Developing a CASPER Survey to Assess the Prevalence of Risk Factors for Neglected Tropical Diseases in Texas

Abstract

While more than a billion people live at risk of neglected tropical diseases in areas of Asia, sub-Saharan Africa, and Latin America, the degree to which such diseases burden countries like the United States is currently unclear. Even though many neglected tropical diseases such as dengue, leishmaniasis, and Chagas disease are not endemic to the United States, the possibility of their emergence is noteworthy, especially in states like Texas, which has high levels of poverty, a large immigrant population, and a climate amenable to the vectors for these diseases and is geographically proximate to endemic areas. Despite the health threat that emerging neglected tropical diseases may pose, little is known about the prevalence of risk factors for them in the United States. Texas House Bill 2055, enacted on September 1, 2015, mandated the establishment of a surveillance program for neglected tropical diseases in Texas. After reviewing the potential risk factors for transmission in Texas, we developed a 41-question survey that could be implemented using the Community Assessment for Public Health Emergency Response (CASPER) method. In concert with public health surveillance and vector population monitoring, data from CASPERs could be used to quickly and cost-effectively assess the prevalence of risk factors for 10 neglected tropical diseases in Texas or elsewhere in the United States. The data generated by future CASPERs conducted using this survey could be immediately actionable, guiding public health priority setting and decision making.

Despite the health threat that emerging neglected tropical diseases may pose, little is known about the prevalence of risk factors for them in the United States. The authors developed a 41-question survey that could be implemented using the Community Assessment for Public Health Emergency Response (CASPER) method.

Neglected tropical diseases are communicable diseases common in subtropical and tropical countries that cause a substantial disease burden because of their high morbidity rates. Across the world, more than a billion people live in at-risk areas.¹ Although neglected tropical diseases are most commonly found in developing countries, developed countries also report them, and it is becoming increasingly clear that, with the spread of vectors and the ease of global travel, no region of the world is free of these infections. In the United States, it appears that Texas is the state with the heaviest potential public health burden associated with neglected tropical diseases because of its high poverty rate, large immigrant population, geographic proximity to endemic areas, and a climate amenable to the vector life cycle.²

Over the past 10 years, Texas has seen the emergence of several vector-borne viral and parasitic diseases; of these, 3 are of major public health concern. Dengue fever has reestablished itself as endemic to the United States-Mexico border region. A 2005 study of Brownsville, Texas, residents found a seroprevalence of 39% and an incidence of 4%.³ In 2013, the Centers for Disease Control and Prevention (CDC) reported an outbreak of 53 confirmed cases of dengue in Texas's southernmost counties.⁴

Suspected cases of locally acquired leishmaniasis have been reported sporadically in southern Texas for decades.⁵ However, leishmaniasis seems to have been increasing in range in a northeastward direction since about 2000.⁶ Cases or clusters of cases of cutaneous leishmaniasis have been identified in Dallas and Waco, Texas, and McCurtain County, Oklahoma—areas that had never previously reported cases.^7,8

Chagas disease is known to regularly infect both human and animal reservoirs in Texas. There are an estimated 300,000 cases of Chagas disease in the United States,⁹ and a recent study estimated a 9% seroprevalence of Chagas in shelter dogs across Texas.¹⁰ Further work using a community mail-in submission program showed a 63.3% prevalence of Chagas disease in submitted kissing bugs.¹¹

Like most states, Texas has a passive surveillance system for infectious diseases, and most neglected tropical diseases are already reportable conditions within 1 week.¹² However, even with such a surveillance program, neglected tropical diseases are most likely being underreported for several reasons. The literature clearly shows that, apart from a few major communicable diseases like tuberculosis, infectious diseases are reported less than 50% of the time.¹³ In the case of dengue and other arboviral diseases, symptoms are usually nonspecific and are frequently misdiagnosed, especially in the case of mild infections. Because most neglected tropical diseases are not yet endemic in the United States, American healthcare personnel are less familiar with these diseases and may not consider them in their differential diagnoses. Additionally, some vector-borne disease infections may have no symptoms, allowing a disease to persist in human, animal, and vector populations and making them unlikely to be detected through passive surveillance. Therefore, assessing the prevalence of risk factors may be one way to inform public health and healthcare authorities about the potential burden of these diseases in their communities.

While passive surveillance and the monitoring of vector populations are useful in establishing priorities and guiding policy decisions, they alone cannot paint a complete picture of the current burden of neglected tropical diseases in Texas. To assess the current and potential future burden of these diseases, systematic collection of risk factor prevalence data is needed.

