smallpox eradication-the final battle' - from bmj and acp · smallpox began to recede,...

J. clin. Path., 1975, 28, 843-849

Smallpox eradication-the final battle'D. A. HENDERSON

World Health Organization, Geneva, Switzerland

If ever there was an appropriate time to pay homageto the remarkable and renowned Dr Jenner, this is it,for today we believe we could be only months awayfrom that day when we will detect and contain theworld's last case of smalJpox.

If a day and a place could be identified whichmight mark the nascent beginning of the globalcampaign, we might select a day in May 179 yearsago-and a place not far from Bristol-when DrEdward Jenner inoculated the boy James Phippswith matter from a cowpox lesion on the finger ofthe dairymaid Sarah Nelmes. The inoculation wassuccessful. Forty-eight days later Dr Jenner inocu-lated the boy with smallpox virus and showed thathe was protected. Despite the obvious difficulties oftravel and communication at that time, it was onlya few years before Jennerian vaccination began to beemployed in Europe, the Americas, Asia, andAfrica. This fact alone bears witness to the signifi-cance of the discovery.And it was Dr Edward Jenner himself who wrote

in 1801, 'it now becomes too manifest to admit ofcontroversy that the annihilation of the Smallpox,the most dreadful scourge of the human species,must be the result of this practice (of vaccine inocula-tion)'. Today, almost 175 years later, the end at lastappears to be in sight. Smallpox persists at present inonly three countries-India, Bangladesh, andEthiopia. But India, a vast country with more than550 million population, detected only seven casesduring the fourth week in April 1974-in fact, the lastknown indigenous case occurred on 20 April in a5-year-old girl vaccinated early in the incubationperiod of the disease. Her illness was so greatlymodified that in previous years it might never havebeen detected. Although this may not be the lastcase, the end is rapidly approaching. In Bangladesh,only 1200 of its 150 000 villages are now infected,and in Ethiopia, 114 villages. For both countriesMay is the usual peak of the smallpox season.In the heat of summer and during the monsoon rains,smallpox is transmitted from one person to anotherwith difficulty. If no measures whatsoever were taken,

'The First Jenner Memorial Lecture delivered at Bristol RoyalInfirmary on 1 May 1975

we would expect between May and October a de-crease of 80 % in the infected villages as well as in thenumber of cases. However, today the most intensivecampaign ever mounted to detect smallpox cases andto stop the spread of smallpox is now in progress.With the end in sight there could be no more

appropriate time to pay homage to the man whosework and writings made this possible.

I think that to appreciate the importance of DrJenner's vaccine to the world in which he lived andto subsequent generations one must appreciate theproblem of smallpox in eighteenth century Europebefore any form of protection was available.

Razell, in his treatise Population Changes inEighteenth Century England, documents vividly theimpact of smallpox in the early 1700s. From parishregisters, bills of mortality, and special smallpoxcensuses of the time he estimates conservatively thatnot less than 15 % of all children who were borneventually died of smallpox. The figure is almostcertainly conservative, for we know now that in un-vaccinated populations essentially all who are borneventually contract the disease, its behaviour beingsomewhat like that of measles in this regard. Sub-clinical infections among the unvaccinated are un-known and there is no treatment even today. Thus,the percentage who died was probably little differentfrom that observed today in Asia-fully 20 to 25 %.One of many contemporary observers commented:'When smallpox is epidemic, entire villages are de-populated, markets ruined and the face of distressspread over the whole country.' In areas of centralEurope at that time it was said that the newbornchild was not given a name until after he had ex-perienced smallpox and survived. Blindness was asignificant problem and smallpox was reported thento have been its chief cause in Europe. No otherdisease, past or present, has come close to wreakingsuch havoc.But by Jenner's time, smallpox in England had

become less of a problem than 50 years previously.The technique of deliberate inoculation of smallpoxvirus into the skin was introduced in the early 1700sand, after a prolonged period of controversy regard-ing its use, began to be widely applied in England inthe 1 760s. Among those artificially inoculated in this

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manner the proportion who died was far less thanamong those who acquired smallpox in the naturalmanner. The data are not precise, but, in contrast tosmallpox which killed one in five, artificial inocula-tion of the virus caused death in perhaps 1 in 100 oreven fewer. By 1776, Daniel Sutton alone claimedto have variolated 300 000 persons or 5 % of theestimated population of England and Wales. Amongthe more prosperous the procedure was relativelycommonplace. But it was also practised among thepoor. Many parish authorities commented that theyfound it less expensive to pay for the inoculation ofall within their parish than to pay the costs of isolat-ing and nursing the sick and burying the dead amongthe poor afflicted with smallpox. Edward Jennerhimself was inoculated (variolated) as a boy atWootton-under-Edge in 1756.

