Cohen Malar J (2019) 18:323 https://doi.org/10.1186/s12936-019-2956-y Malaria Journal

REVIEW Open Access “Remarkable solutions to impossible problems”: lessons for malaria from the eradication of smallpox Justin M. Cohen*

Abstract Background: Malaria elimination and eventual eradication will require internationally coordinated approaches; sustained engagement from politicians, communities, and funders; efcient organizational structures; innovation and new tools; and well-managed programmes. As governments and the global malaria community seek to achieve these goals, their eforts should be informed by the substantial past experiences of other disease elimination and eradication programmes, including that of the only successful eradication programme of a human pathogen to date: smallpox. Methods: A review of smallpox literature was conducted to evaluate how the smallpox programme addressed seven challenges that will likely confront malaria eradication eforts, including fostering international support for the eradication undertaking, coordinating programmes and facilitating research across the world’s endemic countries, securing sufcient funding, building domestic support for malaria programmes nationally, ensuring strong commu- nity support, identifying the most efective programmatic strategies, and managing national elimination programmes efciently. Results: Review of 118 publications describing how smallpox programmes overcame these challenges suggests eradication may succeed as a collection of individual country programmes each deriving local solutions to local problems, yet with an important role for the World Health Organization and other international entities to facilitate and coordinate these eforts and encourage new innovations. Publications describing the smallpox experience sug- gest the importance of avoiding burdensome bureaucracy while employing fexible, problem-solving staf with both technical and operational backgrounds to overcome numerous unforeseen challenges. Smallpox’s hybrid strategy of leveraging basic health services while maintaining certain separate functions to ensure visibility, clear targets, and strong management, aligns with current malaria approaches. Smallpox eradication succeeded by employing data-driven strategies that targeted resources to the places where they were most needed rather than attempting to achieve mass coverage everywhere, a potentially useful lesson for malaria programmes seeking universal coverage with available tools. Finally, lessons from smallpox programmes suggest strong engagement with the private sector and afected communities can help increase the sustainability and reach of today’s malaria programmes. Conclusions: It remains unclear whether malaria eradication is feasible, but neither was it clear whether smallpox eradication was feasible until it was achieved. To increase chances of success, malaria programmes should seek to strengthen programme management, measurement, and operations, while building fexible means of sharing experi- ences, tools, and fnancing internationally. Keywords: Malaria, Eradication, Elimination, Smallpox, History

*Correspondence: [email protected] Clinton Health Access Initiative, 383 Dorchester Ave, Suite 400, Boston, MA 02127, USA

© The Author(s) 2019. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creat​iveco​mmons​.org/licen​ses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/ publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Cohen Malar J (2019) 18:323 Page 2 of 16

