Ticks and Tick-borne Diseases

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Ticks and Tick-borne Diseases 12 (2021) 101728

Available online 8 April 2021

Do tick-borne diseases affect outdoor teaching in Slovenian preschools?

Gregor Torkar *, Marjanca Kos

Faculty of Education, University of Ljubljana, Slovenia

A R T I C L E I N F O Keywords:

Tick

Tick-borne diseases Outdoor education Preschool teachers Attitudes

A B S T R A C T

Childhood experiences with nature are decisive for children’s wellbeing. The need for outdoor activities has been duly recognized in the preschool curriculum in Slovenia. However, there are some obstacles to this approach-

—specifically, tick-borne diseases. This study examines the views and experiences of Slovenian preschool teachers (n =158) with ticks and tick-borne diseases in order to create a safer environment for the further development of outdoor education. The majority of the respondents engage in outdoor teaching once or several times a week. They have very frequent contact with ticks and tick-borne diseases in their professional lives. More than four-fifths of the respondents carry out some tick-prevention measures in preschools, but room for improvement remains. The respondents report rare cases in which parents or guardians have tried to prohibit them from visiting outdoor areas because of tick-borne diseases, and they explain how they dealt with the situation. The attitude of preschool teachers toward ticks and tick-borne diseases did not correlate significantly with the frequency with which they went outdoors in preschools. This study therefore concludes that, despite the objective risks associated with tick-borne diseases, there is still broad consensus among educators and parents on the importance of outdoor education in the early years.

1. Introduction

1.1. Tick-borne encephalitis and Lyme borreliosis: barriers to outdoor play and learning

Tick-borne encephalitis (TBE) and Lyme borreliosis (LB) are tick- borne zoonoses and are the most common tick-borne diseases in Slovenia (National Public Health Institute of the Republic Slovenia, 2020a). Although only a minority of individuals that experience a tick bite will develop a disease, the health impacts can be significant. There has been a marked increase in the incidence of these two tick-borne diseases over past decades, and so they constitute a rapidly growing health risk (Lindquist and Vapalahti, 2008; Slunge et al., 2019; Stanek et al., 2012; Steffen, 2019; Strle, 1999).

LB is the most common tick-borne disease in the northern hemi- sphere. It is caused by bacteria within the Borrelia burgdorferi sensu lato species complex. Infection can be asymptomatic or symptomatic. The skin is the most frequently affected organ, mostly as a skin lesion (ery- thema migrans) but also as borrelial lymphocytoma, which can later be followed by heart and nervous system involvements and arthritis (Sta- nek et al., 2012). Treatment with antibiotics is beneficial for all clinical manifestations of LB. However, such therapy is most effective early in

the course of the illness. Vaccine is currently in development (Eisen, 2021; O’Bier et al., 2021; Strnad et al., 2020; Mihajlovi´c et al., 2019).

TBE is caused by the tick-borne encephalitis virus (TBEV), a flavi- virus transmitted by Ixodes spp. ticks. The virus may cause severe central nervous system infections. After TBE, a third of patients have long- lasting impairment, frequently with cognitive dysfunction and neuro- psychiatric problems (Bogoviˇc and Strle, 2015; Haglund and Günther, 2003; Lindquist and Vapalahti, 2008). The disease arises in patchy endemic foci over a wide area in Europe and Asia, where ecological and climate conditions are suitable for natural circulation of the virus (Bogoviˇc and Strle, 2015). It is maintained in cycles including ticks and wild vertebrate hosts, with humans being only accidental hosts.

Although the disease can be prevented with vaccination, thousands of people develop TBE annually (Lindquist and Vapalahti, 2008). Slovenia is one of the countries with the highest registered incidences of LB and TBE in the European Union; the corresponding incidences of 260/100, 000 and 10/100,000 for TBE exceed the respective average European estimates by twenty-five to thirty times (Arneˇz and Avˇsiˇc-Zupanc, 2009; ˇ Blaˇsko-Markiˇc and Soˇcan, 2012; Bogoviˇc and Strle, 2015; ECDC, 2012;

Mihajlovi´c et al., 2019; National Public Health Institute of the Republic Slovenia, 2020a). Both TBE and LB affect children (on average 10–20%

of all reported cases of TBE) (Arneˇz and Avˇsiˇc-ˇZupanc, 2009). Overall,

* Corresponding author.

