Reporting animal use in scientific papers

Reporting animal use in scientific papers JaneA. Smith', Lynda Birke2 & Dawn Sadler3 'Institute of Medical Ethics, Edinburgh, 2Centre for the Study of...
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Reporting animal use in scientific papers JaneA. Smith', Lynda Birke2 & Dawn Sadler3 'Institute of Medical Ethics, Edinburgh, 2Centre for the Study of Women and Gender, University of Warwick, Coventry and 3Department of Biology,The Open University, Milton

Keynes, UK

Summary This paper reports the results of an examination of the 'methods' sections of a range of experimental research papers in biomedical science, focusing on the descriptions of animal use and housing. Detailed descriptions in the methods should enable replication, and also enable readers to judge scientific quality. Relatively few papers sampled gave adequate descriptions of housing conditions and many failed to give details of physiologically relevant variables such as weight of animals. Thirty per cent of papers omitted the number of animals used, and the deaths of animals (whether as part of the protocol, or accidental death) were not always recorded. Adequate reporting of the conditions of animal maintenance and use are important, both in relation to the quality of the science produced, and also because of public concerns about the ethics of animal experiments. Keywords

Animal experiments; public concern; scientific quality; scientific reporting

The 'methods' section of a scientific report is intended to provide readers with information about how the research was performed. In principle, this should enable readers to follow the process, judge the quality of the science,

into account both the technical procedures involved and the ways in which the health and welfare of the animals are ensured. The second reason for examining descriptions of animal use in scientific papers has to

and allow replication of procedures. Methods

do with public concern about laboratory

sections may include descriptions of how laboratory animals are housed, as well as the experimental procedures performed on the animals. This paper examines the ways in which animal use is reported in a sample of scientific papers. In addition to replicability, there are two further reasons why the adequacy of such descriptions is important. The first concerns scientific quality. If science is to be high quality, the animals used should not be unnecessarily stressed and should be kept under appropriately controlled conditions: poor animals are likely to result in poor science. Thus, a proper evaluation of a scientific report should take

animal use. Some of those scientists most outspoken in defence of animal use for biomedical research believe this concern to be part of a wider anti-science feeling (or even an anti-intellectualism). This complaint is frequently linked to the belief that the general public do not know, or understand, what science is about-and specifically about how laboratory animals are kept or what happens to them (Birke &. Michael 1992). In the context of increasing debate around public understanding of science in general, and of the animal experimentation controversy in particular, we decided to investigate one aspect of the 'public face' of this area of science - what gets reported in scientific journals about animal use. The lay public may not have ready access to such reports, but the anti-vivisectionist

Correspondence to: Lynda Birke, Centre for the Study of Women and Gender, University of Warwick, Coventry CV4 7AL, UK Accepted 7 February 1997

Laboratory Animals (1997) 31, 312-317

Reporting animal use in scientific papers

organizations scan them} as do journalists. What is said in those reports, and how it is said, may thus be crucial to the public perception of animal experiments. Our aim was to sample a number of journals, to see what was said in, or omitted from} the methods sections concerning laboratory animals. Different journals have different guidelines for authors, and different criteria concerning what must be said. Some have explicit guidelines concerning ethical issues. What is published eventually is thus influenced by journal (and editorial) policies, as well as by the assumptions made by reviewers in the process of peer review. Yet there is also likely to be some convergence in the way that the methods are described. As Gross (1990) has pointed out} scientific papers reflect conversations among scientists, thus revealing much about the assumptions they make. He describes scientific papers as 'the most visible products of verbal interaction within the community, posed photographs of continuous activity captured at certain ritually significant moments'. They are also, he notes, }photographs' that are written after the event, and may omit or transform many of the events.

