Letter to the editor
Analgesia for tonsil biopsy
I recently read an article by Lowe et al,1 published in the Journal of Swine Health and Production (JSHAP), that caused me concern. The paper reported a tonsil biopsy procedure (I at first thought it was tonsillectomy) that, as reported, used (in my view) inadequate analgesia and no periprocedural analgesia.
The work was performed under the purview of the university, but no mention was made of its approval by their institutional animal care and use committee (IACUC). I have since learned that the work was approved by their IACUC. In subsequent discussions with the University of Illinois IACUC, they supported the authors and their original decision to approve the protocol. I have also had some conversations with one of the authors that clarified what they did and how it was done.
On first reading, the paper was shocking to me in its apparent cruelty. It seemed obvious to me that the tissue that was removed was of sufficient mass and of sufficient innervation that the pain would be expected to be significant. Some veterinarians disagree with my view. Other veterinarians I consulted were of the view that the work was painful, that topical analgesic does not penetrate very deeply, and that it requires 10 to 20 minutes to be effective. The lack of analgesia is perhaps a larger concern. I also learned that the pig veterinary community is mixed on its view of the possible painfulness of this procedure.
The standard used by IACUC, in unclear situations, is, if the procedure is reasonably expected to cause pain in humans, that it should be expected to cause pain in the animal. How many swine veterinarians would be willing to have a tonsil biopsy using only immediate topical lidocaine and no periprocedural analgesia? Would you allow your family members to undergo the same procedure without infiltrating local anesthesia or periprocedural analgesia?
Considering this specific situation, in my view, the authors did as they should have, even if they were less compassionate then they might have been. The IACUC did not fulfill its regulatory or ethical responsibility, in my view - they did not give the sows the benefit of the doubt and require, at a minimum, chemical analgesia.
I find the evidence of direct observations of sow behavior by the authors to be inadequate. I would be convinced if there were actually data collected on detailed behavioral responses. One must understand that some animals' reactions to pain are to be less active and others, to show behavioral signs of pain. Detailed behavioral reactions of sows to this procedure have not been published, as far as I know.
I publish in several other scientific journals, and many require that the work be approved by the IACUC and that this fact be reported in the journal (see Journal of Animal Science, for example). I recommend that the editors of JSHAP do likewise. I also recommend, when papers that involve potentially painful procedures are reviewed, that an additional animal care review be performed.
Finally, I suggest that the editorial staff of JSHAP and the members of the production animal veterinary community evaluate the techniques they employ in terms of actual or potential pain animals may experience (giving animals the benefit of the doubt), and what could be done to alleviate that pain. Giving analgesics, for example, would do no harm in case the procedure turned out later to be not painful.
John J. McGlone, PhD, PAS Professor Texas Tech University
Reference
1. Lowe, JF, Firkins LD, Banerjee M, Goldberg TL. A novel technique for the collection of antemortem tonsil biopsies from unanesthetized swine. J Swine Health Prod. 2003;11:229-232.
Analgesia for tonsil biopsy - Response
We appreciate Dr McGlone's concerns about our tonsil biopsy paper. Like him, we are strong proponents of animal welfare. In fact, the reduction of animal suffering from infectious disease is what stimulated us to seek an improved method for obtaining tonsil tissue from swine in the first place. We do, however, have a different view than Dr McGlone on the animal welfare implications of the tonsil biopsy procedure that we have described.
It is important to note that our paper describes a biopsy of the tonsil, and not a removal of the entire tonsil (tonsillectomy), as Dr McGlone first believed. The normal porcine tonsil of the soft palate has a surface area of greater than 250 mm2 (1.0 cm x 2.5 cm) in pigs that weigh approximately 22.5 kg. Our procedure removes a 6-mm diameter (28.25 mm2) biopsy from the interior of the tonsil. This results in removal of approximately 10% of the total area of one tonsil in pigs that weigh approximately 22.5 kg, and much less in larger animals. As in most primary lymphoid organs, the innervation and vascular supply to the tonsil is only in the connective tissue on the surface of the tonsil, below the epithelial layer. Most of the tonsil is made up of lymphoid tissue that is avascular.1 Our procedure leaves the highly innervated and vascular tissue of the soft palate undisturbed. We would never advocate that tonsillectomy should be performed without general anesthesia and proper postoperative pain management. However, the biopsy procedure that we described does not cause the soft tissue damage and subsequent pain that is associated with a tonsillectomy.
