Hand Hygiene Interventions Need Some Cleaning Up: A Critique of Current Hand Hygiene Program’s in Hospitals Nationwide - Emily Scheer

Hospital acquired infections (also known as nosocomial infections) are a well documented cause of increased morbidity and mortality among hospitalized patients in the United States. Nearly 2 million patients are affected and almost 80,000 individuals die each year as a result of acquiring such infections making this a serious public health issue in the United States (4). Given the severity of this issue, successful public health interventions are necessary to halt the spread of disease.
Hand hygiene has been identified as an essential evidence based infection control measure to prevent the occurrence of hospital acquired infections, “Hand hygiene by hand washing or hand disinfection remains the single most important measure to prevent nosocomial infections” (9). Nonetheless, hand hygiene policies are not always followed by health care workers and poor compliance is repeatedly documented throughout entire hospitals and hospital systems nationwide. Some interventions have proven successful. However, success has been short lived. Hand hygiene programs in the United States have had difficulty achieving lasting improvement (4). If hand hygiene interventions fail to incorporate a multidimensional approach to behavior change, social norms and self efficacy, and continue to be unsuccessful in effectively educating health care workers, successful hand hygiene programs cannot be sustained.
Lack of an Interconnected Approach to Behavior Change

What many widespread hand hygiene interventions are missing is a multi faceted and creative design to change health behavior (4). Interventions aimed at improving compliance with hand hygiene must be based on the various levels of behavior interaction including the interdependence of individual factors, environmental constraints such as access to hand washing supplies at point of care, knowledge and values that are inherent to the many medical specialties, and institutional culture. Noncompliance with hand hygiene interventions may not only relate to the individual health care worker but to the group or specialty he/ she belongs to.
The complex dynamic of behavioral change involves a combination of education, motivation, and system change that acknowledges social norms and self efficacy. Hand hygiene interventions have traditionally followed the framework of the popular and frequently utilized model of health behavior, the Health Belief Model (3). This model focuses on behavior change at the individual level. It is limited in that it does not look at change in a group context nor does it account for social and environmental factors. Time after time, hand hygiene guidelines focus on the individual and fail to incorporate aspects of the complicated environment that the typical health care worker is in. Many risk factors for non-compliance with hand washing among health care workers are continuously faced including increased workload, stress, lack of time, psychology, the culture of the environment or unit of the hospital, individual values as well as values inherent to certain medical specialties, availability and access to hand washing materials, type and intensity of patient care required, nurse to patients ratios, and education as to what the correct hand-hygiene techniques are (9). Compliance with recommended instructions is commonly poor because hand hygiene models have failed to consider and account for these complex risk factors. Hand hygiene interventions have primarily focused on the individual which is not enough to result in sustainable change (7).
Failure to Establish a Culture of Safety that Incorporates Social Norms and Self Efficacy
Traditional hand hygiene interventions have failed to consider social norms in development of policies. In health care, as in many other environments, behavior will be influenced according to whether or not a person will meet approval or disapproval by his/her social groups, or in this case among the various medical specialties (nursing, physicians, respiratory, etc) (3). For example, if the intervention is driven by the nursing department, a physician may be less likely to comply because his/her group did not “buy in” to the program. The physician-in-chief did not support the program or feel that it was necessary and this attitude and belief trickled down to the rest of the physicians. Hand hygiene interventions must incorporate social norms and above all aim to make compliance the social norm among all medical specialties.
An additional limitation of current hand hygiene programs is the lack of incorporation of self efficacy. Staff must believe that they have the ability and power to make major improvements and that hand washing will lead to these big improvements. Health care workers must be empowered to remind other caregivers, regardless of rank, position, or specialty to practice hand hygiene and comply with all guidelines (4).

