73

Page 2: A critically appraised topic (CAT) to compare the effects of ... Clinical scenario Many cats are kept in captive environments such as re-homing centres (also referred to as rescues/shelters),

Finka et al. BMC Veterinary Research 2014, 10:73http://www.biomedcentral.com/1746-6148/10/73

RESEARCH ARTICLE Open Access

A critically appraised topic (CAT) to comparethe effects of single and multi-cat housing onphysiological and behavioural measures of stressin domestic cats in confined environmentsLauren R Finka1, Sarah LH Ellis1 and Jenny Stavisky2*

Abstract

Background: Domestic cats have evolved from solitary, asocial predators and whilst they may display socialbehaviours, they can still exist as solitary survivors. Over-population and relinquishment of pet cats are ubiquitousproblems worldwide, and rehoming centres (also known as rescues/ shelters) aim to ameliorate this by holding catsin confinement for a variable period until a new home is found. The provision of optimal housing for large numbersof cats in close confinement, such as in rehoming centres, is therefore inherently difficult. Under these conditionsthere is the potential for individuals to develop signs of physical and psychological ill health, and thus experiencecompromised welfare. Available information regarding housing practices that maximise welfare currently providesconflicting results, and as a consequence there are no unanimous housing recommendations. The aim of this studywas therefore to review the evidence on the impact of single housing compared to multi-cat housing on stressin confined cats, as measured by physiological and/or behavioural outcomes. The review was conducted using aCritically Appraised Topic (CAT) format. A systematic search of electronic databases (CAB Abstracts, ZoologicalRecords and Medline) was carried out to identify peer-reviewed literature comparing single and multi-cat housingin confined environments.

Results: A total of 959 papers were initially identified, six of which met sufficient criteria based on their relevanceto be included within this review. All of the studies had significant limitations in design and methodology,including a lack of information on how groups were assigned, inconsistent handling and enrichment provisionbetween groups, and lack of information on the socialisation status of cats.

Conclusions: Whilst some studies suggested that single housing may be less stressful for cats, others suggestedgroup housing was less stressful. Several other important factors were however identified as potential mediators ofstress within the different housing systems, and recommendations based upon these findings are presented.

Keywords: Cat, Feline, Stress, Housing, Welfare

* Correspondence: [email protected] for Evidence-based Veterinary Medicine, School of Veterinary Medicineand Science, The University of Nottingham, Sutton Bonington Campus,Loughborough LE12 5RD, UKFull list of author information is available at the end of the article

© 2014 Finka et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the CreativeCommons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, andreproduction in any medium, provided the original work is properly credited.

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BackgroundClinical scenarioMany cats are kept in captive environments such as re-homing centres (also referred to as rescues/shelters),often for indefinite periods of time. In trying to accom-modate these individuals as optimally as possible, it isimportant that they are provided with suitable housingconditions, which aim to minimise exposure to stress inorder to maximise welfare.Whilst recommendations for the housing of the domes-

tic cat in laboratories, rehoming centres and other facil-ities have been put forward [1-3], the strength of evidencein support of these recommendations is rarely consideredcritically, and can be contradictory. This study was con-ceived as part of the development of evidence-basedguidelines on the housing of cats in such contained en-vironments, specifically cat rehoming centres. The aimwas to assess the evidence on whether housing cats singlyas compared to groups of two or more in these types ofenvironments results in changes to physiological and/orbehavioural measures of stress, and therefore which sys-tem should be recommended as preferable in order tominimise stress.

IntroductionA recent survey of cat rehoming organisations withinthe UK estimated their total intake of cats over a12 month period to be 156,826, and 70% of these organi-sations were usually or always operating at full capacity[4]. Unfortunately, the provision of optimal housing forsuch large quantities of cats within these environmentsis inherently difficult, and under such conditions there isthe potential for individuals to develop signs of physicaland psychological ill health.As a species, Felis catus is thought to have originated

from primarily solitary dwelling felids [5-7], and whilstpopulations of free living F. catus may reside in groups,they may also live independently [8-11]. The feline socialsystem is therefore one of variability and flexibility. Incat colonies, social structuring, relationships and poten-tial conflicts may be the result of complex interactionsbetween age, gender, sex ratio, relatedness and individu-ality [12]. It is thought that the occurrence of group liv-ing and the subsequent population densities of freeranging cats are ultimately influenced by the abundanceof food resources rather than an inherent need for pro-tection or regular social contact/interaction per se[13-17]. In contrast to free ranging populations, groupliving in domestic companion cats may often take theform of temporary or transitory housing during a stay ina rehoming centre, or when living in a domestic homeenvironment. In both contexts, individuals may havelimited choice or control over the nature of their ‘groupliving’, especially when their environment prevents them