The Community Assessment for Public Health Emergency Response (CASPER) is a method that can be used to accomplish these goals. CASPER is an epidemiologic method designed to provide household-level information about an affected community's needs quickly and at a relatively low cost. Although initially adapted by CDC from the World Health Organization's Rapid Needs Assessment for use post-disaster, CASPER has been used to assess household preparedness, underlying vulnerabilities, and community perceptions regarding public health emergencies such as H1N1 novel influenza A and other hazards.^14,15

Recently, CASPER was used by the Austin-Travis Public Health Department¹⁶ and the Galveston County Health District to assess their community's knowledge of Zika virus and mosquito bite prevention. While this CASPER was novel in that it was focused on aspects of Zika virus, the utility of CASPER to systematically assess the prevalence of risk factors for infectious diseases has not yet been documented. In concert with public health surveillance and vector population monitoring, we believe that data collected using this survey and the CASPER method can provide state and local health departments with relatively quick and cost-effective data that can be used to make informed decisions about the allocation of resources to address risk factors for neglected tropical diseases, such as targeting health information and vector elimination strategies to returning travelers, owners of pets or livestock, or residents with certain demographic, behavioral, or household characteristics.

In response to the potential threat posed by neglected tropical diseases, Texas House Bill 2055 established a sentinel surveillance program in Texas focusing on neglected tropical diseases of interest in the state, particularly Chagas, leishmaniasis, dengue, ascariasis, hookworm, trichuriasis, taeniasis/cysticercosis, echinococcosis, paragonimiasis, and fascioliasis.¹⁷ Our objective in this article is to justify CASPER's utility in assessing the prevalence of risk factors for neglected tropical diseases and to provide a CASPER survey that could be implemented locally to provide health departments with relevant information to establish priorities in their jurisdictions.

Methods

Survey Development

In order to identify elements that should be included on the CASPER survey to assess the prevalence of risk factors for neglected tropical diseases, a literature review for each of the diseases in question was performed, focusing on the dynamics of neglected tropical disease transmission in Central and South America. This literature review was performed during July 2016, using both Web of Science and Google Scholar databases. Papers included in the review were not limited by publication date, but only papers published in English were considered. Several factors were associated with an increased risk of most or all of the diseases of interest. For example, immigrant status is considered a risk factor, because many immigrants come from countries with higher prevalence of neglected tropical diseases.¹⁸ Therefore, communities with large numbers of immigrants or migrant workers or high percentages of population that regularly travel to and stay in endemic areas should be categorized as having a higher risk. Most of these diseases are also highly associated with rural poverty.²

Because of differential transmission dynamics, each of these diseases also has unique risk factors (Table 1). Risk factors for dengue and other mosquito-borne illnesses include a lack of window screens or in-house air conditioning; urban density, in the form of tightly packed housing and high house residency; standing water near the household; failure to use DEET;³ and not regularly wearing long sleeves when outside.

Table 1.

Vectors, Risk Factors, and Cases of Neglected Tropical Diseases of Interest in Texas

Neglected Tropical Diseases (Vector)	Risk Factors	Cases in Texas
Chagas (triatomine bug)	Housing quality and cleanliness; presence of stray dogs or infected chickens near home	9% seroprevalence of Chagas in shelter dogs across Texas;¹⁰ 63.3% prevalence of Chagas disease in submitted kissing bugs¹¹
Leishmaniasis (Lutzomyia sandfly)	Rural residence; interaction with nature; wildlife hosts residing in or near the home	Vector range moving northeast since about 2000;⁶ cases or clusters of cases of cutaneous leishmaniasis have been identified in Dallas and Waco, Texas, and McCurtain County, Oklahoma.^7,8
Dengue (Aedes aegypti mosquito)	Population density; housing quality; window screens or air-conditioning; standing water near the household; failure to use repellent with DEET; not regularly wearing long sleeves when outside	Brownsville, Texas, study found a seroprevalence of 39% and an incidence of 4% among residents in 2005;³ in 2013, an outbreak of 53 confirmed cases of dengue in southern Texas.⁴
Helminthes (Ascaris lumbricoides, Hookworm, Trichuris trichiura (whipworm), Taenia Tapeworm, Echinococcus granulosus tapeworm, Paragonimus flatworm, Fasciola hepatica (liver fluke))	Ingestion of soil, water, or produce contaminated with infected feces	Cross border seroprevalence of 3.3% in El Paso and Ciudad Juarez, with most Taenia infections occurring on the El Paso side of the border²

Leishmaniasis is a parasitic disease caused by Leishmania mexicana, the vector of which is sandflies of the genus Lutzomyia. These vectors have a wide and increasing geographic range in the United States.¹⁹ While risk factors for this disease include many of those mentioned above for mosquito-borne illnesses, unique risk factors include rural residence, frequent interaction with nature, and wildlife hosts residing in or near the home. Reservoirs include wood rats, cotton rats, opossums, and armadillos.⁵

