Systematic review of comparative studies examining alternatives to the harmful use of animals in biomedical education

Gary J. Patronek Center for Animals and Public Policy, Cummings School of Veterinary Medicine at Tufts University, North Grafton, MA 01536.

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Annette Rauch Center for Animals and Public Policy, Cummings School of Veterinary Medicine at Tufts University, North Grafton, MA 01536.

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Abstract

Objective—To systematically review the published literature for controlled studies comparing learning outcomes of traditional methods that require the terminal use of animals (eg, dissection, live-animal surgery, and live-animal laboratory demonstrations) with outcomes obtained with alternative teaching methods.

Design—Systematic review.

Study Population—Controlled studies published between 1996 and 2004.

Procedures—PubMed was searched with the following keywords, used alone and in combination: educational alternatives, nonlethal teaching methods, veterinary alternatives, medical education, and nonterminal animal use. Cited references of retrieved reports were reviewed to identify additional reports. Reports were selected for review only if a comparison group was included.

Results—17 studies that were randomized controlled trials or nonrandomized trials that included a comparison group were identified. Five involved veterinary students, 3 involved medical students, 6 involved university undergraduate students, and 3 involved high school biology students. Sample size ranged from 14 to 283 students. Eleven studies appeared to be randomized, parallel-group trials, 4 involved comparative groups to which participants were not randomly assigned or for which the randomization process was not clear, 1 was a 2-period crossover study, and 1 involved a retrospective review of grades. In all 17 studies reviewed, results associated with the alternative method of instruction were not significantly different from or superior to results associated with the conventional method.

Conclusions and Clinical Relevance—Although the number of controlled studies identified was small, the results seem to support more widespread adoption of alternative teaching methods in biomedical education.

Abstract

Objective—To systematically review the published literature for controlled studies comparing learning outcomes of traditional methods that require the terminal use of animals (eg, dissection, live-animal surgery, and live-animal laboratory demonstrations) with outcomes obtained with alternative teaching methods.

Design—Systematic review.

Study Population—Controlled studies published between 1996 and 2004.

Procedures—PubMed was searched with the following keywords, used alone and in combination: educational alternatives, nonlethal teaching methods, veterinary alternatives, medical education, and nonterminal animal use. Cited references of retrieved reports were reviewed to identify additional reports. Reports were selected for review only if a comparison group was included.

Results—17 studies that were randomized controlled trials or nonrandomized trials that included a comparison group were identified. Five involved veterinary students, 3 involved medical students, 6 involved university undergraduate students, and 3 involved high school biology students. Sample size ranged from 14 to 283 students. Eleven studies appeared to be randomized, parallel-group trials, 4 involved comparative groups to which participants were not randomly assigned or for which the randomization process was not clear, 1 was a 2-period crossover study, and 1 involved a retrospective review of grades. In all 17 studies reviewed, results associated with the alternative method of instruction were not significantly different from or superior to results associated with the conventional method.

Conclusions and Clinical Relevance—Although the number of controlled studies identified was small, the results seem to support more widespread adoption of alternative teaching methods in biomedical education.

Prior to the late 1970s, the terminal use of animals in biomedical education was routine. By the mid 1980s, however, objections to the use of animals for this purpose began to arise, reflecting the overall change in social attitudes towards animals. Veterinary medicine has been at the center of this debate from its early days,1–4 with an increasing number of schools and colleges of veterinary medicine eliminating, reducing, modifying, or replacing educational experiences that involve euthanasia of animals or pain.5–8 As an example, at least 8 schools and colleges of veterinary medicine in the United States have established programs whereby clients can donate the bodies of their animals for use in anatomic and surgical training programs,8 reducing or eliminating the need to obtain purposebred animals for these programs. In contrast, it is difficult to gauge the degree to which alternatives to the terminal use of animals have been incorporated into undergraduate, high school, and middle school educational programs.