from making the choice to live independently (for ex-ample, multiple cats kept in a single enclosure at a re-homing facility, or multiple cats kept strictly indoors inthe home).It is likely that most rehoming centres will contain diverse

populations of cats of varied ages and temperaments. Somecats may be related or familiar with each other (which mayfacilitate more amicable relationships in certain instances[18]), but the majority are potentially unrelated and alsounfamiliar. For many individuals, being forced to reside inclose proximity to other cats under these types of condi-tions may result in stress, conflict and potentially compro-mised health and welfare [19,20]. Organisations caring forsuch animals often operate under conditions of limited re-sources of space, staffing, time and finances. Currently,there is conflict in which housing practices are recom-mended to maximise use of resources but simultaneouslypreserve a basic standard of welfare for the cats.The aim of this study was therefore to review the evi-

dence on the impact of single housing compared tomulti-cat housing on stress in cats, as measured byphysiological or behavioural effects.

Focussed clinical questionIn [cats kept in confined environments] does [single hous-ing compared to multi-cat housing] result in [changes inphysiological and/or behavioural measures of stress]?

MethodsSearch strategyThe search strategy included the use of three separateelectronic databases; CAB Abstracts (1910 – present, viathe Ovid interface), Zoological Records (1998 – 2007)and Medline (In-process & other non-indexed citations,1946- present, via the Ovid interface). The search wasconducted in October 2012.After accounting for specific syntax associated with

each database, each search had similar components(search terms are listed in Additional file 1) and all weresearched as both keywords and subject heading terms,joined using Boolean operators. All references obtainedwere imported into Endnote, combined into a masterdatabase, and all duplicates (identified based on title,date published and authors) were removed.

Inclusion criteriaStudies were not excluded on any grounds of quality,only on relevance to the study aim. For inclusion, papershad to include:

� Domestic cats kept in an enclosed area from whichthey were unable to exit (omitting the domestichome), for example, rehoming centres, boardingcatteries and laboratories.

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Search – 959 Published studies, letters, abstracts, book chapters and review articles

Stage 1 - 835 excluded on a title basis, foreign language papers removed (2 person consensus)

Stage 2 –107 Reports retrieved for further detailed evaluation (3 person consensus). Full text articles were obtained where decisions could not be made based on a title/abstract basis alone.

6 studies were included in the final review and were critically appraised.

Figure 1 Results of searches and screening processes used toidentify relevant papers.

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� Comparison of both single and multi-cat (i.e. twoor more cats) housing conditions within a singlestudy, with outcome measures that were eitherbehavioural, physiological or both, and were classedas indicators of stress. Our working definition ofstress was:“an inferred internal state which denotes a realor perceived perturbation to an organism’sphysiological homeostasis or psychological well-being”,as used by Ward et al. [21], and similar to thatused by McEwen [22], as we felt it was appropriateto this context. However many other definitionsexist [23-25], and in the present study papers werenot included or excluded on the basis of thisdefinition.

� Original observed or experimental data.

Studies were also required to be peer-reviewed, withthe full text available in English.

Screening processTwo stages of eligibility screening were carried out. Thefirst stage was completed independently by two of theauthors (LF and JS), and any references that clearly didnot fit the eligibility criteria were excluded. After this, instage two, the remaining references were screened againby all three authors. For this stage, full text was retrievedfor any papers where the information contained withinthe abstract was deemed insufficient to make a decisionupon eligibility. Where there was initial disagreementover eligibility, the papers were read and discussed untilconsensus was reached among the reviewers [26].

Critical appraisalAll remaining papers were independently appraised by allthree authors, using critical appraisal tools developed bythe Department for Emergency Medicine at ManchesterRoyal Infirmary (www.bestbets.org/) and used extensivelyin the literature [27-29]. These appraisals were then col-lated by the lead author (LF) into a summary table. Allthree authors re-checked this summary of evidence forconsistency of interpretation.

