Study on public perceptions and protective behaviors regarding Lyme disease among the general public in the Netherlands: implications for prevention programs

Lyme disease (LD) is the most common tick-borne disease in the United States and in Europe. In the Netherlands, the number of General Practitioner (GP) consultations for tick bites has increased from 191 per 100,000 in 1994 to 564 per 100,000 in 2009 [1]. In 1994, the incidence of patients visiting the GP for Erythema migrans (EM, an asociated symptom) was estimated at 39 per 100,000 inhabitants. This number increased to 134 per 100,000 in 2009 [1]. Similar trends have been observed in other European countries [2]. The emergence of Lyme borreliosis may have been partly caused by an increased awareness among citizens and medical personnel, and changes in pathogen and vector populations [3].

Transmission of LD requires the presence in the area of: (1) the spirochete Borrelia burgdorferii sensu lato (in Europe) in an animal reservoir that is capable of transmitting the spirochetes to feeding ticks; (2) the vector, in European ticks belonging to the Ixodes ricinus group; and (3) susceptible hosts, including humans. Forested areas and recreational sites such as parks and gardens are associated with a higher risk of tick bites [4].

In humans LD develops in three stages. In the first stage (the early localized infection), people may experience fever, headache, fatigue and depression. The most commonly recognized symptom at this stage (occurring in about 90% of patients) is a circular red skin rash around the place of the tick bite: erythema migrans. Antibiotics administered at this stage will prevent further stages developing. Untreated, the infection may spread from the site of the bite to other parts of the body, producing an array of distinct symptoms that may come and go, including: additional EM lesions in other areas of the body, facial or Bell’s palsy (loss of muscle tone on one or both sides of the face), severe headaches and neck stiffness due to meningitis (inflammation of the spinal cord), pain and swelling in the large joints (such as knees), shooting pains that may interfere with sleep, heart palpitations and dizziness due to changes in the heartbeat. This is called the second stage (early disseminated stage). Many of these symptoms will resolve over a period of weeks to months, even without treatment. However, a lack of treatment can result in additional complications. Approximately 60% of patients with an untreated infection may begin to have intermittent bouts of arthritis, with severe joint pain and swelling. Without treatment, LD enters the third stage after several months. During this stage, the patients develop chronic symptoms that can affect a wide range of body parts, including the brain, nerves, joints and the heart [5].

Recommendations for first line treatment from most European countries and the USA specify doxycycline or amoxicillin, with minor differences in doses and treatment duration. Both agents have proven efficacy, but a small proportion of patients have persistent symptoms following appropriate treatment for LD [6]. Because no vaccine is available and effective measures for controlling tick populations are still in the experimental phase or insufficient, health education is considered the most important approach for preventing LD. The National Institute of Public Health and The Environment (RIVM) provides information on public health topics to professionals and to the general public. This includes a national guideline on the prevention and control of LD for professionals [7] and several brochures for the general public. In the Netherlands, the local public health services are responsible for sending out the guideline and brochures to professionals (e.g. GP’s, camping holders) and to the public.

Preventive strategies include the avoidance of tick-infested areas, the use of protective clothing (e.g. wearing long-sleeved shirts and long trouserpants, which reduce the area of exposed skin), routine body checks for ticks after being outdoors, and the use of tick repellents on either the skin or clothing.

Despite the availability of Lyme prevention advice, public compliance with the LD-guidelines could be improved [8]. Surveillance of perceptions and behavioral responses of the general public to ticks and LD is required for improving health risk communication and achieving successful changes in public behavior [9–13].

However, in the Netherlands very little is known about the perception and protective behavior of people in relation to the prevention of tick bites and LD [14]. In 2010 Maat and Konings found in their study among 600 residents in the Southwest of the Netherlands that many respondents lacked skills for recognizing and removing ticks, underestimated their personal risk for tick bites and found protective measures exaggerated [15]. They concluded that new prevention strategies should focus on self-efficacy, risk perception, and the presentation of alternative measures, e.g. skin check instead of wearing protective clothing. In the present study our aim was to examine the knowledge, perceived risk, feelings of anxiety, and behavioral responses of the Dutch general public related to ticks and LD. The questionnaire was based on an integrated model to explain health behavior, including constructs from the Protection Motivation Theory and the Health Belief Model [16, 17]. Protection Motivation theory has been used as a model for predicting health behavior. A threat appraisal is formed by an individual based on their perceived likelihood of a particular event occurring and their perceived severity of the event. The way in which an individual chooses to respond to a threatening situation is termed their coping appraisal, and is based on both the belief that uptake of a recommended behavior will resolve the threat (response efficacy), and an individual’s belief in his/her own ability to effectively perform the behavior (self-efficacy).