The primary objections to the terminal use of animals in biomedical education include a belief that it is ethically wrong to kill healthy animals for educational purposes5,9 and a conviction that medical and surgical skills can be obtained without such use of animals.6,10 It has also been suggested that the terminal use of animals could lead to decreased sensitivity among professional students11 and to a sense of irreverence for life.10,12 In addition, some have considered the use of animals from particular sources (eg, shelter animals, animals obtained from the racing industry, and purpose-bred animals) to be ethically unacceptable. Finally, there are concerns about the effect on biodiversity and species survival when large numbers of animals, such as frogs, are indiscriminately collected from the wild. The latter is not an unimportant concern, given that in 2000, 9 million vertebrate animals were used for biomedical education in the United States, with the number of invertebrate animals used thought to be equal to the number of vertebrate animals.13

Apart from ethical concerns, it has been noted that some medical and graduate students have a strong emotional response to seeing, for the first time, an animal immobilized under anesthesia in preparation for an invasive procedure. Some students have described this experience as “shocking,” and this emotional response detracts from learning, even in the presence of excellent teaching.14 There are also economic and logistic considerations associated with the use of live animals in training programs, particularly because such programs require extensive close supervision by professional faculty, whereas alternatives, such as computer simulations, require less faculty input, putting less pressure on faculty time and budgets. Several reports14,15 have documented time and cost savings when nonanimal alternatives were implemented.

The advantages and disadvantages of alternatives to the terminal use of animals in biomedical education have been widely discussed. Deeply held opinions about the essential elements of biomedical education and about what constitutes appropriate use of animals, along with the personal experiences of faculty members and the perception that accepting alternatives in education may suggest that other uses of animals are equally inappropriate, all influence how individual students, faculty members, administrators, and institutions have approached the issue.

The range of alternatives to the terminal use of animals in biomedical research is currently quite large.16–19 However, despite the passionate arguments and strongly held opinions by advocates on both sides of the issue, there has been surprisingly little focus on the actual learning outcomes achieved when alternatives replace conventional teaching methods. The purpose of the study reported here, therefore, was to systematically review the published literature for controlled studies comparing learning outcomes of traditional methods that require the terminal use of animals (eg, dissection, live-animal surgery, and live-animal laboratory demonstrations) with outcomes obtained with alternative teaching methods (eg, interactive videodisk or computer-based simulation, surgical models, and ethically sourced cadavers). Studies involving any area of biomedical education from secondary school through postprofessional training were considered.

Methods

Published reports for inclusion in the present study were identified by searching archival materials maintained by the Center for Animals and Public Policy at the Cummings School of Veterinary Medicine and an unpublished bibliographya of studies of student performance. In addition, PubMed was searched for articles published between 1966 and 2004 with the following keywords, used alone and in combination: educational alternatives, nonlethal teaching methods, veterinary alternatives, medical education, and nonterminal animal use. Cited references of retrieved reports were reviewed to identify additional reports. Published reports were included in the present study only if a comparison group was included.

Results

Studies retrieved—The systematic review process yielded 17 studies that were either randomized controlled trials or nonrandomized trials that included a comparison group. Five of the 17 studies involved veterinary students,20–24 3 involved medical students,14,25,26 6 involved university undergraduate students,27–30,b,c and 3 involved high school biology students.31–33 Two studies were reported only in abstract formb,c; the remainder were full manuscripts. Sample size ranged from 14 to 283 students.

Eleven of the studies appeared to be randomized, parallel-group trials,20–25,27,30–32,c 4 involved comparative groups to which participants were not randomly assigned or for which the randomization process was not clear,26,28,29,33 1 was a 2-period crossover study,14 and 1 involved a retrospective review of grades.b

Types of alternatives studied—A wide range of alternatives were compared with traditional animal-based instructional methods (Appendix). The studies involving veterinary students included a study of intestinal anastomosis performed on cadavers versus anesthetized dogs,20 a comparison of an interactive videodisk simulation versus a live animal demonstration or participation laboratory,21 studies of surgical training with animal models versus anesthetized dogs22 or cadavers,23 and a study24 comparing a hemostasis model with splenectomy in anesthetized dogs.

All but 1 of the 17 studies consisted of comparison of an alternative method that involved a nonharmful use of animals with live-animal demonstration, liveanimal surgery, or animal dissection. In the remaining study,20 surgical training with cadavers was compared with surgical training on anesthetized animals. This study was included because at the time, use of cadavers for surgical training in veterinary medicine represented the state-of-the-art alternative to live-animal surgery. In addition, it is possible to obtain cadavers from animals euthanized for medical reasons and several schools and colleges of veterinary medicine have implemented client donation programs.