Results959 papers were initially identified. Following screeningas in Figure 1, six papers fulfilled all of the inclusion cri-teria. The results of the appraisal can be seen in Table 1.

Summary of the evidenceThe findings of the appraisals are summarised in Table 1.There was a lack of agreement overall as to whether sin-gle or multi-cat housing was associated with higherlevels of stress. The majority of the studies (four out ofsix) showed no difference in stress levels between single

and multi-cat housing [30-33]. However, one of thesestudies only compared single cats with those housedwith one or two other familiar conspecifics and not withlarger multi cat groups [33]. One study suggested thatstress levels were higher in cats housed singly in barrenenvironments as compared to singly and group-housedcats provided with varying levels of enrichment [34].Thefinal study included showed no difference in stress levelsbetween single and group housing in socialised cats, butfound that cats previously unsocialised to conspecificsshowed fewer signs of stress when single housed [35].There were significant limitations to all of the identi-

fied studies. These included differential treatment of thegroups within the study. For example cats in the singlehousing conditions either had inconsistent handing [34],were exposed to their housing condition for a muchshorter period of time [30,34], were deliberately givenbarren, non-enriched housing [34], or experienced anon-stable environment over the course of the studyperiod [30], when compared with group-housed cats.Sample size calculation was performed in only one study

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Table 1 Summary of appraisal of the six papers meeting the inclusion criteria of assessing single versus multi-catenvironments on physiological and behavioural measures of stress in confined domestic cats

Author, dateand title

Uetake and others [30] Lichtsteiner and Turner [31]* Gourkow N,Fraser D [34]

Ottway, D. S. & Hawkins,D. M. [33]*

Kessler M. R. &Turner D C. [35]

Kessler M. R, &Turner D C. [32]

Effects of single caging andcage size on behavior andstress level of domesticneutered cats housed in ananimal shelter [30]

Influence of indoor-cat groupsize and dominance rank onurinary cortisol levels [31]

The effect of housing andhandling practices on thewelfare, behaviour andselection of domestic cats(felis silvestris catus) byadopters in an animalshelter [34]

Cat housing in rescueshelters: A welfarecomparison betweencommunal and discrete-unithousing [33]

Socialization and stress in cats(felis silvestris catus) housedsingly and in groups inanimal shelters [35]

Stress and adaptation ofcats (felis silvestris catus)housed singly, in pairs andin groups in boardingcatteries [32]

Study design Randomised controlled trial Controlled trial Randomised controlledtrial

Cohort Randomised controlled trial Cohort

Stated aim ofpaper

• To provide information onthe minimum spatialrequirement for singly cagedcats in animal shelters

• The relevant aim was todetermine “whether theurinary cortisol levels of thecats are related toenvironmental parameters…additionally the cortisol levelsof cats from privatehouseholds were comparedwith shelter cats to check foran influence of location”

• To examine howdifferent housing andhandling conditionsaffected the welfare,behaviour, adoption rateand selection of individualcats by adopters

• To test the hypothesis that,in long-term shelter care, catshoused communally withunfamiliar conspecificsexperience higher levels ofstress than do cats housed indiscrete units, due toinappropriate and unstablesocial grouping

• To provide recommendationfor the most suitable housingtype for cats with knownsocialization status

• To investigate levels ofstress in cats housed singly,in pairs and in groups

• To compare stress levelsin newly arrived cats to alonger-term control group

Subjects • 6 cats between 2–15 yearsold residing in an animalshelter

• Twenty-one shelter cats • 165 cats entering ananimal shelter

• 74 cats residing in 2 animalshelters, randomly selectedfrom the shelter population

• 169 cats between 1–8 yearsold residing within an animalshelter

• 140 cats between 1–15 years old, residing in aboarding cattery in 2categories, plus a “control”group of 45 un-owned cats

• All cats had lived in theshelter for at least 3 weeksand were considered“adoptable”

• Inclusion criteria: mixedbreed, 1–7 years of age,neutered, healthy

• Excluded: feral cats • Excluded: cats having beenin the shelter < 1 month

• Excluded: ill cats, “highlystressed” cats (in “control”group only)

Environmentprior tostudy

• All cats had previously beenkept in a socially stable groupenvironment for at least7 months

• All cats had been in theshelter for at least 3 weeks

• Cats were from bothstray and domestic homeenvironments (numbersof each not specified)

• Cat were from both strayand domestic homeenvironments (numbers ofeach not specified) and hadbeen in the studyenvironment for a least1 month

• All cats were relinquished/unwanted (no history ofprevious long-term livingexperiences)

• 140 cats were owned,from single or multi-cathomes

• Single housed cats weretransferred to single housingat least one week beforesampling

• No history of backgroundprior to this 7 month period

• Origin of 45 “control”shelter cats not specified.