Background endemic countries, to fnance a long-term enterprise, and Te World Health Organization (WHO) has called for to ensure countries act in concert to minimize importa- the eradication of malaria since 1955 [1], when the Global tion from neighbors means the malaria community will Malaria Eradication Programme urged countries to seek be “forced to navigate complex administrative and soci- to interrupt transmission through an efort involving etal terrains, where knowledge gleaned from scientifc campaigns of indoor spraying of insecticide on a “total and medical journals can only be partially useful” [9], but coverage basis” [2]. Although the 1969 World Health where past experiences managing similar programmes Assembly “re-examined” that goal [3], it was never of- may prove valuable. cially abandoned. Today, the WHO’s Global Technical Strategy [4] calls for gradual progress towards eventual Methods global eradication, defned as the “permanent reduction To investigate potential lessons for malaria in the small- to zero of the worldwide incidence of infection caused by pox literature, PubMed was searched on 7 Feb 2017 human malaria parasites as a result of deliberate activi- for “smallpox” and “eradication” in the title or abstract ties” [5]. To reach this goal, the WHO targets having at of publications. Seven hundred results were returned. least ten new countries achieve malaria elimination— Abstracts were evaluated to assess whether the publi- defned as the “interruption of local transmission (reduc- cation would provide information about how smallpox tion to zero incidence of indigenous cases) of a specifed programmes overcame seven challenges that malaria malaria parasite in a defned geographical area as a result eradication will likely face, selected in collaboration with of deliberate activities” [5]—by 2020, ten more by 2025, members of the WHO’s Strategic Advisory Group on and another 15 by 2030. Achieving these targets with the Malaria Eradication. Tese challenges included the inter- imperfect, impermanent tools available to malaria elimi- national issues of (1) how support for the undertaking nation programmes will require internationally coor- was fostered internationally, (2) how the campaign was dinated approaches, high degrees of engagement from internationally coordinated, and (3) how it was fnanced. politicians and communities, efcient organizational At a national level, issues included (4) how support was structures, and well-managed programmes. As govern- fostered nationally and (5) at community level, (6) what ments and the global malaria community seek to over- programmatic strategies were found to be most success- come the associated challenges, their eforts should be ful, and (7) how national elimination programmes were informed by the substantial past experiences of other dis- most efectively structured and managed. Additional ref- ease elimination and eradication programmes. erences cited in the PubMed results that seemed relevant, Smallpox is the only infectious disease of humans to including several books, were also included in review. have been eradicated globally. Te Intensifed Small- Abstracts of all results were examined for relevance to pox Eradication Programme of 1966–1977 was a global one of these seven areas of interest. Te full texts of all efort to conduct mass vaccination in combination with relevant publications were read by the author, who noted surveillance to detect cases and control outbreaks [6]. and collated any information provided on how smallpox Dr. Donald A. Henderson, the director of the WHO-led programmes addressed these diverse challenges. Te campaign, recounted that smallpox eradication “proved potential ramifcations or lessons for malaria eradication to be infnitely more difcult than I or anyone else had were evaluated by the author based on his experience imagined it would be” [7], and believed that the success providing operational, technical, and fnancial support to against smallpox could not be replicated against malaria numerous malaria elimination programmes over the past with the currently available tools [8]. decade in his role as the director of a malaria programme Given that malaria eradication remains the stated at a non-governmental organization. global goal, however, it is worth examining the smallpox eradication experience to understand what lessons can Results be learned about how to approach such an ambitious Of 700 results returned by the PubMed search, 118 pub- undertaking. Drawing lessons for malaria from the small- lications were selected for full-text review. Tese docu- pox programme is inherently challenging due to the dif- ments, which ranged in publication year from 1959 ferent disease dynamics and interventions (i.e., a highly to 2015, included contemporary accounts of the cam- protective, long-lasting vaccine for smallpox versus paign from specifc countries, assessments of global imperfect anti-vector and parasite tools for malaria that programme process, and refections on the eradication must be repeatedly re-distributed). Yet it is plausible to accomplishment by its participants in both journal article expect there are also political, operational, fnancial, and and book form, along with several reviews of the small- administrative commonalities to any global undertaking pox experience. A number of themes emerge from the lit- of this nature. Te need to coordinate stakeholders across erature across the seven areas of interest (Table 1). Cohen Malar J (2019) 18:323 Page 3 of 16 - tifcation of malaria champions asm and support implementation ment and measurement to increase and demonstrate its impact and demonstrate increase to ment and measurement keep to malariachampions, a priority as visibility even wanes countries as they arise bottlenecks across address supporting countries to iteratively improve programmes based on programmes supporting improve countries iteratively to quality data and analysis commodities like bed-nets best practices uptakeencouraging of proven capacityand operational/logistical fexibility and nimbleness ensure nisms to for visibility for Build external national support including iden - outside government, private sector partnershipsCreate maintain elimination enthusi - to Ensure optimal allocation of available funding and strong manage funding and strong optimal allocation of available Ensure Continue advocacy business and political Continue including through eforts, Increase availability of small but fexible funding that can be used to Maintain malaria global quality products for assurance structures while and development, globally in research investing Continue building local manufacturingConsider high volume capacity for encourage participationUse funding to Encourage countries try while to strategies context-appropriate countries build both technical with embedded advisors to Provide mecha - coordination Reduce bureaucracy in global and regional Need to maintain public relations and advocacy for campaign and advocacy maintain public relations for Need to Malaria Report trackerWorld and opportunityMaintain as progress hold political leadership accountable to Use global forums Lessons for malaria Lessons pions tive management schemes to achieve greater impact greater achieve management schemes to tive without substantial budget increases would reduce prevention costs in high-resource costs in high-resource prevention reduce would countries nisms testing the encouraged by of new strategies, and testing tools WHO tries pation try help build efcient programmes to programmes best practices following diferent simultaneously across approaches many test contexts sociocultural and epidemiological - institutional rules and leverag circumventing respond, possible ing backchannels wherever Identifcation of politically-connected domestic cham - Engagement of private sector actors - efec more to existing domestic resources Transitioning Agreement that eliminating in low resource countries resource that eliminating in low Agreement mecha - funding accounts and reimbursement Flexible Clear quality standards and reference labs for quality labs for and reference Clear quality standards of new including development innovation, Decentralized manufacturingLocal of vaccine in large-volume coun - encourage country to Small fnancial incentives partici - support and logistical staf embedded in coun - Technical Embrace independent actions countries to by as a way quickly hands to fexibility their own WHO staf took into Backing major global superpowers from well-connected central leader Strong, Health Assembly World national leadership at Engaging and challenges report released on progress Widely Smallpox success factors success Smallpox limited support,limited particularly as burden diminishes or when less virulent strains common were loss of prior political support country waned with decreasing case counts waned with decreasing staf and bottlenecks in paying created transport costs start of campaign and research innovation large-volume countries connected countries, between regionally impactand limited of international declara - tions views on and disparate of programme, between diferent persisted approaches WHO of the levels Competition with other disease prioritiesCompetition often led to Government leadership turnover Resources were being used inefciently in were Resources Interest in allocating funds to the programme the programme in allocating funds to Interest or insufcient funds processes Bureaucratic Low quality products with stability issues at Low ongoing challenges necessitated Unforeseen Insufcient vaccine to donate donor funds to or synchronization Lack of coordination bureaucracy speed and agility limited WHO’s Lack of global political endorsement and resources profle Limited Smallpox challenges Smallpox Summary of challenges by the smallpox faced factors described in the published eradication, that enabled literature to overcome them, programmes 1 nation National support Financing International- coordi International support Table eradication lessons for malaria and potential Theme Cohen Malar J (2019) 18:323 Page 4 of 16 - technical areas of malaria and public health areas technical managers of strong retention ongoing surveillance functionality while maintaining vertical and cost-efectiveness, community mobilization, and fundraising, facilitate elements to political buy-in rather than only measuringcome metrics, the number distributed sible working in endemic regions in person with local programmes they are most necessary, rather than only evaluating the number of most necessary, they are them people receiving when they will be most impactfulfed at the time of year approaches encourage countries adopt proven to high quality data ensure otherwise of transmission that may identify areas to lance designed be missed build support populations afected and engagement from increase to community control) health, vector illness, (childhood participation nity buy-in and cooperation Hire fexible problem solving staf with backgrounds not limited to to not limited solving staf with backgrounds Hire fexible problem leaders and aim for programme management training to Provide Leverage basic health systems for routine case management and routine for basic health systems Leverage improve to malaria the health system Integrate elimination into in out specifc reductions to related measurable targets Set clear, Encourage managers from all levels to spend as much time pos - to all levels Encourage managers from Focus on targeting prevention and treatment to the places where the places where to and treatment prevention on targeting Focus Understand malaria- interventions seasonality intensi and ensure are and operational guidelines technical update to Continue and supervision feedback all reporting routine to points to Provide reporting health facilities with active surveil routine from Augment - Conduct community research to understand how to most efectively most efectively to understand how to Conduct community research initiatives malaria health system Tie elimination eforts larger to commu - ensure village leaders to to at local level Increase outreach Lessons for malaria Lessons - gramming facilitated identifcation of local solutions facilitated gramming serve to work hired as catalysts and hard imagination, rather than controllers execution ensure to integrated with basic health systems, allowing allowing with basic health systems, integrated horizontal leverage to programmes smallpox-specifc surveillance for systems and support with prioritization and of qualityresults, measurement quantity verifcation over encouraged to frequently travel into the feld to review review the feld to into travel frequently encouraged to activities problems and work with feld staf in resolving focused vaccination in the areas where smallpox was smallpox where vaccination in the areas focused observed the weakest point of the transmis - seasonal incidence, sion cycle evidence accrued of what worked best good participationensure case detection activities surveillance of both strengths leverage to eforts with other community initiatives (neonatal care, eforts with other community (neonatal care, initiatives census taking, market days) engagement with community leaders engagement and enthusiasm and education eforts Problem-solver staf with reputations for adaptability, adaptability, for staf with reputations Problem-solver managers and operations ofcers strong Hire and retain Vertically managed and measured programmes were were programmes Vertically managed and measured on a focus and measurable goals drove specifc, Clear, pro Experimental of formalized learning and avoidance WHO, national, and state or provincial supervisory or provincial and state national, staf WHO, Shift from national mass vaccination to surveillance national mass vaccination to Shift from and during fnding intensifed the periodCase of lowest WHO as by and disseminated Global guidance updated all reporting to points to feedback up and routine Follow Developed a network of agents who conducted active reporting both health facilities and activeIntegrated from Engaged or combined mobilization and awareness Engaged or combined mobilization and awareness Gained proactive community acceptance through keep in the endgame to up Used fnancial incentives private sector partnershipsCreated extend to vaccination Discouraged compulsory vaccination Smallpox success factors success Smallpox - - - achieve necessaryachieve surveillance and vacci - but communities, of at-risk nation coverage inefciency and unsustainability of a fully vertical program such as the in terms of activity, progress numbers of vaccinations performed, rather achieved than the result no set checklist vacci - how of methods for and case fnding should nation campaigns be carried out was possible gramme areas to observe to areas problems gramme loads and insufcient travel into pro into loads and insufcient travel populations despite high overall vaccina - high overall populations despite tion rates ent statistical units and other health system of the entities not within the control programme smallpox ceived adverse events adverse ceived munity participation community from reactions negative Supervision work was insufcient due to Limitations of existing health system to to Limitations of existing health system assess to tended National programmes Diversity of contexts and challenges meant Transmission persisted in unvaccinated in unvaccinated persisted Transmission Disease reporting depended on independ - Mistrust of vaccination due to real or per Mistrust real of vaccination due to com - reduced have may Single disease focus Compulsory elicited vaccination approaches Smallpox challenges Smallpox (continued) structure and structure management strategy National programme National programme Programmatic Programmatic Community support 1 Table Theme Cohen Malar J (2019) 18:323 Page 5 of 16