Failure to Educate and Communicate
A key element in implementing a successful hand hygiene program is educating and motivating the staff. Unfortunately, hand hygiene interventions based on the Health Belief Model assume that all health care workers have enough education and knowledge to make a rational decision surrounding hand washing. In reality, there is an overall lack of knowledge among health care workers regarding how hands are easily contaminated, how infection is spread, the efficacy of hand hygiene in reducing this spread, and lack of awareness of the recommended and most effective hand-washing techniques (8). The Centers for Disease Control and Prevention’s Healthcare Infection Control Practices Advisory Committee published Guideline for Hand Hygiene in Health-Care Settings in 2002. Within these guidelines, it strongly recommended that alcohol-based hand rubs are the preferred method of hand hygiene because they are easy and quick to use and are extremely effective in killing bacteria and viruses that cause nosocomial infections. Introduction of alcohol-based hand rubs and education materials must be introduced as a part of hand hygiene programs and spread at a group level. Hospital employees need to be able to express knowledge and understanding that alcohol based hand rubs are extremely effective, are accessible, and are very quick and easy to use. Current hand hygiene programs have failed to ensure that staff entirely comprehend the rationale behind implementing hand hygiene programs. They are not designed in a way that results in high levels of staff “buy in” and high staff comprehension of the danger of not complying with the policies, not only to their patients but to themselves (2).
When asked, health care workers report the following reasons that they believe make it difficult to comply with hand hygiene programs: skin irritation caused by constant washing or use of the disinfectant rubs, “being too busy”, and “not thinking about it” (9). Health care workers must be educated that alcohol-based hand rubs have advantages to traditional hand washing because they require less time, are extremely fast acting and effective in preventing transmission of infection, and are less irritating to the skin. Studies have found that alcohol based hand rubs do contribute to the sustainability of high program compliance rates and are associated with decreased infection rates (7).
The Future of Hand Hygiene
Traditional hand hygiene programs may be successful short –term in some hospitals as an effective way to reduce hospital acquired infection rates but this intervention is not likely to be both effective and sustained for long periods of time. A more appropriate hand hygiene intervention would focus on health care worker’s behavior at the group level. Hand hygiene programs must be further developed to move beyond a model that focuses on individual behavior and include more psychosocial elements that will influence intention, attitude toward the behavior, perceived social norms, perceived risk of infection for self and patient, habits of hand hygiene practices, knowledge, and motivation at both the individual and group level. (7) Interventions must grow to incorporate a multidimensional approach to behavior change, social norms and self efficacy, and figure out how to effectively educate health care worker. Until then, morbidity and mortality due to hospital acquired infections will remain high in hospitals across the United States. Hand hygiene interventions must be changed so that quality of life can be improved for millions of patients in this nation’s health care system.
Hand Hygiene Programs in the United States: All Cleaned Up!
An unfortunate reality for the current health care system in the United States is that the prevalence of drug-resistant organisms in nosocomial infections is high and continues to be on the rise. The impact that this has on patient outcomes is incredibly severe. In light of all of this, it is well documented that prevention is possible. The key intervention suggested and supported by endless evidence is surprising in that it seems so simple. It is something that many of us were taught to do regularly since we were fairly young – wash our hands (7)! Although evidence based, proven important, and simple sounding, “hand hygiene by hand washing or hand disinfection remains the single most important measure to prevent nosocomial infections,” (9) hand hygiene interventions have been complicated and difficult to implement and sustain. Experts estimate that health care workers comply with recommended hand hygiene procedures less than 50 percent of the time — contributing to some terrible consequences (7).
Due to increased morbidity, mortality, and health costs that can result from health care workers failing to comply with hand hygiene protocols, this has become a major public health problem in the United States. Clearly, it is an issue that is worth working on and devoting substantial resources to. An alternative program must be implemented nationwide that moves away from policies based on the traditional health behavior models. A new program should incorporate an interconnected approach (specifically dealing with the health care environment and access issues), social norms, messages of empowerment and self efficacy, and improved education and communication of vital information.
Incorporating an Interconnected Approach to Behavior Change
An improved hand hygiene model should concentrate on taking an interconnected approach to improving compliance with hand hygiene programs. Unfortunately, many current hand hygiene programs currently take an “x causes y” approach to forming new policies and dealing with the issue. This type of approach does not deal with the “messiness of life.” Major risk factors for poor compliance with standard policies include lack of time or opportunity and poor access to hand washing facilities (7). These risk factors move beyond individual behavior and indicate that there are many external factors that can make behavior and life “messy” at times. This indicates that to implement a sustainable program these factors in the environment of the health care worker must be acknowledged.
In an ICU setting there is high workload and high demand of care. To improve access, opportunity, and deal with time constraints, the main hand hygiene agent promoted should be an alcohol based hand rub because it is quick to use, easy to access, and highly effective. Here, a focus study should be done with staff that examines various locations of the gel dispensers to ensure best possible access. The dispensers should be trialed at different locations at the bedside to determine where they are most easily accessed and most often remembered and used. Another proposal to improve access is to look at where health practitioners already keep items and information they want to have immediate access to. For example, many physicians keep tools the need to use in their white coat pockets such as patient notes, calculators, blackberries, etc. Leading alcohol based hand rub manufacturers have developed smaller and slightly flatter bottles. These could easily be stored in physician’s pockets without getting in the way. This would make hand hygiene available right at his/her hip in a location that is easy to remember and already part of their culture and behavior.
Establishing a Culture of Safety that Incorporates Social Norms and Self Efficacy
One major critique of current hand hygiene interventions is that they have traditionally followed the framework of the popular Health Belief Model (3). As mentioned previously, this model focuses on behavior change at the individual level instead of in a group context. It does not account for social and environmental factors. A hand hygiene program that changes focus to an alternative health behavior model that values and emphasizes social norms, such as Social Norms Theory, would prove to be a more successful and sustainable intervention. Social norms theory states that the behavior of an individual is greatly influenced by the way they perceive behavior of his/her social group (1). In the health care environment, if the worker views his/her medical specialty as being non-compliant with hand hygiene interventions, the urge that individual may feel to conform to that idea will negatively impact the compliance behavior of that entire group or specialty. However, if the various health care groups are educated effectively and hand hygiene is framed in ways that portray it as the norm and supported practice of the group, there may be more overall “buy in” to the program which would result in an overall higher compliance rate for the specialty group as well as the entire unit. Parallel to that, nosocomial infection rates and associated health costs would hopefully decrease.
Developing a culture of empowerment would help to foster compliance and change the social norm. There is an inherent hierarchy in the medical setting among the various specialties. Work should be done to eliminate this hierarchal structure and ensure that, for examples doctors and nurses feel that they are on the same level and have the same worth in influencing care of their patient. The feeling of empowerment developed by each group would trickle down to the individual and help him/her to be an advocate for a patient’s safety by kindly reminding his/her colleague to comply with hand hygiene policies. Hand hygiene is something that has to be practiced at every opportunity in order to get positive results. Therefore, self efficacy is an important component to any hand hygiene program. If health care workers believe that they have the ability and power to make major improvements by completing the simple task of washing hands per policy, compliance rates may rise. The action must be promoted as one small piece of a giant puzzle that makes up this major improvement.
Implementing Widespread Education and Communication
Many current hand hygiene programs have incorporated some type of education about hand hygiene through poster display or leaving pamphlets in staff mailboxes. However, merely making the poster is not an improvement and it is not adequate education and information. Instead, all efforts must be focused on placement and use of the poster. Posters should be informative, captivating, and placed in locations where they will not be missed (on the door to the unit, at the front desk, in the bathrooms, etc). Focus group should be formed by quality improvement staff and surveyed to assess whether or not people report noticing it, whether staff can answer questions about the material on the poster, and to ask people directly whether they believe it worked or not. The poster can be tested in various locations of visibility on the unit. Once the most ideal location is decided upon based on focus group feedback, information should be changed in and out on a regular basis to update, inform, and reeducate staff. To enhance communication, improvement leaders should make sure that data and audit results are disseminated to staff and posted where it can be seen. In many widespread surveys, health care workers report that they don’t see the numbers or results they just get the order to “do better” and this does not make them happy. Health care workers need to be made aware that hands need washing in certain situations. They should be educated on the specific definitions of hand hygiene “opportunities”, what supplies are available to them, and the location of such supplies. A hand hygiene program should identify and educate a few “champions” from each medical specialty who will go through training and evidence based education sessions. Each champion would be responsible for educating his/her appropriate group and advocating for change (5).
Education and communication also goes beyond the health care practitioners. A successful hand hygiene program should have a patient and visitor component, as well. A patient/visitor educational brochure and program should be developed that includes an orientation to the unit’s policies on hand hygiene and the negative outcomes that can occur as a result of failed compliance by health care workers. This will ensure that patients and families are aware and empower and encourage them to remind health care workers to wash their hands when caring for the patient (5).
Future
It is clear that a hand hygiene intervention that focuses on health care worker’s behavior at the group level will be successful and sustainable. Hand hygiene programs must move beyond a model that focuses on individual behavior and acknowledge that noncompliance with hand hygiene interventions may not only relate to the individual health care worker but to the environment and group or specialty he/ she belongs to. Therefore, a proposal to improve hand hygiene must incorporate the main attributes of social norms theory in order to make effective and sustainable change within hospital systems in the United States. It must also focus on access and environmental issues and utilize innovative education techniques. Overall, hand hygiene program designers and implementation managers must truly try to understand what really motivates people, specifically the medical staff in question, and work to gain better understanding of human behavior.
References:
1. Best Practices; Social Norms. http://wch.uhs.wisc.edu/13Eval/Tools/Resources/Social%20Norms.pdf
2. Boyce JM, Pittet D, et al. Guideline for Hand Hygiene in Health-Care Settings: Recommendations of the Healthcare Infection Control Practices Advisory Committee and the HICPAC/SHEA/APIC/IDSA Hand Hygiene Task Force. Morbidity Mortality Weekly Report, 2002.