• Cats in the single cagecondition had previouslybeen housed singly for 10–20 days in the studyenvironment

• The study commencedon day one of exposureto the study environmentfor all individuals • 85-87% of the owned cats

had been exposed to thestudy environment on aprevious separate occasionCats in the group condition

had previously been housedin a group with changingcompositions for 10–20 daysin the study environment

• Control cats had spentbetween 2 and 16 weeks inthe study environment

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Table 1 Summary of appraisal of the six papers meeting the inclusion criteria of assessing single versus multi-catenvironments on physiological and behavioural measures of stress in confined domestic cats (Continued)

Intervention/groupdefinition

• All individuals were exposedeither to small, medium orlarge single cages in varyingorders, all without humansocial contact. This wascompared with their baselinestress levels when previouslygroup housed (it is assumedthe group size at this pointwas six)

• Two groups, comprising sixand seven cats housedcommunally

• Assigned to one of fourhousing conditions:

• In one shelter, individualswere already housedcommunally in one of threegroups (either 33, 47 or 65individuals per group)

• Cats housed in individualunits or in a group enclosure(specific group sizesunspecified but at least >5)

• Boarding cats housedsingly (60), in pairs (40) orgroups (40) (each groupsize unspecified but at least>2) according to ownerpreference

- basic single (minimalhuman interaction)• Four of these group-housed

cats were removed fromeach group and housed sin-gly for one week prior to be-ing sampled

- enriched single (withconsistent humanhandling and humaninteraction)

- basic communal (eightcats per group), withconsistent humanhandling and humaninteraction

• “Control” cats (45) wereliving in six groups (sizeunspecified), which hadbeen stable and un-alteredfor at least 2 weeks prior tothe study

• In the other, 12 cats werehoused in pairs and nine catswere divided into threes.These cats were previouslysocialised together orsiblings. Additionally, 15 catswere housed singly- enriched communal

(eight cats per group),with consistent humanhandling and humaninteraction and extrahiding places and toys

Outcomemeasures(refer toTable 2 forfurtherinformationon measures)

• Urinary cortisol: creatinineratios

• Urine cortisol: creatinineratio on a single voidedsample

• Cat Stress Scores (CSS) • CSS scores and time budgets(including eat, drink, groom,play, rest, stereotypic behaviourand agonistic encounters)

• CSS • CSS taken 4 x daily

• Human-Approach-Test(HAT), Cat-Approach-Test(CAT) and socialisation ques-tionnaire used to determinewhether cats were socialisedtowards conspecifics orhumans

• Outcome of stay i.e.adopted, not adopted,euthanized or isolated forphysical health reasons

• Behavioural time budgets(including resting, drinking,eliminating, vacuumbehaviour, and others,locomotion, social/solitaryplay, exploring and self-grooming)

• Time to adoption

Datacollectionperiod andfrequency ofrelevantmeasurestaken toassess stress.

• Cats were exposed to eachcondition for six days, i.e. thestudy period was a total of18 days

• A single urine sample wastaken for each cat on aconvenience basis during thestudy period (14 days).

• The study period lasted21 days

• Data on individuals wascollected each day over 15consecutive week days,however, it is unclear if allcats were sampled for fullduration due to cat turnoverduring the study period

• Data collected over a 7 dayperiod

• Data collected over14 days

• Cats were observed for2 minutes each day, andassigned a Cat StressScore for the first 10 daysof the study period,however, not all cats wereassessed for the full10 days

• Cat-Stress-Score was assessedevery l0 minutes during thefirst hour post placement intothe test condition, then twice(within a 15-min interval) after6 hours. For the following days,2 observations were made inthe morning and 2 in theevening

• CSS were initially recordedafter the first two hours ofentry into the testenvironment and werethen taken 4 times daily,each day, twice in themorning and twice in theevening

• Behavioural observationsmade over 3 hours duringthe last 2 days in each of thedifferent housing conditions

