Effect of Hibernation on Course of Infection and Immune Response in Citellus tridecemlineatus Infected with Nippostrongylus brasiliensis

Abstract

The course of infection of Nippostrongylus brasiliensis in abnormal Citellus tridecemlineatus is prolonged, with comparatively few larvae developing to adults. Twenty-three animals placed in hibernation either soon after a single infection, or after mature worms were present, lost infection during hibernation period, with exception of one animal having a single adult worm. Antisera from ground squirrels receiving multiple infections were titrated using tanned-cell hemagglutination technique. Hibernating ground squirrels of this group showed a dramatic drop in antibody titer over 10-week hibernation period, with a major part of decrease occurring in first 4 weeks of hibernation. In one such group, median titer before hibernation was 1:1,280, after 4 weeks 1:320, and after 10 weeks hibernation median hemagglutination titer was 1:80. The nonhibernating controls showed little or no decrease in antibody over this same period. The serum antibody titer increased during 11 days following arousal from hibernation. The status of infection in hibernating animal and immune mechanisms operative during this physiologically interesting period have been subject of few investigations. There is, for example, little known concerning fate of infecting organism or of humoral and cellular responses of profound hibernator during this period. Although increased resistance to infection in hibernating animals has been reported by a number of workers (Kalabukhov, 1958; Kayser, 1961; Chute, 1964), there is no evidence that this is or is not related to a specific immune response. It has been suggested that three factors intervene in resistance of hibernators to certain infections: temperature, as slowing metabolic processes; low temperature, as more harmful to development of parasite than to host; seasonal modification of chemical composition of host (Kayser, 1961). General aspects of hibernating state of Citellus have been studied, and described by Kayser (1961). Chute (1961) found that 48 to 72 hr of hibernation completely protected golden hamsters, Cricetus auratus, infected with TrichiReceived for publication 24 June 1966. * Department of Microbiology, University of Chicago. t Division of Biological and Medical Research, Argonne National Laboratory, Argonne, Illinois. This research was supported in major part by Grant AI-00884 of Division of Research Grants of NIH, USPHS. nella spiralis larvae, if temperature reduction occurred during first 36 hr of infection. Later in infection, longer periods of hibernation were required to retard development of parasite. Dormice, Eliomys quercinus, in hibernation 3 to 4 days after a measured infection with T. spiralis, yielded a mean of 125 larvae; nonhibernating dormice yielded a mean of 1,920 larvae (Chute, 1960a). In bats infected with T. spiralis, larvae regularly develop to adult stage when bats are held at 30 to 34 C, but adults are seldom found if infected bats are held at 5, 23, or 26 C. In this experiment, the effect of lowered temperature is inhibitory rather than lethal, since majority of recovered worms, even after longest exposures to below temperatures, were alive and appeared normal (Chute and Covalt, 1960). None of these studies was conducted with prolonged hibernation as in present experiments. It has been shown that several species of parasitic helminths tend to be eliminated from their hibernating hosts over course of hibernation period (Simitch and Petrovitch, 1953, 1954). Chute (1960b) examined wild woodchucks, Marmota monax, which had just emerged from their hibernation burrows. In 50% of animals from four to 50 viable nematodes were found, while other animals had no intestinal worms. No reports have been found in literature with respect to antibody production or im-