International support for the eradication programme International coordination of the eradication programme Henderson declared, “For a global programme against International coordination was considered important a disease to be undertaken, universal political commit- to avoid “ping-pong smallpox” [25] in which infections ment is necessary” [10]. In the case of malaria, support would be continually reintroduced from country to coun- for fghting the disease seems strong, with malaria con- try. A 1960 Inter-Regional Smallpox Conference organ- trol activities frequently cited as one of the “best buys in ized by the WHO reported that since “the eradication of global health” [11–13]. However, the pursuit of malaria smallpox cannot be considered on the basis of individual eradication is more controversial, and whether it repre- territories,” the Conference “therefore urges the health sents a feasible or even a worthwhile goal has been fre- administrations of all countries in endemic regions to quently debated [14–21]. synchronize their eradication campaigns” [26]. While this Support for the smallpox eradication programme declaration was sufcient to spur action in some coun- was similarly far from universal. Te failures of prior tries [27], others, including Brazil—the country with the eradication or regional elimination eforts including largest burden in the Americas—and many African coun- hookworm, malaria, yellow fever, and yaws increased tries [28], declined to initiate vaccination programmes, skepticism, as did a perception that vertical eradication compromising the possibility of regional success [29]. campaigns detracted from provision of basic health ser- Provision of dedicated smallpox funding in 1967 proved vices [7]. Although the WHO was tasked with coordinat- critical to allow the WHO to incentivize countries to ing the efort from Geneva, its diverse departments and scale up their national programmes [10], even when com- regional ofces were not uniformly behind the efort, in mitted funding was small [29]. Te provision of donor part because “their ofcials competed with each other funding for malaria—increasing from about $170 mil- for fnite fnancial resources and administrative infu- lion in 2000 to $2.5 billion in 2016 [30]—has likely been ence” [22]. Te Director-General of WHO reportedly similarly important to convince countries to prioritize had so little faith in the programme that he explained to malaria programming. Henderson—a secondee from the United States’ Centers Despite the international push from the WHO, the for Disease Control and Prevention—that “he wanted an smallpox eradication efort would always remain a collec- American as the director so that when the programme tion of individual national programmes, each attempting failed, as he was sure it would, the Americans, not the to solve their own problems through their own systems WHO, would be seen as responsible” [23]. and in their own ways [28], rather than a top-down, cen- Te smallpox programme survived at the WHO in part trally managed global undertaking. Dr. William Foege, an because of strong backing from both the United States American epidemiologist who helped design the surveil- and the Soviet Union [23], the major powers of the era. lance-driven vaccination strategy that likely enabled suc- Henderson himself was seen as a trustworthy leader by cess in countries including Nigeria and India [31], called both rival countries despite ongoing Cold War hostili- it “20 programmes trying diferent things to more quickly ties because of his strong track record as an “honest and discover truth” [32]. a good scientist” whose “only objective [was] to eradi- “Te campaign to eradicate smallpox worldwide is cate smallpox” [23]. Still, maintaining smallpox’s profle often described in simplistic terms… Te picture pre- within the WHO and encouraging countries to contrib- sented is of a unitary programme of action, where the ute funding and resources was an ongoing challenge. many cogs in the wheel apparently worked in almost per- Henderson used the annual meeting of the WHO assem- fect harmony, causing orders from the top of an admin- bly as an important opportunity to keep eradication on istrative pyramid to be unquestioningly implemented the minds of health ministers [8] and tried to maintain in localities across the globe… the organized drive to smallpox’s public profle by widely releasing surveillance expunge smallpox was a much more complicated and reports with summaries of progress and problems. Hen- disjointed entity” [33]. derson later suggested that a mistake he made was not Current malaria guidance embraces an aligned belief adding dedicated staf to his team focused on public rela- that “adapting and tailoring interventions” to the local tions and donor advocacy [10]. Malaria today appears to context will be important for elimination success [34]. have a more visible profle internationally than smallpox While encouraging local solutions, the WHO and other did, in part due to similar communications eforts, such international entities including the United States’ Centers as the annual World Malaria Report which provides for Disease Control and Prevention [35] added substan- opportunities for visibility and public engagement [24]. tial value to these independent programmes, including: Cohen Malar J (2019) 18:323 Page 6 of 16

Sharing best practices across countries Provision of technical and operational support WHO’s guidance to countries changed substantially Te WHO’s smallpox eradication unit provided national over the course of the programme as understanding of programmes with both feld epidemiologists for technical best practices evolved. Its initial recommendation for advice and administrators to help manage logistics. Over every country to vaccinate at least 80% of the popu- the 12 years of the programme, 687 diferent individuals lation increased to a goal of 100% vaccination [28], from 73 countries participated in the WHO-sponsored before being replaced with a dramatically diferent rec- programme [45]. Te expansion of WHO’s role from ommendation to invest heavily in surveillance and to solely providing technical advice to actively enabling focus vaccination on the places where transmission was operations was a learning experience for the Geneva- observed. Many countries resisted this latter change based programme [46]. Tis evolution allowed Geneva despite evidence that that surveillance-driven target- to strengthen global logistics, moving supplies from one ing was more efcient [31], and the WHO’s leadership country to another as needed, or fexibly providing nec- in pushing for adoption of proven approaches was thus essary funds to overcome bottlenecks [10]. It was noted critical [36]. Today, regular revisions of malaria guid- that the WHO was most efective when its staf, includ- ance (e.g., [34, 37, 38]) demonstrate that such dissemi- ing senior leadership, spent their time working in country nation of best practices remains an important WHO with programmes [47]. Henderson stated his opinion that role. the most efective WHO staf “were those who took an active role in feld operations. Tose who assumed a pas- Ensuring the quality of tools sive role of detached technical adviser were encouraged Smallpox programmes relied upon having a stable, reli- to leave the programme” [10]. Similar sorts of temporary able, efective vaccine [39]. Yet when the newly estab- feld advisors have been deployed under the “Stop Trans- lished eradication headquarters in WHO established a mission of Polio” programme [48] and can prove useful system for testing batches of vaccine produced in more for building capacity in malaria programmes if deployed than 40 diferent countries, it found < 10% of samples thoughtfully [49]. Te United States President’s Malaria were acceptable [40] due to potency and heat stability Initiative today provides technical advisors to malaria issues [41]. Te WHO engaged vaccine experts to write endemic countries in this mode, as do several non-gov- simple manuals of production that explained best avail- ernmental organizations. able production methods, and the WHO consultants worked with laboratories to improve their production Encouraging research and innovation processes [42]. Local production of vaccine was set up In Henderson’s view, “Te importance of problem- at government-owned facilities or associated institutes oriented research that was conducted throughout the in the largest population countries including Brazil, course of the smallpox eradication programme can- India, and Indonesia, since donations would otherwise not be too emphatically stated” [10]. Development have been insufcient [42]. Two high quality laborato- of a heat-resistant vaccine may have been the single ries from the Netherlands and Canada were selected to most impact factor in global success [7], while ongoing serve as vaccine reference centres [39], and they per- operational research enabled resolution of unforeseen formed batch testing to evaluate improvements. As a challenges that inevitably occurred over the course of result of these eforts, the fraction of batches meeting the long, complex undertaking of eradication [21]. Te quality standards rose to 31% in 1967, 76% in 1972, and WHO encouraged such studies through its convening 96% in 1976 [36]. Te WHO today provides an analo- power [14], though innovation was typically decen- gous quality control and assurance function for cer- tralized. “An important lesson was that parallel activi- tain malaria commodities, prequalifying malaria drugs ties and research, with many groups seeking better (https​://extra​net.who.int/prequ​al/), evaluating the approaches, could speed up the process of improve- accuracy of diagnostics [43], and inspecting manufac- ment,” Foege wrote [50]. Te jet injector, for example, turing sites for vector control tools, though the com- a new tool for increasing the speed and efciency of plex landscape for malaria commodities makes it more vaccine delivery [51], was frst developed in the United difcult to assess the overall quality of the tools being States at the National Communicable Disease Center used in endemic countries. Te smallpox experience during the 1960s [52]. Te development of a low-tech, suggests that investment in the production of bed nets simpler solution—the bifurcated needle—by a private in high-volume countries could be considered as a pos- company, Wyeth Laboratories (which waived patent sible means of reducing reliance on imported, donor- costs for any manufacturer supplying them exclusively funded products [44]. to the WHO [53]), proved both simpler [29] and ulti- mately more successful [54]. An examination of Cohen Malar J (2019) 18:323 Page 7 of 16

