Problems in the resuscitation of mammals from body temperatures below 0°C

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Abstract
Two hundred and seventy-five years have passed since Robert Boyle discovered that extreme cold prevented the putrefaction of animal tissues. He found that frogs and fish actually survived for short periods when the water surrounding them had frozen, but succumbed after several days’ encasement in ice. Boyle described these as promiscuous experiments. He also reported two modes of death in humans exposed to intense cold. Usually the extremities were gradually invaded by numbness which spread over the entire body so that the individual died insensibly. By contrast, horsemen wearing armour were seized violently around the waist by the cold. It caused them unspeakable abdominal pains and other torments which continued until the subjects died from exhaustion (Boyle 1683). Boyle’s observations have since been amply confirmed, and today it is well known that cold blooded animals do not survive complete freezing of all their body water (Scholander et al . 1953). Warm blooded animals, including the hibernators, are even more sensitive to chilling. Their breathing and heart beats stop at deep body temperatures well above freezing point. The animals do not recover spontaneously when rewarmed and were therefore assumed to be dead (Adolph 1951; Lyman & Chatfield 1955). A few years ago there seemed little possibility that mammals could be resuscitated from body temperatures below 0° C, and no prospect whatsoever that the work on storing isolated mammalian cells at very low temperatures would ever be applicable to the intact animal. There were, however, reports from Russia that bats and ground squirrels had been revived from sub-zero temperatures (Kalabuchov 1934; Murigin 1937). Then we heard that Dr Andjus of the University of Belgrade had shown that rats chilled till breathing and heart beats stopped were not necessarily dead (Andjus 1951). We developed his techniques at Mill Hill so that rats and mice can now be easily revived after an hour of suspended animation at body temperatures just above zero (Andjus & Smith 1955; Andjus & Lovelock 1955; Goldzveig & Smith 1956). Meanwhile Dr Parkes and Dr Lovelock and I had found that golden hamsters survived respiratory and cardiac arrest at deep body temperatures below 0° C (Smith, Lovelock & Parkes 1954). In some animals the deep body temperature fell as low as –5° C without the formation of ice in any of the tissues. These supercooled hamsters were readily resuscitated and recovered fully. Others froze progressively until, when the internal temperature had been below freezing point for 1 h, they were rigid and, when supported only by the neck and tail, would uphold an additional load equivalent to their own body weight of 100 g. Such animals were completely re-animated by warming the whole body with diathermy and simultaneously giving artificial respiration. The skin and superficial tissues contained large quantities of ice. Nevertheless, the extremities showed no signs of frostbite unless they had been forcibly bent when frozen (Smith 1954). The eyes, which were sometimes clouded for a short while after thawing, usually cleared completely, although occasionally lens opacities developed later. Ice crystals were also present in the brain and internal organs. Calorimetry suggested that as much as 50% of the body water had frozen in some animals which recovered fully. This work, which was reported last year (Smith 1956 a, b ; Lovelock & Smith 1956) has raised many problems. Some of these problems arose when we tried to repeat the experiments on larger mammals.

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