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Aedes Aegypti and Aedes Aegypti-borne Disease Control in the 1990s: Top Down or Bottom Up

Duane J. Gubler 49th Franklin Craig Lecture delivered before the American Society of Tropical Medicine & Hygiene, Washington, DC 12/7/88

Publication date: 01/01/1989


Table of Contents

Article

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Article

It is a great honor to be asked to present the Charles Franklin Craig Lecture of this Society. I initially accepted this responsibility with some trepidation, and after reviewing the list of previous Craig Lecturers, I became even more nervous about the prospects of addressing you. It is indeed an honor to be added to that list.

I would like to express my sincere thanks to those responsible for my selection as the Craig lecturer, including the committee who selected me for this honor, the many collaborators who over the years have made my work much better than it would have otherwise been, and last, but not least, my wife Bobbie whose understanding and tireless support made it all possible.

Charles Franklin Craig helped establish the viral etiology of dengue fever in 1907, (1) so it is appropriate that I talk about this disease today. In 1954, Albert Sabin delivered the nineteenth Craig Lecture and reviewed existing knowledge of dengue and sand fly fever. (2) Considerable information has accumulated since then and we have learned a great deal about the dengue viruses, their epidemiology and pathogenesis. (3-5) Unfortunately, we have not made much progress in our ability to control the mosquito vectors that transmit dengue viruses, and thus in our ability to prevent epidemic disease. (6) And that is what I want to talk about today. First, to put things in perspective, I will briefly review the current problem of dengue and dengue hemorrhagic fever (DHF), and of Aedes aegypti-borne disease prevention and control from a historical standpoint. Second, I will discuss current options available to us for prevention and control of epidemic dengue and then briefly review our program in Puerto Rico which is directed toward this goal. Last, I will outline the approach I think is required to prevent major epidemics of Ae. aegypti-borne disease in the 1990s. Some of the things I am going to say are controversial, but I think the time has come to candidly discuss an emerging disease problem that has been ignored for too many years.

In 1968, David Sencer delivered the 33rd Craig Lecture and discussed health protection in a shrinking world. (7) His basic theme was that our quarantine laws for infectious diseases were outdated and not very useful because of the increased frequency and rapidity of air travel. He also called for a review of the concept of Aedes aegypti eradication, his rationale being that unless there was global eradication, it was a waste of time and money.

As you probably know, Sencer's recommendation was followed. The result was that the Ae. aegypti eradication and control programs in most countries of the American region were disbanded and merged with malaria eradication programs. You also probably know that today, Ae. aegypti has reinvaded nearly every country in the American region that had achieved eradication during the 1950s and 1960s (Pan American Health Organization, personal communication). Only Bermuda, the Cayman Islands, Costa Rica, Uruguay, and Chile remain free of this mosquito.

Moreover, Ae. aegypti densities are at an all-time high in most tropical countries. The world has changed in the past 30 years and it is not surprising that Ae. aegypti is doing so well. There has been an explosion in the number of artificial containers that make ideal larval habitats for this mosquito. These include the many non-biodegradable plastic containers that are used for domestic consumer goods, used automobile tires, and many other artificial water-holding receptacles found in the domestic environment. The problem is further compounded by our throwaway society, the uncontrolled urbanization in many tropical cities of the world, and by the general ignorance of mosquito-borne diseases in those cities.

In 1968, Sencer discussed Ae. aegypti eradication from the context of yellow fever prevention. He did not mention dengue fever. At that time, with only occasional outbreaks limited to a few Caribbean islands, dengue was not a major public health problem. Urban yellow fever, on the other hand, was perceived as a very real threat by some health officials. Today, the situation is reversed. In the 20 years since the overt decision was made to abandon the Ae. aegypti eradication campaign, dengue and DHF have become an important public health problem in the Americas. (8)

Dengue is a rapidly expanding disease in the tropics of the world. (6) In that same 20 year period, it has become the most important arbovirus disease of humans. There are now over 2 billion people at risk of infection, and millions of cases occur each year. The severe form of disease, DHF, is a leading cause of hospitalization and death among children in Southeast Asia. (9) Incidence has continued to increase each year and in 1987 alone, over 600,000 cases of this severe form of dengue were reported in that region compared to only 2,060 in 1967, a 300-fold increase in 20 years (10) (World Health Organization, personal communication). Dengue hemorrhagic fever moved into the American region in the 1980s. (8) This geographic expansion and increasing incidence poses a major dilemma for those of us who are charged with the responsibility of developing strategies for prevention and control.