innovation in the smallpox programme concludes that Financing the programme what was important was to “insure that the problem has Achieving malaria eradication will require each of the been defned clearly and that intervening variables and world’s endemic countries to invest in eliminating trans- technological factors do not becloud that defnition”, mission. Financial analyses typically suggest that sub- while building organizations that scientifcally evalu- stantial short term budget increases will be required to ate evidence and seek to improve themselves according end endemic transmission, after which long term sav- to measurement of what does and does not work [39]. ings can be realized due to the lower costs of preventing Tis perspective suggests the importance of contin- its re-establishment [58, 59]. Surprisingly, in the case of ued investment both in malaria’s $540 to $600 million smallpox, Henderson argues no such surge in funding research and development pipeline [55] as well as in was required, with existing domestic budgets sufcient to eforts to help countries collect, analyse, and apply data cover programmatic needs: for ongoing organizational improvements within their “Te burden of expenditure has been borne by the own programmes. endemic countries themselves… But, with few excep- In playing these roles, there was agreement that the tions, the expenditure by the countries has been little WHO’s success was strongly linked to the ability to be more than what they were already spending to con- as fexible and non-bureaucratic as possible [21]. Some- trol smallpox. In other words, WHO and its mem- times, as when fying to countries with outbreaks with- ber countries, with only a very modest additional out receiving travel approvals, this meant breaking WHO input in resources, have transformed a never ending rules [41], something Henderson deemed necessary control programme to a successful eradication pro- given “a sclerotic… administration that often thwarted or gramme.” [29] actively impeded what appeared to be logical initiatives” [7]. In one example, an emergency request for vaccine Te idea that smallpox could be eliminated from coun- supply from Uganda took 5 months to be transmitted to tries with essentially the same budget previously used headquarters by the regional WHO ofce, during which to control it is remarkable, and suggests that how funds time the Geneva ofce had already learned about the were spent proved far more critical than the total amount outbreak via informal backchannels and addressed it [8]. of those funds. As Henderson describes: Internal WHO disagreements also led to challenges, with “For all of us it has been a revelation in so many Henderson noting, “Ofcials located within diferent lev- countries to fnd at the periphery such an array of els and departments of the regional ofces continued to unproductive health staf and facilities. It has been hold disparate views right till global smallpox eradication a revelation to discover how efectively they may be was formally certifed” [33]. He complained that, “Te mobilized with a comparatively small input involv- regional ofces of WHO… were more a hindrance than ing leadership in the feld and defnition of a series a help,” leading him to adopt a “policy of quietly short- of activities with defned objectives and a modest circuiting the regional ofce, when necessary” [8]. element of management. Other health programmes, Te challenge for a complex bureaucracy like WHO especially those involving immunization, but others to nimbly respond to dynamic circumstances have as well, could, I believe, be similarly transformed.” been echoed in recent years by criticism surrounding [29] its response to the 2013–2016 Ebola outbreak in West Africa [56, 57]. Te success of the WHO’s smallpox team Te importance of using available funding better was may provide a model for how a Geneva-based team can raised both nationally and internationally. Te WHO fexibly facilitate malaria operations across endemic internal dynamics and disagreements between regional countries. However, the fact that Henderson and col- ofces complicated the efcient expenditure of avail- leagues viewed their success as something they achieved able funding. In the Americas, for example, in the early despite WHO’s structures and procedures—for exam- 1960s, the Pan American Health Organization (PAHO) ple, by creating a new unit within a regional ofce that chose to distribute available funding for mass vaccination reported directly to Henderson rather than through the across the entire region, even though Brazil was the only normal channels [33]—rather than because of them, sug- remaining endemic country [6]. As a result, Brazil’s fund- gests that consideration will need to be given to how to ing was insufcient and elimination programmes were ensure a central malaria coordination team is encouraged prolonged unnecessarily [14]. Te WHO’s South-East and enabled to be agile and fexible, as is required by the Asia Regional Ofce (SEARO) chose to pass up the avail- rapidly evolving nature of a global eradication enterprise, able funding rather than participate in the programme, while still respecting and sometimes deferring to local which it disagreed with; Henderson then channeled the solutions and expertise. SEARO money to PAHO in hopes it would be spent in Cohen Malar J (2019) 18:323 Page 8 of 16