Chagas disease is a parasitic infection caused by Trypanosoma cruzi; it is transmitted by kissing bugs of the genus Triatoma. Although the highest density and diversity of kissing bug species can be found in the Southwest, kissing bug species have been reported in at least 26 states.⁸ Risk factors for Chagas include poor housing quality, such as cracks, gaps, poor roofing, and a dirty interior; infected dogs in or around the home; and raising chickens near the home, which increases vector density by providing a stable food source.²⁰ Previous data also suggest that stray dogs in shelters are documented carriers; therefore, large numbers of stray dogs in a community should also be considered a risk factor.⁹

The soil-transmitted helminthes, which include ascariasis, hookworm, trichuriasis, taeniasis, cysticercosis, echinococcosis, paragonimiasis, and fascioliasis, heavily affect most Latin American countries. Recent estimates suggest that most Latin Americans live at risk of ascariasis, trichuriasis, and hookworm.²¹ Although infection rates are still low in the United States, infections do occur in areas with the proper conditions. For example, a 2004 cross-border seroprevalence study of El Paso and Ciudad Juarez found a 3.3% prevalence of Taenia spp., with most Taenia infections occurring on the El Paso side of the border.²² To prevent these infections from becoming endemic in poor areas with high numbers of Latin American immigrants, careful surveillance may be warranted. The agents of these diseases, caused by various types of parasitic worm, are transmitted by the ingestion of fully developed eggs, commonly found in soil, water, or produce contaminated with infected feces. Therefore, risk factors for these infections revolve around unsanitary conditions.²³ Some examples include lack of proper sewage disposal, drinking unsanitary water, poor hygiene,²⁴ not washing produce before consumption, and consumption of undercooked pork and seafood. Some of these diseases involve animal reservoirs; for example, cysticercosis is highly associated with pig husbandry, and cystic echinococcosis commonly occurs in sheep ranchers.

Review of Past CASPERs

To establish that CASPER can be used to quickly collect reliable data on the prevalence of risk factors, a literature review was performed focusing on past CASPER reports. Reports were limited to those published in peer-reviewed journals that included at least 1 type of response rate. In total, 40 CASPERs published between 1998 and 2015 met the criteria for inclusion. These papers were reviewed for 3 different types of response rate—completion, contact, and cooperation—as well as the number of days it took to complete the CASPER. According to the CDC CASPER toolkit, completion rate is the total number of interviews received divided by the goal number of interviews; contact rate is the total number of interviews received divided by the number of houses approached; and cooperation rate is the total number of interviews received divided by the number of eligible homes approached.²⁵

Results

Survey Development

Based on the literature review of neglected tropical disease risk factors, a CASPER survey was developed (see Appendix A, supplementary material, http://online.liebertpub.com/). The survey was composed of 41 questions and included sections on demographics, travel history, housing characteristics, vector contact and prevention, and pets and animals. The survey and associated consent materials were reviewed and approved by the Texas A&M University Institutional Review Board (IRB 2016-0495D).

Demographics

Because factors such as overcrowding and poverty are associated with the transmission of neglected tropical diseases,^2,3 respondents were asked to report the number of people living in their household and whether or not their household's average income is above or below 200% of the federal poverty guidelines.²⁶

Travel History

Although autochthonous transmission of neglected tropical diseases in Texas has been documented, travel remains an important risk factor for these diseases. Accordingly, the survey asked respondents to report if anyone in the household had traveled outside the United States in the past 3 months, specifically to countries in South and Central America and the Caribbean, as well as the duration of the trip. Survey participants were also asked whether they had hosted visitors from other countries in their household and, if so, the country of those visitors' residence.

Household Characteristics

Housing quality is an important determinant of individual risk, largely because low-quality housing often increases interaction between humans and vectors.^3,19 Certain aspects of a home can encourage households to act in ways that put them at risk. For example, people who live in households without air-conditioning are encouraged to open their windows, allowing vectors access to the indoors. To gauge the level of human-vector interaction inside the home, questions about air-conditioning, window screens, cracks or gaps in home structure, and questions about the presence of bugs inside the home were included. Respondents can be provided with photos of Aedes aegypti mosquitoes, sandflies, and kissing bugs to assist with identification, a method that has frequently been used in research related to agricultural pests and pesticides.^27,28

Also included in the housing quality section were questions about water usage, food cleanliness, and waste removal services. Questions such as these are intended to gauge people's risk of soil-transmitted helminthiases, as these diseases generally require unsanitary conditions or the ingestion of unsanitary foods to spread to human hosts.

