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A History of Influenza 573 Journal of Applied Microbiology 2001, 91, 572±579 A history of in¯uenza C.W. Potter Division of Molecular and Genetic Medicine, University of Shef®eld Medical School, Shef®eld, UK and Department of Pathology, Perak College of Medicine, Ipoh, Perak Darul Ridzuan, Malaysia 627/11/00: received 9 August 2000, revised 20 December 2000 and accepted 30 June 2001 1. Summary, 572 4.2. Pandemics before 1700, 574 2. Introduction, 572 4.3. Pandemics from 1700 to 1830, 574 3. In¯uenza epidemics, 572 4.4. Pandemics since 1830±3, 575 3.1. History, 572 4.4.1. Pandemic of 1918±20, 575 3.2. Antigenic drift, 573 4.4.2. Pandemic of 1957±8, 577 4. In¯uenza pandemics, 574 4.5. Features of pandemic in¯uenza, 578 4.1. History, 574 5. References, 578 disappear after a few weeks or months; these epidemics are 1. SUMMARY commonly heralded by an increase in hospital admissions of From the history of in¯uenza epidemics and pandemics, elderly patients with bronchopneumonia, particularly associ- which can be traced back with some accuracy for the past ated with Staphylococcus aureus, and an excess of deaths, three hundred years, and with less certainty before this mainly in the elderly and those suffering from chronic heart time, it is apparent that outbreaks occur somewhere in the and lung disease. From these observations outbreaks can be world in most years. Annual epidemics are due to antigenic identi®ed in the historical record without dif®culty, although drift; and pandemics, occurring at 10 to 50 years intervals, this identi®cation becomes less secure as one goes back are due to new virus subtypes resulting from virus further in time; and reference to in¯uenza can be found in reassortment. Nothing has been introduced during the past both scienti®c and lay publications since 1650. More 100 years to affect the recurrent pattern of epidemics and dramatically, pandemics of in¯uenza occur: these appear pandemics; and our future in the new century is clearly suddenly in a speci®c geographical area, spread throughout indicated by our past. This past experience is reviewed in the world infecting millions and cause a large numbers of the present paper. deaths. Evidence of pandemics is also present in the historical record which include 10 probable and three possible pandemics since AD 1590 (Potter 1998); and allusion to 2. INTRODUCTION earlier possible pandemics is suggested throughout history. Since 1932, when the in¯uenza virus was ®rst isolated in the With the above in mind, it is not surprising that in¯uenza laboratory, the history of this infection can be recorded and remained the most studied of viruses and virus diseases, con®rmed by laboratory diagnosis. In the two centuries before until the advent of HIV two decades ago. It has focused the this time, infections can be identi®ed by the known signs and interests of researchers, epidemiologists, physicians and the symptoms of disease and the explosive nature of outbreaks. pharmaceutical industry, whose studies are reported in a Thus, although sharing many symptoms with other respir- vast literature. Despite this, little has been done in the past atory infections, in¯uenza presents in addition as a sudden century to change the pattern of in¯uenza infections; and onset of three-day fever, with muscle pain and a degree of our future is clearly indicated by the past. prostration out of all proportion with the severity of other symptoms. Secondly, epidemics usually occur suddenly 3. INFLUENZA EPIDEMICS without warning, infecting a large percentage of people, and 3.1. History Correspondence to: C.W. Potter, Division of Molecular and Genetic Medicine, Epidemics of in¯uenza occur in most countries in some University of Shef®eld Medical School, Shef®eld, S10 2RX UK. years, and in some countries in most years: for many they ã 2001 The Society for Applied Microbiology A HISTORY OF INFLUENZA 573 are common annual events, unpredictable in time and The pattern of in¯uenza epidemics is shown diagram- severity. However, history indicates certain features which matically in Fig. 1. In a seven-year period, which can be any make in¯uenza epidemics more likely. Firstly, epidemics seven-year period during the past 50 years, epidemics of tend to occur in winter months when cold, crowding of in¯uenza have been recorded in all countries where people and higher humidities are a feature: indeed, in areas monitoring of infection has been studied. The diagram where continuous high humidity is a characteristic, infec- shows that during the winter months there is an excess of tions may occur throughout the year. Secondly, in more deaths in the years when in¯uenza is not recorded. In recent times epidemics are often ®rst seen in Eastern or epidemic years, 10% or more of a population may be Southern Hemisphere