Evaluation methods—With the exception of the 2-period crossover study,14 which compared faculty and student impressions of a software program demonstrating cardiovascular principles versus live animal demonstration, all of the studies20,22-24 incorporated some type of standardized, quantifiable outcome, such as an assessment of surgical performance. In 1 study,20 burst pressure of anastomoses was examined. Other quantifiable outcomes included performance on laboratory reportsb and grades on examinations.21,25-33,c

Outcomes—In all 17 studies, results associated with the alternative method of instruction were either not significantly different from or superior to results associated with the conventional method of instruction.

Discussion

In the present study, although we were able to identify a relatively limited number (17) of controlled studies that evaluated leaning outcomes of traditional versus alternative methods, in all studies that were identified, the alternative method yielded results that were not significantly different from or were superior to results obtained with the conventional method of instruction. These findings appeared to be robust, as they involved a wide range of participants, alternatives, and outcomes. All studies used a comparison group, and most were randomized. All but 1 included quantifiable outcomes, such as examination grades, and in the veterinary studies that involved subjective assessments of surgical skills, the evaluators were blinded to teaching method. Thus, our findings seem to support more widespread adoption of alternatives to the terminal use of animals in biomedical education.

Our review of the literature revealed that alternative methods have been developed for a wide range of teaching outcomes. In the field of veterinary education in particular, models of parenchymal abdominal organs that have been developed have been found to be as realistic in regard to tissue handling properties as actual organs.34 This seems to suggest that barriers to more widespread adoption of alternatives are not technological.

Many of the studies that we reviewed are > 10 years old. Thus, some of the alternative methods that were used are themselves now outdated. This is particularly true for films, videotapes, and early computer-based alternatives, which have become outmoded because of subsequent advances in computer technology. In contrast, animal-based dissection, demonstration, and surgical teaching exercises have likely changed little in terms of the technical aspects of the learning. Thus, many of the comparisons in the present study in which no differences were found between alternative and conventional teaching methods likely represent worst-case scenarios. It could be argued that with the use of currently available virtual-reality technology, alternatives might score considerably higher in formal comparisons.

Some of the advantages cited for alternative teaching methods include reductions in faculty teaching time, costs associated with purchasing animals and maintaining animal colonies, and the number of animals killed; an increased ability for students to repeat procedures until skills are mastered; greater flexibility in terms of when students can complete exercises; greater ability for students to work at their own pace; and, for many students, equal or superior academic mastery of the subject matter and the required manual dexterity skills. In addition, alternative methods provide students and faculty members who have ethical objections to the terminal or harmful use of animals a viable method for achieving their educational objectives.

Virtual reality technology has the potential to revolutionize alternative teaching methods,35 and virtual reality methods are being applied in veterinary medicine.16,19 However, even relatively unsophisticated methods can be used to provide students with training in basic surgical skills.36–40

Importantly, studies included in the present review had some limitations. Some studies20,28 included small sample sizes, and some measured outcomes of individual students when groups or teams were used for randomization purposes,20,21,31,33 included only vague descriptions of methodology and testing methods,25 provided insufficient information about the extent of use of conventional methods in the alternative teaching group,27 or provided limited head-to-head comparisons of alternative with conventional groups.14 The 2 studiesb,c published only in abstract form were difficult to assess because of the limited amount of information provided.

Despite these limitations, none of the studies included in the present review reported that the alternative method that was studied was inferior to the conventional method. This finding, coupled with the successful implementation of alternative teaching methods in a wide variety of veterinary school programs, argues that alternatives are a viable method of instruction in the field of biomedical education. Thus, we would encourage biomedical educators to consider how adopting alternative teaching methods could be of benefit to their teaching programs, students, and faculty members.

a.

Balcombe J, De Boo J, Knight A. Comparative studies of student performance: humane teaching alternatives demonstrate superior efficacy to harmful animal use. Available at: www.eurca.org/downloads/animaled/comp.doc. Accessed Dec 11, 2006.

b.

Dewhurst DG, Meehan AS. Evaluation of the use of computersimulations of experiments in teaching undergraduate students (abstr). Br J Pharmacol 1993;108(suppl):238.

c.