Brazil. Less than half actually was, with the remain- instead. New accounts were set up to give team leads der divided across 10 other countries [8]. When 5 years advances for these minor but essential charges so that later Brazil was fnally free of smallpox, PAHO refused they could avoid weeks of paperwork to receive necessary to donate its funds back to SEARO in turn to assist India funds, instead providing receipts at subsequent meetings [8]. on a biweekly or monthly basis. Tis approach dramati- Henderson’s comparison of the relatively similar costs cally improved the fexibility of the elimination eforts for control versus eradication refer only to domestic and Henderson deemed it “one of the most important contributions, and do not include the 407 million doses initiatives of the programme” [8]. of vaccine that were donated over the course of the pro- Malaria programmes today frequently experience simi- gramme, primarily by the Soviet Union and the United lar delays due to challenges with fnancial expenditure. States [29], at an average estimated value of $17 per 1000 Many countries have failed to spend grants from the [6] (approximately $7 million in total). Between 1967 and Global Fund to Fight AIDS, Tuberculosis, and Malaria on 1979, $67 million in cash and kind (including the donated schedule due to a wide variety of issues, including lack of vaccine) was donated to the WHO’s special account for human resources, delays in procurement, weak data sys- smallpox eradication while $33.6 million was spent from tems, and other challenges [61]. Te smallpox experience WHO’s regular budget [6]. Tis total of approximately suggests that the proactive creation of a fexible fund that $7.7 million per year would translate to approximately could be used to address bottlenecks across countries as $30–$50 million in today’s dollars—far less than the they arise could be a valuable tool for malaria as eradi- $2 billion per year currently contributed by international cation proceeds, though the challenges of ensuring those donors to malaria programmes [60]. funds are well spent would be substantial, and safeguards Te argument made to donors to secure these funds would be needed to ensure funds are spent for their was that “all should be willing to contribute to carry the intended function. Tis history also emphasizes the criti- attack to the remaining endemic regions until there is no cal importance of having strong measurement and man- more smallpox” [51]. Te United States, for example, was agement of programmes to ensure available funds are said to be domestically spending $140 million annually in allocated and used as efectively as possible. 1968 to prevent re-establishment of smallpox transmis- sion domestically, and thus its modest investment of $15 Domestic support for the programme million to eliminate in West and Central Africa meant Political will has been cited as one of the most important that it could help 20 countries become smallpox free for factors in the success of smallpox eradication [14] and a the price of 39 days of preventing its reintroduction back necessity for eliminating malaria [34]. Not all countries home [35]. A similar argument was used to successfully viewed smallpox elimination as an urgent priority given convince the Swedish government to make a critical con- many other public health issues [28], just as malaria elim- tribution to the programme in India, since “every country ination is often a low priority today for countries facing is in danger until the last case of smallpox has been elimi- more visible threats [62]. Competing disease priorities, nated” [22]. including ongoing malaria eradication eforts [29], led Te availability of even small amounts of funding that governments such as that of Ethiopia to have “absolutely could be used fexibly, with minimal bureaucracy, was no interest in the eradication of smallpox” [63]. Non-gov- seen as critical to bypassing bottlenecks. “It was essential ernmental actors such as the United Nations Children’s to have an allocation of funds that could be used for any Fund (UNICEF) also had prior commitments to malaria necessary purpose and in any country” [10], yet nearly all eradication that took precedence over contributions available funds for smallpox eradication were earmarked to smallpox [8]. Today, the need to devote substantial for specifc uses. As a result, staf were often not paid on resources to ongoing eforts to eradicate other diseases, time, insufcient fuel allowances meant vehicles were not including guinea worm and polio, may present similar available when needed, and funding for car repairs was challenges for malaria. lacking in multiple countries [10]. In Zaire, for example, Countries where the less virulent variola minor pre- operations would frequently grind to a halt after the gov- dominated over the far more deadly variola major, ernment failed to release the necessary funds; the pro- mostly in Africa, tended to downplay the importance gramme solved the issue by setting up an auxiliary bank of embarking on an elimination programme, given that account in which they deposited back-up funds whenever this strain of the disease was “little more serious than possible to cover expenditure during these gap periods chicken pox” [8]. Henderson cited this reticence as one [8]. In Bihar, India, “staf were fearful of paying too much of the two primary factors compromising the young [for vehicle maintenance] and being held accountable programme (the other being the absence of funding) for extra charges” [46], so vehicles were often neglected [10]. Tis challenge is echoed by questions of whether Cohen Malar J (2019) 18:323 Page 9 of 16

malaria eradication should aim to include all species of Community support for the programme the disease or only (or initially) the more virulent Plas- Community participation with the smallpox programme modium falciparum given its outsized contribution to was considered generally strong [8], although the litera- mortality as well as its development of resistance to ture contains numerous accounts of specifc anecdotes artemisinin-based drugs in the Greater Mekong subre- of resistance to vaccination particularly following real gion [64, 65]. Accounts of smallpox eradication do not or perceived adverse reactions to the vaccine [28]. Some clarify whether an efort to only eradicate variola major commentators note that the narrow focus on smallpox could have succeeded (and thus whether a P. falcipa- was sometimes counterproductive given the range of rum—only attempted might be feasible), though the health issues aficting communities. In Bangladesh, for similarity of symptoms between the two would have example, vaccination occurred in the midst of a cholera complicated case fnding directed only at the major epidemic, yet the vaccinators could provide no assis- variant. tance with the more visible and urgent problem, result- Political backing also sufered with changes in gov- ing in community frustration [68]. As the programme ernment and thus the loss of advocates: “Within 4 years proceeded, additional components were therefore added after the West African programme began, there were 23 onto the responsibilities of surveillance agents to keep changes of governments in the 18 participating coun- them engaged and motivated despite the infrequency tries,” causing “changing leadership and staf in the with which smallpox was observed, including surveys nation’s smallpox programme” [47]. In India, it was noted investigating access to clean water, vitamin A, family that the Prime Minister’s enthusiasm for smallpox typi- planning, and rates of childhood mortality [68]. Simi- cally increased when outbreaks were observed—and thus larly, malaria-only health workers may prove less success- when the electorate was most concerned about the dis- ful than those that have been trained to treat a variety of ease—and declined with smallpox incidence [22]. Pres- common illnesses [69]. sure from powerful allies outside the government was Gaining the support of community leaders was com- thus seen as critical to ensure the programme remained monly cited as a crucial step towards community accept- sufciently well supported even when smallpox was ance. In Nigeria, Foege believed that people participated not in the headlines. An agreement to begin a vaccina- less because they were convinced by vaccinators to do so tion programme in Ethiopia only occurred due to the and more because they trusted their leaders [31]. In one intercession of a senior Austrian physician with a close extraordinary case, vaccinators were reported to have relationship with the Emperor [63], while in India, the awed a village chief into supporting the programme by intervention of J.R.D. Tata, the well-connected head of releasing a trained bird to swoop overhead and drop pro- a large corporation, played a critical role in convincing vaccine leafets while vaccinators were meeting with him the Prime Minister to continue supporting the smallpox [29]. Despite such anecdotes, Tarantola and Foster note programme at a pivotal moment [22]. In Bhutan, where that little research was conducted into how the commu- the WHO initially lacked visibility into smallpox eforts nity could best be engaged [68], though attempts to do so due to the secrecy of its government, an acquaintance of included deployment of midwives and other village work- Henderson’s with access to the royal family was eventu- ers to engage and educate the community [39, 70] as well ally able to build communications with Geneva [66]. as provision of monetary awards for report of a smallpox A lesson for malaria is thus the importance of getting case in the fnal stages of the programme [71]. In India, well-connected leaders from business and high-profle for example, a 100 rupee reward was ofered for anyone institutions to act as advocates. Te opinion of politicians reporting a previously unknown outbreak [29]. Te evi- can change based on what seems important for the next dence base for what drives patient participation with the election, but smallpox programme examples show how health system has increased in subsequent decades, iden- they can be convinced by counsel from those they trust tifying factors related to cost, proximity, and confdence or respect. Malaria appears to already be doing a better [72], but the relative ability of diferent interventions to job of identifying high-profle advocates; organizations infuence those factors likely still requires additional with the explicit goal of maintaining malaria’s global or research. Best practices for proactive engagement of regional visibility, such as Malaria No More or the Afri- community leaders and ongoing communication and col- can Leaders Malaria Alliance, identify champions who laboration with at-risk populations should be encouraged can contribute funding and political backing to national to make communities active participants in malaria elim- eforts [67], while the End Malaria Council (http://endma​ ination programmes [73]. laria​counc​il.org/) seeks to bring business leaders together Where eforts to improve participation failed, small- with public sector leaders to keep malaria a global pox programmes would sometimes use compulsory vac- priority. cination, an approach that dispensed with “the need to Cohen Malar J (2019) 18:323 Page 10 of 16

