https://orcid.org/0000-0002-1793-5983
Figures
Abstract
Over the past decade, Lyme and other tick-borne diseases have expanded into urban areas, including Staten Island, New York. While Lyme disease is often researched with a focus on human risk, domestic pets are also at risk of contracting the disease. The present study aims to describe differences in tick exposure, knowledge, attitude, and practices (KAP) between pet owners and non-owners, and to understand preventive strategies practiced by pet owners for themselves and their pets. We conducted KAP surveys via phone in 2020 and via face-to-face interviews in 2021, and we analyzed unique responses from 364 households on Staten Island. Pet owners were more likely to have ever found a tick on themselves or their household members (63%) than non-owners (46%) (p<0.001). Among pet owners, those who owned dogs (dog-only or both dog and cat owners) were more likely to have ever found a tick on their pets than cat-only owners (p<0.001). Compared with non-pet owners, pet owners were more likely both to know that ticks transmit Lyme disease (p<0.001) and to avoid gardening to reduce their tick exposure (p = 0.032), but they were less likely to wear protective clothing or adjust clothing (p = 0.013). Compared with cat owners who had never found a tick on their cats, cat owners who had ever found a tick on their cats were more likely to let their cats go outside (p<0.001). However, reported preventive measures on cats did not differ between pet owners who did and did not report tick exposure. The results indicate that encouraging pet owners to engage in preventative measures, both to protect themselves and their pets, is a potential avenue for healthcare providers and veterinarians to reduce risks from ticks.
Citation: Tamari N, Ernst KC, Enriquez AJ, Diuk-Wasser MA, Fernandez MP, Berry K, et al. (2024) Urban tick exposure on Staten Island is higher in pet owners. PLoS ONE 19(11): e0311891. https://doi.org/10.1371/journal.pone.0311891
Editor: Brian Stevenson, University of Kentucky College of Medicine, UNITED STATES OF AMERICA
Received: March 24, 2024; Accepted: September 25, 2024; Published: November 14, 2024
This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Data Availability: All relevant data are within the manuscript and its Supporting Information files.
Funding: This publication was supported by the Cooperative Agreement Number U01CK000509-01 between the Centers for Disease Control and Prevention and Northeast Regional Center for Excellence in Vector Borne Diseases awarded to MAD, and the National Science Foundation's Coupled Natural Human Systems 2/Dynamics of Integrated Socio-Environmental Systems (CNH2/DISES) program (Award #1924061) awarded to MAD (PI), MPF (co-PI), KCE (co-I), MHH (co-I) and KB (co-I). Its contents do not necessarily represent the official views of the Centers for Disease Control and Prevention, the Department of Health and Human Services, or the National Science Foundation. the funders had no role in the study design, the data collection and analysis, the decision to publish, or the preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Over the past decade, Lyme and other tick-borne diseases have expanded into urban areas, including Staten Island, a borough of New York City (NYC) coextensive with Richmond County, New York [1]. The incidence of Lyme disease per 100,000 was estimated at 10.8 in Richmond County between 2019–2021, which is less than half of the 34.8 per 100,000 incidence in the state of New York during that same time period [2]. However, ticks were found in one-third of yards in 2018, 2019 and 2021 within a half mile of green spaces across Staten Island [3]. Species identified included blacklegged ticks (Ixodes scapularis), lone star ticks (Amblyomma americanum), and Asian longhorned ticks (Haemaphysalis longicornis); I. scapularis transmits the agents of Lyme disease, human babesiosis, and anaplasmosis [3, 4]. The population density of tick species in sampled yards on Staten Island increased from 2020 to 2021, with blacklegged ticks increasing from 0.2 to 0.4 ticks/100m2, lone star ticks from 0.3 to 0.9 ticks/100m2, and Asian longhorned ticks from 1.0 to 4.0 ticks/100m2 [4].
While tick-borne diseases are often researched with a focus on human risk, domestic pets, particularly dogs, are also at risk of contracting Lyme disease. Lyme disease in dogs is generally milder and less frequent than in humans, and it is rare in cats [5, 6]. Sentinel surveillance using dogs has been proposed in multiple contexts [7–10], but the relationship between having pets in a household and risk of tick exposure and/or Lyme disease in humans is poorly defined. Jones et al. [11] conducted a study of pet ownership (hereinafter referred as “dog or cat owners”) in high Lyme disease incidence areas which indicated that individuals who own pets have more frequent tick encounters but similar risk of tick-borne diseases compared to individuals without pets. However, increased frequency of tick exposure is associated with increased tick-borne disease risk in other studies [12].