Henman MC, Leach GDH. An alternative method for pharmacology laboratory class instruction using biovideograph tape recordings (abstr). Br J Pharmacol 1983;80(suppl):591.

References

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    Rosin E. The importance of using living animals in the small animal student surgery laboratory. J Vet Med Educ 1986;13:1113.

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    Kahler SC. Will nonrecovery surgery courses survive?. J Am Vet Med Assoc 2000;216:1201, 1204.

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    Loew FM. Tufts develops alternative program for teaching surgery. J Am Vet Med Assoc 1989;195:868870.

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    White KK, Wheaton LG, Greene SA. Curriculum change related to live animal use: a four-year surgical curriculum. J Vet Med Educ 1992;19:610.

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    Comparison of alternatives offered by veterinary schools. Altern Vet Med Educ 2006;31:67.

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    McBride M. Student attitudes toward use of animals in surgery laboratories surveyed. J Am Vet Med Assoc 1989;195: 886.

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    Chambers JN. Prospective peer review of animal use in teaching and research. J Vet Med Educ 1986;13:57.

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    Wood MW, Hart LA, Weng HY. Effective bibliographic searching for animal alternatives in veterinary medical education: the UC Davis Web site. J Vet Med Educ 2005;32:468472.

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    Hart LA, Wood MA, Weng HY. Mainstreaming alternatives in veterinary medical education: resource development and curricular reform. J Vet Med Educ 2005;32:473480.

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Appendix

Appendix

Summary of 17 comparative studies involving alternatives to harmful use of animals in biomedical education.