In the original paper, we point out that tonsil biopsy procedures have been previously described in the literature. We have spoken with many professionals who have used available tonsil biopsy procedures for research and diagnostics. Unfortunately, techniques commonly used prior to the development of our method employed mare uterine biopsy forceps, which tear, rather than cut, tissue. Our technique is therefore less traumatic.
We designed our procedure to be as quick as possible, and therefore to minimize stress to the pig. Although our procedure may appear at first glance to be stressful and painful, our best assessment is that it is only minimally so. We made direct observations on all pigs that we sampled. And while these observations were not conducted for research purposes, those of us making the observations each have over 20 years experience both treating pigs, and more importantly, providing daily care for pigs. Our success as both clinicians and pig farmers has required us to clearly understand and identify normal and abnormal behavior. While we understand the need for a science-based approach to measuring an animal's state of being, we also believe that where objective data collection is not possible or impractical, good sound clinical judgment is our best tool to improve the state of being for all animals. Our observation and judgment indicated that the procedure caused no adverse effects on individuals that were sampled.
In addition, the producers who own the pigs have observed the pigs daily for months. There have been no reports from producers of any long-term adverse effects from the procedure. We therefore conclude that our procedure causes minimal discomfort to pigs. We further conclude that the disadvantages of causing transient minor discomfort to pigs are outweighed by the advantages of having an improved research and diagnostic tool for diseases such as porcine reproductive and respiratory syndrome, which cause considerable suffering for animals and significant economic losses for producers.
This paper underwent peer review by the Journal of Swine Health and Production (JSHAP), and all procedures were approved by the Institutional Animal Care and Use Committee (IACUC) at the University of Illinois Urbana-Champaign. All authors of the paper have completed training and certification in animal care and use procedures as required by the University of Illinois. The approval process was very thorough and involved numerous discussions with the university IACUC prior to initiation of the study.
As for Dr McGlone's suggestions about changes in JSHAP, we will defer to the editors. However, we feel very strongly that JSHAP, its editors, the AASV, and the veterinary community are committed to improving animals' state of being through research, daily care, and open discussion of challenging issues. As an example, the editor of JSHAP published an insightful commentary about our paper2 and the responsibilities that we as veterinarians have for insuring the well being of animals. Journals such as JSHAP have a responsibility to provide a forum for intellectual discourse on such matters, both for the good of the profession and for the good of the animals.
We remain open to suggestions and criticisms and would very happily welcome constructive ideas from Dr McGlone or anyone else about how we might improve this procedure. Any modifications to our procedure that would reduce time, discomfort, and stress even further would be a valuable contribution.
Sincerely,
James Lowe, DVM, MS Larry Firkins, DVM, MS, MBA Tony Goldberg, DVM, PhD
References
1. Horter DC, Yoon KJ, Zimmerman JJ. A review of porcine tonsils in immunity and disease. Anim Health Res Rev. 2003;4:143-155.
*2. Dewey CE. Does oil contain fat? J Swine Health Prod. 2003;11:275.
* Non-refereed reference.
Analgesia for tonsil biopsy - Editor's response
I appreciate Dr McGlone's concerns about the Journal of Swine Health and Production publishing manuscripts that report results of research conducted on animals without also publishing the fact that the researcher's institutional animal care and use committee had approved the research. It was not the intension of the editorial board to do so. The editorial staff has instituted a policy whereby this information will be reported by the authors of manuscripts that involve animals. The revised guide to authors published in this issue reflects this policy. For manuscripts that have already been submitted for publication, the editors will ask the authors for the information.
Cate Dewey, DVM, MSc, PhD Executive Editor Journal of Swine Health and Production