E-mail address: gregor.torkar@pef.uni-lj.si (G. Torkar).

Contents lists available at ScienceDirect

Ticks and Tick-borne Diseases

journal homepage: www.elsevier.com/locate/ttbdis

https://doi.org/10.1016/j.ttbdis.2021.101728

Received 29 October 2020; Received in revised form 28 March 2021; Accepted 31 March 2021

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the clinical course of TBE is milder compared to adults. However, severe courses of TBE with sequelae and even death have been reported (Arneˇz and Avˇsiˇc-ˇZupanc, 2009; Weisshaar et al., 2006).

Effective preventive measures include behaviors such as wearing appropriate clothes (long-sleeved shirts, white or light-colored clothing, closed shoes), use of repellent, careful (self)inspection for ticks, and prompt removal of attached ticks. Educational prevention, which com- prises disseminating information through the media, is also important (Hayes and Piesman, 2003; Pearson, 2015; Richardson et al., 2019;

Slunge et al., 2019; Weisshaar et al., 2006). Slunge et al. (2019) reported a general lack of knowledge about ticks and tick-borne diseases which concerns awareness of the problem and general knowledge about LB and TBE. Providing information that leads to increased knowledge about ticks and tick-borne diseases was suggested as a relevant public health strategy by Slunge et al. (2019).

Among the barriers hampering children’s outdoor activities, Slove- nian educators have clearly highlighted the problem of tick-borne diseases (Kos and Jerman, 2013). Research by Weisshaar et al. (2006) shows that attending a forest preschool (i.e., preschools located in a forested area where children spend all seasons outdoors full time) is a risk factor for encountering ticks or being bitten by ticks and for suffering from LB. Children in a forest preschool have a 2.8-times higher risk of having at least one tick bite and a 4.6-times higher risk for coming down with LB than children in conventional preschools.

1.2. The benefits of children’s engagement with nature

Childhood experiences with nature are crucial for children’s lives because they contribute to various developmental outcomes and influence various areas of wellbeing. Several studies have shown the benefits of nature for child development. Nature has been identified as a space that supports physical and mental health, emotional wellbeing, and a better ability to cope with stress (Adams and Savahl, 2017; Gill, 2014).

When outdoors, children are more interested, concentrate more, and enjoy learning more. Nature promotes learning by improving learners’ attention and self-discipline, and reducing their stress levels. It provides a more supportive, calm, and safe learning context (Kuo et al., 2019;

Mårtensson et al., 2009). Nature offers an incredible wealth of loose items, open materials, and objects for children to manipulate (Dankiw et al., 2020; Klofutar et al., 2020; Wilson, 2012).

Many studies have shown that children are physically more active when they are outdoors (Cleland et al., 2008; Dankiw et al., 2020; Gill, 2014; Torkar and Rejc, 2017). Walking over rough terrain, climbing trees, and running around in the natural environment has positive effects on children’s motor development, improving gross and fine motor skills and endurance, coordination and balance, and health-related fitness (Fjørtoft, 2004; Santana et al., 2017). Physical activity is also important for reducing the risk of obesity. This is particularly important in early childhood, and patterns in the early years are transferred to patterns of physical activity in adult life (Cleland et al., 2008; Dankiw et al., 2020; Herman et al., 2009).

Nature has prosocial effects and promotes warmer, more cooperative relationships (Dankiw et al., 2020; Scott et al., 2013, 2018). In the natural environment, children feel more autonomy and freedom (Adams and Savahl, 2017; Dankiw et al., 2020; Kuo et al., 2019). Outdoor play and learning have a positive impact on children’s self-esteem, self-- confidence, and self-perception, as well as on their decision-making and risk-taking (Gill, 2014; O’Brien and Murray, 2007; Sandseter, 2009;). It helps children acquire perseverance, self-efficacy, resilience, teamwork, leadership, and communication skills that are important later in adult life (Kuo et al., 2019).

