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Viruses and Myocarditis NORMAN R Postgrad Med J: first published as 10.1136/pgmj.48.566.750 on 1 December 1972. Downloaded from Postgraduate Medical Journal (December 1972) 48, 750-753. Viruses and myocarditis NORMAN R. GRIST THE observations described here were made in the inoculated into newborn mice. Nevertheless, signi- course of the work ofthe Regional Virus Laboratory, cant differences have been observed between the Glasgow, which provides a widely-used diagnostic associations of different types of echovirus with service. Our investigations of cardiac cases have cardiac and Bornholm disease suggesting that some concentrated particularly on enteroviruses, the main (notably types 6 and 19) may occasionally mimic group of viruses associated with acute myocarditis. Coxsackie viruses by causing illnesses of this type Within this group the Coxsackie viruses have (Bell & Grist, 1970b). received particular attention, their well-known Some problems of virological interpretation are causal role in acute carditis and Bornholm disease illustrated by an adult male with acute pericarditis being possibly related to their characteristic proper- whose sera on the eighth and seventeenth days of ties of causing acute myositis in experimentally illness showed diagnostic rising antibody titres to infected newborn mice. Virological diagnoses were Coxsackie virus B types 1, 3, 4, and 6, high un- based on isolation of virus from faeces, and/or a changing titres to type B2, and a low rise (< 16 : 16) four-fold or greater rise in neutralizing antibody to type B5. These cross-reactions are fairly commonProtected by copyright. titres in paired sera (rarely a four-fold fall in titre and pose problems in specific interpretation; in this with acceptable time relationships) or an unusually particular case the infecting virus was demonstrated high antibody titre without significant fluctuation. to be type B3 by isolation from faeces. One of our Unfortunately our first contact with a case is often echovirus 6 infections, a boy with acute pericarditis, too late in the course of infection for successful also showed a cross-reactive antibody response, in virus isolation or detection of rising antibody titre. this case to Coxsackie virus B3 (case 4: Bell & The clinical diagnoses were those of the clinicians Grist, 1970a). In earlier days when it was technically concerned, separating the categories of pericarditis too difficult to test for Coxsackie virus antibodies (without recorded features of myocarditis) and except on a very limited scale, one would have been myocarditis (including cases with features also of happy to make a diagnosis of infection with a pericarditis). particular virus on the basis of a significant rise in titre of antibodies to that Coxsackie virus type. Results Our wider range of routine testing has shown that As a general illustration of our findings, the the situation is not so simple, though monotypic analysis is presented of twenty-three cases found antibody responses are commoner in infants and during the period 1959-67 in which both clinical and young children. http://pmj.bmj.com/ virological findings gave acceptable evidence of an Questions of pathogenic mechanism are raised by enteroviral aetiology for acute cardiac disease. They a female infant in whom Coxsackie virus A9 infection show the usual picture in that Coxsackie viruses of was demonstrated by virus isolation and rising group B predominated (seventeen cases), these antibody titre (case 3: Grist, 1966). She had acute infections showing male excess of 12: 5, an older carditis with persisting failure and cardiomegaly, age distribution (twelve cases over 10 years old) and and died 4 months later showing pathological a Did the predominance of pericarditis over myocarditis features of severe interstitial myocarditis. on October 1, 2021 by guest. (10: 7). The other enterovirus infections (five virus infection persist in the myocardium, or did it Coxsackie virus A, one poliovirus) were mainly initiate some process which continued after the virus associated with acute myocarditis in female infants. had disappeared? Coxsackie viruses of group A are less often In 1966 my colleague Dr Eleanor J. Bell intro- implicated as causes of heart disease, though the duced a simple microneutralization test for antibodies greater technical difficulties of detecting most of to group B Coxsackie viruses (Bell & Grist, 1970a) them militate against successful diagnosis of these which revolutionized our approach by enabling us to infections. We have reviewed elsewhere the evidence accept for testing all specimens submitted from cases concerning this group of enteroviruses (Grist & with suspected cardiac or Bornholm disease; pre- Bell, 1969). Unlike Coxsackie viruses, echoviruses do viously we had been highly selective in accepting not typically cause myositis or other disease when cases for examination because of the difficulty and Postgrad Med J: first published as 10.1136/pgmj.48.566.750 on 1 December 1972. Downloaded from Viruses and myocarditis 751 expense of serological tests by earlier techniques. 