Our current problems began in the 1960s, when jet aircraft became widely used for commercial travel. This has provided the ideal mechanism for the transport of dengue viruses between population centers of the tropics. As a result of increased movement of dengue viruses in infected travelers, the frequency of epidemic dengue activity began to increase, first in Asia in the 1950s and 1960s, followed by the Pacific and Caribbean basin countries in the 1970s and subsequently to Africa in the 1980s. (6) During this time, new dengue virus serotypes were introduced into the American and African regions, dengue 1 and 4 in the Americas, and dengue 3 and 4 in Africa.

In the Americas, we now have a hyperendemic situation with multiple virus serotypes (dengue 1, 2, and 4) circulating simultaneously in most countries. (8) All 3 viruses are endemic and have been responsible for major epidemics in nearly all parts of the region. Only dengue 3 virus is absent, but increased activity of this serotype in Asia and Africa in recent years will insure its introduction at some time in the near future.

Coincident with the appearance of hyperendemicity in the Americas has been the appearance of DHF. Although sporadic cases of suspected DHF were reported from several Caribbean island countries in the 1970s, most health authorities did not question the conventional wisdom that this disease syndrome did not occur in the Americas. This belief began to change in 1981, when Cuba experienced a major epidemic of DHF. (11) With an estimated 24,000 cases of severe hemorrhagic disease, Cuban authorities averted a major disaster only by implementing a massive hospitalization program. Over a 3 month period, 116,243 patients were hospitalized and placed on fluid replacement therapy. This prompt action saved many lives, but there were still 158 fatalities.

Since 1981, cases of laboratory confirmed DHF have been documented in 10 other American countries. (8) In addition, cases of severe and fatal hemorrhagic disease with confirmed dengue virus etiology, but which did not meet the World Health Organization case definition, have also been reported in many of these same countries. As of 1988, many dengue endemic countries of the American region are having sporadic cases of DHF on a regular basis.

All available evidence suggests that the dengue disease pattern is evolving in the Americas in the 1980s as it did in Southeast Asia in the 1960s. (8) Dengue hemorrhagic fever was not known to most physicians in Southeast Asia 30 years ago, but over a period of approximately 20 years, epidemic DHF spread throughout that region. In every country where epidemic DHF is a problem today, the disease first occurred sporadically for several years, ultimately culminating in a major epidemic. Subsequent epidemics were progressively larger. If that pattern continues to evolve in the Americas, we can expect sporadic cases of today to become major epidemics of severe disease tomorrow, much as they did in Southeast Asia 20 years ago.

There are some who might say we are being alarmist in predicting this scenario for the American region. Maybe, but I do not think so. In view of the current dengue situation and the way it has evolved in the last 10 years, I do not think we can afford to gamble by waiting for this prediction to be verified or refuted. To do so could result in hundreds, perhaps thousands of children dying of DHF over the next 10 years. Action must be taken to prevent history from repeating itself.

There is, of course, another disease transmitted by Ae. aegypti. We tend to forget that yellow fever epidemics were common prior to Ae. aegypti eradication. The ease with which these viruses can move in today's shrinking world insures that urban yellow fever can and probably will reappear in the absence of responsible public health planning in the Americas. Fortunately, we have an effective vaccine for this disease which, properly used, could prevent that from happening. This is not the case for dengue. We do not have vaccines for dengue viruses and the best estimates are that it will be 10 to 15 years before they are available for general use.

The obvious question then becomes how do we prevent epidemic DHF? There are many risk factors associated with severe and fatal dengue disease, some of which are still controversial, (5,12,13) but this is not the time nor place to discuss the pathogenesis of DHF. Whatever the ultimate truth regarding pathogenesis, the major problem is really one of increased disease incidence. The iceberg has increased drastically in recent years. We know that the probability of DHF occurring can be dramatically reduced by simply reducing incidence. In other words, we have to reduce the incidence of dengue back to where it was 20 years ago if we hope to prevent major epidemics of DHF.