1.3. Scope and focus of the research

Preschool education and care in Slovenia are optional. Children can enroll in preschool as early as 11 months of age, and they can attend

until the start of compulsory education at age six years. The preschool education system is set up in a uniform manner for all children and is subsidized by the state. Most children attend public preschools (94 % in 2018/2019). The curriculum is divided into six fields, with “nature” as the science-education field. Hands-on activities, outdoor education, and experimental learning are explicitly encouraged in the curriculum.

Knowledge of the local natural environment is one of the learning ob- jectives (Eurydice, 2020). The many benefits of playing and learning in a natural environment and the considerable time children spend in preschools require the full integration of outdoor activities into the curriculum. This need has been duly recognized in Slovenia in the preschool curriculum. It is important to follow this directive from early childhood in order to avoid irreparable damage to the development and teaching of children’s environmental ethics due to a lack of the many positive experiences available in the natural environment. Slovenia, as a densely forested country with more than half of its territory covered by forests (State of Europe’s Forests, 2011), has good opportunities to include outdoor play and learning in education. A study by Kos and Jerman (2013) showed that forests are easily accessible to the majority of Slovenian preschools. Although outdoor activities are routine in Slove- nian preschools, parents and preschool teachers share the opinion that more attention and time should be devoted to playing and learning in the natural environment. However, there are some limits to this approach. One of them is tick-borne diseases—in particular, TBE and LB.

Slovenian educators (Kos and Jerman, 2013) pointed out this fact, which could be a major obstacle to including outdoor activities in the educational program in Slovenia. Whether this obstacle is a reason to prefer indoor activities to outdoor activities remains controversial.

The aim of this study was to determine the views and experiences of Slovenian preschool teachers regarding ticks and tick-borne diseases.

The main objective was to explore the practices of preschool teachers in the prevention of tick bites and tick-borne diseases, their communication with parents on this topic, and their attitudes toward ticks and tick- borne diseases, to thereby create a safer environment for the further development of outdoor education. The aim was also to organize a small workshop with a focus group of preschool teachers to discuss the findings and get feedback on the presented tick bite-prevention activities for preschool children.

The research questions underlying this study are as follows:

1 What experiences have preschool teachers had with ticks and tick- borne diseases and outdoor education?

2 Which tick bite-prevention measures do preschool teachers take?

3 How do they communicate with parents about this topic?

4 How does the attitude of teachers toward ticks and tick-borne diseases correlate with the frequency with which they engage in outdoor activities?

5 How does the attitude of preschool teachers correlate with their experience with ticks and tick-borne diseases?

2. Methodology 2.1. Sample and procedure

Table 1 presents data on teachers’ sex and work experience, the location of preschools, and vaccination against TBE. Our sample con- sisted of 158 Slovenian preschool teachers, four (2%) male and 154 (98

%) female, who worked in public (state-financed) preschools.

Teachers completed an online questionnaire designed for this study.

Participation in the study was voluntary and anonymous, and no benefits were offered to the participants. According to Slovenian rules, such surveys do not need the approval of an ethical or similar body. Based on the knowledge of the population and the purpose of the study, a purposive sampling technique was used. In purposive sampling, researchers select the cases to be included based on their assessment of the typicality or presence of the characteristics they are looking for, thus creating a

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sample that meets their specific requirements. It can be used to access those who have in-depth knowledge on specific topics (Cohen et al., 2017). There are currently 409 public and private preschools in Slovenia. Data on preschool education by statistical regions of Slovenia, 12 regions in total, were used to invite preschool teachers. In each re- gion, a total of 10 preschools were randomly selected and contacted through the official email available on the website of the Ministry of Education, Science and Sports (2021).