3. Edberg, Mark. Essentials of Health Behavior: Social and Behavioral Theory in Public Health. Sudbury, MA: Jones and Bartlett Publishers, 2007.

4. How-to Guide: Improving Hand Hygiene. Institute for Healthcare Improvement. 2006. http://www.ihi.org/NR/rdonlyres/E12206F9-6A81-4520-B92F-4BCB844133C2/3266/HandHygieneHowtoGuide1.pdf

5. Institute of Health Care Improvement. Improving Hand Hygiene Practice with Six Sigma. St. Paul, MN: HealthEast Care System. http://www.ihi.org/IHI/Topics/PatientSafety/SafetyGeneral/ImprovementStories/ImprovingHandHygienePracticewithSixSigma.htm
6. Institute of Health Care Improvement. The Sound of Two Hands Washing: Improving Hand Hygiene. http://www.ihi.org/IHI/Topics/CriticalCare/IntensiveCare/ImprovementStories/FSSoundofTwoHandsWashing.htm
7. Pittet, D. Improving Adherence to Hand Hygiene Practice: A Multidisciplinary Approach. Emerging Infectious Diseases 2001.

8. Pittet D, Boyce JM. Hand hygiene and patient care: Pursuing the Semmelweis legacy. Lancet Infect Dis 2001.

9. Pittet D, et al. Effectiveness of a hospital-wide programme to improve compliance with hand hygiene. The Lancet 2000.
10. WHO Guidelines on Hand Hygiene in Health Care (Advanced Draft): A Summary. World Health Organization, 2005. http://www.who.int/patientsafety/events/05/HH_en.pdf

The Failure of Current Antimicrobial Resistance Campaigns to Affect a Wider Population – Lynn Tran

Introduction

Antimicrobial resistance has been a persistent public health problem in recent years. As the development of antimicrobial agents evolve to allow for effective treatment of bacterial ailments, there has also been an evolution of misuse that has given opportunities for microorganisms to form a resistance, rendering the treatment ineffective. Medical advancement to develop new antibiotics cannot keep up with the rise of resistant bacterial strains, posing a significant issue to finding and maintaining effective treatments for bacterial illnesses.

Several reasons have been posed as to why antimicrobial resistance has been so difficult to address, many of which rely heavily on perceptions on how antibiotics should be prescribed and subsequently used. While these perceptions provide valuable insight into how people are contributing to this problem, they have been commonly misapplied in public health campaigns. The failure of current antimicrobial resistance campaigns will be addressed in the context of how relying on interventions based on individual and biomedical beliefs overlook higher level social factors that are more appropriate to address a larger audience.

The Reliance on the Health Belief Model and Other Individual Level Theories

A number of attempts aimed to reduce the development of antimicrobial resistance have relied on components of individual level theories. The most prevalent of these theories is the Health Belief Model (HBM). This model is comprised of four factors: perceived susceptibility, perceived severity, perceived benefits of action, and perceived barriers to taking that action (1). From these perceptions, the individual identifies his/her intentions to perform the behavior. The hallmark of the HBM is its assumption of rationality; that is, given a set of perceptions that has high benefits and minimal barriers, the individual would be expected to enact on this behavior.

While the HBM is among the most widely used theory for developing public health interventions, it is not always the most effective in reaching the general population. As will be demonstrated in the ensuing paragraphs, people often do not act rationally and that intention does not always translate into behavior.

In a study conducted by the UK Department of Health (DH) Standing Medical Advisory Committee on Antimicrobial Resistance (SMAC), the perception and attitude of the public towards antibiotics was assessed. The results of the household survey rejected the notion that people acted rationally, given that the majority were quite knowledgeable on the topic of antibiotics (2).

Overall, it was found that patients believed that antibiotics aided their recovery process and sought medical counsel for them and physicians were compelled to prescribe antibiotics due to the perception they had that patients wanted them. The DH-SMAC determined that it was necessary to break these perceptions by both patients and physicians in order to control the misuse of antibiotics (2). In this sense, the DH-SMAC modeled its study on the HBM by identifying the perceived susceptibility and perceived severity of the patients (i.e. patients’ perception that not having antibiotics would leave them susceptible to prolonged sickness or increased severity of sickness), coupled with the perceived barrier of not receiving antibiotics to outweigh perceived benefits (i.e. the decrease of antimicrobial resistance in the community).

The DH-SMAC, despite acknowledging that people were not acting rationally, added various caveats as to why this may have happened to essentially justify the place of the HBM as an effective model. First, McNulty et al. claimed that the number of survey respondents (of which there were over 7,000 people) were not sufficient enough to declare irrationality about antibiotic use. However, note that the survey identified 11.3% of respondents who did not finish their last antibiotic course as prescribed (with incomplete antibiotic courses being a factor in the development of antimicrobial resistance), with 87% of these respondents also saying that a course of antibiotic should always be completed (2). This suggests irrationality and that intention does not always lead to behavior, which the HBM assumes will occur. Instead of addressing this irrationality, the authors chose to counter that not enough people were assessed to make such an assumption.

Secondly, the authors claimed that the reason intention did not translate into behavior is that penetration of the current public health campaign was poor. The DH-SMAC had developed a program named the Andybiotic Campaign, where an animated character named Andybiotic introduced topics of the sensible use of antibiotics. Only 20% of English respondents and 25% of respondents prescribed antibiotics in the past year had seen or heard of the campaign. McNulty et al. suggested that with better funding and prolonged exposure, the campaign would have had a greater impact (2). However, they neglect to admit that the entire premise of the campaign was to inform the public on how to sensibly use antibiotics to influence their behavior, which from the survey results, it appears that most people actually are aware but they simply are not acting. Thus, the campaign fails to change behavior, but relies on the concepts of the HBM to change individual perceptions in hopes that it will lead to a change.