As I have already noted, there are no vaccines for dengue viruses. The only viable way to decrease incidence, therefore, is by controlling the principal vector mosquito of dengue, Ae. aegypti. Therein lies our problem. For nearly 20 years, we have been told that the most effective way to control adult Ae. aegypti in urban areas is by using ultra low volume or ULV application of insecticides, primarily malathion. (14) Application has been from both truck-mounted units and from airplanes. Unfortunately, it has taken us 20 years to realize that the ULV approach has little or no impact on the wild Ae. aegypti population. Those of you who have investigated dengue/DHF epidemics and who have observed the recommended perifocal spraying with ULV applied toxicants, also know that it has little or no impact on dengue transmission. In 1975, William Horsfall of the University of Illinois was chastised for stating that ULV applied toxicants have about the same impact on both mosquito and human populations as driving a fire truck up the street spraying water into the air (W. R. Horsfall, personal communication). He was implying that ULV has more impact on the human population than it does on the mosquitoes, and in most cases where the method has been used for Ae. aegypti, I think that is correct.

We at CDC have just completed 3 years of intensive investigation of these methods in Puerto Rico. Our approach has been to evaluate the impact of ULV fumigation on the natural adult mosquito population, i.e., those mosquitoes that are transmitting the virus, rather than rely solely on selectively placed caged mosquitoes (bioassay) as most workers have done in the past. Our results indicate that neither ULV nor thermal fog applications of insecticides are effective in significantly reducing the adult mosquito population. Aedes aegypti is a highly domesticated mosquito and many adults are resting indoors in hidden places such as closets. Our studies have shown that the insecticide simply does not reach them. Time prevents me from going into further detail on the methods and results of these studies. The important take home message is that we cannot rely on aerial toxicants for prevention or control of epidemic dengue. In other words, there is no magic bullet, and to claim that this method works is to continue misleading millions of people who live in dengue endemic areas.

It is clear that if we are going to be successful in reducing mosquito densities to the level where large urban dengue or yellow fever epidemics will not occur, we must return to the only approach that has ever been truly effective. Larval source reduction, which was pioneered by William C. Gorgas and perfected by Fred Soper, is our only hope for decreasing the incidence of dengue to the point where DHF will not be a threat to millions of people living tropical Asia and America.

As noted above, the world has changed a lot in the past 30 years. It has become more difficult to implement the type of large, paramilitary, vertically-structured programs that were used so successfully to eradicate Ae. aegypti from much of Central and South America. Those days are probably gone forever. Exceptions are Singapore in Asia and Cuba in the Americas. Both countries have strong centralized governments. Stimulated by a major epidemic of DHF in 1981, Cuba reduced the Ae. aegypti density to the point where dengue transmission is no longer likely to occur. The latest figures put the Ae. aegypti house index at less that 0.001% (Pan American Health Organization, personal communication). Most countries, however, lack the resources to employ the thousands of inspectors and other support staff needed to implement and maintain an effective, vertically-structured source reduction campaign. Moreover, they lack the political structure and will to enact and enforce legislative control or, more simply put, to enforce laws that prohibit property owners from allowing mosquito production on their land. Finally, citizens of most tropical countries have come to expect and even demand that governmental agencies control the mosquitoes breeding in the domestic environment, mosquitoes that are present primarily because of improper management of water holding receptacles by those same citizens. And because of their paternalistic nature, most governments have accepted this role as protector of the people. Thus, most governments continue to promise results that they cannot possibly achieve using current approaches to mosquito control.

If there was one aspect of the Soper approach to Ae. aegypti control that failed, it was the lack of sustainability. It did not place the ultimate responsibility for urban mosquito control where it belongs: with the citizens of the community. Instead of learning to accept responsibility for their own health destiny, people became dependent upon the government for this service. The result is an entire generation which blames government for a disease which exists, in part at least, because citizens refuse to participate in larval source reduction practices in the immediate vicinity of their home. Of course, government help will be required, especially in those areas where water is stored for domestic use, but there are inexpensive and easy ways to reduce mosquito populations in these containers.