converse with villagers at all” [74]. Compulsory vaccina- successfully led to elimination in some countries, but tion was believed to be justifed by the need to achieve elsewhere it failed, likely because the vaccinated and sufcient coverage for the greater good, but it raises trou- unvaccinated fractions of the population were not bling ethical questions. Greenough quotes Stanley Music, homogenously mixed [36]. In Central Java, for example, a an epidemiologist who worked in the Bangladesh pro- 1969 survey found greater than 95% vaccination rates had gramme, on the tactics sometimes employed: been achieved across the population of 23 million people, yet that same year over 1700 cases were recorded, nearly “In the hit-and-run excitement of such a campaign, all amongst the 5% of the population who had been women and children were often pulled out from missed [78]. Te WHO Expert Committee responded under beds, from behind doors, from within latrines, by telling countries they should strive for 100% vaccina- etc.… Attempts were made to secure the cooperation tion rates, a target scorned as impossible [29]. Attempts and ‘blessing’ of village headmen, thereby putting to conduct greater numbers of vaccinations were under- social pressure on the villagers to stand their ground taken, but “accessible groups, like schoolchildren, were and accept vaccination. Still, however, some form of vaccinated repeatedly so that high ‘scores’ were achieved, minor chaos was the rule, as headmen’s authority but there always remained a large pool of unvaccinated did not extend into individual’s homes… People were persons” [47]. Tis language is mirrored in a recent inves- chased and, when caught, vaccinated… We went tigation of bed net coverage across Africa by Bhatt et al., from door to door and vaccinated. When they ran, which concluded: we chased. When they locked their doors, we broke down their doors and vaccinated them.” [74] “We found substantial over-allocation of nets to households already owning a sufcient quantity… While these aggressive approaches did in some cases What is certain is that over-allocation becomes a attain the narrow goal of achieving high vaccination cov- major barrier to achieving universal coverage when erage, they seem unwise for a programme such as malaria levels of [insecticide-treated bed net] provision are in which long-term participation and repeated delivery high because most new incoming nets are simply cycles is needed. Ethically, they were controversial even leading to surpluses in many households, while else- at the time, and “the organized and sustained use of com- where there remains a shortfall. Tis may have a pulsion was, generally speaking, instituted with great disproportionately high public health impact if those care and only after broad administrative and political surplus nets are concentrated in households at low- consensus had been achieved” [22]. est risk.” [79] Engagement with the private sector was reported to be generally minimal outside a few eforts to integrate Te critical change in smallpox programmes was a shift private health care providers into the vaccination pro- away from mass vaccination towards an approach called gramme [68]. India proved one of the main exceptions, “surveillance-containment” [35] in which programmes with the Tata Group playing a critical role in vaccinat- sought out smallpox cases and then concentrated vacci- ing the population of Bihar State, where its steel plant nation eforts in their proximity and towards those who was located. Tey provided “medical and paramedical may have come into contact with the cases. In short, the personnel, transportation, managerial support and com- new strategy meant focusing vaccination on the places munication facilities to implement the programme activi- where it was most likely to matter, rather than laboring ties. Te assistance in kind provided by the Company and to achieve implausibly perfect coverage everywhere. In their local knowledge of the area were so valuable that Bangladesh, for example, the programme successfully south Bihar became smallpox-free in a record period of ended transmission after abandoning eforts to achieve 6 months” [75]. Malaria’s recent history includes several 80% vaccination nationally and focusing eforts instead examples of similar partnerships [76]. Given the impor- only on the northern districts where cases were reported tance of private providers and drug shops for provision [41]. of malaria treatment [77], malaria eradication will neces- Te 1964, the WHO Expert Committee report did sitate much greater engagement with the private sector not even mention surveillance [8], but the new focus on than occurred during smallpox eradication. fnding cases, tracking down all of their contacts, and concentrating vaccination operations in the most nec- Programmatic strategy essary places was considered by many to be one of the Smallpox eradication was predicated on the idea of mass keys to eradication’s ultimate success [14, 80]. Identify- vaccination of the population. Te WHO’s Expert Com- ing where smallpox was being transmitted required a mittee initially called for countries to achieve at least network of agents who visited all health units (usually in 80% vaccination of the population [29]. Tis approach teams of two to four per administrative unit) to ensure Cohen Malar J (2019) 18:323 Page 11 of 16