But variolation was hazardous-a person soinoculated can transmit the natural disease to others,and many outbreaks developed as a result of vario-lated persons coming in contact with susceptiblepersons.

Jenner's cowpox offered extraordinary advantages.Death following administration of cowpox was al-most unknown, and the cowpox virus could not bespread naturally from person to person as the small-pox virus could.The technique of Jennerian vaccination spread

world-wide. Initially the cowpox virus was trans-ferred from person to person. Matter was taken fromthe vesicle or pustule of one inoculated person andtransferred to the next, an approach called arm-to-arm vaccination. However, there were problems. Ifonly a few were being regularly vaccinated, failureto obtain a satisfactory take meant that freshmaterial must be obtained-specifically, anotherindividual in the early stages of development of avaccination reaction. In isolated areas-and therewere many-this was not easy. And sometimes whenvaccination was performed, syphilis and hepatitiswere simultaneously transferred.

Eventually, the technique of scarifying the entireflank of a cow came into practice, thus making avail-able a large quantity of cowpox virus for inocula-tion. An Indian colleague of mine, now in his 80s,recalls vividly the practice when he was a boy inIndia of leading from door to door an inoculatedcow and scraping off a bit of matter for inoculationat each house.As vaccination became increasingly common,

smallpox began to recede, especially in temperateclimates where preservation of vaccine was less of aproblem. And the refrigerator played a role. In fact,Dr James Leake attributes the marked reduction ofsmallpox in the Americas in the 1930s to the wide-spread introduction of the refrigerator.

The elimination of smallpox in Europe and NorthAmerica surprisingly did not occur until the 1940s.Primarily, I believe this resulted from the fortunateor unfortunate replacement of the virulent variolamajor strain of smallpox by variola minor (1 %death rate). This strain appears to have originated inSouth Africa but spread subsequently to theAmericas and to Europe about the turn of the cen-tury. In Europe and North America, interest in thecontrol and elimination of smallpox waned. Asrecently as 1927, the United Kingdom alone re-corded some 14 900 cases, but only 47 deaths; theUnited States reached its peak in incidence in 1930with some 49 000 cases and 173 deaths. For reasonsunknown, however, variola minor never extendedmuch beyond the Americas, Europe, and SouthAfrica. In the rest of the world variola major re-mained the dominant type.

In the 1940s, North America and Europe finallybecame free of smallpox as a result of more wide-spread vaccination and as a result of local effortsof varying intensity to stop outbreaks where theyoccurred. The tropical areas, although beset with thefar more malignant variola major, were at a greatdisadvantage as vaccines of satisfactory stabilitywere not available, health services were limited,and transport was a problem.

Jenner's hope for annihilation of the smallpoxremained frustrated until in 1950 the venerableproponent of the concept of disease eradication, DrFred Soper, propounded a programme for smallpoxeradication in the Americas. Smallpox transmissionwas interrupted in most countries. But Brazil, thelargest of the countries in South America, remaineda non-participant. Inertia set in, pious resolutionswere passed annually at the Pan America HealthOrganization's Annual Governing Council Meetingsbut little further progress was made.