• Urine samples werecollected in the morning andevening of each day andthen averaged, repeated eachday of the study period

• Cats instantaneously scansampled and assigned a CSSeach day, every 30 minutesfrom 08:30 am to 15:30. Allother behavioural data wascollected via one–zerosampling in between eachscan interval

• HAT and CAT randomlyassessed twice a day for4 days across the testpopulation, once in themorning and once in theevening

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Table 1 Summary of appraisal of the six papers meeting the inclusion criteria of assessing single versus multi-catenvironments on physiological and behavioural measures of stress in confined domestic cats (Continued)

Key results • Time spent in locomotionand solitary play were lowerin individual cages than ingroup housing conditions

• Urinary cortisol:creatinineratios were highly variable

• CSS were highest in thebasic single housingtreatment

• No differences in CSS scoreswere found between catshoused individually andthose housed with either oneor two other familiar cats

• Cats that were considerednon-socialised with peoplehad higher CSS levels thanthose considered socialised,irrespective of housing type

• The highest reduction inCSS scores occurredbetween the first and fourthand first and fifth dayswithin the boarding cattery• These cats also had the

lowest adoption rate.• Urinary cortisol: creatinineratios were higher in singlyhoused cats (not statisticallysignificant)

• No statistically significantdifferences between groups

• No significantdifferences notedbetween other housingconditions

• Where cats were consideredsocialised to other cats, CSSdid not differ between singleand group housing

• “Control” group cats hadsignificantly lower stresslevels than boarding cats

• Overall CSS scores werehigher in cats housedcommunally than cats housedin discrete units alone or withpreviously familiar conspecificsHighest scores were only seenin communal housing**

• Those considered non-socialised to conspecifics hadhigher CSS than those whichwere socialised to conspecifics,when housed in groups

Housing type did notappear to influence CSS inboarding cats

• Cats considered non-socialised to conspecifics hadlower CSS during the first hourof the study and on the lasttwo days when housed singlycompared with group housing

• Play and resting/sleeping inclose contact withconspecifics were observedin more instances in catshoused in pairs or threesthan in communal housing**

• Group housed cats hadhigher CSS when a catconsidered non-socialised toconspecifics entered thegroup, compared to when acat considered socialised withconspecifics entered

• Agonistic encounters wereobserved in more instancesin communal housing than indiscrete–unit housing**

Conclusion • The experience of catsbeing exposed to a rotationof individual cages ofvarying sizes for 18 consecutivedays (6 days in 3 differentcages) appears to be morephysiologically stressing thanwhen they are housed in afamiliar group environment,with no intervention

• Group versus singlehousing did not result in asignificant difference incortisol: creatinine ratios

• Cats in barren singlehousing had higher stresslevels than cats in theother 3 housing typesand lowest adoption rates

• Whether cats are housedindividually or with one totwo other familiar conspecificsdoes not appear todifferentially affect stress levels

• Cats which have not beenpreviously socialised tohumans may find the shelterenvironment more stressfulthan those accustomed tohumans

• Cats appeared to find anestablished colonyenvironment to be lessstressful than any of theboarding environments,whether single or grouphoused with novel orfamiliar conspecifics• Cats which are not

successfully socialised toconspecifics may find grouphousing more stressful thanthose socialised to conspecifics

• Housing cats in largegroups appears to be morestressful than housing cats indiscrete units (1–3 individualsin a single unit)**

• Suggests that the noveltyof the environment may beassociated with a stressresponse

Mainlimitations

• No sample size calculation,but sample size very small.

• No sample size calculation,but sample size very small.

• No sample sizecalculations

• No blinding of observer • No sample size calculations • No sample size calculation

• No blinding of observer • Non-random assignment ofcats to groups

• No blinding of observer• No blinding of observer

• Comparisons madebetween two very differenttypes of cats

• No blinding of observer • Randomisation method notdescribed

• Insufficient detail todetermine if groups werecomparable at baseline• No blinding of observer

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Table 1 Summary of appraisal of the six papers meeting the inclusion criteria of assessing single versus multi-catenvironments on physiological and behavioural measures of stress in confined domestic cats (Continued)

• Randomisation methodsunclear

• Sample size relatively smallconsidering 8 sub-groupsanalysed

• The single and pair housingenclosures were lessenriched than the grouphousing enclosures, whichcould have confounded theresults

