INTRODUCTION
Rocky Mountain spotted fever (RMSF) is a serious bacterial disease caused by Rickettsia rickettsii. It is transmitted to humans through tick bites. Medical researchers in both Mexico and the United States have observed that RMSF morbidity and mortality are disproportionately higher in low-income communities. 1–3 Multiple factors may influence vulnerability in low-income communities, and understanding of the role of social factors in disease ecology is essential for developing effective RMSF prevention and control strategies.
In Mexico and the southwestern United States, the brown dog tick, Rhipicephalus sanguineus sensu lato, is the primary vector of RMSF. 4 Rhipicephalus sanguineus preferentially feeds on dogs, allowing the maintenance of the tick and pathogen within urban peri-domestic environments. 5 By contrast, the primary vector species in most regions of the United States are Dermacentor variabilis and Dermacentor andersoni, which feed on a wide variety of mammalian hosts, including wild rodents. These different host–vector dynamics have led to distinct patterns of disease transmission. In much of the United States, RMSF occurs as individual cases associated with spending time in rural, sylvatic habitats, although transmission is spreading to suburban and even urban areas. 6 In the southwestern United States and Mexico, however, outbreaks occur in both rural and urban peri-domestic environments and are typically clustered.
After decades with only sporadic cases, RMSF outbreaks began occurring in the Arizona/Sonora region in the early 2000s. Between 2003 and 2017, at least 1,394 human cases with 247 deaths were reported in the border state of Sonora, Mexico, alone. 1,3 Cases in Sonora were most common in low-income communities with limited access to health care, particularly among indigenous migrant agricultural workers. 7 Children younger than 10 years appeared especially vulnerable to serious health complication, and fatality rates of 40% were observed in indigenous patients at the Sonora Children’s Hospital. 8,9
In the recent epidemics of RMSF in Mexico, social factors influencing transmission have operated at multiple scales, from the individual level (i.e., knowledge and practices regarding preventive measures) to the community level (i.e., large numbers of free-roaming dogs) to the national level (i.e., social deprivation). 1 Previous research on vector-borne diseases, including dengue 10,11 and malaria, 12 indicates that people’s participation in preventive measures is related to their knowledge, attitudes, and practices (KAPs) regarding transmission and disease symptoms. Low levels of KAPs are associated with low levels of participation in prevention practices. 13 The peri-domestic nature of RMSF transmission in Mexico and the southwestern United States requires concerted efforts to engage individuals and communities in prevention and control efforts. Efficacy of public health interventions in resource-limited settings largely depends on individual and community capacity to recognize risk factors and to execute specific activities to reduce the likelihood of acquiring a disease. 14 Thus, assessment of community KAPs is necessary to improve integrated measures to reduce the RMSF burden in Sonora, one of the Mexican states with the highest morbidity and mortality in recent years. 8 This study aimed to evaluate RMSF-related KAPs of individuals residing in an urban endemic area with high burden of the disease.
MATERIALS AND METHODS
Study area.
Hermosillo is the capital city of the state of Sonora and has approximately 820,000 inhabitants. 15 The city is located in the Sonoran Desert in northwestern Mexico (latitude 29°05′N, longitude 110°57′W, and altitude 216 m above sea level) (Figure 1). It has an average annual temperature of 25°C and low annual precipitation (around 100 mm). 16 Daily maximum temperatures in summer are often greater than 43°C. Rocky Mountain spotted fever transmission has been documented annually since 2003. 17 In the last 5 years, 194 cases of RMSF were confirmed in the municipality of Hermosillo, with a case fatality rate of 33% (G. Alvarez, unpublished data). To reduce RMSF morbidity and mortality, the Ministry of Health (MOH) implemented a public health program in 2012 aimed at reducing tick exposure both in humans and dogs. Activities include tick control in high-risk areas as well as enhancing public awareness and educating medical personnel about symptoms, treatment, and preventive measures.
Location of sampling areas in Hermosillo, Mexico.
Citation: The American Journal of Tropical Medicine and Hygiene 104, 1; 10.4269/ajtmh.20-0181
Study design.