Interest in smallpox eradication spread to theWorld Health Assembly where interminable dis-cussions about smallpox were conducted annually.But neither funds nor a coherent World HealthOrganization programme evolved. In 1958, theSoviet Union spearheaded a resolution to have theAssembly accept the principle of eradication as apolicy, and this was adopted, but most countrieswere much too preoccupied with a new scheme toeradicate malaria to do more than give a passing nodto a smallpox eradication programme. Between 1958and 1966, a number of countries undertook pro-grammes, and some in North Africa, Iran, and a fewother countries appeared to be successful-I say'appeared', because at that time not the slightesteffort was made to try to improve the reporting ofsmallpox cases. As we later discovered, somecountries reporting a nil incidence during this period

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had in fact simply eliminated smallpox by govern-ment decree. But finally, in 1966, delegates of severalcountries proposed to the Assembly that a specialbudget for smallpox eradication be approved tointensify activities. Some officials in the WorldHealth Organization were less than enthusiastic,having gradually come to an appreciation of thedifficulty, if not impossibility, of malaria eradica-tion and were hardly anxious to take on a seconderadication programme; a number of prominentdelegates were highly sceptical of the theoretical orpractical feasibility of such a project; some hadreservations in regard to the Organization's abilityto execute such an extensive programme. The resolu-tion passed, however, and under this less than auspi-cious cloud, the programme was launched inJanuary 1967 with the hope expressed that eradica-tion might be achieved in 10 years. As John Hunterhad once advised Jenner, the delegates to theAssembly were saying, 'But why think? Why not trythe experiment ?'.The intensified global programme of smallpox

eradication began in January 1967. At that time 42countries reported cases of smallpox and in 30 ofthese the disease was considered to be endemic(fig 1). In that year 131 000 cases were reported.However, subsequent surveys in Africa and Asia'showed that much less than 5 % of all cases werereported. Thus, in all, there occurred that year atleast 2 500 000 cases.

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The budget provided to the programme by theAssembly was less than US $3 000 000, a patheticallysmall sum considering the task set out, but fully 3 %of the Organization's total budget.The vaccine needs alone were estimated to be

between 200 and 250 million doses. If purchased, thecost for the vaccine would have been greater than theentire budget for smallpox which was provided toWHO. A number of laboratories in the endemicareas were producing freeze-dried vaccine but ex-amination of specimens showed that almost none ofthis vaccine met WHO standards in regard topotency, stability, and purity. Some samples ofvaccine, in fact, revealed no detectable virus what-soever. The quandary as to how to provide vaccineto the programme was approached by solicitingdonations of vaccine and by providing assistance inthe form of equipment and supplies, consultants, andstandard production manuals to laboratories inthe developing countries. During the first few yearsof the programme, the Soviet Union donated ap-proximately 140 million doses annually and theUnited States of America 40 million doses, butdonations were also received from almost 20 addi-tional countries. All vaccine which was donated wastested in one of two international reference centres,in Canada and in the Netherlands, and provisionwas made for testing samples of vaccine producedin other production laboratories throughout theworld. Vaccine production in the endemic areas

Fig. 1 Smallpox cases per 100 000 inhabitants, 1967



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gradually increased, and now some 80 Y. of thevaccine used in the programme is produced inlaboratories in the developing countries themselves.All of this vaccine is subjected to quality control bythe countries, and sample batches are regularlyassessed by the international reference centres.A second problem confronting us when the pro-

gramme began was in regard to vaccine administra-tion. The scratch technique was widely used through-out much of the world, but this technique produceda lower proportion of satisfactory takes than did themultiple pressure technique. Unhappily, the multiplepressure technique was very difficult to teach tovaccinators. An alternative and new technique, thejet injector, was initially introduced for use in pro-

grammes in South America and western and centralAfrica. This device proved most efficient in admini-stering vaccine to large numbers of people, and takerates were as high as those obtained with themultiple pressure technique. However, the jet in-jector, like any other mechanical apparatus, re-

quired maintenance, repair, and a continuing supplyof spare parts. In the developing countries, it was

difficult to assure adequate repair and maintenance.In 1968, however, Wyeth Laboratories in the UnitedStates developed a forked needle intended for mul-tiple pressure vaccination. This needle offered con-

siderable advantages in that only one-fourth as muchvaccine was required for vaccination as with theconventional techniques. Studies were undertaken byWHO to determine if the needle could be used formultiple puncture vaccine, a vaccination techniquein which the needle is held at right-angles to the skinsurface and a series of punctures are made. Studiesshowed that this technique of vaccination, evenwhenblood was drawn, produced as high a proportion oftakes as the multiple pressure technique. The needlescould be re-used many times and thus were a very