The survey included some basic sociodemographic variables (sex, years of work experience, and location of the institution). Next, the teachers answered closed (yes/no) and open-ended questions about their experiences with ticks and tick-borne diseases and about outdoor education, prevention of tick-borne diseases, communication with parents, and their attitudes toward ticks and tick-borne diseases (using the 5-point Likert scale: 1 =completely disagree to 5 =completely agree). A tool was developed to measure teachers’ attitudes toward ticks and tick- borne diseases (see Table 2). It was primarily used to determine how their attitudes toward ticks and tick-borne diseases influence the frequency of outdoor activities. In addition, we investigated relationships with several measures; namely, vaccination against TBE, the incidence of tick bites on children, personal knowledge about people with tick- borne diseases, and years of work experience. All questionnaires were completed between September 2016 and May 2017.

In addition, the preliminary results of the study were presented in

May 2017 to a focus group of teachers and preschool directors (n =9) that voluntarily participated in a workshop held at the University of Ljubljana’s Faculty of Education. A workshop was prepared for them, where the findings of the study and tick bite-prevention activities for preschool children were presented and discussed. Three tick bite- prevention activities were particularly well received and are presented in the Results section.

2.2. Data analysis

Data entry and analysis were conducted using IBM SPSS Statistics 22 (IBM Corp. Released, 2013). Data were treated at the level of descriptive and inferential statistics. Basic descriptive statistics of attributive and numerical variables were employed. Teachers’ answers to the open-ended questions were sorted into categories, and frequency counts were done. Coding is the interpretive process by which data is broken down analytically (Corbin and Strauss, 2008). Coding of answers to the open-ended questions was made independently by the first author and corresponding author, and then compared. Some deviant and ambig- uous coding was later redefined and added, based on discussion between the independent coders. The quantitative data met the assumptions that are required for the use of an independent samples t-test and the Pearson correlation coefficient. The ten items of teachers’ attitudes toward ticks and tick-borne diseases were subjected to principal component analysis (PCA) with Oblimin rotation. The Kaiser–Meyer–Olkin value was 0.76, exceeding the recommended value of 0.60 (Kaiser, 1970, 1974), and Bartlett’s test of sphericity (Bartlett, 1954) reached statistical signifi- cance (χ²=484.90, df =45, p <0.001), supporting the factorability of the correlation matrix. The scree plot proposed by Cattell (1966) sup- ported three components for further investigation. The three factors obtained represent the important natural role of ticks (Crombach’s α = 0.83), learning about ticks (Crombach’s α =0.69), and fear of ticks (Crombach’s α =0.72). These three factors explained 66.7 % of the total variance. For further details, see Table 2.

3. Results

3.1. Teachers’ experiences with tick-borne diseases and outdoor education

Almost half of the preschool teachers (72; 46 %) stated that they had found ticks on children after outdoor activities. The majority of these teachers stated that they found ticks attached to the children in their class once a year (38; 52 %). Ten (14 %) of the respondents stated that they had found tick-bites more than three times (see Table 3). They were asked to name the months in which they usually found ticks. They reported finding ticks in March (f =2), April (f =25), May (f =49), June (f

=41), July (f =14), August (f =12), September (f =12), and October (f

=2). In addition, the respondents indicated the body parts of the child where they usually found ticks attached (Fig. 1). Ticks were most frequently attached to the head and neck (18; 25 %) and the arms (18;

25 %). They used tweezers (36; 50 %), oil (3; 4.2 %), or a finger (9; 12 %) to remove ticks, and informed the parents (10; 14 %). Only four of the respondents (2.5 %) knew of cases of children with tick-borne diseases.

Table 4 contains the numbers and percentages for answers regarding Table 1

Frequencies (f, f%) for the sample of Slovenian in-service preschool teachers (n

=158).