As part of a larger study designed to investigate mosquito abundance and KAP information on dengue fever risk factors in Hermosillo, 18 a cross-sectional study design using a non-probabilistic household survey was conducted from August 12, 2014 to September 3, 2014. The survey included questions about RMSF risk, symptoms, and prevention. Forty residential point sites were randomly selected across the city, with a minimum distance of 1 km apart to achieve good geographical coverage (Figure 1). Recruitment of participants was conducted by selecting 10 households around each site (N = 400) using the following algorithm: the first participant was recruited from the households across the street from the point site. Every third household of that block and the blocks one street further out from the point site were approached for recruitment until the required sample was completed. Households were not revisited. One individual aged ≥ 18 years who resided in each of the selected houses was interviewed after consenting to participate. A total of 1,251 households were visited. The overall response rate was 31.7%, with 171 refusals (13.7% refusal rate) and 688 households where the residents were not home (55.0%). The University of Arizona Human Subjects Review Board approved the study and declared it exempt.
Questionnaire.
A KAP survey module was developed to include awareness of RMSF, dog/tick-related risk, RMSF knowledge, medical care–seeking behavior, and sociodemographic and household information. A socioeconomic index was created from a list of durable goods/assets. Categorical principal component analysis (CATPCA) was used to extract the factor with the highest explained variance, and standard (z) scores were computed. The set of unidimensional variables retained were ownership of a laundry machine, car, landline phone, personal computer, and Internet as these showed adequate internal consistency (Cronbach’s α = 0.731). Three broad socioeconomic status (SES) levels were defined based on the lack of goods: high (median = 0), medium (median = 1.5), and low (median = 4).
Statistical analysis.
All analyses were performed accounting for the clustered structure of the data with robust variance estimates determined by the geographical distribution of the 40 sites. Descriptive statistics including means and SDs and proportions and CIs were reported. Significant differences among SES levels were determined using χ2 and F tests (P < 0.05) for categorical and continuous variables, respectively. In addition, simple logistic regression with standard errors adjusted for the 40 cluster sites was used to assess the association between RMSF awareness/perception of risk questions and SES (independent variable). Odds ratios (ORs) and 95% CI were reported. The statistical analysis was performed in STATA 15.1 (StataCorp, College Station, TX) and the CATPCA in SPSS 25 (IBM Corp, Armonk, NY). The map of Figure 1 was created in ArcMap 10.1 (ESRI, Redlands, CA).
RESULTS
Residents and household characteristics.
A total of 400 households were surveyed. The majority of the respondents were women (71.5%), with a median age of 44.3 years (SD = 15.4). The median household size was four residents (interquartile range = 3–5); 48.7% had children aged between 5 and 18 years, and 33.0% of households included children younger than 5 years. Respondents were distributed in high (39.7%), medium (33.5%), and low (26.8%) SES categories. Lower SES was significantly associated with lower educational attainment (P < 0.001), lower house ownership (P < 0.05), higher proportion of overcrowded conditions (≥ 2 persons per bedroom) (P < 0.001), and a higher proportion on public insurance (Popular Health Insurance, which is mainly designed for people outside of the contributory social security system) (P < 0.001; Table 1).
Residents and household characteristics by SES in Hermosillo, Mexico
Characteristic | Total (N = 400) | SES (lack of goods) | P-value* | ||
---|---|---|---|---|---|
High (n = 159) | Medium (n = 134) | Low (n = 107) | |||
Continuous variables, mean (SD) | |||||
Age (years) | 44.3 (15.4) | 45.7 (13.7) | 41.8 (14.8) | 45.2 (18.0) | 0.066 |
Number of residents in the household | 3.9 (1.6) | 4.0 (1.4) | 3.9 (1.5) | 3.8 (1.9) | 0.806 |
Categorical variables | N (%) | % | % | % | – |
Children younger than 5 years | 132/400 (33.0) | 27.0 | 35.1 | 39.3 | 0.167 |
Children aged 5–18 years | 195/400 (48.7) | 49.5 | 48.5 | 49.2 | 0.934 |
Gender | |||||
Female | 284/397 (71.5) | 71.7 | 67.9 | 75.7 | 0.529 |
Male | 113/397 (28.5) | 28.3 | 32.1 | 24.3 | – |
Basic schooling (≥ 9 years of schooling) (yes) | 345/399 (86.5) | 98.1 | 85.7 | 70.1 | < 0.001 |
Type of health insurance† | |||||
Mexican Social Security Institute | 203/400 (50.7) | 51.6 | 52.9 | 46.3 | 0.727 |
Institute for Social Security and Services for State Workers | 33/400 (8.2) | 10.7 | 8.2 | 4.0 | 0.140 |
Institute for Social Security and Services for State Workers of Sonora | 54/400 (13.5) | 15.7 | 14.2 | 9.4 | 0.608 |
Popular Insurance | 63/400 (15.7) | 5.7 | 13.4 | 33.6 | < 0.001 |
Private | 48/400 (12.0) | 20.7 | 9.0 | 2.8 | < 0.01 |
None | 42/400 (10.5) | 9.4 | 11.9 | 10.3 | 0.788 |
House ownership | |||||
Owner | 351/397 (88.9) | 94.3 | 85.6 | 84.9 | 0.05 |
Rent | 44/397 (11.1) | 5.7 | 14.4 | 15.1 | – |
Overcrowding (≥ 2 persons per bedroom) (yes) | 66/398 (16.6) | 9.4 | 14.9 | 29.0 | < 0.001 |
SES = socioeconomic status. Bold values represent statistically significant associations (P ≤ 0.05).