To build on the concept set forth in the HBM, the Theory of Planned Behavior (TPB), which is based also on the idea that people act rationally, takes into account a person’s attitude towards a behavior and the person’s perception of social norms associated with this behavior (1). The TPB is also a commonly used model in public health and shares similar flaws seen with the HBM.

As briefly mentioned earlier, when patients do not complete the antibiotic course prescribed, they are aiding in antimicrobial resistance by allowing for these resistant traits to be selected and transferred to other bacteria to render the antibiotic ineffective. In a study by Jackson et al. based on the TPB, intentions were evaluated to determine whether a person would implement a particular behavior. The authors of this study focused on the element of perceived behavioral control as a potential aspect of the TPB to help develop interventions against antimicrobial resistance (3). Perceived behavioral control refers to the degree in which a person believes that they have control over a certain behavior and relies on two concepts, control beliefs and perceived power, of which would prompt an individual to change his/her behavior (1). To address this, they allowed participants the option of implementing their own plan, phrased on the questionnaire as, “You are more likely to carry out your intention to take these antibiotics as prescribed if you make a decision about when and where you will do so. Decide now when and where you will take these antibiotics. You may find it useful to take a tablet before or after something else that you do regularly, such as brushing your teeth in the morning in the bathroom. We now need to decide when and where you will take each dose of antibiotics.” (3, p.214) Unfortunately, even by empowering participants to develop their own implementation plan, there was no significance between implementation groups. Again, as with the McNulty et al. study, these authors rationalized their results, citing that perhaps students were not representative of the groups of people that need to take prescribed medicines and the good adherence seen by the control group was due to the fact that they knew that someone would follow up with participants at the end of the antibiotic course (3).

Both the McNulty et al. and Jackson et al. studies exemplify a common theme seen with campaigns using individual level theories: the need to rationalize flaws or failures instead of accepting them and find ways to improve rather than adapt to the model. Jane Ogden critically reviewed these individual level theories and came to a very similar conclusion, that researchers often claim that their models are useful, but always preface this statement with some caveats. Mainly, Ogden found that researchers often cited that perhaps the wrong variables were used in the model, certain sample characteristics explained the results (e.g. how Jackson et al. cited students as not a representative group), or simply that their model needs to be extended (4).

This is not meant to entirely discount the HBM and TPB as useless models, but to provide awareness that while these models provide an understanding of how a person approaches health, it does not provide an effective framework for how to affect behavioral change in all instances. This is especially true when the flaws of the model are not taken into consideration when developing and improving upon public health interventions.

Basing Interventions on Biomedical Beliefs and Academic Theory

The issues surrounding antimicrobial resistance are inherently medical in nature in regard to how microorganisms are developing these resistance mechanisms. Understanding that adhering to the complete antibiotic course prescribed, avoiding unnecessary antibiotic prescriptions for illnesses not bacterial in nature, and what the difference between bacteria and viruses are is essential to form the foundation for these public health campaigns. Nonetheless, biomedical beliefs and academic theories alone do not automatically translate into behavior change (2-3).

Realizing that antimicrobial resistance and the need to extend the life of antimicrobial drugs are becoming significant dilemmas, the Centers for Disease Control (CDC) has enacted a Public Health Action Plan to Combat Antimicrobial Resistance by an Interagency Task Force on Antimicrobial Resistance. This Interagency Task Force consists of several federal health agencies, but no social science or public health consultants were mentioned as participants. Some areas of focus for this group are ensuring patient adherence to an antibiotic regimen through directly observed therapy and to identify areas where rapid diagnostic tests and consultation are not readily available. The strong biomedical foundation of these antimicrobial resistance interventions ignore non-biomedical barriers to implementation to the public. For example, implementing directly observed therapy to ensure adherence by having a health care worker observe the patient take a dose of medication is unrealistic when taking into consideration cost, access, infrastructure, transportation, and other external factors that would prevent effective implementation (5).

Another popular tool for assessing the effectiveness of antimicrobial resistance interventions is the use of mathematical modeling. The benefits of using mathematical models are that they are cost effective and produce rapid results. And while additional factors can be added to models to address the complexity of the environment in which microorganisms live, it will never be on par with direct, participatory observations in a community. Discrepancies have been identified with the reliance on mathematical models, particularly that these models often have important variables missing and make incorrect assumptions. One of these assumptions is that a community is generally regarded as homogeneous, which it is certainly not. One community can encompass a range of diverse situations that, at the same time, can both promote and reduce antimicrobial resistance and these community traits are not readily transferable to other communities (6).

Part of the reason why interventions are heavily theory based is the historically academic nature of the epidemiological studies of which these interventions are relying on to identify which factors to focus its attention. Carl Shy stated in his commentary on this topic that “epidemiologists have failed to provide the public health community with scientifically tested choices among alternative community actions for promoting health.” (7, p.480). He further elaborates that academic epidemiology has limited itself to a narrow biomedical perspective of disease, neglecting to incorporate upstream factors to understand population behavior (7). These upstream factors oftentimes provide more insight into behavior than academic theory or biomedical concepts can provide, as will be discussed in further detail in the following section.

Neglecting to Acknowledge Societal Factors in Addressing Antimicrobial Resistance

While the emphasis on theory and mathematical modeling has allowed for conceptualizing how different factors may play into devising an effective intervention, it does so at the expense of realizing higher level circumstances that potentially have a larger role in why people are not changing their behavior for the betterment of the public.

To help aid in realizing the implications of understanding societal factors in a group setting, further analysis will be performed on survey results assessing knowledge on antimicrobial resistance. In the household survey conducted by McNulty et al., the issue of left-over antibiotics was addressed. Thirty-one percent of survey respondents indicated that they had kept left-over antibiotics in case they needed them again and 8% in case the same infection occurred. Another survey question had asked if participants agreed with the statement, “A course of antibiotics should always be completed,” of which only 3% of respondents disagreed with. Looking at these survey questions in conjunction, it is evident that people are knowledgeable about the situation, so merely educating the public will not rectify this issue. One must look beyond the facts of the situation to social factors that may be driving why people are saving their left-over antibiotics at the cost of losing efficacy and promoting resistance in the future (2).

