Body temperature patterns during natural fevers in a herd of free-ranging impala (Aepyceros melampus)

Transcription

1 Body temperature patterns during natural fevers in a herd of free-ranging impala (Aepyceros melampus) Peter R. Kamerman, Andrea Fuller, Alida S. Faurie, Graham Mitchell and Duncan Mitchell Department of Physiology, University of the Witwatersrand, Medical School, 7 York Road, Parktown 2193, South Africa. Peter R. Kamerman, BSc (Hons) Andrea Fuller, BSc (Hons), PhD Alida S. Faurie, BSc (Hons), MSc, PhD Graham Mitchell, BSc, BVSc, PhD, DVSc, MRCVS Duncan Mitchell, BSc (Hons), MSc, PhD, FRSSAfr Address for correspondence: Peter Kamerman Department of Physiology, University of the Witwatersrand, Medical School, 7 York Road, Parktown 2193, South Africa. Tel: (+2711) Fax: (+2711) ned@chiron.wits.ac.za

2 In a clinical setting, rectal temperature of a sick animal typically is measured sporadically, often no more than once or twice, so that the time profile of the fever never is established. Also, because animals are examined usually only when overt signs of sickness behaviour, which typically accompany a fever, have presented, the genesis of the fever is complete before the first temperature measurement is made. Thus, body temperature patterns, during fevers of natural origin, never have been described properly in any animal. We present here what we believe to be the first complete characterisation of the body temperature response to a spontaneous infection. Moreover, our data provide the first evidence for fevers developing in, and spreading between, free-ranging animals in their natural habitat. The fevers were observed serendipitously in seven free-ranging adult female impalas (Aepyceros melampus), which had been instrumented for a study to determine the effect of capture on body temperature. Body core temperature was measured at ten-minute intervals, in the animals, by miniature temperature data loggers implanted under general halothane anaesthesia into the abdominal cavity, according to techniques described previously (Fuller and others 1999). The implantations took place over a two-day period. After surgery, the impalas were released into a 62 ha fenced game enclosure at the Lichtenburg Game Breeding Centre, South Africa. The animals were left undisturbed for three months in preparation for subsequent capture. Throughout this period, black globe temperature - an integrated measure of air temperature, solar radiation and wind speed - was measured at the study site. On completion of the capture study, 162 days after implantation, the loggers were retrieved from the animals under halothane anaesthesia. Inspection of the data revealed that the animals had experienced febrile episodes during the period they had been left undisturbed, long after they had recovered from surgery. Figure 1 shows the mean (± SD) daily body temperature of each impala (A - G) over a fifty-twoday period. A fever (defined here as mean daily body temperature at least 0.5 C above normal) was evident first in impala A. Within a few days, five other animals (B-F) also developed sustained elevations in body temperature, with varying latency. The whole herd exhibited fever over about a month, with some animals displaying more than one febrile episode, and each episode lasting between one and seven days. The maximum temperature attained during each febrile episode also varied between animals, from.4 to 41.5 C. There were no unusual climatic conditions at the times when body temperature was elevated, and no similar body temperature changes occurred during the remaining 90 days of body temperature measurement. We believe that these fevers reflect the spread of one or more contagious pathogens. The temperature patterns also show that resistance to these pathogens, or the pathogen load, differed between individuals; there was high intra- and inter-individual variability in the responses.