χ2 and F tests for categorical and continuous variables, respectively.
The sum of frequencies can exceed 100% because it is possible to have more than one health insurance. Therefore, each health insurance is reported as a separate variable.
Rocky Mountain spotted fever awareness and dog/tick-related risk perception.
More than half the respondents (59%) had heard of RMSF, but there was an association between awareness and SES. Awareness was lower among respondents in the medium SES (60.3%) and low SES categories (44.9%) than among those in the high SES category (67.9%) (P < 0.001). Knowledge of where ticks are found (on dogs and in dirt) was similar (60%), but lack of knowledge was higher among respondents from the low SES stratum (14%) than among those from medium/high strata (6%) (P < 0.05).
About 66% of respondents expressed a perception of many free-roaming dogs in their neighborhood, and this perception was inversely associated with SES stratum (high stratum = 53.5%, medium = 68.9%, and low = 83.2%, P < 0.001). Half of those surveyed (50.8%) had contact with dogs. Among those reporting contact with dogs, 67.3% allowed dogs to enter their home, backyard, or place of work. With respect to prevention practices, 76.4% of respondents in contact with dogs reported using tick collars or other products to avoid ticks, with a nonsignificant but trending negative difference between SES strata (high = 82.7% versus medium = 75.0% versus low = 67.3%, P = 0.160). Finally, although most respondents (88.9%) in contact with dogs checked them for ticks, only 76.9% (P < 0.01) from the low SES respondents reported doing this preventive practice (Table 2).
Rocky Mountain spotted fever awareness and perception of risk by SES in Hermosillo, Mexico
Variable | Total (N = 400), N (%) | SES (lack of goods) | P-value* | ||
---|---|---|---|---|---|
High (n = 159) % | Medium (n = 134) % | Low (n = 107) % | |||
Have you heard about RMSF? (yes) | 237/400 (59.3) | 67.9 | 60.5 | 44.9 | < 0.001 |
Where do you think you can find ticks?† | |||||
Dogs | 243/400 (60.7) | 64.8 | 60.5 | 55.1 | 0.339 |
Dirt | 247/400 (61.7) | 59.1 | 64.2 | 62.6 | 0.807 |
Other | 58/400 (14.5) | 13.2 | 17.2 | 13.1 | 0.589 |
Do not know/unsure | 32/400 (8.0) | 5.6 | 6.0 | 14.0 | < 0.05 |
Are there many free-roaming dogs in your neighborhood? (yes) | 265/398 (66.6) | 53.5 | 68.9 | 83.2 | < 0.001 |
Do you have contact with dogs? (yes) | 201/396 (50.8) | 55.4 | 46.6 | 49.1 | 0.364 |
Do dogs enter your home or work? (yes)‡ | 134/199 (67.3) | 67.4 | 73.8 | 59.6 | 0.428 |
Do you use tick collars or any other product to avoid ticks? (yes)‡ | 152/199 (76.4) | 82.7 | 75.0 | 67.3 | 0.160 |
Do you check your dogs for ticks? (yes)‡ | 176/198 (88.9) | 93.0 | 93.3 | 76.9 | < 0.01 |
RMSF = Rocky Mountain spotted fever; SES = socioeconomic status. Bold values represent statistically significant associations (P ≤ 0.05).