weekly reporting, sought out cases in the community, treatment are targeted to those who most need them has including by collaborating with teachers or visiting mar- great potential for improving the efciency and efective- kets [78], and distributed surveillance reports so that the ness of our eforts. health staf saw how their reports were being used [81]. “Undoubtedly, the greatest stimulus to reporting was the National programme structure and management prompt visit of the surveillance team for outbreak inves- Discussion of the wisdom of eradication programmes tigations and control whenever cases were reported,” often revolves around the relative merits of “vertical,” Henderson wrote. “Tis simple, obvious and direct indi- single disease programmes versus “horizontal” health cation that the routine weekly reports were actually seen systems eforts [14], which were increasingly coming and were a cause for public health action did more, I into favour at the WHO around the time of smallpox am sure, than the multitude of government directives eradication. Henderson advocated for having a specifc which were issued” [81]. Case fnding was intensifed vaccination programme distinct from, yet linked to, during the period of lowest seasonal incidence, since routine health services, worrying that fully integrated that low transmission season represented the weakest programmes would lack clear objectives, evaluation point in the smallpox cycle and the best opportunity to systems, and management structures. “Te ‘horizontal break transmission, despite the operational challenge of programmes’ I have seen best describe the sleeping pos- fnding cases at that time of year [82]. Active case fnd- tures of the workers” [80], he wrote. In contrast he con- ing was integrated with routine reporting from public sidered a “targeted and time-limited special programme health facilities rather than conducted entirely in parallel with funds specially allocated for it, both in the WHO [81]. Challenges to setting up good surveillance systems budget and in most national budgets, and with full-time included the fact that in many countries, disease report- technical staf responsible for its supervision” [10] to be ing fell under the purview of independent statistical units superior since it would more easily attract resources and and were not thus within the control of the smallpox pro- community support and likely be more efcient and bet- gramme [10] (the same is true for malaria today in many ter managed given the singular focus. Such programmes countries). were also viewed as attractive because they could be con- Te operational strategy of directing vaccine only to ducted even while basic health services remained weak known transmission areas may not be directly trans- [51]. Te vertical versus horizontal health programme latable to malaria’s tools. First, the approach may have debate has persisted since smallpox [88] and will not be worked in part because the reproductive rate for the resolved here, yet a few clear lessons for malaria emerge virus was relatively low [35], estimated at approximately from smallpox’s successes. 3.5 to 6 [83], while estimates for malaria are variable but First, smallpox programmes were well integrated with potentially far higher [84]. Second, case fnding was far basic health systems, enabling routine case manage- easier because the symptoms of the disease were so dis- ment and surveillance, with active case fnding used as tinctive and recognizable even to schoolchildren [81], a supplement rather than a replacement. Tis integrated and smallpox—unlike malaria [85]—very rarely caused design improved upon the design of the Global Malaria asymptomatic infections [6]. As a result, mathematical Eradication Programme preceding it in the 1950s and modeling of an analogous reactive case detection strat- 1960s, which largely circumvented basic health systems. egy for malaria suggested that such approaches may Te malaria eradication programme measured malaria increase the probability of elimination in certain con- primarily via population prevalence surveys [89] and texts, but would be “a highly resource intense, long-term other active means [90] and conducted insecticide spray intervention that is inappropriate in many settings where campaigns as vertical eforts. Malaria staf were also bet- resources are limited” [86]. ter paid than other workers and reported to heads of Nevertheless, the critical shift in smallpox programmes state rather than ministries of health, creating unsustain- from judging success based on the volume of vaccina- able systems [7]. In contrast, smallpox programmes were tions to whether vaccination was achieved in the most still part of the health system, leveraging the same basic necessary places still suggests a good model for malaria health services and staf to identify and report the dis- programmes, despite the extensive presence of asymp- ease [10, 33]. Tis integration meant that smallpox teams tomatic carriage. Malaria programmes that seek only were not required to set up fully parallel surveillance to distribute commodities such as nets or drugs in high systems, instead augmenting existing ones and leaving volumes in an attempt to achieve “universal” coverage behind some added capacity within health programmes. may be missing more inaccessible populations which Similarly, reliance upon the routine, albeit imperfect, may also be the highest risk for malaria [79, 87]. Shifting measurement of malaria that basic health systems pro- towards a risk-focused approach in which prevention and vide across endemic regions seems likely to greatly Cohen Malar J (2019) 18:323 Page 12 of 16

improve the cost-efectiveness of surveillance given that and tactics,” wrote Henderson. “In fact, few programmes it requires minimal expenditure beyond keeping health do so. Responsible authorities tend to ignore such infor- facilities stocked with diagnostic tests, training staf in mation or dismiss eforts to obtain the data and, instead, their use, and linking them to efective reporting systems. assess progress in terms of activity, such as the num- Such investment in core case management systems is a bers of vaccinations performed or patients treated” primary component of WHO’s Global Technical Strategy [10]. Arguably, today’s malaria programmes continue to for malaria [4]. focus more on activities conducted rather than impact, Second, multiple authors highlight the importance to in part because key performance indicators reported as smallpox programmes of creative, problem-solving staf proof of performance on grants such as those from the [32] who could fgure out how to overcome any obstacle Global Fund to Fight AIDS, Tuberculosis, and Malaria that arose, tailoring solutions to the unique challenges tend to focus on the number of nets delivered [93], and contexts faced by each country [10]. Henderson rather than whether they are delivered to those most at described: risk or achieve desired reductions in malaria. Te small- pox experience suggests that successful elimination may “Te essence of what has made the programme what require shifting focus from simply tallying how many it is is, very simply, an imaginative and dedicated commodities have been distributed towards assessment feld staf, both national and international, who, of whether those tools are being used as efectively as given scope and encouragement to work out prob- possible. lems according to local circumstances and support In West and Central Africa, smallpox programmes in their eforts to do so, have responded with some used three diferent types of evaluation approaches: frst, remarkable solutions to impossible problems.” [29] evaluators would follow-up to assess whether what vac- Tese resourceful workers, described by former United cinators claimed to have done had truly been accom- States Surgeon General Julius Richmond as “simply too plished; second, tally sheet comparisons were made to young to know it couldn’t be done” [50], were supported compare vaccination records against any available cen- by a similarly fexible international team at WHO, who sus data, as a quick if somewhat inaccurate estimation were described as: of whether numbers were approximately what should be expected; third, spot checks for vaccine scars were con- “Essentially problem-solvers, they viewed themselves ducted at markets and other convenient gathering places as catalysts rather than as controllers. Tey under- to provide an independent confrmation of coverage [94]. stood from the onset that experimental learning Henderson stressed that in measurement, quality was ofered the only possibility for success. Tey avoided more important than quantity: “a few indicators of over- formalized programming, opting instead for innova- all performance, closely followed, were more useful than tion, fexibility, communication and experiment, by a broad spectrum of indicators measuring many aspects means of a number of deliberate policies and mech- of programme execution” [10]. anisms. Tey recruited people with practical feld How to build appropriate teams and processes to con- experience in epidemiology (as opposed to previous duct this measurement and verifcation was determined work with smallpox per se). Tey sought people with on a country by country basis. In Bolivia, one inspector reputations for adaptability, imagination, and hard was appointed for every eight to 12 vaccinators, ensur- work. Tey preferred younger people, assuming they ing everyone’s work was reviewed at least biweekly would be more receptive to new approaches and [95]. In India, a Central Appraisal Team oversaw evalu- ideas.” [91] quoted in [39] ation processes, including frequent travel to trouble Henderson contrasted the fexibility with which small- spots to assess what was going wrong [8]. Ensuring pox programmes worked with the unsuccessful prior accurate reporting was sometimes compromised when malaria eradication efort, which he said “was conceived workers avoided reporting true cases because they and executed as a military operation to be conducted in thought they would be punished for allowing transmis- an identical manner whatever the battlefeld” [92], pre- sion in their region [70], underscoring the importance venting it from adapting to local contexts, structures, and of clear and frequent communication between central systems. and local levels, with regular meetings to discuss prob- Tird, smallpox programmes placed great emphasis lems and progress [10]. Widespread distribution of on careful measurement and verifcation. “Logic sug- smallpox indicators was encouraged, such as through gests that all disease control programmes should provide surveillance bulletins in Brazil which were distrib- continuous measurements of disease incidence, and that uted on a monthly basis to a wide audience, providing these measurements should dictate changes in strategy updates on progress, putting pressure on non-reporters Cohen Malar J (2019) 18:323 Page 13 of 16