Method The study focused on a selection of journals published in 1990-91. The journals were chosen to reflect a range of biomedical problems and uses of animals, but the selection was otherwise arbitrary. It was assumed that these journals would, in broad terms, be representative of the corpus of scientific writing insofar as they describe animal use; the choice of particular journals was in no way intended to select out those journals for possible criticism, or praise. Rather, the journals provided case studies of scientific writing. For these reasons} quotations have not been attributed to particular authors or journals, so they cannot be directly identified. One hundred and forty-nine papers in eight journals were sampled: Life Science (1990) Vol. 46, Parts 3, 10, 17}22 (26 papers); Journal of Neuroscience (1990) Vol. 1O}No.5 (20 papers); Journal of Immunology (19901Vol.

313

145, No.8 (20 papers); Journal of Comparative Psychology (1991) Vol. lOS, Nos 1 and 2 (23 papers); Journal of Experimental Biology (19901Vol. 148 (20 papers!; Tournal of Cardiovascular Surgery (1990)Vol. 31, Parts 1-6 (10 papers); Tournal of Surgical Research (19901Vol. 48, No.1 (10 papers); Laboratory Animals (1990)Vol. 24, Nos 1 and 2 (20 papers). The countries of origin of the papers are shown in Table 1. Not all papers within one issue of a journal necessarily involved animals: papers that reported clinical work with humans or in vitro work were excluded. Table 2 shows the total numbers of papers reporting experiments using particular species. For each paper it was noted whether} and in how much detail} the following were reported: numbers of animals used; sex, Table 1 paper

Country of residence

of first author*

Country

Number of papers

U~

~

Canada

of

9

UK

13

Other European country Japan Other

26 13 7

*14 papers involved authors from more than one country. Table 2

Species used in the studies

Species Mammals Rats Mice Guineapigs Other rodents Rabbits Cats Dogs Primates Other mammals Birds Reptiles Amphibians Fish Invertebrates Crustaceans Insects Molluscs Gastropods Cephalopods

Number of papers

58 45 8 3 17 2

16 10

4 23 2 2

8 5 8 1

2

Smith, Birke & Sadler

314

strain, age, weight and source of animals; information about the animals' housing; and information about the experimental procedures to which the animals were subjected. Some of these data provide a broad quantitative picture; some are more descriptive. Results Information about the animals used Tables 3, 4, 5 and 6 respectively, show the numbers of papers specifying sex, strain, age, weight and source of animalsj the number of papers specifying particular conditions of housingj the number of papers specifying numbers of animals used; and, where applicable, the number of papers specifying the death of animals. Table 3 shows that just over a quarter of all the papers sampled (28%) did not specify the sex of the animals used, whilst nearly Table 3

Papers giving details of animals used

Sex of animals Sex specified

Number of

Percentage

papers

of papers

100

67

Sex not specified

41**

Sex not applicable* Strain of animals

8

Strain specified Strain not specified Strain not applicable* Age of Age Age Age Weight

animals specified not specified not applicable* of animals

Weight Weight

specified not specified

Weight not applicable* Source of animals Source specified Source not specified

5 61 7

47

32

60 77 12

40

35 106*** 8

23 71

70

Table 4

Papers specifying housing conditions

Number of

Percentage of papers

Condition

papers specifying

specifying

Humidity

15 (+12 papers which involved

11

28

91 11

79

one-half of all the papers (47%) did not specify the source of the animals. A large number of papers also omitted to mention the age or weight of the animals: 52 % did not specify age, whilst 71% did not specify weight. However, a greater proportion of papers stated the strain of animals involved in the experiments: in cases where it was possible to specify strain, 89% of papers did so. Table 4 lists five aspects of the animals' housing. The table shows that the aspects of husbandry most commonly mentioned were the numbers of animals in the cages (27% of papersl, the temperature at which the animals were maintained (28%1 and the light/dark cycle (28%). Cage size and/or type was mentioned in only 21 % of papers and humidity was recorded relatively rarely, being specified in only 11% of papers involving terrestrial animals.