economical instrument. These were introduced latein 1968 and have been employed subsequentlythroughout the world.The problems of vaccine supply and vaccine ad-

ministration having been solved, attention was

directed to the strategy of the programme. For manyyears, the approach in virtually all countries en-

deavouring to eliminate smallpox was, simply, mass

vaccination. Little attention was paid to reporting,to the detection of cases, or to the containment ofoutbreaks. A WHO Expert Committee con-

sidered the question and had initially recommendedthat a target be established calling for vaccination of80 % of the population. However, experience showedthat even when 80 % were vaccinated, smallpox oftenpersisted. The only solution which the Committeeoffered was to suggest vaccination of 100 % of thepopulation, an objective which obviously is im-

possible to achieve. However, early in the course ofthe global campaign it was found in eastern Nigeriathat the detection and containment of smallpox out-breaks alone resulted rapidly in a cessation of small-pox transmission even in a population which waspoorly vaccinated overall. Similar observations weresoon made in other countries of Western Africa andsubsequently in Brazil and Indonesia. Because ofthis, the strategy of the campaign was shifted toemphasize that detection and containment of out-breaks was not of equal but of greater priority thanmass vaccination. Gradually this became a policywhich was followed throughout the endemiccountries. While mass vaccination was still con-ducted in most countries, it was definitely relegatedto a secondary, supporting role.

Just over eight years have passed since the pro-gramme began. As noted, the World Health As-sembly, when it decided to embark on the pro-gramme, expressed the hope that it might be com-pleted within 10 years. This goal we believe can andwill be achieved. When the programme began, fourareas were delineated-South America, Africa,mainland Asia, and Indonesia. It was consideredthat the amount of communication between any twoof these areas was sufficiently small that if smallpoxwere eliminated from one of the areas, it was notlikely to be re-introduced. In fact the experience ofthe past eight years has revealed no importation ofsmallpox from one of these areas into a second. Thefirst of the areas to become free of smallpox wasSouth America, the last case having been reportedfrom Brazil in April 1971. The second area,Indonesia, detected its last case in January 1972(fig 2). In each of these areas, just over two yearsafter the last case, international commissions wereconvened to determine whether or not the commis-sion was satisfied that smallpox had been eliminatedfrom the areas. In both cases, after a full review ofthe programmes and selected field visits, the com-missions agreed that smallpox had been eradicated.In all of Africa only one country (Ethiopia) nowremains endemic for smallpox, and on the mainlandof Asia only two countries (India and Bangladesh).The smallpox epidemics in India only nine

months ago were the subject of international head-lines. As of the end of April 1974 only 29 villageshad experienced one or more cases of smallpoxwithin the preceding six weeks and so were con-sidered infected-18 of these were due to importa-tions from Bangladesh. The last known case in Indiahad its onset on 20 April. Undoubtedly others willbe found, but they should be few. And now with a100 Rupee (about £5) reward to anyone reportinga previously unknown outbreak, cases are beingfound very quickly. In the process, literally thou-

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Smnallpox eradication-the final battk

U 1974 (Dec.) 1 9 7

Fig. 2 Smallpox endemic countries, 1967 and 1974

sands of cases of chickenpox, scabies, and other skinrashes are being checked daily. To double-check thesituation, an India-wide house by house search wasconducted. One hundred thousand workers visited110 000 000 households-and to make sure that thework was really done, a sample of 5 to 10% of allvillages was cross-checked by independent fieldteams. Only one previously unknown outbreak oftwo cases was discovered. Although importationsfrom Bangladesh will undoubtedly continue tooccur, the last indigenous case in India should occurin a matter of days to, at most, a few weeks.