P-values based on χ2 test.
The sum of frequencies can exceed 100% because it is possible choose more than one option. Therefore, each option is reported as a separate variable.
Proportion for those who have contact with dogs.
Significant associations between RMSF awareness and SES reported in Table 2 were also interpreted in terms of probabilities through simple logistic regression using high SES stratum as reference (Table 3). Individuals in the low SES stratum were less likely to have heard about RMSF (OR: 0.39; 95% CI: 0.25–0.59). In other words, low SES respondents were 2.5 times less likely to have heard about RMSF than those in the high strata. Also, the odds of ignoring ticks or being unsure of potential sources of ticks was 2.7 times higher (95% CI: 1.21–6.05) for low SES respondents.
Differences in RMSF awareness/perception of risk between socioeconomic strata in Hermosillo, Mexico
Variable | Medium | Low |
---|---|---|
OR (95% CI) | OR (95% CI) | |
Have you heard about RMSF? | 0.74 (0.49–1.12) | 0.39 (0.25–0.59) |
Where do you think you can find ticks? | ||
Dogs | 0.80 (0.47–1.35) | 0.65 (0.37–1.15) |
Dirt | 1.18 (0.72–1.95) | 1.13 (0.67–1.91) |
Other | 1.38 (0.68–2.79) | 0.95 (0.45–2.01) |
Do not know/unsure | 1.06 (0.34–3.36) | 2.70 (1.21–6.05) |
Are there many free-roaming dogs in your neighborhood? | 1.84 (1.05–3.21) | 4.19 (2.10–8.38) |
Do you have contact with dogs? | 0.70 (0.41–1.17) | 0.74 (0.44–1.26) |
Do dogs enter your home or work? | 1.37 (0.63–2.95) | 0.73 (0.31–1.70) |
Do you use tick collars or any other product to avoid ticks? | 0.67 (0.30–1.52) | 0.40 (0.17–0.99) |
Do you check your dogs for ticks? | 1.03 (0.31–3.44) | 0.25 (0.09–0.74) |
OR = odds ratio; RMSF = Rocky Mountain spotted fever; SES = socioeconomic status. Odds ratio > 1: higher odds of awareness/risk perception compared with high SES group (reference); OR < 1: lower odds of awareness/risk perception compared with high SES group (reference); OR = 1: no association. Bold values represent statistically significant associations. Significant associations were considered when the 95% CI did not include 1.00.
Individuals in the lower SES strata were more likely to perceive high numbers of free-roaming dogs in their neighborhood (medium and low SES strata were 1.84 [95% CI: 1.05–3.21] and 4.19 [95% CI: 2.10–8.38], respectively). Of those who had contact with dogs, low SES respondents were less likely to use tick collars or any other product to avoid ticks on their dogs (OR: 0.40; 95% CI: 0.17–0.99), or check their dogs for ticks (OR: 0.25; 95% CI: 0.09–0.74).
Rocky Mountain spotted fever–related knowledge.
From the 59.3% (n = 237) who had heard of RMSF (RMSF-aware), 84.4% thought the disease was transmitted through tick bites and 4.2% associated the disease with living close to dogs with ticks. Some individuals incorrectly related transmission to contact with lice (5.0%), mosquitoes (4.2%), or other exposures (3.4%), and 7.2% did not know or were unsure about the mechanism of transmission (Table 4).