3 Body temperature, averaged over one-hour intervals, for one representative animal (C) is shown in Figure 2. Like that of other small free-ranging antelope (for example Mitchell and others 1997), body temperature normally fluctuated by ~ 1 C each day. This circadian variation was maintained during febrile episodes, even during the development and resolution of fever (Students t-test P>0.05). The phases of the circadian rhythm were not affected by the presence of a fever, with a trough in body temperature consistently occurring at ~ 06:00 and a maximum at ~ 17:00 (Figure 3). The body temperature of the impala, like that of the eland (Fuller and others 1999), was lowest at the same time as black globe temperature was lowest (~ 06:00), but peaked around sunset, five hours after black globe temperature had reached its maximum (Figure 3). The maintenance of the circadian rhythm, which also has been observed in febrile humans (Musher and others 1979, Dinarello and Wolff 1990), has important implications for the detection of fever in a clinical setting. Positive diagnosis of fever, in any animal with a febrile pattern similar to that of our impala, is much more likely to be made when body temperatures peak, in the late afternoon (15:00 to 18:00), but the fever may go undetected if body temperature is measured only in the morning. Indeed, afternoon body temperatures in healthy animals often exceeded morning temperatures in febrile animals. This overlap of body temperatures reveals the importance of specifying time of day when identifying a so-called normal body temperature range, and also the value of making multiple measurements of body temperature when seeking to diagnose fever. Also, our results illustrate the differences in the temperature profile of a natural fevers and an experimentally-induced fever. Experimentally-induced fevers, using purified pyrogens (e.g., Gram-negative endotoxin), typically are biphasic, resolve within six hours and are not superimposed on the circadian temperature rhythm (van Miert and others 1982, Kluger 1991). The development of spontaneous long-duration fevers in free-ranging animals, as evident in our impala, has consequences for game management practices. Hyperthermia often is implicated in the mortality of animals during game capture, particularly in impala (Murray and others 1981), and capture attempts therefore routinely are carried out in the early morning or late afternoon, when the environmental heat load is low. Body temperature, however, is highest not in the middle of the day, but in the late afternoon, in diurnal ungulates (for example, Mitchell and others 1997; Fuller and others 1999). If intense exercise is induced at this time, and particularly if the animal is febrile, the body temperature will reach potentially lethal levels much earlier than if similar exercise was induced in the morning. We therefore believe that capture in the afternoon should be avoided.

4 Acknowledgements We thank André Matthee and Raymond Cherry for their assistance, Dr Ferdi Schoeman and the Research Committee of the National Zoological Gardens of South Africa for granting us access to the facility, and the National Research Foundation for funding. The experiment was approved by the Animal Ethics Screening Committee of the University of the Witwatersrand (clearance certificate 99/90/5). References DINARELLO, C. A. & WOLFF, S. M. (1990) Pathogenesis of fever. In Principles and Practice of Infectious Disease. 3rd edn. Eds. G. L. Mendell, R. G. Douglas, J. E. Bennett. New York, Churchill Livingston. pp FULLER, A., MOSS, D. G., SKINNER, J. D., JESSEN, P.T., MITCHELL, G. & MITCHELL, D. (1999) Brain, abdominal and arterial blood temperatures of free-ranging eland in their natural habitat. Pflugers Archiv European Journal of Physiology 438, KLUGER, M. J. (1991) Fever: role of pyrogens and cryogens. Physiological Reviews 71, MITCHELL, D., MALONEY, S. K., LABURN, H. P., KNIGHT, M. H., KUHNEN, G. & JESSEN, C. (1997) Activity, blood temperature and brain temperature of free-ranging springbok. Journal of Comparative Physiology B 167, MURRAY, M. G., LEWIS, A. R. & COETZEE, A. M. (1981) An evaluation of capture techniques for research on impala populations. South African Journal of Wildlife Research 11, MUSHER, D. M., FAINSTEIN, V., YOUNG, E. J. & PRUETT, T. L. (1979) Fever patterns: their lack of clinical significance. Archives of Internal Medicine 1, VAN MIERT, A. S. J. P. A. M., VAN DUIN, C. T. M., VERHEIJDEN, J. H. M. & SCHOTMAN, A. J., H. (1982). Endotoxin-induced fever and associated haematological and blood biochemical changes in the goat: the effect of repeat administration and the influence of flurbiprofen. Research in Veterinary Science 33,

5 Legends Figure 1. Mean (±SD) daily body temperatures of 7 impalas (A G) over 50 autumn days. Figure 2. Hourly means of body temperature of one impala (C). Note the two febrile episodes. Figure 3. Mean ±SD of body temperature of one impala (C) on 11 febrile days (fever) and 41 non-febrile days (normal) and black globe temperature (mean, SD, minima, maxima) for the study period as a function of time of day. SD shown at one-hour intervals.

6 A B Body temperature ( C) C D E F G Days after surgery

7 41 Body temperature ( C) Days after surgery

8 41 Body temperature ( C) Fever Normal Black globe temperature ( C) Time of day