Vector Contact and Prevention

When considering vector-borne diseases, it is important to capture the level of interaction between humans and vectors as well as what community members are doing to control vector populations around their households. Therefore, this section of the survey included questions asking about the frequency with which respondents are bitten, their use of bite prevention behaviors like applying DEET and wearing long-sleeved clothing, and the number of artificial mosquito-breeding habitats such as tires and flower pots that exist around their home.

Pets and Animals

Animals can also increase the risk of neglected tropical diseases in a household, acting as food sources, carriers, and intermediate hosts of infection. For example, dogs, especially stray dogs, have been found to be infected with both Chagas and leishmaniasis, and, therefore, a high prevalence of dogs in an area, combined with other known risk factors, could elevate a community's risk. Therefore, questions in this section asked about household pets, whether chickens or pigs are raised in or near the house, and the prevalence of stray dogs near the residence.

Interviewer Observations

In addition to directly asking questions of household members, surveyors can ask permission to assess certain aspects of the household, such as the number of visible artificial containers, any noticeable housing quality defects, and the distance between homes. Surveyors can also take note of other things they notice in the community, such as drainage ditches filled with stagnant water, large numbers of stray animals, and whether the community is largely rural or urban.

Review of Past CASPERs

Of the 40 published CASPER reports reviewed, 11 (27.5%) were for preparedness and 29 (72.5%) for emergency response. Overall, CASPERs completed 88% of their target interviews (typically 210), well above the 80% cutoff that the CDC typically finds acceptable for generalizablity.²⁵ CASPERs targeting topics such as preparedness or accreditation actually achieved higher completion rates (mean = 91.4%), perhaps due to the fact that some preparedness topics, such as pandemic influenza A(H1N1), are of high interest to respondents. Interviewers can expect to successfully complete a survey at 53.1% of the houses they approach and at 76.4% of households with an eligible resident at home. Typically, CASPERs take about 2.5 days to complete. Additionally, it is important to note that interview teams for CASPERs are almost always recruited on a volunteer basis from employees of health departments, employees of other state and local departments, and students from local public health schools.

These data suggest that CASPER could be a relatively quick and inexpensive method to collect household-based data on the prevalence of risk factors for neglected tropical diseases. With proper planning, health departments can feasibly attain the 168 (80% of 210) interviews required to make the assessment representative of their population, often in less than 3 days and using volunteers to some extent. CASPER allows public health departments to collect data in a standardized, validated way, with response rates that minimize bias.

Discussion

At this time, no data have been collected using the described CASPER sampling methodology. However, Texas House Bill 2055 will require the establishment of a surveillance program for neglected tropical diseases in Texas at some point in time. Although the Texas population of more than 25 million resides in the second largest state in the United States, targeted CASPERs would still allow high-risk areas to be identified at the city, county, or regional level. After locations with a high prevalence of risk factors are identified, additional public health studies and interventions—such as seroprevalence studies, case interviews and contact tracing, and vector surveillance and sampling—can be used to study transmission dynamics in greater detail. Once the prevalence of risk factors for neglected tropical diseases in Texas is better understood, public health departments can help reduce transmission by making people more aware of the diseases and stressing vector source reduction and avoidance of potential hosts like stray dogs, addressing housing quality issues, and encouraging the use of DEET.

Limitations

Although CASPER is well known for its ability to be used to gather reliable data quickly and at relatively low cost, it has been criticized for several possible limitations. If certain demographic or socially vulnerable groups are less likely to be included in the survey, there is the potential for response bias. Recall bias can also be a concern when asking about travel or food handling behaviors that may have occurred in the past. Because of the nature of a household survey, only the prevalence of risk factors for households can be assessed. Risk factor prevalence elsewhere (eg, public spaces) are typically not assessed as part of CASPER. Therefore, the effectiveness of programs to reduce the prevalence of risk factors put in place by local governments or public health agencies cannot be assessed.

Although neglected tropical diseases may increasingly pose a threat to health in the United States, insufficient data exist to ascertain the prevalence and geographic distribution of risk factors relevant to these diseases. While this article does not present findings from a CASPER using this survey to assess the prevalence of risk factors for neglected tropical diseases, because of the rapid changes in the incidence of neglected tropical diseases in Texas (eg, the first confirmed case of autochthonous cutaneous leishmaniasis in McLennan County was reported during summer 2016), we hope that others will be able to rapidly implement the survey in their local jurisdictions. We plan to pilot test the survey with local public health partners in December 2016. CASPER is one quick and relatively cost-effective way to learn more about the prevalence of risk factors for neglected tropical diseases in Texas or elsewhere. The data generated by CASPERs can be immediately actionable, guiding public health priority setting and decision making.

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