In Ethiopia, despite civil strife and some of themost difficult geographical problems encounteredanywhere, the work goes on. Fortunately, Eritrea,where the fighting has been most intense, has beensmallpox-free for almost three years. In the remain-ing highly circumscribed infected areas, over 200Ethiopian sanitarians and health worker volunteersfrom Japan, Austria, and the USA are continuing towork. Government support is in fact better thanbefore, and since November 1973 two helicoptershave beeen working in support of the team.Periodically, the staff must now withdraw fromlocalized areas because of civil disorders but, so far,

Eradlration conflrmed

they have been able to return to these areas to work.Cases are almost 60 % below the number of a yearago, and now just over 100 villages are infected. Butthe outbreaks are small, and the villages which arecomparatively isolated now have higher levels ofimmunity. When the summer rains begin in Junemovement becomes difficult, smallpox spreads moreslowly, and experience shows that at low levels ofincidence, such as we now have, it frequently diesout spontaneously. Such, we hope, is the script thatEthiopia will follow.The great tragedy and setback for the programme

in 1974 occurred in Bangladesh, which at the end ofApril harboured more than 90% of the world'ssmallpox. As long ago as August 1970, smallpox hadbeen eliminated from Bangladesh-the first of theAsian countries to succeed since the intensified pro-gramme began. But 18 months later, in February1972, massive numbers of importations occurred asthousands of infected persons from a refugee campnear Calcutta returned after liberation, and smallpoxspread rapidly through the war-torn country. In thesummer of 1974 victory again appeared to be withingrasp when, suddently, the worst floods in more than20 years inundated the northern districts, the only

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areas at that time which were still endemic. Healthstaff were diverted for flood relief work, food distri-bution, and cholera control, and hundreds ofthousands of refugees began to move in search offood and employment, and smallpox began tospread. In January 1975 came the final blow whenalmost overnight the slums in Dacca, housing some400 000 persons, were cleared by bulldozers. Fullyhalf the population left for their home districts and,what were limited outbreaks in Dacca, becamedozens of outbreaks scattered across the southerndistrics. In February 1975, an emergency programmewas begun under Presidential directive; more than 60international staff were brought in but only in mid-April was the previously explosive spread stopped.A tough and difficult battle still lies ahead but witha bit of good luck and a great deal of hard work thelast case could be found before the end of August.But, even with less than optimal circumstances, it isdifficult to foresee smallpox being present afterDecember 1975.The essence of what has made the programme

what it is is, very simply, an imaginative anddedicated field staff, both national and international,who, given scope and encouragement to work outproblems according to local circumstances and sup-port in their efforts to do so, have responded withsome remarkable solutions to impossible problems.The primary strategy of the programme, as I

noted, is rapid detection of each outbreak and itscontainment. Since smallpox must spread from manto man in a continuing chain of infection, theobjective is to break each of the chains by isolatingthe case and vaccinating the contacts. In some areas,this is easier said than done. In more primitive areas,villagers resist vaccination. Bihar, India was aspecial problem last year. Persuasion and sometimespolice helped to overcome resistance. Highly effective,however, proved to be what was called the 'dawnraid'. A large vaccination team was formed and thisdescended on the sleeping villagers at 4.30 am.Vaccination was quickly completed and surprisinglythe team then enjoyed a convivial breakfast withvillage elders who explained that, by tradition, theywere supposed to resist vaccination but, oncedefeated, their tradition called for hospitality. How-ever, in one case, even this and all other efforts failedas the team was repeatedly driven off by spears andarrows. The epidemiologist decided to make onelast effort and approached the village one morningfor his fifth attempt in as many days. A long andfutile discussion ensued with the well-armed chiefand his villagers as to whose powers were greater-the chief's or the epidemiologist's. Finally, keepinghis eye on his watch, the epidemiologist raised hishand, a great silver bird miraculously appeared,

dived on the village, and dropped a large number ofpicture cards about smallpox and vaccination. Thechief capitulated, the village was vaccinated, and thelocal flying club received a letter of thanks.While such events are dramatic, I think we must

describe most of the work of both national andWHO staff as arduous and tedious, involving hoursand days of walking, of fording rivers, riding oncamels, mules or sometimes elephants, and bounc-ing over rough roads by bicycle, motorcycle orlandrover; of living under the most difficult of fieldconditions and surviving as best they can on the foodwhich is available. Not surprisingly, consultantsserving in India and Bangladesh customarily lose4-10 kg in weight over a three-month period ofservice. But morale and enthusiasm are high.A not atypical example is a young woman