In the Health Belief Model, perceptions of the individual are at the core of the model, which posits that the beliefs of individuals about their own susceptibility to a health threat, their perceptions about the severity of that threat, and their perceptions about the benefits and barriers associated with a particular protective action, will determine whether or not they adopt that action. Extensions to the model suggest that the ‘self-efficacy’ (their belief in their own ability to perform a given behavior) of an individual also plays a strong role in determining whether a behavior is adopted, as does the existence of cues to action that prompt or remind someone to engage in a particlar behavior.

The results will act as a guide for further development of effective LD prevention programs by identifying those measures most likely to be adopted by the general public in the Netherlands.

A total of 550 panel members were invited to participate in this study, of whom 362 completed the questionnaire (response rate 66%). Of the 362 respondents, 51% was female (data not shown). The age varied from 18-29 years (14%), 30-49 years (35%) and ≥50 years (51%). Thirty-seven percent had a low educational level (i.e. primary education, lower general or lower vocational education or less), 38% an intermediate (i.e. secondary general or vocational education), and 25% a higher education (i.e. higher professionals education or university). More than half of the respondents were employed, and in 36% of the households there were one or more children. The overall majority were of Dutch origin. Most respondents lived in the middle (45%) and the south (46%) of the Netherlands. Twelve percent of the respondents had had a tick bite once and 9% had repeatedly had tick bites in the Netherlands. Around half of the respondents were regularly (every week/once a month) physically active in a garden, 37% visited the woods regularly and 21% visited open areas regularly.

In this study we identified the main predictors and motivators that influence protective behavior for preventing tick bites and LD. We did this by investigating the knowledge, perceptions and efficacy beliefs of healthy people in the general population in the Netherlands, a country in which the incidence of LD has increased sharply throughout the past two decades.

Insight into public perceptions and protective behavior regarding LD is crucial in order to develop a successful prevention program [9]. We conclude that good general knowledge about preventing tick bites and LD is scarce, while the perception of risks and self-efficacy of the measures varies greatly among the respondents.

Only 35% of the respondents reported a good general knowledge of LD, and only a quarter were aware that using repellent skin products can protect against tick bites. Suboptimal public knowledge regarding LD was also found in other studies in endemic areas. For example, Heller et al conducted a questionnaire study among 103 Brazilian residents -living in a Lyme disease endemic area in the United States-, and reported that 36% of the respondents had never heard of the disease and 62% were not certain they could recognize the symptoms [9]. Higher levels of knowledge seem to positively influence protective behavior as demonstrated by Gould et al. [10]. However, research in areas where LD is endemic has demonstrated that despite adequate knowledge about its symptoms and transmission, many people do not perform behaviors to reduce their risk of infection [25]. These findings suggest that a lack of knowledge is not the only reason for poor uptake of protective behavior.

Nearly all respondents perceived high severity of LD, but perceived vulnerability and feelings of anxiety were lower. The fact that the majority of the respondents perceived low personal risk of LD, implicates some public underestimation, especially, given the fact that people in the Netherlands, in particular those who often visit woodland areas, have a real risk of getting tick bites and developing LD [26]. The underestimation of risk is found to have been caused by factors such as lack of knowledge. Furthermore, if people underestimate their personal risk they will be less willing to engage in preventive behavior [13, 27].

Higher levels of self-efficacy, respons efficacy and intention were observed for checking the skin after being outdoors and removing ticks if necessary. However, lower levels of (self-)efficacy and intention were observed for wearing protective clothing and using insect repellent skin products. The fact that most respondents in our study were unaware that using repellent skin products can protect against tick bites, might also be related to the lower levels of intention to use these products.

The percentage of respondents taking preventive measures ranged from 6% for using insect repellent skin products, to 40% for wearing protective clothing. These percentages are rather low, compared to other studies. Studies in the US reported that 66%-99% of the respondents took measures to prevent LD [10, 22, 23]. Furthermore, Heller et al found that the majority (78%) of the Brazilian respondents wore long trousers when outdoors and Herrington reported that one-half of the US respondents also did this [9, 24]. The lower levels of wearing protective clothing in the Netherlands, especially in the summer, could be caused by the climate. The Netherlands has a maritime climate, with cool summers and an average temperature of 19 °C in July. People in the Netherlands like wearing (light) clothing, such as shorts and short sleeved shirts, if the temperature increases. Also the fact that people believe that wearing protective clothing in nature areas is overdone, as reported in this study, might be a reason for the low levels of wearing protective clothing as reported by Cartter et al. [13].

One-third of the respondents in our study reported checking their skin after being outdoors. This is comparable with other studies; i.e. Heller et al who described that only 28% of the Brazilian population check their skins for ticks [9]. The main barriers for checking skin for ticks reported in our study were low perceived personal risk and not knowing how to recognize a tick.