Thus, we finally come to an explanation of the title of my presentation. "Top down" refers to the Soper approach of a paramilitary, vertically-structured, mosquito control program. As I noted above, we lack the resources and political discipline to implement and maintain such programs in the 1990s and beyond. Moreover, it is now clear that the only long-term, cost-effective approach to mosquito control is to convince the people who live in the homes where most transmission occurs to help the government control the mosquito vector. Thus the term "bottom up," which refers to a community-based approach to mosquito control by source reduction. To be successful in the 1990s and beyond, we must have the assistance of the people who unwittingly create the problem.

There is considerable disagreement among mosquito control specialists as to which of these approaches to use. The obvious advantage of the Soper "top down" approach is that we know it works. (15) If implemented properly, it insures complete coverage of an area, leading to rapid success and even eradication. Obvious disadvantages are that it is very expensive and that it has no long-term effect because it is not properly directed. Once the goal of control or eradication is achieved, government agencies are reluctant to continue financial support for "top down" mosquito control programs. The result, as I have already noted, was reinvasion of the Americas by Ae. aegypti, followed by large epidemics of dengue and the emergence of DHF. The current distribution of Ae. aegypti in the Americas, therefore, is a painful reminder that the "top down" approach has no lasting effect.

The community-based "bottom up" approach to mosquito control has the advantage of being the most cost-effective over the long-term. Moreover, by educating citizens of the community to be more responsible for their own health destiny, we are insuring that mosquito control programs will have a lasting impact. The major disadvantage of the community-based approach to controlling Ae. aegypti is that it is slow, and may take many years before human behavior is modified enough to impact on disease transmission. Moreover, this approach will probably never lead to eradication of the species.

In 1984, we developed a new program to prevent epidemic dengue/DHF in Puerto Rico. The approach was based on the following observations that I and others have made on surveillance and mosquito control activities while investigating epidemics of dengue. First, surveillance systems, which depend upon the medical community to report cases of dengue-like illness to health authorities, are very unreliable and insensitive. During interepidemic periods, dengue is seldom reported even though endemic transmission may persist, and epidemics are seldom detected before peak transmission is reached. By contrast, after an outbreak has been confirmed and reported, there is gross over reporting of dengue cases. Thus, routine surveillance as practiced by health ministries in most dengue endemic countries is reactive and does not have any early warning, predictive value for epidemic dengue. Unfortunately, most health agencies are crisis oriented, and while they may advocate prevention, few of them practice preventive measures.

Second, Ae. aegypti control as currently practiced by most health ministries has little or no impact on dengue transmission. Moreover, insensitive surveillance insures that emergency measures are usually implemented after epidemic transmission has already peaked. Finally, there has been a dependency on ULV, which, as I noted above, does not work very well. The increased frequency of and larger epidemics of dengue in most endemic countries of the tropics in the past 15 years underscores the lack of efficacy of ULV for prevention and control of epidemic dengue. Puerto Rico is a classic example. In the first 50 years of this century, the island experienced only 2 dengue epidemics, in 1915 and 1945. (8) In the next 15 years (1950-1975), 3 epidemics occurred (1963, 1969, and 1975), and in the last 11 years ( 1977-1988) there have been 7 epidemics (1977, 1978, 1981, 1982, 1986, 1987, and 1988) caused by all 4 dengue serotypes. During this same period, beginning in 1977 ULV malathion applied from truck-mounted units became the method of choice of Ae. aegypti control in Puerto Rico. The lack of efficacy of ULV applied toxicants is further compounded in Puerto Rico and many other countries by providing a false sense of security to citizens of the affected community, and reinforcing their belief that mosquito control is the government's responsibility. The result is that when increased dengue transmission is reported in Puerto Rico, citizens inundate the health department with calls to fumigate their neighborhood rather than discarding or cleaning potential larval habitats in and around their own home.