52 8

aquatic animals) Photoperiod

41

28*

Temperature

42

28**

Cage size or type Stocking density

32 40

21 27

*Plus one paper which said that the animals (chickens) were kept in 'well-lit'conditions. **Plus two papers which said that the experiments were conducted at 'room temperature'.

Table 5 used

Papers specifying number of animals

5 53 47

*Note, for example, that 'sex' was 'not applicable' for hermaphrodite or larval forms; 'strain' was only applicable for purpose-bred animals; 'age' was 'not applicable' for wildcaught animals; 'weight' was 'not applicable' where it was impractical to weigh animals-e.g. in the case of Drosophila. **Includes three papers which stated that 'adults of either sex' were used, but which did not say how many of each. ***Includes one paper which said that dogs of a 'minimum weight of 10 kg' were used.

Number of papers

Percentage of papers

Numbers given in methods section Numbers given in results section Numbers given as legends to graphs Numbers not given clearly (see text)

78

52

11

7

14

9

Numbers not given

45

30

Reporting animal use in scientific papers

Table 5 shows that just over half the papers sampled reported the numbers of animals used in the methods section, where it might be expected. Eleven papers (7%) gave the numbers in the results section, and one paper gave the numbers only as legends to graphs. Fourteen papers (9% of the sample) gave incomplete information in the text: thus one reported '3-4 per group', and another '10 or more per group'. In similar vein, one paper reported that a 'minimum of 84' animals was used, and another gave 'n> or =6'. Yet another paper quoted 24 animals (dogs) in the methods section and then referred to an n of 28 in both the results and conclusion, and another stated only that the work involved 9 animals (Holstein calves I 'divided into two· groups'. Two papers reported results as means and standard errors of, for example, '10-25 observations' (i.e. animals), '10-14 flies', etc. One paper, which involved the use of primates and rats, gave the number of primates used but omitted to mention the number of rats. Nearly one-third of all papers (30%) did not give the number of animals used at all. Reporting the death of animals Ninety-eight of the papers described procedures which must have involved the death of the animals involved, yet 44 of these papers did not mention that death. The papers described, for example, experiments in which heart tissue was sampled (rats), and in which animals' livers were removed (rats), yet the use of terminal anaesthesia was not mentioned. Several such papers involved invertebrates, and one of these described the virtual destruction of the animals (shore crabs) without any mention of the use of anaesthesia or of the animals' eventual death: 'After autotomy of the chelae and walking legs, the dorsal carapace, heart, viscera, gills and brain were removed. The thoracic ganglion, anterior nerve trunks and ventral arterial system to the mouthparts region were left intact. The preparation was pinned down ... '. Simply not mentioning the death of animals appears to be the most direct of several ways in which the death of laboratory

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animals may be obscured in scientific publications. Our study also provided more qualitative data about this issue, and this is described elsewhere IBirke & Smith 1995). Of the 54 papers which did mention the death of the animals involved, 14 (26%) did not describe the method of killing (Table 6). Reference to guidelines or codes of practice Five papers (all originating in the US) did not provide detailed descriptions of animal housing, but instead stated that animals were maintained in accordance with certain nonstatutory guidelines or codes of practice, such as the NIH Guide (National Institutes of Health, 1985), or guidelines drawn up by a University Animal Care and Use Committee. Three papers gave no descriptions of animal husbandry, but instead referred the reader to previously published work. Unaddressed concerns over severity In some cases, work was described which caused substantial adverse effects on the animals involved. Only in rare cases, however, was mention made of the steps taken to minimize these harms. One paper, for example, describing a novel method for removal of the livers of dogs, followed by recovery, in order to study the integrated metabolism of the extrahepatic tissues, reported that '25 of the 28 experimental dogs survived the duration of the experiment (4-5 h post-op) without complications'. The paper was describing a method for others to follow, yet no mention was made of postoperative care, nor why three of the dogs

Table 6

Terminal procedures

Procedures not terminal Death and method of killing stated Death only stated Death not stated

Number of papers

Percentage of papers

51 40

34 27

14 44

9 30

316

died. Another paper reported an experiment on sepsis in rats. The methods stated that '24 hours post-operatively all animals appeared clinically septic'; but the results. showed that seven animals had died. There was no indication of any steps being taken to monitor or alleviate the effects of the procedures on the animals.