• “Discretely-housed” catscould be housed singly, or intwos or threes with other catsthey were previously socialisedto. This limits the extent towhich such comparisons meetthe criteria of this CAT

• Randomisation methodnot specified

• Inappropriate comparisonsused – stable enriched socialgroup versus relatively barrensingle housing with minimalhuman contact

• No detail of how cats wereassigned to groups

• Groups not treatedequally – all but basicsingle received extrahuman interactioncausing potentialconfound

• The validity of Cat-Approachand Human-Approach-Tests isquestionable based on themethods used, (Non-conform-ity between the two differentmeasures used to assesswhether cats were socialisedwith conspecifics and withhumans led to 30% of individ-uals being excluded from thedata analysis)

• Single cortisol: creatininemeasure of uncertainsignificance

• Stress measures may haverelated to barrenenvironment/ frequentchanges to housingconditions, especially in catsaccustomed to a stable grouphousing situation

• Validity of the CSS as ameasure of ‘Stress’ in cats(see Table 2)

• Excluding individuals thatwere ‘highly stressed’ apotential confounder

• Singly housed cats mayhave had an increase incortisol due to having had achange in environment aweek previously • No physiological

measures considered• Validity of the CSS as ameasure of ‘Stress’ in cats(see Table 2)

• No physiological measuresconsidered

• Total residence time of eachindividual within the shelterprior to study not accountedfor but could have acted as aconfounder if notappropriately controlled for

• No physiological measuresconsidered

• Cats were in two differentshelters - the external envir-onment varied between eachgroup

• Cat density per unit variedconsiderably in the discreteunit housing depending onwhether there were 1,2 or 3individuals housed together,whereas density was moreconsistent betweencommunally housed groups

• Cats had already had onemonth to acclimatise toshelter environment prior tosampling – external validity

• Behavioural time budgetspotentially a crude form ofmeasurement to assess stress

• No physiological measuresconsidered

• Main aims of this studywere not related to the topicof the CAT

• Behavioural time budgetspotentially a crude form ofmeasurement to assess stress

*The primary aims of this study were unrelated to the CAT question. However, a small sub-component of the study was relevant, and the critical review refers only to this portion.**This portion of the study relates to comparisons that did not meet the inclusion criteria of the CAT due to the way that data was concatenated prior to statistical comparison. Such results are however includedbecause they are considered otherwise highly relevant to the topic of the CAT

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[33], and some of the studies involved very small num-bers of cats, which in one case amounted to six cats eachexposed to three different interventions [30]. In none ofthe studies was the assessor of the outcome blinded tothe intervention.Additionally, the diverse populations under study and

variations in methodology complicate comparison.Group sizes in the multi-cat environment were variable,from 2 to eight [33,34]. The effect of population densitywas not assessed, as this information was not availablefor all studies; however this may clearly be a potentialconfounding factor. The previous social experience ofthe cats varied, with some cats living in established so-cial groups [30], some having been assessed as non-socialised to other cats by shelter staff [35] and otherswith no known or stated history of socialisation. A catsprior social experience was identified by one study as afactor in its stress levels in group housing, and the samestudy showed that the introduction of an “unsocialised”cat to a stable group caused an increase in the stresslevels of all of the cats under observation [35].There were also substantial differences in duration of

the data collection periods across all studies, rangingfrom a single instance [31] to fifteen days [34], whichcould have affected the extent to which the cats had theopportunity to habituate to their respective study envi-ronments, or resulted in some cats exhibiting acute andothers chronic signs of stress.Thus these studies may not be truly comparing single

and multi-cat environments, so much as suggesting thepresence of several other factors that may be equally im-portant in determining stress levels. These include: howconsistent handling and husbandry routines are [34], aswell as the amount of environmental manipulation, suchas changes in housing location and type, that the indi-vidual is exposed to [30]. In one study, stress levels intheir stable, long-term and group housed control popu-lation were lower than in any other experimental condi-tion (i.e. individual, pair and group) [32], suggesting thatgroup stability (and presumably familiarity) were alsoimportant mitigators of stress levels.