Our program in Puerto Rico is based on the rationale that we may have to live with a little dengue, but not with DHF. Thus the emphasis is on disease prevention rather than mosquito control. The program has 5 main components. The first is to develop a more effective, proactive surveillance system that will provide an early warning, predictive capability for epidemic dengue. Thus, if you can predict epidemics, you should be able to prevent them, or at least decrease the overall incidence of disease. Closely tied to improved surveillance is a second component of the program to develop a rapid-response, emergency vector control unit that can immediately respond to the surveillance data and prevent the spread of an incipient epidemic. By reducing the magnitude of epidemics, we reduce the probability of severe and fatal disease. Unfortunately, as I have already noted several times, our principal emergency mosquito control measure, ULV, is not very effective. We are working hard to develop an integrated approach that can be used in an emergency situation.

A third component is a contingency plan to hospitalize large numbers of people in case we have an epidemic of DHF before our prevention and control programs are effectively implemented. Early DHF epidemics in Southeast Asia taught us that an apathetic and uninformed medical community can lead to high fatality rates during an epidemic. We also learned from the Cuban experience that mortality can be minimized by placing potential DHF patients on fluid replacement therapy during the critical stage of illness.

The need for expensive hospitalization can be reduced, however, if physicians understand the basic pathophysiologic changes that occur in DHF. A fourth component, therefore, is education of the medical community. We want to increase their awareness of the disease and to teach them how to diagnose and manage DHF. This will help keep mortality rates low. Because physicians are among the most respected members of a community whose instructions are usually followed by their patients, we are also enlisting their help in educating the people of Puerto Rico on methods of prevention and control.

The fifth and most important component of our program, is to develop a long-term, community-based, integrated Ae. aegypti control program in Puerto Rico and the U.S. Virgin Islands. The objective is to change the public's perception about dengue and make them understand that it is an important and potentially fatal disease. We want them to understand that most transmission occurs in and around the home by a mosquito that is there because of their bad habits, that the disease can be prevented, but that the ultimate responsibility for prevention and control must be theirs, not the government's. Finally, the community must be motivated to accept that responsibility. In the long run, it is this "bottom up" approach that will be responsible for preventing epidemic DHF.

An important component of a community-based program is education. We must learn to communicate with lay persons if we hope to convince them to help us control the disease. Anyone who has worked in health education soon realizes that we do not know how to communicate effectively with all segments of society. We therefore contracted a medical anthropologist to help us identify the different ethnographic segments of the population in Puerto Rico, and to advise us on how to devise more effective methods of communication that would motivate members of the different communities to help us. Although the data are still being analyzed, we have already used some of the ideas. For example, a segment on DHF was written into a local television "novella" or "soap opera." Because of the popularity of the novella in Puerto Rico, this is potentially a very powerful educational tool. This and other ideas have convinced me that we must use social scientists to identify different community groups and to help us develop educational materials that are targeted specifically at those groups.

Our program in Puerto Rico has been developed on the assumption that if we are to succeed, we must leave no stone unturned. Every segment of society must become involved and accept appropriate responsibility. This includes federal, state or provincial and local government agencies, business groups, civic organizations, youth, community, religious, and medical groups. Thus, everyone in the community must share the responsibility for control of Ae. aegypti.

A complete description of our program in Puerto Rico is beyond the scope of this paper. However, we are working with many of the above organizations, and have projects with the public school system, Boy Scouts, Head Start, Project Hope, various religious groups, and a number of community and civic organizations. The most important group we have recruited is Rotary International. Rotarians are generally the most prominent business and civic leaders in the community. More importantly, Rotary exists to provide service to the community. Properly mobilized and directed, this organization can provide desperately needed expertise and resources to government health agencies.

Many information research/survey organizations are either managed by Rotarians or provide services to companies managed by Rotarians. They advise client companies on how to influence people to purchase their products. This tremendous resource can and should be utilized in public health education. Rotarians are also involved with the mass media, many of whom are anxious to help us get our message to the community. The San Juan Rotary Club and Rotary International, either directly or indirectly, has financed most of the educational materials for our program in Puerto Rico. Moreover, because of their influential positions in the community, Rotarians have provided the stimulus that has motivated reluctant members of both the private and public sectors to become involved in dengue prevention and control. More than any other organization or group, Rotary involvement has made our program in Puerto Rico truly community-based.