Discussion The most striking aspect of these data is how often information is not given. The llUmber, sex, and source of animals must surely be the basic requirements of any description of a scientific procedure involving animals, yet it is surprising how often even this information is omitted or obscured. How experimental data are analysed depends crucially in many experiments on the numbers of animals used, and omission of this information in a paper must seriously jeopardize its scientific quality. Moreover, if numbers are given incompletely or are given only in tables or figures comprising the experimental results, the reader is given no idea of how many animals were used, only how many contributed to the final data. Relatively few papers gave information about the conditions in which the animals were kept, yet variables such as temperature and stocking density may well affect the outcome of the experiment (see Fox 1986 for example). Most of those papers that did give such information were found in two journals: one that focused on experiments in animal behaviour, for which conditions of husbandry may be especially relevant, and the other that focused on the use of animals in science. It might be argued that restrictions on space in journals limit what can be said about the housing and care of animals. However, examination of the reports contained in one journal in our study (Laboratory Animals), which requires detailed descriptions of the animals and their husbandry (based on the guidelines prepared by GV-SOLAS, 1985), shows that a full description can be achieved using a maximum of only 50 words. Furthermore, in many of the papers reviewed for this study, it was found that the instances of poor reporting of animal procedures

Smith, Birke & Sadler

contrasted sharply with much more detailed descriptions of the mechanical, chemical and in vitro procedures involved in the same experiments. Of the studies involving the death of some or all of the animals used, 59% did not describe the method used to kill the animals, and 45 % did not mention the deaths at all. Furthermore, a number of papers contained descriptions of procedures which had the potential to cause considerable pain and/or distress to the animals involved, but included no indication of the steps taken to ameliorate such effects. Reporting details such as method of killing, or indeed that animals were killed, and giving details of the methods used to limit the severity of animal procedures are important. These details are vital both for the maintenance of high quality science, and for the public image of scientific research involving animals and the scientific endeavour itself. Better reporting of these aspects of the procedures would help to ensure that other scientists who wish to follow the methods described also follow best practice. The standard of reporting seemed in many cases to be related to the context in which the animals were used. Examples of the 'worst' reporting included studies in which animals became 'preparations' las, for example, in some neurophysiological and surgical work), in which the animals might be considered to be evolutionarily 'lower' (that is, where vertebrate ectotherms or invertebrates were used), or where the animals were used as 'tools' (in the production of antibodies, for instance). The 'best' reporting was found where animals were being studied for their own sakes, or to improve their usefulness as scientific models, or when they were used in non-invasive studies, especially in behavioural work. Whatever the reasons for poor reporting, researchers surely ought to take seriously both the need for good science, and the adverse image that inadequate descriptions can give to animal research. If poor reporting also means that proper guidelines were not followed, the quality of the science is likely to suffer. Our study points to the need for journals to establish more rigorous guidelines

Reporting animal use in scientific papers

and editorial procedures, in order to ensure adequate reporting. Such a policy should help to improve both the science itself and the public image of animal research. The published paper is, after all, part of the 'public face of science'. References Birke L, Michael M (1992) Views from behind the barricade. New Scientist 4 April, pp 29-32 Birke L, Smith JA (19951 Animals in experimental reports: the rhetoric of science. Society and Animals 3 (1), 23--42

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Fox MW (1986) Laboratory Animal Husbandry: _ Ethology, Welfare and Experimental Variables. Albany: State University of New York Gross AG (1990) The Rhetoric of Science. Cambridge, MA: Harvard University Press, p 129 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, 106-8 National Institutes of Health (1985) Guide for the Care and Use of Laboratory Animals. Bethesda, MD: NIH Publication No. 86-23

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