physician whom I met on leaving India after threemonths of service, regretting bitterly that herinstitute would not permit her to stay a further sixweeks. She had been posted in a small district capitalwhere she lived in a village house, subsisting onchapattis, vegetables, eggs, and an occasionalchicken, and returning to Lucknow two days eachmonth for a state-level planning and coordinationmeeting. The work was done by bicycle, bullockcart, on foot, and, on two occasions, by rentedelephant. But the classic story of transport problemsstems from Ethiopia and the report of two cases ofsmallpox from an area near the Sudan borderthought to be free of smallpox. The message had beencarried from a small mission station by a runner whotravelled for two days to the nearest police radio. Atthe time the only airstrip anywhere near the area wasunder water. The only way to check the report wason foot-315 miles. The surveillance officer took 15days to reach the area-both cases were chickenpox.The examples are many: an Afghan surveillance

team who travelled for four days on foot and horse-back through metre-deep snow to reach an outbreak;an Indian District Health Officer and his team whowere captured by tribal villagers and saved at thelast minute from execution by burning, but whoreturned to control the outbreak; a Pakistan surveil-lance agent captured and held for ransom by insur-gents, but who on return refused transfer from hisassigned area.Although one might assume that classroom train-

ing of the national staff involved in the programmewould assure a satisfactory result with much lessstrain, it has become abundantly clear to all of usthat this is at best only a partial answer. Successfulexecution of the programme consists of perhaps 10 %technical skill and 90% organization and leadership.But effective leadership to solve the problems facedby field workers cannot be supplied by an army of

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physicians and senior supervisors who never leavetheir desks. Regrettably, these types are all tooplentiful throughout the world. A classic illustrationof the armchair disease came to light in India when adistinguished Indian professor of social and preven-tive medicine, who volunteered for three months'service, admitted that never in his life had he visitedan Indian village. And perhaps the disease is not souncommon in WHO, for in 1967, when we under-took our first full assessment of a programme, Iasked our Regional Office if they could provide therequisite sleeping bags and mosquito nets. The re-quest was met with astonishment as I was told thatconsultants never required such things as they neverventured that far into the field.With senior national as well as WHO smallpox

staff moving actively in the field, many of theirhitherto desk-bound counterparts have frequentlyresponded as well, and the effect has been surprising-lower level staff have worked harder and withgreater enthusiasm and, in the process, they havefound better and more effective methods for copingwith the problems.

It is the field staff who have shaped the strategyand tactics of the eradication programme. New con-cepts and alternate approaches to problems are con-stantly being experimented with. I can say withoutqualification that no two national eradication pro-grammes are identical and, further, that in any onecountry the programme of today is considerablymodified from that of a year ago, or even six monthsago. More significant is the fact that almost everynew development in the programme has stemmedfrom field staff.

But at what cost has all this been done? In termsof international resources, if one adds together allthat has been provided through WHO's regularbudget plus all of the funds provided to WHO's

Special Account for Smallpox Eradication, plus allthat has been given through bilateral donations, thetotal over 8j years is $57 million, almost preciselythe cost of one large C-5 transport plane. The burdenof expenditure has been borne by the endemiccountries themselves, a total which is several timesthis figure. But, with few exceptions, the expenditureby the countries has been little more than what theywere already spending to control smallpox. In otherwords, WHO and its member countries, with only avery modest additional input in resources, havetransformed a neverending control programme to asuccessful eradication programme.For all of us it has been a revelation in so many

countries to find at the periphery such an array ofunproductive health staff and facilities. It has been arevelation to discover how effectively they may bemobilized with a comparatively small input involv-ing leadership in the field and definition of a series ofactivities with defined objectives and a modestelement of management. Other health programmes,especially those involving immunization, but othersas well, could, I believe, be similarly transformed.For all of us in the smallpox eradication pro-

gramme a tough, difficult final battle remains, butthe end is in sight. At the same time, for WHO Ibelieve there are new horizons opening as we studythe lessons of this programme and apply these toother areas.

Jennerian vaccination antedated the developmentof any other vaccine by fully 80 years, but theprinciple employed was the inspiration for LouisPasteur in his development of the next vaccines. Atthis time we do not have the technology to permitthe eradication of another disease, but hopefully theprogramme of smallpox eradication will serve topioneer more effective programmes in public healthandeventuallytheeradication of other diseases aswell.

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smallpox eradication-the final battle' - from bmj and acp · smallpox began to recede,...

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