We hypothesized that pet owners may spend more time in recreational and natural areas including tick habitats than non-pet owners and may differ from non-pet owners in the types of preventive activities that their households take to reduce tick exposure (i.e., tick encounters or interactions with environments where ticks occur) on individuals and their pets. Further, we hypothesized that preventive measures may vary between dog and cat owners. For example, this could be due to dog owners perceiving themselves as having higher exposure to the outdoors due to spending time outside playing with or walking their dogs, on their properties and elsewhere. Alternatively, they may be concerned about their dogs bringing ticks in from the outside. Cat owners may not perceive these same risks, especially if they have indoor-only cats. To date, there has been limited research on how tick exposure and preventive measures differ between pet owners and non-owners. Understanding knowledge, attitudes, and practices (KAP) around tick prevention for pets and their owners may provide insights for educational messaging, particularly in areas where tick-borne diseases are newly emerging, and where people are less familiar with the risk factors for tick-borne disease. The present study was conducted on Staten Island, where the population density of tick species has recently increased in yards and parks [1, 3]. The aims were to: 1) determine if tick exposure differs between pet owners and non-owners on Staten Island, 2) describe differences in KAPs between pet owners and non-pet owners, 3) understand preventive strategies for pets practiced by pet owners, and 4) determine if these preventive strategies vary by self-reported tick exposure on individuals and their pets.
Materials and methods
Study area and target population
The study area was on Staten Island (149 km2), which is the least populated of the five NYC boroughs (Bronx, Brooklyn, Manhattan, Queens, and Staten Island), with a population of 495,747 in 2020 [13]. Of 712 identified cases with Lyme disease in NYC in 2019, 48 cases were confirmed on Staten Island, which was less than the 284 cases in Brooklyn and the 243 cases in Manhattan [14]. Transmission of tick-borne disease agents has occurred locally on Staten Island, while most cases in Brooklyn and Manhattan were contracted during travel outside of NYC [14, 15].
Blacklegged ticks, the primary vectors of the agents of Lyme disease, human babesiosis and anaplasmosis, are spread across Staten Island [14]. Lone star ticks and Asian longhorned ticks are also present; no human pathogens have been found in these ticks on Staten Island [15]. Although American dog ticks are found in all five NYC boroughs, blacklegged tick, lone star ticks and Asian longhorned ticks were found only on Staten Island and in the North Bronx. Staten Island is a newly emerging area for tick-borne diseases, and regular tick monitoring in NYC primarily takes place in its parks [1, 15].
We conducted KAP surveys via phone from June 8, 2020 to August 19 in 2020, due to the COVID-19 pandemic, and via face-to-face interviews from May 20, 2021 to July 20, 2021. Because exposure to ticks in urban areas is restricted to urban greenspaces and residents around these areas, our target ‘at-risk’ populations were residents living in a house with a yard within 500m of parks on Staten Island. The presence of ticks in the parks was verified by performing tick sampling [1, 3]. We focused our sampling on populations living and recreating in residential areas around urban parks because our focus was on local exposure; other urban residents could be exposed by long distance travel, which was beyond the scope of our study.
Data collection
For the 2020 phone surveys, phone lists for Staten Island were purchased from InfoUSA, Inc. (https://www.infousa.com/) and all households located within 500m of parks where ticks had been found in prior research investigations were eligible to be surveyed. In 2021, we carried out the survey at households located within 500m of park edges on Staten Island as described previously [3]. Briefly, we employed a random cluster sampling strategy and actively recruited 10–15 residents per cluster from randomly selected starting points. We also passively recruited residents through targeted advertising in newspapers and online platforms [3].
The KAP survey included demographics (age, self-reported race/ethnicity, gender, and education), tick exposure history (ever had Lyme disease, personally know anybody who has had Lyme disease, and ever found a tick on individuals or pets), perception on Lyme disease and tick-transmitted diseases (believe Lyme disease on Staten is increasing, and perception of how serious a problem are tick-transmitted diseases on Staten Island), knowledge about diseases that ticks can transmit, and prevention practices to reduce tick exposure on individuals and pets (self/body protection, actions related to avoiding a place/activity to reduce tick exposure on individuals during peak tick season, spending time in parks/natural areas on Staten Island in the past two weeks, gardening/working/playing in a yard in the last two weeks, living environment for pets, products used for pets, and whether or not pet owners let pets go outside) (S1 Appendix).