to participate, and generally helping to foster a shared have been a wise idea, though it was not done at the time sense of purpose across the diverse network of individ- [10]. uals participating in the campaign [8]. Fourth, the smallpox programme emphasized the Discussion importance of strong management in all aspects of the Te successful eradication of smallpox holds many les- programme. Henderson suggests that, “Successful execu- sons for malaria eradication eforts, despite the consid- tion of the programme consists of perhaps 10% techni- erable diferences between the programmes. Smallpox cal skill and 90% organization and leadership” [29]. He succeeded as a collection of individual country pro- stressed the importance of leaders actually spending sub- grammes each deriving local solutions to local problems, stantial time out in the villages where the work is being yet with an important role for WHO and other inter- done, leading by example and helping motivate workers: national entities to facilitate and enable these eforts by “efective leadership to solve the problems faced by feld ensuring the best possible tools were available, maintain- workers cannot be supplied by an army of physicians and ing the disease’s profle globally, fundraising, and arm- senior supervisors who never leave their desks. Regretta- twisting in reluctant countries to ensure coordinated bly, these types are all too plentiful throughout the world” action. Te documented experience of smallpox pro- [29]. Tese opinions were substantiated by an evaluation grammes suggests that such coordinating eforts must be of unsuccessful programmes in India, Pakistan, Argen- nimble and fexible to stay relevant to rapidly changing tina, Iran, and Ghana, which found that: country situations, and burdensome bureaucracy must “First and most important, failure appeared to be be avoided if international agencies such as WHO are to associated with inadequate supervision and assess- add value rather than increasing the challenge of disease ment. Programmes that failed normally showed elimination. the following shortcomings: (a) supervisory person- Smallpox programme leaders stress the importance of nel did not check at the family level to assure that empowering countries to solve problems locally. Where broad overage by vaccination of the population was a strategy or tool has been proven to work well, efcient being achieved; (b) supervisors were too burdened mechanisms for sharing those experiences are essen- by other responsibilities to give more than nominal tial. Yet each country will need to adapt those efective supervision; (c) inadequate provisions for travel and approaches given their diversity of populations, systems, expenses; and (d) disinclination of supervisors to strengths, and weaknesses. Global leadership for malaria undergo the inconvenience of feld work.” [22] eradication must ensure countries are able to access the most efective tools available and understand the best William Foege described how “the real problems” of principles for how to use them, but the smallpox experi- “developing routines, documenting the implementation ence suggests there is no script to be followed in elimina- of those routines, hiring the right people, supervising, tion, no simple set of check-boxes that if ticked will result motivating, and evaluating” required “managers, admin- in success. Countries did beneft from the provision of istrators, and logistics experts—people who knew how international technical advice and logistical support, to solve problems and how to get things done. Te pro- helping build staf capacity. Te particular importance gramme would not fail for lack of scientists, but it could of administrative support to national programmes sug- fail—even with the best strategy—if we didn’t attract gests distinct cadres of staf can add substantial value the very best managers” [32]. Strong management was to malaria elimination programmes: advisors from pub- required to keep up staf enthusiasm for searching for lic health backgrounds can help with technical aspects, smallpox when there was nothing left to fnd [22]; in one but logistical experts are needed to help plan and exe- case, near the very end of the programme in Ethiopia, a cute efcient operations. Te smallpox experience also surveillance agent walked for 15 days to check on two emphasizes the critical importance of hiring programme reported cases which turned out to be chickenpox [29]. leaders and managers who are enthusiastic about spend- Programmes accordingly sought to hire non-medi- ing time with communities and local programmes, and cal, logistics-oriented staf with experience in admin- who are creative thinkers who can derive context-appro- istration in addition to those with a more conventional priate solutions to the challenging problems that will public health background [82]. Once brought into the inevitably arise. programme, strong managers had to be retained: in Bra- Smallpox eradication is reported not to have involved a zil, for example, fve diferent directors were appointed in substantial increase in domestic budgets, but rather was the 5 years between 1967 and 1971 [14] with unsurpris- achieved by better managing programmes and streamlin- ingly weak results. Henderson suggested that providing ing how they spent the available funds. A clear lesson is programme leaders with management training would that data-driven approaches that target resources to the Cohen Malar J (2019) 18:323 Page 14 of 16

places where they are most needed will be more success- for malaria eradication to be successful. What is instead ful for elimination than mass attempts to achieve univer- required is for national programmes and the interna- sal coverage everywhere; such a shift in mindset proved tional institutions that support them to be scientifc in similarly successful in the eradication of rinderpest, with their approaches and efcient in their execution—to surveillance-targeted vaccination proving much more be open to new tools and strategies, to weigh evidence, impactful than total coverage [96]. Minimizing inef- revise approaches, and to make data-driven decisions as fciencies in malaria programmes to ensure available best they can given imperfect intelligence. funds have the greatest possible impact should be a high priority, even while the malaria community continues Abbreviations to advocate for increased funding from donors. In addi- PAHO: The Pan American Health Organization; SEARO: WHO’s South-East Asia tion, the importance of fexible funding—even in small Regional Ofce; UNICEF: The United Nations Children’s Fund; WHO: The World Health Organization. amounts—was repeatedly stressed. Setting up a central malaria account that can be rapidly and fexibly used for Acknowledgements flling gaps and bypassing bottlenecks could be an impor- Joe Novotny reviewed a draft of this paper and made numerous helpful suggestions for improvement. Thanks to Pedro Alonso, Kim Lindblade, and tant step towards enabling malaria eradication. Means the WHO Strategic Advisory Group on Malaria Elimination for suggesting this of reducing dependence on donor-funded commodities, review and providing advice on its structure. such as investment in local manufacturing, may also need Authors’ contributions to be considered. JMC conducted the review, the analysis, and wrote the manuscript. The author Building a malaria elimination programme that is vis- read and approved the fnal manuscript. ible for fundraising and that has its own discrete, measur- Funding able milestones will drive programmes to hold themselves This work was supported by the Bill & Melinda Gates Foundation accountable and focus on achieving results rather than [OPP1109772]. The funder had no role in the design, analysis, or interpretation just distributing commodities. However, nesting those of this investigation nor in the writing of this manuscript. programmes within basic health services is critical to lev- Availability of data and materials erage routine case management and reporting, increas- Not applicable. ing the sustainability and reach of the programme. While Ethics approval and consent to participate government programmes may direct the fght against Not applicable. malaria, the experience of smallpox eradication also sug- gests afected communities and the private sector will Consent for publication Not applicable. have critical roles in whether success is achieved. An innate limitation of this review is that it depends Competing interests upon the published literature, which is constrained by The author works for the malaria program at the Clinton Health Access Initia- tive, which receives funding to provide operational support to governmental the availability of viewpoints of those who have pub- programs seeking to control and eliminate malaria. lished [66]. Smallpox was a global undertaking with diverse contributions of healthcare workers at all levels Received: 12 August 2019 Accepted: 11 September 2019 of international and national programmes, yet accounts in the literature are primarily written by director-level staf from the United States and Europe. Accordingly, this References review is biased substantially towards the viewpoints of 1. WHO. The World Health Organization and malaria eradication. Geneva: those few individuals who dominate the literature. World Health Organization; 1956. Report No.: WHO/Mal/162. 2. WHO. WHO Expert Committee on Malaria [meeting held in Athens from 20 to 28 June 1956]: sixth report. Geneva: World Health Organization; Conclusions 1957. Report No.: World Health Organization Technical Report Series No. In Henderson’s view, many of the political challenges 12. 3. WHO. Twenty-second World Health Assembly: Part I. Resolutions and to eradication were unforeseeable, and ultimate suc- Decisions; Annexes. 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