A possible explanation is that antibiotics can be costly and if one does not have health insurance, the cost is even greater, so it might drive a person to ration their drug supply to save money. Compound this with the fact that many bacterial illnesses are recurring and that within a family structure, the illness can be readily transmitted from one person to another. Also add to this that once a person feels better, he/she can decide that the treatment is no longer necessary, further rationalizing keeping the antibiotic for future use. So in this instance, current educational campaigns would be rendered ineffectual.

It is necessary to study the characteristics of populations to better affect behavioral change. By looking beyond the immediate causes, as Shy suggested, interventions can communicate a broader perspective instead of the narrow biomedical, individualistic viewpoint expressed today. Regularly, studies are performed where societal context is either completely omitted or superficially mentioned. For instance, the CDC has indicated that antimicrobial resistance will require the assistance of behavioral scientists and health communications experts, but these experts are absent as members of the Interagency Task Force to address this issue. Also, the CDC expressed interest in identifying interventions that are effective in decentralized, heterogeneous environments, but current CDC campaigns are quite homogeneous itself in nature, making it difficult to imagine how it could affect a greater population (5,7).

Another unique aspect of antimicrobial resistance is the increase in global movement and international travel. This has allowed for more rapid emergence of new resistant bacterial strains that not only is easily spread from person to person, but environment to environment. Globalization of trade and increased prevalence of developing countries and their contributions to the market have greatly influenced the proliferation of resistant bacterial microorganisms (8). So, not only should interventions consider societal factors, but global factors also.

An Alternative Approach to Public Health Interventions

Current interventions targeted at reducing antimicrobial resistance have failed due to the pervasiveness of individual level theory based on biomedical beliefs that dominate the field of public health. By ignoring sociocultural factors that drive people to behave the way they do, we are essentially ignoring innovative methods that could be implemented to more profoundly affect behavioral change in the general population. Until we can learn to break from the norm and begin to incorporate more comprehensive methodologies from social sciences, we will always be lacking in truly affecting the public in the campaign against decreasing antimicrobial resistance.

An alternative approach using marketing and social learning theory is proposed in to address some of the inherent flaws seen in current public health campaigns.

An Intervention Aimed at Marketing Antimicrobial Resistance Prevention

Instead of approaching the intervention using conventional public health theories, this proposed intervention draws on theories from marketing and social learning. Posing a general framework for this intervention, several aspects must be addressed to ensure program effectiveness:

1. Identifying the target population and interviewing people within this community to identify how to better market the behavior.

2. Consider the barriers that might exist, within a social context.

3. Identify what aspect of antimicrobial resistance should be marketed, e.g. knowledge of bacteria, outcome of not following through with a prescribed antibiotic regimen.

4. Identify what the type of media is most appropriate to transmit the message.

5. Conceptualize a brand to solidify the message.

6. Putting it all together to aid in people forming new linkages to the behavior where it becomes a social and cultural norm (9-11)

How would this new intervention to antimicrobial resistance address the flaws of current campaigns? This will be discussed in further detail in the following sections.

Addressing the Current Reliance on Individual Level Public Health Theories: How to Address a Message to the Masses vs. Individuals

Relying on how an individual may perceive a situation or why a person acts the way s/he does ignores the fact that they live in an environment affected by others. Individual level factors provide great insight into attitudes and perceptions, but not into how to affect a wider population to change behavior. These individual factors are related to the issue at hand, but do not get to the root of the problem upstream. Instead, the intervention must be aimed at groups of people, whole societies, a culture, essentially to the masses to effect a change.

Theories that take into account societal norms and factors need to be considered instead. Social learning theory provides an excellent framework to base an intervention on; it states that, “how individuals observe other people’s actions and how they come to adopt those patterns of action as personal modes of response to problems, conditions, or events in their own lives.” (11, p.212) By influencing groups of people, others begin to respond to the new behavior and adopt it as their own.

Aspects of marketing theory using these social perceptions can be used to mass market a public health message to a broad population base. The goal is to affect as many people as possible, in a mass, rather than individually. The next question would be, what public health message needs to be addressed? Ideally, there needs to be a connection made between antibiotic usage and the prevention of resistance. People are already well aware of the consequences of improper antibiotic use, so bombarding them with more information would be counterproductive. A review by Evans et al. stressed how potent public health branding can be to change behavior. Branding creates a symbol that is used as a tool to communicate a message to an audience, building a relationship and encouraging execution of the health behavior. There needs to be a creation of a brand for preventing antimicrobial resistance. The effectiveness of branding has been shown in brands such as Nike, but also in public health such as the Truth campaign to stop smoking (10). For antimicrobial resistance, the brand created would communicate the message to foster an understanding of when antibiotics should be used and when how to properly use them, rather than telling the public information such as what the difference between bacteria and viruses are (9-10).

Moving Away from Academic Theory to Create a More Effective Intervention

As mentioned, people are quite knowledgeable about the consequences of improper antibiotic use. However, current interventions are still focused on the transmission of knowledge and information that is already well known. Goossens et al. used as an example how many campaigns tended to emphasize the distinction between viral and bacterial respiratory tract infections. Instead of educating people, this type of information may cause confusion and promote the perception that all bacterial infections must be treated with antibiotics. They suggest that instead, a message to foster an understanding of when antibiotics should be used and encouragement to consult with health professionals would be more effective (9).

Reliance on statistics, scientific theory, and medical theory has its place, but not when speaking to the public in a way to change their behavior. Using the fact that people are not finishing their prescribed antibiotic course, the proposed intervention would look within the social context of why people might be doing this. A possible reason might be that mothers are saving some of the medication for future use for their children due to the high cost of the drugs or because they cannot afford to make frequent visits to their physicians. There are a myriad of other reasons that may not have to do with cost: what is the cultural perception of antibiotics, are people basing the incompletion of their antibiotic course on how they feel, etc. Realizing how health behaviors are motivated by social context is important in developing an effective intervention, rather than relying on statistics and the mechanics behind how bacteria develop into a resistant strain.