Question Answer f f%

Sex Male 4 2.5

Female 154 97.5

Years of work in preschool education

<5 years 37 23.4

5 to 10 years 41 25.9

11 to 20 years 31 19.6

21 to 30 years 17 10.8

>30 years 31 19.6

Missing 1 0.6

Preschool location

Countryside 59 37.3

Suburb 56 35.4

City 42 26.6

No answer 1 0.6

Vaccination against TBE Yes 53 33.5

No 104 65.8

No answer 1 0.6

Note: f – frequency, f% - percentage of teachers.

Table 2

Factor structure for teachers’ attitudes toward ticks and tick-borne diseases.

Items Important

natural role of ticks

Learning

about ticks Fear of ticks

Nothing would happen if all ticks were to die out. *

¡0.88 0.40

Ticks are not very useful in nature.

* ¡0.85 0.43

Ticks are important for

maintaining a natural balance. 0.82 I would like to learn more about

ticks. 0.86

I would like to read more about

ticks. 0.82

I would like to take a closer look at

ticks. 0.71

I would not want to go camping somewhere where there are lots of ticks.

0.76

I am afraid of ticks. 0.73

I am afraid of diseases that are

transmitted by ticks. 0.73

I hate ticks. −0.51 0.69

Table 3

Number of times respondents found tick-bites on children playing outdoors (n = 72).

Question Answers f f%

How many times a year have you found tick-bites on children playing outside?

1 38 52.8

2 13 18.1

3 11 15.3

>3 10 13.8 Note: f – frequency, f% - percentage of teachers.

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the frequency of visits outdoors in preschools. More than two-thirds of teachers reported that preschool children spend time and play outdoors multiple times a week (109; 69 %). Almost ninety percent (141; 89 %) of teachers agreed that tick-borne diseases do not have an effect on the frequency of visiting the outdoors with preschool children.

3.2. Teachers’ tick bite-prevention measures and communication with parents

Good tick bite-prevention measures are crucial, and so respondents were asked to briefly describe the measures they take to protect preschool children from ticks. Their answers were coded into six categories.

Teachers most frequently reported the use of repellents (68; 43 %) and giving instructions for appropriate clothing (36; 23 %); they also examine the children’s bodies and clothing after outdoor lessons (10; 6.3

%) and avoid high grass and bushes (6; 3.8 %). No preventive measures were taken by 28 (18 %) respondents.

Some of the respondents (22; 16 %) ask the parents to protect their children with repellents in the morning before they come to preschool and examine their bodies after spending time outdoors. Two-thirds (106;

67 %) of the respondents inform and instruct parents or guardians about tick-borne diseases. The majority provide them with practical instructions, such as proper clothing for outdoor activities (74; 47 %) and protection with repellents (44; 28 %). Some instruct them to examine the children when they return home (19; 12 %) and give them leaflets with guidelines on tick-borne diseases (5; 3.2 %). We were also interested in whether the children participate in prevention activities such as properly dressing or self-examination. Overall, 54 (34 %) respondents reported that children actively participate in prevention activities.

Teachers also stressed that they would participate in teacher training on LB, TBE, and tick bite-prevention measures (131; 83 %).

The respondents were also asked how parents or guardians reacted when they noticed a tick on their child. Parents or guardians often report to preschool teachers (once: 22; 14 %, or several times: 21; 13 %) that they have found ticks on a child’s body. They usually receive positive feedback or a positive reaction (11; 32 %)—that is, they understand that this is something normal and part of outdoor education—or a neutral reaction (16; 47 %); that is, they are informed about the tick. In some cases (6; 18 %), respondents reported negative reactions from parents, who say that preschool teachers should be more careful or restrict outdoor education. In rare cases parents or guardians tried to forbid them from visiting the outdoors because of tick-borne diseases (6; 3.8 %). We were interested in how preschool teachers reacted in these rare cases.

Here are examples of their responses:

• We describe our tick bite-prevention measures to them and tell them that we will inform them when they have to check their child for ticks.

• We tell them that being outdoors is part of the curriculum and that it is not possible to avoid the outdoors.