Knowledge from those residents who had heard about Rocky Mountain spotted fever before in Hermosillo, Mexico
Characteristic | Total (N = 237) |
---|---|
Forms of transmission | |
Tick bites | 200/237 (84.4) |
Contact with lice | 12/237 (5.0) |
Living close to dogs with ticks | 10/237 (4.2) |
Mosquitoes bites | 5/237 (2.1) |
Other | 8/237 (3.4) |
Do not know/unsure | 17/237 (7.2) |
Symptoms | |
Fever | 70/237 (29.5) |
Headache | 28/237 (11.8) |
Body ache (myalgia) | 17/237 (7.2) |
Join pain (arthralgia) | 8/237 (3.4) |
Diarrhea | 7/237 (2.9) |
Rash on feet | 6/237 (2.5) |
Petechiae | 6/237 (2.5) |
Abdominal pain | 1/237 (0.4) |
Other | 23/237 (9.7) |
Do not know/unsure | 152/237 (64.1) |
Prevention behaviors | |
Use tick collar | 108/237 (45.6) |
Clean up the backyard of old furniture | 61/237 (25.7) |
Avoid contact with dogs | 42/237 (17.7) |
Do not let kids play in the dirt | 3/237 (1.3) |
Do not allow dogs enter to home or work | 4/237 (1.7) |
Check for ticks on people | 2/237 (0.8) |
Do not know/unsure | 62/237 (26.2) |
Only one-third of RMSF-aware respondents (35.9%, n = 237) knew any RMSF symptoms. Of those who identified signs and symptoms, the most frequently identified were fever (29.5%), headache (11.8%), and body ache (7.2%). Arthralgia (3.4%), diarrhea (2.9%), rash on feet (2.5%), petechiae (2.5%), and abdominal pain (0.4%) were also mentioned, however, less frequently.
The most frequently reported (45.6%) preventive behavior among RMSF-aware respondents was tick collar use; other preventive practices included yard cleaning and disposal of old furniture (25.7%), and avoiding contact with dogs (17.7%). However, one in four of RMSF-aware respondents (26.5%) did not know or was unsure about any preventive strategy. The level of knowledge of disease prevention did not vary by SES among RMSF-aware respondents.
Medical care–seeking behavior.
After informing the respondents about the RMSF symptoms, a third of the total subjects (31.2%) reported that they would go to the hospital if they had any symptoms. Use of both private physicians and health department services was reported by 23.9% of surveyed. However, differences were observed by SES; private physicians would be more frequently visited by respondents in the high SES stratum (high = 36.1% versus medium = 19.6% versus low = 11.2%, P < 0.001). By contrast, a higher proportion of low stratum respondents reported that they would visit the health department facilities (high = 13.9% versus medium = 14.1% versus low = 38.3%, P < 0.001) (Table 5).
Medical care seeking for RMSF symptoms by SES in Hermosillo, Mexico
Medical care seeking | Total (N = 400), N (%) | SES (lack of goods) | P-value* | ||
---|---|---|---|---|---|
High (n = 159), % | Medium (n = 134), % | Low (n = 107), % | |||
In the presence of RMSF symptoms† | |||||
Hospital | 125/398 (31.2) | 36.7 | 30.1 | 25.2 | 0.447 |
Private physician | 95/398 (23.9) | 36.1 | 19.6 | 11.2 | < 0.001 |
Health department | 95/398 (23.9) | 13.9 | 14.1 | 38.3 | < 0.001 |
Emergency room | 69/398 (17.3) | 12.7 | 21.8 | 18.7 | 0.330 |
Physician in private pharmacy | 38/398 (9.6) | 7.0 | 10.5 | 12.2 | 0.423 |
Other | 2/398 (0.5) | 0.6 | 0.0 | 0.9 | – |
Not seek | 10/398 (2.5) | 3.8 | 2.3 | 0.9 | – |
Missing | 2 | – | – | – | – |
RMSF = Rocky Mountain spotted fever; SES = socioeconomic status. Bold values represent statistically significant associations.
P-values based on χ2 test (categories with 0–4 observations were excluded).
The sum of frequencies can exceed 100% because it is possible to attend more than one health facility. Therefore, each health insurance is reported as a separate variable.
DISCUSSION
Overall, although respondents in Hermosillo, Mexico, showed some familiarity with RMSF, four of 10 had never heard of it. Given recent outbreaks and the high case fatality rate, this is a serious concern. In neighboring Mexicali, Baja California, where RMSF was first detected in 2008, basic awareness of RMSF was higher, with 80% of individuals reporting they had heard of the disease. 19 Among Hermosillo residents who were aware of the disease, most knew it was transmitted by ticks, but their knowledge of symptoms and prevention strategies was low, which is similar to findings in Mexicali. 19 Our survey results indicate a serious gap in public awareness of RMSF and how to prevent it, particularly among the low SES respondents.