1966-70. Although we cannot make a precise evalua- Over a period of 5 years we examined 308 patients tion of the role of enteroviruses from these figures, of a wide age range from infancy to old age, with a it seems clear that viruses of this group contributed at male predominance of 210 : 98. Based on the final least one-third of the cases classified as acute myo- diagnosis of the clinician concerned, with follow-up carditis and at least one-tenth of those classified as enquiry where required, each case was classified to acute pericarditis. my best ability within one of five categories: Because of the limited range of even our extended Bornholm disease (without cardiac features), acute battery of virological tests, and because many cases myocarditis (including peri-myocarditis; excluding come to attention too late to provide satisfactory cases of vascular origin), acute non-bacterial peri- virological evidence, our findings must underestimate carditis, other cardiac diseases, and non-cardiac the contribution of enteroviruses to this problem. diseases which had been suspected as being ofcardiac It may be noted that Levi & Proto (1971) estimated origin when the initial specimens were submitted for from their experience that Coxsackie viruses prob- examination. ably caused about 300 cases of carditis per year in In Table 1 these cases are tabulated according to the Italian province of Brescia (population about the virological findings: (a) those in whom virus one million). It is also interesting that a London isolation and/or four-fold or greater rising antibody epidemiologist, Professor Rose, drew attention a titre provided unequivocal evidence ofcurrent entero- few years ago to errors in classification of fatal peri- virus infection, (b) those with static antibody titres carditis, contributing to a persisting and even higher of 256 or more to one or more of the six group B reported mortality-rate for 'rheumatic fever' in Coxsackie viruses, i.e. titres so high as rarely to be adults in England and Wales despite the precipitous found except after recent infection with one of these decline in the figures for younger people (Rose, (or occasionally other) enteroviruses, (c) those with 1966). It appeared likely that a non-rheumatic group, Protected by copyright. borderline titres of 128 (sometimes 'significant' but probably 'acute pericarditis, not otherwise specified', often found as residual titres in the general popu- was being misclassified as 'rheumatic' by the lation) and (d) those with insignificant titres of 64 Registrar General. Could these fatal, adult cases of or less. acute non-specific pericarditis be of enteroviral It can be seen that cases with definite or probable origin? evidence of infection comprised (combining viro- There may be an analogy with paralytic polio- logical groups a and b) fifteen (72 %) of those classi- myelitis, another enteroviral infection with which fied as Bornholm disease, twenty-seven (48%) of our ecological relationship changed during the first those with acute myocarditis, thirteen (21 %) of those half of this century as a result of improved hygiene with acute pericarditis, thirteen (11 %) of those with and living conditions. It is believed that the delay of other cardiac diseases, and five (11%) of the non- primary infections until older and adult ages led to cardiac group. In effect, the first and last groups the consequent emergence of the new phenomenon provide positive and negative virological control of epidemic paralytic poliomyelitis involving these groups against which to evaluate the others. The older groups. Coxsackie viruses and other entero- descending order of virological 'positivity' from viruses spread in the same way as polioviruses, and Bornholm disease through myocarditis and peri- would be expected to share this ecological change http://pmj.bmj.com/ carditis to the 'other-cardiac' and non-cardiac groups whereby more primary infections and associated is not significantly changed by analysing the data by diseases are to be expected in older and adult age- age-groups and is therefore not due to different age- groups than a few decades ago. It is, therefore, structures of the diagnostic categories; the order is distinctly possible that enteroviral heart disease of also unchanged for each of the separate years adults is genuinely increasing in developed countries. TABLE 1. Results of tests for enterovirus infection in cases of suspected cardiac disease on October 1, 2021 by guest. Disease group Number of cases in each virological group* (a) definite (b) probable (c) borderline (d) negative Totals Bornholm disease 8 7 1 5 21 Acute myocarditis 10 17 7 22 56 Acute pericarditis 3 10 10 39 62 Other cardiac diseases 3 10 13 97 123 Non-cardiac diseases 1 4 4 37 46 Totals 25 48 35 200 308 * (a), Cases of virus isolation and/or rising antibody titre; (b), cases with antibody titre 256 or more to one or more group B Coxsackie viruses; (c), cases with highest antibody titre of 128 to any group B Coxsackie virus; (d), cases with antibody titres of64 or less to group B Coxsackie viruses.
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