Incorporating Knowledge of Societal Influences into an Intervention

As alluded to throughout this discussion, people are greatly influenced by the society in which they live. The norms, culture, and views all play into how people behave. These cannot be neglected, but have been in traditional public health campaigns. People make deliberate choices in adopting certain behaviors and this must be taken into account when developing an intervention. More importantly, people make these choices based on language and symbols.³ This is why branding of the antimicrobial resistance message is essential to the intervention. DeFleur et al. cites Bandura, when he states that “through verbal an imagined symbols people process and preserve experiences in representational forms that serve as guides for future behaviors.” (11, p.215)

Once the brand and message are created, it needs to be communicated. Typically, antimicrobial resistance campaigns have been distributed in print media. A more effective medium to use would be television advertising, which proved to be successful in France and Belgium antimicrobial resistance campaigns (9). Visual symbolism is very powerful, and can be easily used to convey the importance of proper antibiotic use. For example, imagery involving children would be very effective. One could show how using only some of the antibiotics does not entirely kill the microorganisms by visually showing, by use of color and imagery, survival of the bacteria in a child’s body. Subsequent proliferation of the bacteria into resistant strains could be shown by a change in color and size of the bacteria. Then, the child can be shown to be ill with the same symptoms, be prescribed the same antibiotic, but it does not work (shown by none of the bacteria being killed off). More visits to the doctor to receive alternative antibiotics can either show how the new treatment can be somewhat effective, but that continuing the bad health behavior will lead to more resistant strains until no medication is left to help the child. Various commercials in this vain would be shown to different markets, adapted to fit the views of that particular society, with the specified branding and message repeated along with the visual imagery.

Conclusion

Public health campaigns rooted in traditional behavioral theories view people as singular entities living in a vacuum. It is necessary to break free from this mindset in order to create more innovative and effective interventions. In regards to antimicrobial resistance campaigns, populations need to be addressed in masses with a strong message as to how misuse of antibiotics can lead to harm. After this general message is addressed, specific interventions need to be developed in the same manner, through interviews with the target population that would better be able to identify root problems dealing with poverty and related societal issues.

References

1. Edberg M. Chapter 4: Individual Health Behavior Theories. Essentials of Health Behavior: Social and Behavioral Theory in Public Health 2007; 35-49.

2. McNulty CAM, Boyle P, Nichols T, Clappison P, Davey P. The public’s attitudes to and compliance with antibiotics. Journal of Antimicrobial Chemotherapy 2007; 60(Suppl.1):i63-i68.

3. Jackson C, Lawton RJ, Raynor DK, Knapp P, Conner MT, Lowe CJ, Closs SJ. Promoting adherence to antibiotics: a test of implementation intentions. Patient Education and Counseling 2006; 61:212-218.

4. Ogden J. Some problems with social cognition models: a pragmatic and conceptual analysis. Health Psychology 2003; 22(4): 424-428.

5. Bell DM. Promoting appropriate antimicrobial drug use: perspective from the Centers of Disease Control and Prevention. Clinical Infectious Diseases 2001; 33(Suppl.3):S245-250.

6. Kristinsson KG. Mathematical models as tools for evaluating the effectiveness of interventions: a comment on Levin. Clinical Infectious Diseases 2001; 33(Suppl.3): S174-179.

7. Shy CM. The failure of academic epidemiology: witness for prosecution. American Journal of Epidemiology 1997; 145(6): 479-484.

8. Williams RJ. Globalization of antimicrobial resistance: epidemiological challenges. Clinical Infectious Diseases 2001; 33(Suppl. 3): S116-117.

9. Goossens H, Guillemot D, M Ferech et al. National campaigns to improve antibiotic use. Eur J Clin Pharmacol 2006; 62:373-379.

10. Evans WD, Blitstein J, Hersey JC, Renaud J. Systematic Review of Public Health Branding. Journal of Health Communication 2008; 13:721-741.

11. DeFleur ML, Ball-Rokeach SJ. Theories of Mass Communication (5^th edition), Chapter 8 (Socialization and Theories of Indirect Influence), pp. 202-227. White Plains, NY: Longman Inc., 1989.

Designing More Effective Dengue Control Programs – Colleen Longacre

Designing More Effective Dengue Control Programs – Colleen Longacre

Dengue is a mosquito-borne infection that causes severe flu-like symptoms and can give rise to a deadly complication called dengue hemorrhagic fever (DHF). Dengue is found in tropical climates worldwide, and DHF is the leading cause of death among children in some Southeast Asian countries (1). The global incidence of dengue has increased dramatically over the past 30 years, making it a major international health priority. Because there is currently no vaccine and no specific treatment for dengue, public health programs have focused primarily on vector control programs that target the mosquitoes that carry the virus. Early control programs were vertical in nature and focused on large-scale chemical spraying of standing water sources. When these efforts alone proved ineffective, public health professionals stressed the importance of community-level campaigns to promote behavior change to promote vector control. However, these community campaigns have been designed primarily using the Health Belief Model and other individual-level models of behavior change. As a result, these campaigns have also failed to inspire community-wide behavior change and decrease the incidence of dengue among the populations at risk.

Components of Current Community Vector Control Programs

Community-level vector control programs are comprised of three elements – insecticide application to potable water supplies, environmental management, and community awareness campaigns. The World Health Organization (WHO) currently approves five insecticides for use in drinkable water. In addition, biological control agents, such as larvae-eating fish, may be introduced into water supplies to kill the mosquito larvae without adversely affecting human health (2). Environmental management consists of clean-up campaigns, installation of water supply systems, solid waste management, and better urban planning (2). Campaigns designed to raise community awareness and participation in vector control efforts are the newest addition to these programs. These campaigns seek to increase control activities at the household level, such as “covering or frequently cleaning water storage vessels, removing discarded food and beverage containers, and disposing of used tires in such a way that they do not collect rainwater” (2).

The Health Belief Model has been widely used in designing these campaigns. The Health Belief Model, one of the most widely used individual behavior change theories in public health, states that health behavior is primarily motivated by four factors: perceived susceptibility, perceived severity, perceived benefits of an action, and perceived barriers to taking that action (3). This model assumes that an individual rationally weighs the costs and benefits of taking action and then acts (or chooses not to act) according to whether or not the benefits outweigh the costs. Additionally, individuals respond to specific cues to action to initiate behavior change, and will take action only if they feel they have a certain degree of self-efficacy in taking that action (3). Recent dengue control campaigns have attempted to address each of the elements of the Health Belief Model. One organization working in dengue control published a bulletin of targeted messages for NGOs to take back to the communities in which they work. These messages addressed perceived susceptibility and severity (“So, you don’t think that dengue is a real problem? It is here in our community now! Young and old get sick with dengue.”), perceived barriers (“Little time to do clean-up to reduce mosquito breeding sites? No problem! Use the action plan checklist. Use it once a week.”), and perceived benefits (“If everyone spends just a few minutes each week to clean up stagnant water, throw away unneeded containers, or cover them, then it will go a long way to reduce dengue fever.”) (4). The inclusion of these messages in posters and public service announcements is designed to serve as the cue to action.