• We tell them that they have the option to leave their child in the preschool with another group when they go outdoors.

• We tell them that the children can stay at home during our visit outdoors.

3.3. Teachers’ attitudes toward ticks and tick-borne diseases, and some factors affecting them

The frequency of outdoor activities and teachers’ attitudes toward the natural role of ticks were not significantly correlated, r(152) =0.01, p =0.93. Similarly, frequency of outdoor activities was not correlated with learning about ticks (r(152) =0.04, p =0.59) or fear of ticks (r (153) =0.05, p =0.57). However, it is noteworthy that respondents with more positive attitudes toward the natural role of ticks also express positive attitudes toward learning about ticks, r(153) =0.21, p =0.010.

Furthermore, respondents with more positive attitudes toward the natural role of ticks are less fearful of ticks, r(152) = − 0.44, p <0.001.

Results from an independent samples t-test indicated that re- spondents that were vaccinated against TBE (M =3.37, SD =0.76, n = 52) scored higher (i.e., higher agreement) regarding the natural role of ticks than respondents that were not vaccinated against TBE (M =3.06, SD =0.86, n =102), t(152) =2.22, p =0.028, two-tailed. Cohen’s d of 0.38 indicates a small effect size. The differences between respondents that were vaccinated against TBE (M =3.89, SD =0.59, n =52) and respondents that were not vaccinated against TBE (M =3.75, SD =0.72, n =102) were not significant for learning about ticks, t(152) =1.19, p = 0.24. Cohen’s d of o.21 indicates a small effect size. Similarly, results from an independent samples t-test showed no significant differences between respondents that were vaccinated against TBE (M =3.60, SD = 0.75, n =52) and respondents that were not vaccinated against TBE (M

=3.75, SD =0.71, n =103) regarding fear of ticks, t(152) = − 1.23, p = 0.22. Cohen’s d of 0.21 indicates a small effect size.

The results from an independent samples t-test indicated that the differences between respondents that had already found ticks on children after outdoor activities (M =3.09, SD =0.88, n = 76) and respondents that had not found ticks (M =3.23, SD =0.79, n =79) were not significant for the important natural role of ticks, t(153) = − 0.96, p

=0.34, two-tailed. Cohen’s d of 0.17 shows no effect. Similarly, the differences between respondents that had found ticks on children after outdoor activities (M =3.89, SD =0.59, n =76) and respondents that had not found ticks (M =3.75, SD =0.72, n =79) were not significant for learning about ticks, t(153) =1.50, p =0.13. Cohen’s d of 0.21 indicates a small effect size. The results from an independent samples t-test also showed no significant differences between the respondents that had already found ticks on children after outdoor activities (M =3.70, SD = 0.73, n =76) and the respondents that had not found ticks (M =3.72, SD

=0.76, n =79) with respect to fear of ticks, t(153) = − 0.15, p =0.88.

Fig. 1. Frequency (f%) of ticks on children’s body parts reported by respondents with experience (n =72).

Table 4

Frequency of visits to the outdoors in preschools (n =157).

Question Answers f f%

Frequency of visits (playing) outdoors with preschool children

Multiple times a

week 109 69.0

Weekly 30 19.0

Twice a month 11 7.0

Monthly 6 3.8

Rarely 1 0.6

Note: f – frequency, f% - percentage of teachers.

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Cohen’s d of 0.02 indicates no effect.

Results from an independent samples t-test indicated that the dif- ferences between respondents that knew someone personally that had tick-borne diseases (M =3.22, SD =0.83, n =109) and respondents that did not (M =3.02, SD =0.84, n =45) were not significant for the important natural role of ticks, t(152) = 1.33, p = 0.19, two-tailed.

Cohen’s d of 0.24 indicates a small effect size. Similarly, the differences between respondents that knew someone personally that had tick- borne diseases (M =3.77, SD =0.75, n =109) and respondents that did not (M =3.80, SD =0.59, n =45) were not significant for learning about ticks, t(152) = − 0.19, p =0.84. Cohen’s d of 0.04 indicates no effect size.