A high proportion of respondents (64.1%) did not know or were unsure about clinical manifestations of the disease. This lack of knowledge could result in delays in seeking medical care. Furthermore, lack of familiarity with the clinical profile of RMSF among healthcare providers may lead to delays in diagnosis even when care is sought. 9 Even after diagnosing the patient with RMSF, a study by Alvarez-Hernandez et al. 20 found that only 36% of physicians knew to prescribe the recommended treatment of doxycycline, particularly to children younger than 10 years. This highlights the need for integrative strategies to ensure recognition of symptoms in community members and primary care providers, and to ensure appropriate treatment protocols are being followed.
In our study, respondents in the low SES stratum were less likely to know that RMSF is transmitted by ticks and were less likely to engage in prevention activities than respondents in the middle and high SES strata. Associations between a range of SES indicators and elevated risk of mosquito-borne disease have been widely observed, with lower SES populations having a higher risk of transmission. 21–23 A study by Arellano et al. 24 in Hermosillo, Mexico, found related factors such as education and house structure showed a stronger relationship with occurrence of mosquito-borne diseases than simply household income. Few studies, however, have examined the association between socioeconomic determinants and tick-borne diseases (TBDs). A study based on county-level data from the central United States found poverty was the factor most strongly associated with RMSF prevalence, even more than environmental variables. 2 Another study conducted in 14 European countries found that background socioeconomic conditions, such as unemployment, poor nutrition, and economic uncertainty, increase susceptibility and the risk of TBDs. 25 By contrast, a study on Lyme disease incidence throughout the United States found more cases in wealthier areas, possibly reflecting the tick vector Ixodes scapularis’ abundance in wooded suburban habitats. 26
The lower levels of awareness of RMSF and knowledge of prevention strategies among respondents in the low SES stratum are worrying, as those individuals may be at the highest risk of RMSF infection. In particular, indigenous groups employed in agricultural activities in certain geographic areas of Hermosillo have been negatively impacted by a high burden of RMSF morbidity and mortality. 7 To effectively tackle the limited awareness of the population, educational strategies should consider the heterogeneous makeup of the target population, and use a One-Health approach addressing factors related to environment, humans, and nonhuman hosts. 27 Educational materials must be engaging and deliver clear, actionable messages that are inclusive of multiple backgrounds and include messaging in indigenous languages. Such materials could improve the level of awareness about preventive measures such as cleaning the home environment, restraining the ability of dogs to move about freely, removing ticks as soon as possible, and identifying disease symptoms promptly to seek treatment.
The study design had some limitations. Although the rate of refusals was low, a high proportion of households had no one at home, creating the potential for a nonresponse bias. Moreover, health-related practices and environmental assessment were not independently assessed but were based on self-report. Reports of “too many free-roaming dogs” were based just on the perception of participants, and respondents were not asked to specify how many dogs were “too many.” Finally, we did not have the capacity to explore previous RMSF infection and KAPs. The integration of disease data and community risk perception will strengthen future research and disease prevention activities at the regional level.
Promoting awareness among vulnerable populations about preventive measures and the timely identification of RMSF is key to mitigating the elevated fatality rates observed in this endemic region of Mexico. 1,9 Educational efforts should consider the heterogeneity of RMSF distribution in the population. For example, although we did not observe a significant association between levels of RMSF knowledge and age, RMSF mortality has recently begun increasing among adults (MOH, unpublished data). The shift toward adult populations challenges prevention programs as the profile of those at the highest risk comprised hard-to-reach populations who are at a high risk of severe illness. They usually have risk factors potentially related with adverse outcomes of the disease, such as chronic comorbidities, alcohol consumption, and social disadvantages (i.e., low level of education and lack of access to social media). 28
Our findings highlight the need to implement educational strategies to improve knowledge and awareness of RMSF, particularly clinical symptoms and prevention measures. Health promotion and educative efforts should emphasize the associated risk with dogs and the environmental presence of ticks, as well as the importance of early medical treatment of suspected cases. Improving KAPs in areas of high RMSF risk is likely to reduce disease burden, particularly among the more vulnerable populations.
ACKNOWLEDGMENTS
We thank all the staff involved in the field work: Lucía Castro, Rolando Díaz, Maria de los Ángeles Cabral, Christian Serna, Arlene Cabral, Eloísa Pinto, Edgardo Montoya, Guadalupe Insunza, Natalia Servín, Emmanuel Bernal, and Gustavo Cumplido.
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