Although these vector control programs have attempted to engage with communities and have recognized the importance of widespread behavior change on program effectiveness and sustainability, their results to date have been unremarkable (5). Several flaws in the design of these programs are impeding their success in reducing the incidence of dengue throughout much of the world.

The Health Belief Model is an Inadequate Predictor of Individual Behavior

The awareness-raising element of vector control programs assumes that individuals are unaware of their susceptibility to dengue fever and the severity of the disease. However, community-level studies conducted in South America and Southeast Asia have proven that this is not the case. One study in Brazil, for example, found that 95% of the population recognized dengue as a severe illness, and 75% had either a relative who had suffered from dengue in the past or had suffered it themselves (6). In addition, 94% of the population could identify at least one method of vector control (6). However, only 18-31% of the population actually reported employing methods of vector control (6). Similarly, in Cambodia, a study among primary school students found that 73% could identify the cause, symptoms, and consequences of dengue, and 83% could identify at least one method of vector control (7). However, when researchers examined the households of these students, they found that few employed vector control strategies (7).

These findings are at odds with what is predicted by the Health Belief Model. Among these communities heavily affected by dengue, there is apparently widespread awareness of the susceptibility and severity of the disease. There is also seemingly widespread knowledge of the desired action and the benefits of that action. Mass communication campaigns have attempted to reduce the perceived barriers through easy-to-follow checklists and action plans. However, the use of vector control strategies remains low.

The failure of the awareness-raising campaigns to inspire actual behavior change exposes critical shortcomings in the Health Belief Model approach. Most importantly, the Health Belief Model assumes that everyone has equal access to, and an equivalent level of, information to make rational decisions. In developing countries and especially in rural communities, access to information is not uniform. In fact, both the campaigns themselves and the studies conducted to evaluate them may have missed their target completely. In many communities, elderly women are primarily responsible for household tasks such as cooking and cleaning. These women should be the primary targets of any intervention designed to encourage the regular cleaning and covering of water containers and the proper disposal of garbage; however, they are also the least likely to be literate or to be exposed to outside media sources that promote such behaviors. Furthermore, school-aged children and adult members of the household who are exposed to the awareness-raising campaign may feel it is outside their sphere of influence to instruct their mothers or mothers-in-law as to how they should carry out their daily tasks (8). As a result, there is a significant disconnect between those with the information and those with the self-efficacy to enact behavior change that stems from the roles different individuals play within the greater household dynamic. The Health Belief Model fails to take into account these social factors that inform individual decision-making. To develop more effective community vector control programs, public health practitioners should consider alternative behavior change models that address these social issues.

Environmental Management Strategies Fail to Take into Account Maslow’s Hierarchy of Needs

As previously discussed, the environmental management component of vector control programs consists of mass clean-up campaigns, installation of water supply systems, solid waste management, and better urban planning (2). However, the provision of these services requires considerable investment in the overall public health infrastructure of many communities. In order to recoup this investment, cost-recovery mechanisms have been introduced into many communities (2). In rural areas, environmental management often takes the form of the installation of metered community water services, whereby each household pays for the amount of water they extract from a common, certified clean source. In effect, the households are asked to pay for the assurance that they will not contract dengue from their water supply. Mass clean-up campaigns have aimed to eliminate sources of standing water that serve as breeding grounds for mosquitoes. These sources include old tires, wheelbarrows, tin cans, and oil drums that household members may leave around their property (9). Clean-up crews offer to remove these items at no cost to the households.

While these environmental management strategies would be effective in reducing the incidence of dengue, they have been met with extensive resistance from communities. Among some poor communities in Southeast Asia, households resorted to collecting rainwater from roof catchments at no cost, rather than paying for the use of community water supplies. Contrary to its intent, the introduction of community water services has actually increased the incidence of dengue in certain areas (2). Similarly, communities were unwilling to allow clean-up crews to remove tires from their property, because they used these tires during the windy season to anchor the tin roofs of their houses to keep them from blowing away (9).
The response of poor communities to the environmental management strategies is a clear expression of Maslow’s hierarchy of needs. Psychologist Abraham Maslow theorized that all human beings desire to grow and attain their full potential; however, before human beings can pursue any kind of higher-level growth, they must be able to satisfy a set of needs (10). According to this theory, safety of health is a higher-order need than the basic needs of water and housing. Until these basic needs are met, individuals are unlikely to focus on their higher-order needs. Therefore, even if individuals recognize the importance of dengue control, they will value their access to free water and secure housing more highly than they value the implementation of vector control strategies. Public health practitioners must consider alternative strategies of environmental management that either do not disrupt people’s ability to meet their basic needs, or are able to meet them simultaneously.

Some Insecticide Treatment Practices are Not Culturally Acceptable in Communities Where They are Employed

The use of insecticides to treat water supplies has long been the primary means of vector control in dengue campaigns. Households are encouraged to add insecticides to the stored water supplies they use for drinking, cooking, and bathing. These insecticides have been certified by the WHO as safe to ingest, and there are no documented adverse health effects of adding these chemicals to the water supply. However, despite these assurances, many communities disapprove of the use of these insecticides for cultural reasons.

Anthropologist Linda Whiteford studied what she describes as the “indigenous typology of water” in the community of Villa Francisca in the Dominican Republic (8). Because water is a scare commodity in this community, different water from different sources is used for different purposes. Tap water is generally brackish and slightly sour, so people prefer to use this water for cleaning. For drinking and cooking, people relied on so-called “sweet water” purchased from public water sources. The idea of adding chemical agents, which slightly altered the taste of the sweet water, was considered ridiculous. Why would they “unsweeten” the water that they had paid for? Similarly, agricultural communities in Central and South America have been resistant to adding chemicals to their drinking water supplies, in part due to public health campaigns in these regions designed to alert farmers to the dangers of pesticide poisoning. Farmers reported that “[the insecticides] had bad smells, so must be harmful to the health”, because this was how they were taught to identify water that might be contaminated with harmful agricultural pesticides (6). Finally, the use of biological control agents has met with resistance in Southeast Asian countries such as Thailand, where there are strict cultural taboos about bathing with water that contains small fish or other creatures (2). For insecticide treatment programs to be effective, public health practitioners must take into consideration the cultural beliefs and practices of the communities in which they work. They must demonstrate an understanding of current community behaviors before they attempt to induce behavior change.