Carpenter LG, et al20
Purpose—To determine whether substitution of cadavers for anesthetized dogs when teaching surgical skills would result in an equivalent learning experience.
Design—Randomized parallel-group study.
Subjects—24 second-year veterinary students.
Subject selection—Subjects were randomly selected from those who applied to complete an elective surgery laboratory.
Alternative method—Student surgery teams performed procedures on 3 days on cadavers; on the fourth day, student teams performed an intestinal anastomosis on a live dog.
Control method—Student surgery teams performed procedures on 3 days on anesthetized dogs.
Measured outcomes—Surgical performance was scored by blinded evaluators. Anastomoses were tested for burst strength.
Results—There were no significant differences between the scoresfor the 2 groups.
Author conclusion—The cadaver experience seemed to strengthen student preference for use of live animals; cadavers might be bestsuited for preliminary skill-building.
Dewhurst DG, et al28
Purpose—To evaluate the effectiveness of an interactive computer-assisted learning program versus a traditional laboratory.
Design—Parallel-group study.
Subjects—14 second-year undergraduate honors physiology students.
Subject selection—Students were allotted to 2 groups (8 controland 6 experimental).
Alternative method—Computer-assisted learning program and independent study.
Control method—Students performed a series of laboratory experiments evaluating nutrient transport in rat small intestine under close supervision.
Measured outcomes—Scores on tests of knowledge and attitude taken before and after the intervention.
Results—Groups had comparable baseline knowledge scores andsimilar improvements in scores after the intervention.
Author conclusion—The live-animal laboratory session was almost 5 times as expensive as the computer-assisted learning program.
Fawver AL, et al21
Purpose—To compare simulated and traditional cardiovascular physiology laboratories.
Design—Randomized, parallel-group study.
Subjects—85 first-year veterinary students.
Subject selection—Self-selected lab groups of 3 to 4 students each were randomly assigned to interventions.
Alternative method—Interactive videodisk simulation of a cardiovascular physiology laboratory.
Control method—Traditional live-animal participation laboratory and traditional live-animal demonstration laboratory.
Measured outcomes—Scores on a 22-item multiple-choice test.
Results—There were no significant differences in test scores among groups; time savings for faculty involved in the alternativelaboratory were substantial.
Author conclusion—The videodisk laboratory for teaching cardiovascular physiology was just as effective and more timeefficient than traditional laboratories.
Greenfield CL, et al22
Purpose—To determine whether use of soft tissue models would prepare veterinary students as well as traditional nonsurvival surgery to perform subsequent survival surgery.
Design—Randomized, parallel-group study.
Subjects—36 third-year veterinary students.
Subject selection—Participants were randomly assigned to groupsby level of previous surgical experience.
Alternative method—Students trained with soft tissue models.
Control method—Students trained on anesthetized dogs that wereeuthanatized at the end of the laboratory period.
Measured outcomes—Student performance during ovariohysterectomy as assessed by blinded evaluators andperformance during fourth-year surgery rotations.
Results—There were no significant differences in scores between groups.
Author conclusion—The models were an acceptable alternative for teaching a part of the small animal surgery curriculum.
Guy JF, Frisby AJ27
Purpose—To determine whether interactive videodisk can replace some laboratories in human gross anatomy for undergraduates seeking careers in allied health professions.
Design—Randomized, parallel-group study.
Subjects—Undergraduate students in prenursing or allied health professions; 190 students in a pilot study and 283 in a full study.
Subject selection—Students were randomly assigned to computeror cadaver demonstration.
Alternative method—Computerized interactive videodisk.
Control method—Cadaver laboratory demonstrations by teachingassistants.
Measured outcomes—Pilot study: unannounced practical examination involving a cadaver 1 week after completing thelaboratory; full study: weekly quizzes and comprehensive examination.
Results—In the pilot study, the computer-trained students scored as well as the cadaver-trained students in 2 of the 3 sections. In the full study, there were no significant differences in scores between groups.
Author conclusion—The visual science of anatomy can be taught by means of interactive videodisk as a supplement to or replacement for cadaver laboratories.
Jones NA, et al26
Purpose—To compare a multimedia program and prosection tutorials with traditional lecture and dissection.
Design—Comparative group trial.
Subjects—First-year medical students.
Subject selection—Every fifth student was selected for the intervention.
Alternative method—Multimedia presentations and prosections.
Control method—Traditional lecture and cadaver dissection.
Measured outcomes—Written and practical gross anatomy examination scores and scores for National Board Examination questions on anatomy.
Results—Overall, student performance appeared similar with both methods of instruction.
Author conclusion—Students in the alternative teaching group learned human anatomy as well as those in the traditional lecture-dissection program.
Leathard HL, Dewhurst DG25
Purpose—To compare 2 approaches to teaching the pharmacology of colonic motility.
Design—Randomized, parallel-group study.
Subjects—156 second-year medical students.
Subject selection—Students were randomly assigned to groups.
Alternative method—A computer-assisted learning program.
Control method—Standard instructor-led demonstration.
Measured outcomes—Scores on a 20-item test.
Results—There was no significant difference in mean scores between groups. Staff resources were considerably less for the computer-assisted group.
Author conclusion—Student learning, as measured by answers to key questions, was not significantly different, but the computer-assisted group did not perform as well as the instructor-led group.
Olsen D, et al24
Purpose—To compare student performance on basic skills in blood vessel separation and ligation following training with a hemostasis model versus splenectomy.
Design—Randomized parallel-group study.
Subjects—40 second-year veterinary students.
Subject selection—Students were randomly assigned to groups.
Alternative method—Hemostasis model.
Control method—Splenectomy on a live dog with ligation of jejunal vessels.
Measured outcomes—Videotaped performance of hemostasis skills, direct traction of ligatures, evaluation of knots under a dissecting microscope, and testing on an electronic suture board.
Results—The model group had a lower number of errors and lower time to complete exercises; more students in the model group tied square knots and tight ligatures, and instrument gripwas rated better for the model group.
Author conclusion—The hemostasis model was at least as effective as use of live animals in teaching basic skills involvedin vessel ligation.
Strauss RT, Kinzie MB33
Purpose—To examine the effectiveness of interactive videodisk simulation of frog dissection as an alternative to frog dissection.
Design—Parallel-group study.
Subjects—2 classes of 17 high school biology students.
Subject selection—Classes were randomly assigned to interventions.
Alternative method—Interactive videodisk simulation.
Control method—Traditional dissection.
Measured outcomes—Scores on a 25-item test before and after the intervention.
Results—Scores were not significantly different between groups.
Author conclusion—The results supported the notion thateducationally effective alternatives to dissection can be developed.