Verbal consent script was used to introduce the study to potential participants, and verbal consent was subsequently obtained from all participants. For consent, we checked a box on the survey once the participant had consented to proceed to the survey, and we stated that the participant could discontinue at any time. The survey was deemed minimal risk and had ethical clearance from The Institutional Review Board of Columbia University (protocol: AAAS9019).
Variables
Respondents’ ages were categorized as under 40, 40–49, 50–59, 60–69, 70 and above. Some variables were also recategorized due to limited data or clear interpretation: race as non-white and white; education level as high school graduate/General Equivalency Diploma (GED) or less, Associate’s/Some college/no degree, Bachelor’s degree, and Graduate or professional degree; and perception of how serious a problem are tick-transmitted diseases on Staten Island as very/extremely, slightly/somewhat, not at all, and not sure. For spending time in parks/natural areas or gardening/working/playing in a yard in the past two weeks, the response “parks are closed due to COVID19” was categorized as never.
Individual tick-preventive measures were classified into self/body protection and actions related to avoiding a place/activity to reduce tick exposure on individuals during peak tick season. Self/body protection included applying tick repellent, wearing protective clothes or treated clothing (long pants/ tuck pants into socks), checking for ticks and taking a shower after being outdoors. Actions related to avoiding a place/activity included avoiding going to parks, avoid engaging in outdoor activities in spring/summer/fall, sitting in yards, gardening, playing with kids outdoors, and areas with tick habitats.
Data analyses
Descriptive tables were stratified by non-pet owners versus pet owners, as well as by dog owners (“dog-only” or “dog and cat” owners) versus cat-only owners, using self-reported tick exposure status on individuals (yes/no), their dogs (yes/no), and their cats (yes/no). We categorized individuals who owned both dogs and cats as dog owners because those with a dog are expected to go outside more to walk the dog, as opposed to those with only cats not necessarily needing to go outside more. Additionally, dogs may bring ticks indoors, which would not be a concern with cats that predominantly stay in the house. We conducted chi-squared tests or Fisher’s exact tests for binary and categorical variables, and t-tests for continuous variables to investigate how demographics, knowledge, attitudes, and practices vary by pet ownership status and self-reported tick exposure status on individuals and their pets. Statistical significance was assessed using 2-sided tests with p-values less than 0.05 considered significant. R (version 4.3.2) was used for all data analyses [16].
Results
We pooled survey data from 2020 (n = 103) and 2021 (n = 262). After excluding one household due to missing information on pet ownership (n = 1), we had unique responses from 364 households. Although the survey was conducted via phone in 2020 and via face-to-face interviews in 2021, no significant differences were observed in demographics between survey years 2020 and 2021 (S1 Table). Of 201 households who owned a dog or cat, 123 had only dogs, 50 had only cats, and 28 had both dogs and cats.
Demographics
Pet owners (mean: 53 years, sd:14) were younger than non-pet owners (mean: 58 years, sd:17) (t287 = 2.6, p = 0.011). While there were no significant differences in gender and education-level between pet owners and non-pet owners, significant differences were observed in race (X2 = 4.0, df = 1, p = 0.046), with white respondents being more likely to own pets than all other respondents. Hispanic or Latino respondents comprised 7.5% of pet owners and 4.3% of non-pet owners (X2 = 1.6, df = 1, p = 0.213) (Table 1).
Tick exposure
Pet owners were more likely to have ever found a tick on themselves or their household members (63%) than non-owners (46%) (X2 = 11.1, df = 1, p<0.001). Among pet owners, those who owned dogs (dog-only or both dog and cat owners) were more likely to have ever found a tick on their pets than cat-only owners (X2 = 20.1, df = 1, p<0.001) (Table 1).
Knowledge
Pet owners were more likely to know that ticks transmit Lyme disease (95% vs. 83%; X2 = 13.2, df = 1, p<0.001). However, 65% of pet owners and 57% of non-owners knew specifically that deer tick/blacklegged tick transmits Lyme disease (X2 = 2.2, df = 1, p = 0.138). While 15% of pet owners and 11% of non-owners were aware that Rocky Mountain Spotted Fever (RMSF) is a tick-transmitted disease, fewer than 5% in either group were familiar with other tick-borne diseases (Table 1).