In the absence of the development of a dengue vaccine, vector control programs remain the most important public health intervention in reducing the incidence of dengue worldwide. By reworking the awareness-raising campaigns so that they target the appropriate audiences, by addressing the effects that changes in public health infrastructure have on the ability of households to meet their basic needs, and by understanding the cultural significance of adding chemicals to water supplies in certain communities, vector control programs will be able to more effectively combat dengue around the world.
Dengue Control Programs Must Engage with Women to Raise Awareness at the Community Level

As previously discussed, there is a significant disconnect between those exposed to current awareness-raising campaigns and those with the self-efficacy to enact the behavior changes necessary to achieve the desired outcome. In order to be more effective, awareness-raising campaigns need to be retooled and redirected. One lesson of the failed campaigns is that it is not the message itself that is the problem. Previous studies have shown that those who were exposed to the message both understood the problem and the necessary course of action to take to fix the problem (6,7). What needs to change is how the message is being disseminated into communities and who is being targeted to receive the message.
Social Networking Theory provides a framework for how this goal might be achieved. Social Network Theory first emerged in the 1950s and has been applied in the diverse fields of sociology, public health, communications, political opinion, mathematics, and systems theory (11). Social Network Theory operates on the assumption that the specific and unique characteristics, beliefs, and attitudes of individuals are not as important as the relationships between and among individuals. The theory posits that it is the nature of those relationships (i.e. family/kin networks, work networks, social groups, etc.) that most influences beliefs and behavior (12). Social networks play an important role in whether individuals adopt specific health behaviors, what information individuals are exposed to concerning their health, and what kinds of social support and coping mechanisms are available to individuals (13).

Researching a community’s social networks would provide public health practitioners with information regarding who the primary targets of their awareness campaigns should be. If they had examined family dynamics in many rural communities, they would have learned that it is the mothers and grandmothers who most need to be exposed to information concerning vector control. Once the targets of the message have been identified, Social Network Theory provides a mechanism for effectively disseminating the message. Public health practitioners identify those women who are central to most of the social groups at play in the community. By engaging with these influential women, public health practitioners will build credibility at the community level for their proposed program. Public health practitioners could host small group discussions with these women, and then encourage them to organize discussions with other members of their social networks. In this manner, the vector control message will eventually trickle out to even the most marginalized members of the social network, and the community will feel a sense of ownership over the message. This sense of ownership increases individuals’ self-efficacy and may encourage more universal behavior change. Moreover, the existing social networks can act as built-in mechanisms of social support – neighbors can check in on each other to ensure that they continue to employ vector control strategies.
Dengue Control Programs Must be Integrated into Broader Development Projects

Environmental management is an important component of dengue control programs; however, it cannot be implemented in a vacuum. More effective environmental management programs would take Maslow’s hierarchy of needs into consideration in their design and implementation. Before public health practitioners decide to install metered community water pumps or organize mass clean-up campaigns, they must first evaluate the ability of communities to cope with these changes. If the average household income in a given community is less than a dollar a day, charging fifty cents for clean water may not be the most effective method of dengue control for that community. If communities cannot afford to pay for clean water, then clean water must be made available to them by another method. Similarly, cleaning crews that offer to remove tires should also be equipped to offer to reinforce roofs by another method. Public health practitioners working on environmental management projects should interface with other organizations doing development work in the communities to ensure that individuals’ basic needs are being met and that they are being provided with alternatives for the behaviors and practices they are being asked to abandon.

Dengue Control Programs Must Utilize Culturally Appropriate Water Treatment Methods

As previously suggested, for insecticide treatment programs to be effective, public health practitioners must take into consideration the cultural beliefs and practices of the communities in which they work. They must demonstrate an understanding of current community behaviors before they attempt to induce behavior change. Cultural theory provides an invaluable tool for addressing these issues. Cultural theory “informs us that we live and behave in subjective worlds of meaning, where behavior and meaning are linked” (14). Decoding the meaning behind behaviors is essential to explaining why individuals are resistant to certain behavior changes. More thorough research is necessary before dengue control programs are introduced into communities. Public health practitioners must be willing to conduct literature reviews of the work of cultural anthropologists in the area, or, alternatively, be willing to employ cultural anthropologists as integral members of their program teams. By incorporating cultural theory, dengue control programs can ensure that insecticides are introduced to communities in ways in which it is more likely to be accepted.

If public health practitioners in Villa Francisca, for example, had been aware of this community’s indigenous typology of water, they could have predicted that simply dispensing insecticides in the community would not induce people to use them. If these practitioners had been familiar with Dr. Whiteford’s research, they could have employed this information in developing their awareness-raising campaigns. They could have reframed the concept of adding insecticides to sweet water as a means of enhancing this water even further by adding a life-saving substance to it, not as a method of unsweetening the water. Similarly, if public health practitioners had known about the cultural taboos in Thailand, they would have invested their resources in procuring chemical insecticides rather than biological control agents for these communities. Ensuring that water treatment methods are culturally appropriate may require more initial research and expenditure of resources during program development; however, dengue control programs that fail to do this run the risk of wasting even more time, effort, and resources on unsuccessful programs.

Dengue is a critical international public health problem that deserves well-designed, well-implemented control programs. Past and current dengue programs have been successful in determining what methods of control are most effective; however, they have been largely unsuccessful in inspiring communities to adopt these methods of control. By utilizing social science theories, such as Social Network Theory, Maslow’s hierarchy of needs, and Cultural Theory, dengue control programs will be able to more effectively target the appropriate audiences, ensure that programs are not disruptive to the overall health and wellbeing of communities, and ensure that water treatment methods are culturally appropriate. The combined effect of these improvements should serve to inspire more widespread behavior change and to begin to reduce the incidence of dengue worldwide.

REFERENCES
1. WHO. “Dengue and dengue hemorrhagic fever.” May 2008. <>.
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6. Augusto, Lia Giraldo da Silva and Solange Laurentino dos Santos. “Control Program of Dengue in Brazil: Critical Reflections.” International Congress on Dengue and Yellow Fever. 2004.
7. Sokrin, Khun, and Lenore Manderson. “Community and School-Based Health Education for Dengue Control in Rural Cambodia: A Process Evaluation.” Neglected Tropical Diseases. 2007; 1: 1-10.
8. Whiteford, Linda M. “The Ethnoecology of Dengue Fever.” Medical Anthropology Quarterly. 1997; 11: 202-223.
9. Correa, Carlos. “Incorporating a New Approach into Dengue Control Programs: Community Participation in Negotiating Behavior Change.” CHANGE Project. AED/USAID. May 2003.
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