DiscussionThe majority of the studies did not find significant dif-ferences between single and group housed cats inregards to their stress levels. Whilst this may suggestthat group size does not in fact impact upon the stressof confined cats in rehoming and similar environments,it is arguable whether this can be assumed unequivo-cally. This is due to the lack of overall agreement be-tween studies, as indicated by the conflicting evidencefound in two of four such studies [34,35], as well as thevarious confounding elements of study designs foundthroughout the reviewed papers. These included factors

such as differential provision of enrichment or humancontact between groups, differences in the cats’ socialisa-tion and housing experience prior to the studies, and po-tential differences in sizes of groups in the grouphousing conditions. These results also suggest that astable environment (both social and physical) may be animportant factor in managing stress, and that some cats(such as those previously successfully socialised to con-specifics) may cope better in a multi-cat environmentthan those with little, or aversive previous experience ofconspecifics. Therefore, when providing housing for cats,it is important to consider their likely prior social experi-ence. When housing cats communally, keeping cats inlarge group sizes may also be more stressful than keep-ing them in smaller groups [33] although there is only asmall amount of relevant data to support this, and it ispossible that population density may also be a confound-ing factor.Measuring stress in non-human animals is inherently

difficult, and it is unlikely that any one measure can ac-curately capture how stressed an animal is [36,37]. How-ever, the more separate (suitable) measures consideredwithin a single study, the greater the potential for ro-bustness. As there is no consistent definition used withinthe scientific literature for this term nor specific aeti-ology or prognosis for stress [23], it is important thatwhere studies attempt to measure stress, a clear defin-ition of this concept is given. This will facilitate in theease of assessing the suitability of study methodology, aswell as determining whether the main aims and objectivesof a study have been achieved. All of the studies aimed tomeasure stress, but only one of them attempted to providea clear definition of it [33]. Of the six papers that werecritically appraised, only one study used both behaviouraland physiological measures to assess stress [30] and onlyone used more than one set of behavioural outcome mea-sures [33]. Only one study assessed whether the study catswere previously socialised with conspecifics [35], whichagain makes direct comparison between group housingconditions across the different studies difficult, becausethis appeared to influence the stress levels experienced bycats when housed in groups.Comparison between the studies is further complicated

by the variety of methods used to assess stress, all ofwhich have their limitations (further details of thesemethods used are provided in Table 2). The duration oftime over which individuals were exposed to specifichousing conditions also varied considerably (both withinand between studies). This affects the comparison of stresslevels between cats under different housing conditionsdue to potential confounds of comparing cats whichare acutely stressed (e.g. from being taken from stableenriched group housing to barren single housing) to catswhich are chronically stressed, or to those that have

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Table 2 Further detail of behavioural outcome measures used in the studies reviewed

Measure Description Evidence of validity of measure

Cat Stress Score (CSS): A 7 rank linear scoring system based on key aspectsof body posture and behaviour, rating cats from fullyrelaxed (1) to terrorised (7). Developed by Kessler andTurner [32], the CSS is a modification of the CatAssessment Score (CAS) [40]

Evidence of correlative relationships with cortisol:creatinine ratios, but not consistent between studies[41,42], although this could be due to variation instudy methodologies

Good inter-observer reliability reported, howeverobserver training required and there is no publishedtraining guide

Important behaviours such as grooming are notincluded in the scoring system, neither are socialbehaviours towards conspecifics or the humanobserver (if they are present during scoring)

Cat Approach Test (CAT): A 6 rank linear scoring system (from extremely friendly(1) to extremely unfriendly (6)) based on the responseof cats to visual contact with a 4 year old male catdescribed as socialised with conspecifics. Cats weredefined as socialized towards conspecifics when themean of eight test ratings resulted in a score below3.0, and non-socialized when they scored higher than4.0. Developed by Kessler and Turner [35]

No evidence of previous attempts to validate

No mention of inter-observer reliability

Human Approach Test (HAT): A 6 rank linear scoring system (from extremely friendly(1) to extremely unfriendly (6)) based on the responseof cats to a staggered human approach to their cage.Cats were defined as socialized towards people whenthe mean of eight test ratings resulted in a score below3.0, and non-socialized when they scored higher than4.0. Developed by Kessler and Turner [35], a modificationof the Stranger-Approach-Test [40]

As above

Socialisation questionnaire A linear scoring system based on information frommultiple-choice questions (answered by the personrelinquishing the cat) referring to the behaviouralreactions of the cat in 10 specific situations wheninteracting with an unfamiliar and a familiar person,and five situations when interacting with an unfamiliarand a familiar cat. Developed by Kessler and Turner [35]