Contributor Notes

Address correspondence to Dr. Patronek.
  • 1

    Gambardella PC. The pros and cons of survival surgery in the teaching laboratory. J Vet Med Educ 1986;13:1314.

  • 2

    Jennings PB. Alternatives to the use of living animals in the student surgery laboratory. J Vet Med Educ 1986;13:1416.

  • 3

    Rosin E. The importance of using living animals in the small animal student surgery laboratory. J Vet Med Educ 1986;13:1113.

  • 4

    Kahler SC. Will nonrecovery surgery courses survive?. J Am Vet Med Assoc 2000;216:1201, 1204.

  • 5

    Pavletic MM, Schwartz A, Berg J, et al. An assessment of the outcome of the alternative medical and surgical laboratory program at Tufts University. J Am Vet Med Assoc 1994;205:97100.

    • Search Google Scholar
    • Export Citation
  • 6

    Loew FM. Tufts develops alternative program for teaching surgery. J Am Vet Med Assoc 1989;195:868870.

  • 7

    White KK, Wheaton LG, Greene SA. Curriculum change related to live animal use: a four-year surgical curriculum. J Vet Med Educ 1992;19:610.

    • Search Google Scholar
    • Export Citation
  • 8

    Comparison of alternatives offered by veterinary schools. Altern Vet Med Educ 2006;31:67.

  • 9

    Patronek GJ. Tufts University School of Veterinary Medicine client donation program. Altern Vet Med Educ 1999;11:23.

  • 10

    Buyukmihci N. Alternatives in veterinary surgical training. In:Humane innovations and alternatives in animal experimentation . Washington Grove, Md: People for the Ethical Treatment of Animals, 1989;3:9697.

    • Search Google Scholar
    • Export Citation
  • 11

    McBride M. Student attitudes toward use of animals in surgery laboratories surveyed. J Am Vet Med Assoc 1989;195: 886.

  • 12

    Chambers JN. Prospective peer review of animal use in teaching and research. J Vet Med Educ 1986;13:57.

  • 13

    Balcombe J. The use of animals in higher education: problems, alternatives, and recommendations. Washington, DC: Humane Society Press, 2000.

    • Search Google Scholar
    • Export Citation
  • 14

    Samsel RW, Schmidt GA, Hall JB, et al. Cardiovascular physiology teaching: computer simulations vs animal demonstrations. Am J Physiol 1994;266:S36S46.

    • Search Google Scholar
    • Export Citation
  • 15

    Hart LA, Anderson DC, Zasloff R. Alternatives to the use of live animals in veterinary school curricula. In:Humane innovations and alternatives. Washington Grove, Md: People for the Ethical Treatment of Animals, 1993:7:499503.

    • Search Google Scholar
    • Export Citation
  • 16

    Scalese RJ, Issenberg SB. Effective use of simulations for the teaching and acquisition of veterinary professional and clinical skills. J Vet Med Educ 2005;32:461467.

    • Search Google Scholar
    • Export Citation
  • 17

    Wood MW, Hart LA, Weng HY. Effective bibliographic searching for animal alternatives in veterinary medical education: the UC Davis Web site. J Vet Med Educ 2005;32:468472.

    • Search Google Scholar
    • Export Citation
  • 18

    Hart LA, Wood MA, Weng HY. Mainstreaming alternatives in veterinary medical education: resource development and curricular reform. J Vet Med Educ 2005;32:473480.

    • Search Google Scholar
    • Export Citation
  • 19

    Martinsen S, Jukes N. Towards a humane veterinary education. J Vet Med Educ 2005;32:454460.

  • 20

    Carpenter LG, Piermattei DL, Salman MD, et al. A comparison of surgical training with live anesthetized dogs and cadavers. Vet Surg 1991;20:373378.

    • Search Google Scholar
    • Export Citation
  • 21

    Fawver AL, Branch CE, Trentham L, et al. A comparison of interactive videodisc instruction with live animal laboratories. Am J Physiol 1990;259:S11S14.

    • Search Google Scholar
    • Export Citation
  • 22

    Greenfield CL, Johnson AL, Schaeffer DJ, et al. Comparison of surgical skills of veterinary students trained using models or live animals. J Am Vet Med Assoc 1995;206:18401845.

    • Search Google Scholar
    • Export Citation
  • 23

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