We have made progress in that we have changed the way people perceive dengue as a disease problem. The majority of people (>70%) in Puerto Rico now perceive dengue as an important disease. More dramatic, however, is that the percentage of people surveyed who think dengue is a controllable disease has increased from 4.6% when we started this campaign in November 1985 to 73% today. In the future, we hope to refine our messages for different segments of society and optimize our limited resources. That is the good news.

The bad news is that we have not yet been able to change the behavior, and thus motivate people in Puerto Rico to help us clean up the community to the point where mosquito densities are low enough to prevent epidemic dengue transmission. And that is why this approach is so frustrating. Even after repeated instruction and demonstration, both citizens and government officials continue to rely on aerial toxicants to control mosquitoes. We are dealing with a generation that has been raised to believe that the government can do it better. We are not naive enough to believe, therefore, that behavior modification will be either easy or rapid. It may, in fact, take a major epidemic of DHF to motivate this behavioral change. If it does occur, however, we will have laid the foundation to take advantage of such an unfortunate event. We know that it will take many years to achieve our goal, but we also know that if we are successful, epidemic dengue and DHF will not be a major problem in the future. The important thing is that we get started now. We cannot wait. Otherwise we will probably still be talking about it when large epidemics of the disease become widespread in the American region.

An exciting recent development has been the renewed interest by the Rockefeller Foundation and their recognition of the urgent need to revitalize Ae. aegypti control programs in dengue endemic countries. It is encouraging that this organization, which began and supported the Soper "top down" approach nearly 50 years ago, has now seen fit to re-enter the field supporting a community-based "bottom up" approach. Rockefeller involvement may be critical if we hope to prevent DHF from becoming a major public health problem in the Americas.

This new initiative will be a collaborative effort between the Rockefeller Foundation; the Johns Hopkins University School of Hygiene and Public Health; the Centers for Disease Control, Dengue Branch; and Ministries of Health in dengue endemic countries. One of our goals is to elevate the status of mosquito control programs in endemic countries and make Ae. aegypti control a respectable occupation again, like it was in the days of Fred Soper. We look to the Rockefeller program to help us solve the current manpower crisis by helping attract bright, imaginative, young professionals. We desperately need better people in the field of Ae. aegypti control.

The plan is to carefully select teams of professionals from each country and provide them with the best academic and field training available to prepare them for the challenge of developing disease prevention programs in their home country. Teams will consist of 4 professionals and several operational staff. The former will include an entomologist who will also act as project director, an epidemiologist, a social scientist, and a health program manager. These individuals will attend the Johns Hopkins University for 1 year of academic training in entomology, epidemiology, and social sciences. They will then transfer to Puerto Rico for 1 year, where training will emphasize hands on experience in developing a community-based, integrated Ae. aegypti control program using our program as a model. During this time, social scientists, epidemiologists, and entomologists from the Centers for Disease Control, Johns Hopkins, and other universities will be working together with the country teams in Puerto Rico as well as their home country to develop more effective methods of controlling mosquitoes through community participation. The objective is to develop programs based on the unique socio-cultural conditions of each country.

This program has already been initiated as a pilot, and students selected from Mexico and Honduras are currently enrolled at the Johns Hopkins University. If all goes as expected, other countries will be enrolled in the program in subsequent years. Emphasis will be given to American countries during the initial phase, but ultimately Asian countries will also be involved. Over a period of years, it is expected that highly motivated teams will begin programs in many dengue endemic countries. Obviously, we will need other sources of funding besides the Rockefeller Foundation. We believe that by developing high quality programs that use hard scientific criteria for evaluation, we can attract other international funding agencies to join in providing financial support for this program.

To summarize, dengue is a rapidly expanding disease problem. Epidemics worldwide have become larger and more frequent. Incidence of the severe and fatal form of disease, DHF, has increased dramatically in Asia in recent years and has moved into the Americas. Two factors are primarily responsible for this change in epidemiology: increased air travel and a total lack of effective mosquito control in tropical urban centers.

