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Studies on Pathophysiology of Sudden Cardiac Death-Type Strongyloidosis Using an Ovine Model

中村, 義男 筑波大学 DOI:10.15068/0002001044

2021.08.17

概要

Strongyloides papillosus is a nematode parasite of ruminant animals and rabbits that is distributed worldwide. Infective larvae of the parasite invade a host by skin penetration to migrate up to the larynx, and mature into parasitic females in the small intestine to lay eggs in parthenogenesis. Beginning in 1978 in Japan, outbreaks of the fatal disease, which would later be identified as sudden cardiac death-type strongyloidosis, were reported with no premonitory signs on farms that raised calves in small pens using sawdust as litter. Field surveys and experimental infections disclosed that heavy infection with S. papillosus causes the disease, in which calves develop continuous sinus tachycardia and final sudden cardiac arrest by ventricular fibrillation (VF).

I considered that two questions are of primary importance for further studies to elucidate the disease mechanism: which developmental stage of the parasite is responsible for the disease; and whether the cardiac disorders are based on reversible and curable change. The research target can be decided by answering the first question. Solving the second question may clarify certain characteristics of the disease, such as whether the disturbance of cardiac regulation is functional or organic lesion-based. The present studies were aimed at solving these questions.

Rabbits never show cardiac disorders following heavy infection with S. papillosus, and therefore are not useful as an animal model. However, if lambs could be used as a model animal, experimental trials would become easier compared to those using calves due to the body size of animals. In Chapter 1, as a preliminary study, the course of heavy strongyloidosis in lambs was analyzed to determine whether they could serve as an animal model of this disease. Lambs were percutaneously infected with 1,000-32,000 infective larvae of S. papillosus per kg body weight. The animals given 3,200 or more larvae/kg developed sudden death on days 11-20 after infection, having high fecal egg output and intestinal worm burdens. Electrocardiogram (ECG) monitoring on several animals revealed a series of arrhythmias consisting of continuous sinus tachycardia and final VF in the intestinal phase of infection. The animals appeared normal with no diarrhea or other clinical signs until the time of death, with the exception that some animals exhibited a loss of body weight. Throughout the course of infection, there was no discernible pattern of elevated endotoxin levels or inflammatory cytokine induction common to the animals that ultimately died. These results indicated that lambs follow almost the same pathophysiological disease course including the development of cardiac disorders as calves after infection, and can thus serve as a model for the study of sudden cardiac deathtype strongyloidosis. The results also suggested that the disease is not associated with endotoxic shock or a shock-like state that is usually induced by inflammatory cytokines.

Parasitic females would appear to be the cause of the disease, since animals developed the cardiac disorders in the intestinal phase of infection. However, the possibility of a few larvae migrating into the heart tissue cannot be excluded as a cause of cardiac dysfunction, since a portion of larvae pass through the lungs during their migration. The study in Chapter 2 was thus aimed at elucidating the responsibility of parasitic females for the disease. For this purpose, I focused on two specific characteristics of parasitic females, namely, they never migrate back from the intestines and their eggs never hatch into larvae inside the intestines. Parasitic females were collected from infected donor rabbits. Recipient lambs were intraduodenally inoculated with sufficient numbers of live and homogenized worms. These animals never had larvae in their bodies. The lambs inoculated with live worms developed continuous sinus tachycardia shortly after inoculation and died of sudden cardiac arrest by VF on days 2-9 after inoculation, having high fecal egg output and intestinal worm burdens. The animals appeared normal until the onset of VF. The course of disease was identical to that observed in the intestinal phase of percutaneous larval infection. Inoculation with homogenized worms did not produce fatal arrhythmias. These results indicated that active parasitic females in the small intestine are responsible for sudden cardiac death-type strongyloidosis regardless of the presence or absence of migratory larvae.

Most reversible and irreversible arrhythmias are likely to result from disorders without and with pathological lesions of the heart, respectively. The study in Chapter 3 was aimed at elucidating the reversibility of arrhythmias in heavy strongyloidosis. For these experiments, I focused on an anthelmintic treatment that is effective against parasitic females during the middle stage of infection. Lambs were percutaneously infected with a lethal dose of infective larvae, and received ivermectin or remained untreated upon developing continuous sinus tachycardia accompanied by prolonged PQ interval (the portion of ECG between the P wave and the QRS complex). In the treated animals, the combined arrhythmia disappeared within 39 h after treatment and thereafter no arrhythmias were detected. Fecal egg output became negative within 61 h after treatment. Untreated control animals developed sudden cardiac death. These results indicated that the supraventricular arrhythmias generated in heavy strongyloidosis are reversible and curable following worm elimination. The functional disturbance of the heart with few or no lesions is more likely to cause the arrhythmias in the disease rather than the organic disorders with lesions.

To date, it has never been demonstrated that any gastrointestinal parasite other than S. papillosus induces fatal cardiac dysfunction in animals or humans having no accompanying diseases. The present studies contribute new and unexpected knowledge to the field of parasitology. Parasitic females of S. papillosus may excrete or secrete a cardioactive substance capable of modulating cardiac rhythms in the disease. The generation of sinus tachycardia accompanied by prolonged PQ interval can hardly be accounted for by a simple unbalance of the autonomic nervous system, since the two arrhythmias are physiologically derived from the opposite phase of the innervation. One possible hypothesis is that parasitic females elicit enhanced automaticity in the atria, which is known to produce both increased heart rate and prolonged PQ interval, via a route independent of the autonomic nervous system. Such abnormal automaticity would lead to an alteration in the pacing rate of the sinoatrial node and disturbance of conduction. The derangement would induce disorganized excitations in the ventricles, ultimately resulting in VF.

The present studies provided clear scientific evidence that worm elimination is effective for recovery from the cardiac dysfunction in sudden cardiac death-type strongyloidosis. The occurrence of sudden cardiac death can be prevented by anthelmintic treatment of animals having high fecal egg output. The results of the present studies make a major contribution to solving an important problem in the field of livestock husbandry in Japan. Further studies are required to clarify the factors associated with the mechanism underlying the cardiac disorders induced by S. papillosus. The ovine model is expected to facilitate such studies.

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