Tick preventive measures/outdoor activities
Pet owners were less likely to wear protective clothing or adjust clothing and avoid gardening to reduce their tick exposure during peak tick season compared with non-pet owners (protective/adjusting clothing: 30% for pet owners, 43% for non-pet owners, X2 = 6.2, df = 1, p = 0.013; avoid gardening: 2% for pet owners, 6% for non-pet owners, X2 = 4.6, df = 1, p = 0.032). Applying tick repellent to individuals and wearing protective clothes/adjusting clothing were the most reported tick preventive strategies for pet owners and non-owners, respectively. Tick checks were performed by 26% of pet owners and 19% of non-pet owners. Very few people practiced avoidance strategies such as avoiding sitting in the yard, gardening, or playing with children outdoors in either group (< 10%). Further, recreation in parks and natural areas was similar between groups (X2 = 3.7, df = 3.0, p = 0.300) (Table 1). Of those who never spent time in parks/natural areas on Staten Island in the last two weeks, two respondents stated that the parks were closed due to COVID19.
Living environment and preventive measures taken on pets
Most dogs went outdoors (96%), but only 31% of cats did. Using at least one product to prevent ticks on pets was reported by 46% of pet owners (63% for dogs, 14% for cats). There were no significant differences in preventive actions taken by pet owners who did and did not report a history of tick exposure on themselves or their household members (Tables 2 and 3). No significant differences were found in preventive actions taken on their pets between dog owners who had ever or never found a tick on their dogs. However, significant differences were observed between cat owners (Table 2). Compared with cat owners who had never found a tick on their cats, cat owners who had ever found a tick were more likely to let their cats go outdoors (Fisher’s exact test, p<0.001) or apply Revolution (spot on) to them for tick prevention (Fisher’s exact test, p = 0.032), whereas they were less likely to prevent cats from going outside (Fisher’s exact test, p = 0.025) (Table 3). While there was a significant difference in using at least one product between cat owners who reported a tick on their cats (39%) and those who did not (13%) (Fisher’s exact test, p = 0.038), no significance was observed in taking at least one tick preventive action for their cats (X2 = 0.2, df = 1, p = 0.647).
Discussion
Our findings based on a sample of at-risk residents on Staten Island, an urban area with significant green spaces where tick-borne diseases are newly emerging were consistent with previous reports of tick exposure being higher among individuals who own pets [11]. There were several differences in knowledge and practices between pet owners and non-owners, but they do not account for tick exposure variability. Pet owners were more likely to know that ticks could transmit Lyme disease, which could theoretically translate into greater adherence to tick prevention practices. However, pet owners and non-owners engaged in similar levels of personal preventive measures except that wearing protective clothing and avoiding gardening to reduce their tick exposure were more prevalent among non-owners. Our hypothesis that pet owners spend more time in recreational and natural areas that support tick habitat was not supported, as reported outdoor activities were similar for pet owners and non-pet owners. Cat owners who reported finding ticks on their cats were more likely to use Revolution for their cats than those who did not report ticks. Other preventive products used for pets did not differ based on self-reported tick exposure for individuals and their pets.
Pet owners reported less use of protective clothing than non-pet owners as a preventive strategy. Pet owners may feel uncomfortable wearing such clothing due to the different types of exercise they engage in with their pets. Since pet owners generally tend to spend more time outdoors than non-pet owners [17–20], wearing protective or adjusting clothes can make them feel too warm, leading them to avoid this measure. Additionally, the difference in the use of protective or adjusting clothing may be explained by the different distribution in age and ethnicity between pet owners and non-pet owners. In the present study, pet owners were younger and included fewer Hispanic/Latino individuals compared to non-pet owners. Factors related to these demographics, such as the type of outdoor activities, occupation, or income, may influence the use of protective or adjusting clothing. For example, similar to pet owners, younger individuals, who typically engage in more physical activities than older ones [21–23], may opt not to wear such clothing.
In the present study, both pet owners and non-owners spent time in their yard on most days (more than three days a week) and rarely checked for ticks or took a shower or bath after being outdoors, despite recommendations by the Centers for Disease Control and Prevention (CDC) [24] and the effectiveness of these measures in preventing tick-borne diseases [25]. Participation in preventive practices among our sample of at-risk Staten Island residents was relatively low, with 20% performing a tick check and 5% taking a shower or bath after outdoor activities, as compared to 30–70% and 15–40%, respectively, in studies of the general population [26] and 55–68% and 40–59%, respectively, in several Lyme disease-endemic areas in the United States [27–29]. Since ticks, including blacklegged ticks, were found in one-third of yards within a half mile of green spaces across Staten Island [3], such preventative practices are an important potential avenue for both pet owners and non-owners to reduce risk, especially considering factors like the potentially high cost of purchasing protective clothes and the safety concerns around chemical repellents [26, 29]. As demonstrated in previous studies [26, 30], community-wide educational intervention may increase preventive actions taken by individuals both for themselves and their pets.