Only 6% of our respondents reported using repellent skin products. The low use of insect repellent skin products was also been found in other studies. For example, in Brazil and the US 66% and 69% of the respondents respectively never used insect repellent skin products for protection against LD [9]. In our study a barrier for using repellent skin products is that people are not convinced about their efficacy or do not like to use these products. Herrington investigated barriers for using insect repellent skin products, and found that a substantial proportion of US respondents believed that using insect repellent could make them ill [24]. This underlines the need for people to “believe” in the effectiveness of a recommended behavior as well as they should have appropriate knowledge on the subject.

There were some differences in public perceptions regarding LD among socio-demographic subgroups. For example, females reported higher levels of perceived efficacy and self-efficacy to check their skin after being outdoors, whereas older respondents (≥ 50 yrs) reported higher levels of perceived efficacy, self-efficacy and an intention to wear protective clothing. However, in multivariate analysis, of all socio-demographic variables only employment status remained a significant predictor for wearing protective clothing for preventing tick bites.

As reported in our study, having had tick bites in the past, higher levels of knowledge and moderate/high levels of concern were significant predictors for checking the skin. Significant predictors of wearing protective clothing were being unemployed/retired, higher knowledge levels, higher levels of concern about LD and higher levels of perceived efficacy of wearing protective clothing. These findings are in accordance with Herrington [24], reporting that having seen ticks, being concerned about being bitten, having heard about LD and knowing someone who had LD are the factors most predictive of specific tick-bite protective behavior. Mowbray et al. showed in his review that both knowledge and attitudes towards tick-borne disease are amenable to change via an education campaign [28]. Unfortunately, in his systematic review of all previous studies that assessed the impact of education or behavioral interventions on the uptake of behaviors intended to protect against tick-borne diseases he could find only nine studies, of which only three took the form of a randomized controlled trial (RCT) [28]. One RCT studied the willingness to the uptake of a vaccine for LD and two focussed on other protective measures. Lawless et all used an instructional video with a mock horror movie theme to improve knowledge, attitudes, and behaviors towards LD prevention in 13- to 16-year-olds from four Connecticut towns [29]. One month and six months after seeing the video, knowledge, attitudes and behavior had increased significantly in the intervention group. Another study investigating the effectiveness of an educational intervention was performed by Daltroy et al. In over 30000 passengers on ferry boats to a Lyme-endemic area of Nantucket Island. In this study controls received education about bike safety, while intervention participants received information on preventing tick-borne disease, particularly LD. Information was delivered on board by entertainers to make the messages more compelling. Two months after the intervention, experimental participants were more likely than controls to adopt precautionary behaviors, as well as to check themselves daily for ticks. In conclusion, future prevention programs for LD should focus on improving public knowledge, i.e. with regard to disease severity and vulnerability, efficacy of measures and on how to take preventive measures.

This is the first national study to evaluate the perceived LD-risk and protective behavior for LD in the general public in the Netherlands. Nevertheless, there are a number of limitations to our study. The majority of respondents (51%) was older than 50 years. This may have limited the generalizability of the results, although older age has not been found to be a distinct factor associated with compliance to preventive measures for LD found in previous studies. Furthermore, potential selection bias may have been introduced in that only respondents with a computer were interviewed by this online survey. Finally, cross sectional studies can prove a rich baseline of data points but should not be used to make causal statements, given the lack of a temporal sequence of events.

Our study has several implications for the development of LD prevention programs. It demonstrates that knowledge, level of concern and perceived efficacy of measures are the main determinants of preventive behavior. Therefore future prevention programs should focus on these determinants, for example, by providing facts and raising awareness about LD and protective measures that can be taken. Since protective measures like wearing protective clothing and using insect repellents are not ‘popular’, it is important that prevention programs focus on removing any barriers for complying with these protective measures, especially in people who have never had tick bites and those who are less concerned about the risks. Furthermore, it is important to tailor the information to specific socio-demographic subgroups and high risk groups.

Promoting preventive measures for LD is really important since reducing the tick population and developing a vaccine can only be seen as long-term solutions for the problems. The results of this study can be used as a base for developing effective prevention programs that connect with the needs of the target group, with the main goal to increase compliance with recommended measures.

The challenge is to take the principles demonstrated in this study and apply them to prevention programs. Some work in this area has already been done. Last year the Netherlands National Institute of Public Health and The Environment redesigned the national public information campaign on ticks and LD in the Netherlands. In this campaign the focus was shifted. First, not all possible evidence based preventive measures on LD were presented in the communication, instead the focus was placed on checking the skin and removing ticks. Also a educational game was developed, called in Dutch: “Teekcontrol.nl“, to teach children playfully about ticks and LD. In this online game children can discover where ticks are most likely to be found and why it is important to check the skin after playing outdoors. Within 8 months of launching over 30.000 children had played this game. The learning effect of the game will be evaluated in 2012. Furthermore, a mobile phone app on ticks and LD is currently being developed. This will be based on a user- centered design. This means that the public will determine the features of this application.