As above

Cortisol: creatinine ratio Comparison of quantity of urinary cortisol withconcentration of urine (as determined by quantityof creatinine present). Cortisol is an indication ofphysiological arousal, often used as an indirectmeasure of stress, although levels can vary withdiurnal rhythm and other metabolic processes [41,43]

Assays based on in-house adaptation of previouslyvalidated measures [44,45]; some details notsupplied in manuscript

Evidence of correlative relationships betweencortisol:creatinine ratios and CSS, but not consistentbetween studies [41,42], although this could be dueto variation in study methodologies

Evidence of correlative relationships between cortisolconcentrations and the exposure to environmentalstressors [43]

Evidence that cortisol levels do not necessarilycorrelate with other physiological indicators ofstress or compromised immunity [46]

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actually begun to habituate to their environment. Thephysiological and behavioural signs of acute as comparedto chronic stress may vary [38,39] making it difficult toisolate the specific effects of the environment, from theeffects of period of exposure, upon the stress levels experi-enced by cats. However, by implication, the acutely raisedstress levels in some of the single housed cats may havebeen as attributable to the acute change in environmentrather than to the actual housing condition itself.Whether individuals have previous experience of the

housing environment may also be another important

mitigator of stress. Previous research indicates that catsthat have been housed in rehoming centre environmentspreviously may cope better under these conditions thanthose that have not [47]. It is unknown if any of thestudy populations within the appraised papers had beenhoused under such conditions before, but this may havebeen an important factor to consider.

ConclusionOn the basis of the evidence available, the below recom-mendations for practice have been provided. It is

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however important to consider the complex nature ofstress, and the methodological limitations of the abovestudies, in relation to their ability to help us isolate andassess the effects of multiple and single housing aloneon stress in cats (Table 1). There are also numerousother factors which have not been considered here, par-ticularly disease control, which is also of great importancein rehoming centres [48-50]. These results should draw at-tention to the importance of other potential mitigatingfactors which may influence how stressful single or mul-tiple housing can be for individuals, and suggest waysthese may be utilised practically to improve the welfare ofconfined cats in these types of environments.

Recommendations for practice

� Especially where the previous social history of catstowards conspecifics is unknown, individuals shouldbe housed singly, but with the appropriateenvironmental enrichment in place (e.g. places tohide and perch, toys, consistent positive humanhandling where appropriate).

� Cats should be exposed to as few environmentalchanges/manipulations as possible during their stayand husbandry routines should be as consistentas possible.

� If cats are to be housed in groups, they shouldideally be housed together with other catsconsidered socialised to conspecifics.

� If cats are to be housed in groups, or with those thatare initially unfamiliar, wherever possible, groupsshould have a stable composition (i.e. groupmembers are not constantly changed).

Additional file

Additional file 1: Search terms used in constructing the CAT.

Competing interestsThe authors declare that they have no competing interests

Authors’ contributionsLF carried out data collection, coordination, analysis and interpretation ofdata as well as the drafting of the manuscript. SE contributed towards theanalysis and interpretation of data as well as critical revision of themanuscript. JS conceived of the study, participating in its design andcoordination, data collection and critical revision of the manuscript. Allauthors read and approved the final manuscript.

AcknowledgementsLF’s PhD is supported by International Cat Care. We also acknowledge therole of International Cat Care in generating the research question in thepreparation of their guidelines for the management of un-owned domesticcats.The Centre for Evidence-based Veterinary Medicine is supported by anunrestrictive grant from Novartis Animal Health and The University ofNottingham.

Author details1School of Life Sciences, Faculty of Science, University of Lincoln, RiseholmePark, Lincoln, Lincolnshire LN2 2LG, UK. 2Centre for Evidence-based VeterinaryMedicine, School of Veterinary Medicine and Science, The University ofNottingham, Sutton Bonington Campus, Loughborough LE12 5RD, UK.

Received: 28 May 2013 Accepted: 14 March 2014Published: 22 March 2014

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doi:10.1186/1746-6148-10-73Cite this article as: Finka et al.: A critically appraised topic (CAT) tocompare the effects of single and multi-cat housing on physiologicaland behavioural measures of stress in domestic cats in confined envi-ronments. BMC Veterinary Research 2014 10:73.

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