The present study demonstrated lower tick prevention on pets (46%) and higher tick exposure on individuals and pets (over 60%) on Staten Island compared to several tick-borne disease endemic areas, where tick prevention for pets exceeded 80% and tick exposure was around 30% [11, 31]. The idea that pets may bring ticks into shared living spaces is an area that needs more exploration. We found that most dogs and some cats were reported to go outdoors, though it was not specified in the question whether respondents related this to tick exposure. Assuming that dogs are more likely to spend time outside than cats, this could explain why people who owned a dog were more likely to have found a tick on their pet than cat-only owners. It could be anticipated that pet owners who took precautions with their pets would be less likely to have pets that harbored ticks and more likely to report lower levels of exposure on themselves and household members. Yet, precautions did not significantly differ between respondents or their household members who were exposed to ticks and those who were not.
Owners of cats reporting ticks on their cats were more likely to treat them with Revolution for tick prevention than cat owners who did not report ticks. These cat owners may have started using Revolution after discovering ticks on their cats. Alternatively, because our data did not distinguish between Revolution (selamectin) and Revolution Plus (selamectin and sarolaner), Revolution alone may have been ineffective against ticks, particularly blacklegged ticks [32]. Further investigations with larger sample sizes and more detailed information could yield additional insights. It is possible that some participants did not report products used to prevent ticks on their pets, or that those who used preventive measures engaged in behaviors that exposed them to more tick habitat. The temporality, frequency, dose, and adherence of medical collars or chews/drops on pets were not captured, nor were their efficacy or costs. Their effects wane over time and may be affected by improper dosing [29].
There are several limitations in the present study. First, we did not account for quantities in some questions. The “ever found a tick” questions did not distinct between finding one tick or 100 ticks on oneself or household members, or their pets. Additionally, our data did not include the amount of time spent outdoors when being outside. The information might influence tick preventative measures they take for themselves and their pets. Second, the survey was conducted during the height of the COVID-19 pandemic. Some people altered their behaviors, including frequency and patterns of outdoor activities, which may not fully represent their lifestyles post-pandemic [33–36]. Third, we did not specify the duration of pet ownership. Global interest in pet adoptions temporally increased during the COVID-19 pandemic [37]. Some pet owners might have been new owners who adopted during the COVID-19 pandemic and had not yet modified their behavior. Duration of ownership might influence tick exposure history, knowledge, or behaviors among pet owners. Fourth, the self/body protection actions and place/activity avoidance actions that were used in the present study were the most common preventive measures for individuals in other geographic areas [27–29], but these variables may not cover all preventive measures.
Conclusion
Pet owners or their household members were exposed to ticks more frequently than non-owners in a sample of at-risk Staten Island residents, an urban area with extensive green spaces. However, reported preventive measures for pets did not differ between pet owners who reported tick exposure and those that did not report tick exposure. The results indicate that healthcare providers and veterinarians could attempt to reduce risks from ticks by encouraging pet owners to engage in preventative measures for themselves and their pets.
We are unable to determine if pet owners might be exposed to higher risk habitats while recreating in natural areas than non-pet owners, whether through their own activities or their pets’ activities. Further investigations into the details of pet, pet owner, and non-pet owner activities in parks or yards, as well as more in-depth assessments of frequencies of administering prevention and control strategies, may yield more insights into the relationship between pets and human exposure to ticks.
Supporting information
S1 Table. Demographic and pet ownership characteristics of at-risk Staten Island residents by survey year.
https://doi.org/10.1371/journal.pone.0311891.s003
(DOCX)
Acknowledgments
We would like to acknowledge our field assistants (Michaela Mincone, Olivia Card, Catherine Grady, Myles Davis, Brigitte Franco, Lily Davenport, Robert Cassidy, Patrick Connelly, Torre Lavelle, Richie Konowal, Gabriela Galindo and Christina Ng) for providing research support. The survey described in this information product was organized and implemented by Columbia University and was not conducted on behalf of the U.S. Geological Survey.
Disclaimer: The survey described in this information product was organized and implemented by Columbia University and was not conducted on behalf of the U.S. Geological Survey.
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