countries, and later spread to infected; 50% of infected persons will develop symptoms, Europe and North America in the winter months of these and an excess number of deaths will occur (Christie 1987). areas: seeding of infection may occur prior to epidemics, to The number of deaths is proportional to the number of be followed by epidemics when conditions are optimal. people infected, usually about 0á1%, and in¯uenza has been Thirdly, epidemics are more likely to occur when a variant described as an invariable disease caused by a variable virus. virus appears which shows antigenic changes from previous Most of the deaths occur among the elderly, such as those strains, and cross-reacting antibody, acquired by previous with chronic heart and lung disease or metabolic disorders. infection, is low in both percentage positive and titre. The Although vaccine against the prevalent virus strains is in¯uenza virus has radiating from the surface multiple produced each year, the use of this has not been wide: only a copies of two glycoproteins termed haemagglutinin (HA) proportion of the `at risk' group receive vaccine, and and neuraminidase (NA): it is antibody to these proteins although shown to protect 60±90% of the individuals which equates with immunity, and it is accumulating against infection, and a higher percentage against hospital- mutations in these glycoproteins, particularly the haemag- ization, immunization has never made an impact on the glutinin, which constitutes the virus variation termed course of an epidemic. antigenic drift. The monitoring of antigenic variation in the in¯uenza virus is a key factor in anticipating epidemics, 3.2. Antigenic drift and in vaccine design where for any year the prevalent virus strain(s) must be incorporated into the current The in¯uenza virus is subject to rapid mutation, particular vaccines. The responsibility for monitoring virus variation to the HA and NA glycoproteins against which immunity is rests with the World Health Organization who have directed, and serum antibody to the virus HA is the most commissioned over a hundred research laboratories in important factor in immunity (Potter and Oxford 1979). various parts of the world to monitor antigenic changes in The different in¯uenza viruses, marked A to E in Fig. 1, the infecting viruses and the incidence and spread of occur in different years and represent the progressive infection. accumulation of mutations with time in the virus HA, 8 7 6 3 10 5 × 4 3 Thousands 2 1 0 Year 1 2 3 4 5 6 7 Virus serotype A A B CDE Fig. 1 Diagram of in¯uenza epidemics over a 7-year period. r, Excess winter deaths in a non-in¯uenza year; e, number of in¯uenza cases; , number of excess deaths from in¯uenza; A±D; different virus variants ã 2001 The Society for Applied Microbiology, Journal of Applied Microbiology, 91, 572±579 574 C.W. POTTER termed antigenic drift, and this correlates with a step-wise by the latter is unchecked. This is a totally different decline in antibody acquired in earlier years to protect phenomenon to antigenic drift, and is termed antigenic against drifting virus. Thus, for the ®ve epidemic in¯uenza shift. viruses A±E occurring in the 7-year period shown in Fig. 1, Despite the reservations that must be imposed on the virus B exhibits the least and virus E the greatest number of reports of pandemic in¯uenza in the older literature, mutations compared to the original virus A. Antisera against numerous commentators have attempted to identify pan- homologous virus HA reacts strongly in Haemagglutination demics throughout the entire historic period: hence, reports Inhibition (HI) tests, less strongly with virus bearing a few of possible in¯uenza can be found in early Greek writings of mutational differences, and not at all where there are 412 BC to the more precise records of the present time numerous mutational differences (Table 1). The meaning of (Potter 1998). The ®rst report of an in¯uenza epidemic, this is that HI antibody acquired by previous infection is less where symptoms were probably in¯uenza, occurred in 1173±4 ef®cient in protecting against mutated virus, and, as (Hirsch 1883); several reports are from the 14th and 15th mutations accumulate, tends towards no protection. This century, and the ®rst convincing report was by Molineux pattern explains the repetition of in¯uenza epidemics, and (1694). Numerous references of in¯uenza epidemics were the pattern has been repeatedly observed since laboratory made for the 17th century in America and Europe. From the tests were available to record it: nothing has happened in the beginning of the 18th century, the quality and quantity of last century to alter this pattern, and all the indications are data increased and medical historians were drawn to that it will continue into the new century.
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