The only option we have to prevent the dengue problem from becoming progressively worse is to reduce incidence of disease, and the only way to achieve that is to control Ae. aegypti. Unfortunately, the conventional methods that have been used over the past 20 years are not very effective. Thus, we have a very real crisis on our hands.

New leaders are urgently required. Moreover, we must educate health planners, most of whom have little or no knowledge of or interest in vector-borne diseases other than malaria, but who determine where and on what diseases the health dollars are to be spent.

If Soper were alive today, he would be very disappointed at the reinvasion of Central and South America by Ae. aegypti, and he would be alarmed at the nonchalant way that health authorities accept the appearance of DHF at their door step. I am equally confident that having seen what has happened in the region in the past 15 years, he would also agree that new approaches are required.

History has taught us that the "top down" approach to Ae. aegypti control has no lasting impact after government support is withdrawn. The "bottom up" approach, on the other hand, is very slow and may take years before results are observed. It is my opinion, therefore, that neither a "top down" nor a "bottom up" approach alone is ideal for controlling Ae. aegypti-borne diseases in the 1990s. What we urgently need today are integrated control strategies that utilize the best of both approaches in the initial phase, with more emphasis directed to the community-based approach as the program progresses. This should insure relatively rapid success, but also that the programs will be sustainable, and that the next generation will understand and, hopefully, accept its responsibility to help maintain Ae. aegypti control in the community. Citizens of each community must be given more responsibility for their own health destiny.

Author's address: Dengue Branch, San Juan Laboratories, Division of Vector-Borne Viral Diseases, Center for Infectious Diseases, Centers for Disease Control, Public Health Service, U.S. Department of Health and Human Services, G.P.O. Box 4532, San Juan, PR 00936.

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Forty-ninth Charles Franklin Craig Lecture delivered before the American Society of Tropical Medicine and Hygiene. Washington. DC. 7 December 1988.

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REFERENCES

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  3. Halstead SB, 1980. Dengue haemorrhagic fever -- a public health problem and a field for research. Bull WHO 58:1-21. UI:80200204
  4. Rosen L, 1982. Dengue -- an overview. Viral diseases in Southeast Asia and the Western Pacific. Australia: Academic Press, 484-493.
  5. Gubler DJ, 1988. The arboviruses: epidemiology and ecology. Monath TP, ed. Dengue, vol. 2. Boca Raton. IL: CRC Press Inc. 223-260.
  6. Gubler DJ, 1988. The global problem of dengue and dengue hemorrhagic fever. Virus Info Exchange News 5:46-47.
  7. Sencer DJ, 1969. Health protection in a shrinking world. Am J Trop Med Hyg 18:341-345. UI:69182760
  8. Gubler DJ, 1989. Dengue and dengue hemorrhagic fever in the Americas. Thongcharoen P, ed. Dengue hemorrhagic fever. New Delhi, India: WHO Monograph (in press).
  9. World Health Organization, 1986. Dengue hemorrhagic fever: diagnosis, treatment and control. Geneva, Switzerland: World Health Organization.
  10. Bang YH, Shah NK, 1987. Review of DHF situation and control of Aedes aegypti in southeast Asia. Dengue News 13:1-5.
  11. Guzman MG, Kouri GP, Bravo J, Soler M, Vazquez S, Santos M, Villaescusa R, Basanta P, Indan G, Ballester JM, 1984. Dengue haemorrhagic fever in Cuba. II. Clinical investigations. Trans R Soc Trop Med Hyg 78:239-241. UI:84275494
  12. Halstead SB, 1988. Pathogenesis of dengue: challenges to molecular biology. Science 239:476-481. UI:88127093
  13. Rosen L, 1986 Oct 11. The pathogenesis of dengue haemorrhagic fever. A critical appraisal of current hypothesis. S Afr Med J Suppl:38-42. UI:87043124
  14. Lofgren CS, 1970. Ultralow volume applications of concentrated insecticides in medical and veterinary entomology. Annu Rev Entotmol 15:321-342. UI:70108844
  15. Soper FL, 1963. The elimination of urban yellow fever in the Americas through the eradication of Aedes aegypti. Am J Pub Hlth 53:7-16.

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