However, the results from an independent samples t-test showed a borederline significant difference between respondents that personally knew someone that had tick-borne diseases (M =3.63, SD =0.75, n = 109) and respondents that did not (M = 3.88, SD = 0.71, n = 45) regarding fear of ticks, t(153) = − 1.95, p =0.052. Cohen’s d of 0.34 indicates a small effect. Respondents that showed less fear of ticks knew someone that had had tick-borne diseases.

Preschool teachers’ years of work experience and teachers’ attitudes toward the natural role of ticks, r(153) = − 0.12, p =0.16, learning about ticks, r(153) =0.02, p =.81, and fear of ticks, r(153) = − 0.11, p = .16, were not statistically significant.

3.4. Proposed activities to improve children’s participation in tick bite- prevention measures

The following three activities are the result of the focus group discussion in May 2017 and were best accepted by the participants. We present them with the aim of improving tick bite-prevention practice in preschools.

3.4.1. Tick hunt

This activity helps preschool children and teachers understand where ticks are found outdoors and therefore to avoid ticks. Attach a white piece of cloth to a long stick and comb the bushes, tall grass, and so on (Fig. 2). Care should be taken when conducting the activity to avoid putting participants at additional risk for tick bites. They should stay on trails and clearings. If the terrain is unsuitable for conducting the activity, it is recommended that the educator demonstrate tick hunting themselves. The participants should look for ticks on the cloth with magnifying glasses and compare the number of ticks caught in different habitats.

3.4.2. Tick, where did you hide?

The preschool children are divided into small groups of three to four children. Each group selects one child, who is led by the teacher into a hidden corner of the playroom, where the teacher draws a small dot on his skin with a black marker, symbolizing a tick. The tick should be drawn by the educator on a part of the body where it occurs most often (see the results of this study). In this way, the children are encouraged to observe closely and examine themselves after finishing their outdoor

education (Fig. 3).

3.4.3. A quiz about the life of ticks

The teacher forms a circle together with the group of children in the playroom or outdoors. One child is sent to the middle of the circle and represents a person, and the other children in the circle represent ticks (Fig. 4). The teacher reads a statement about the life of the tick. The children decide whether the statement is true or not. If they believe the statement is true, they move to the middle of the circle and touch the person (representing a tick). After each statement, the teacher explains the statement to the children. Here are some examples of statements and the correct answer with an explanation in parentheses. This activity was also well received by the group of preschool teachers.

• Ticks can only be found in the forest. (FALSE; they can be found almost everywhere in terrestrial ecosystems, even in backyards because they infest rodents, birds and pets.)

• Each tick has eight legs. (FALSE; larvae have six legs, nymphs and adults have eight legs.)

• A tick should be removed as soon as possible. (TRUE; the longer the tick is attached to the skin, the higher the risk of infection.)

• Ticks suck blood every day. (FALSE; ticks attach only three times in their lives, when they are larvae, nymphs and adults.)

• Ticks only live high in the treetops and jump onto passing animals.

(FALSE; they usually occur in tall grass and shrubs at the height of the animals they are searching for, and they cling to the skin or fur of passing animals.)

• Ticks have a keen sense of smell, which they use to find their host.

(TRUE; they can sense carbon dioxide that animals exhale.) 4. Discussion

The provision of high-quality outdoor education in the early years is both a need and a challenge. A challenge particularly due to some health-related risks (Prezza et al., 2005). As mentioned above, Slovenia has a high incidence of tick-borne diseases (Arneˇz and Avˇsiˇc-Zupanc, ˇ 2009; National, 2020a), which is an important factor to be considered when conducting outdoor activities in preschool. This section discusses the study’s five research questions.

The first research question underlying this study focused on the experience of Slovenian preschool teachers with ticks and tick-borne diseases and outdoor education. The teachers’ experiences showed that they have very frequent contact with ticks and tick-borne diseases in their professional lives. One-third (34 %) of the respondents reported having been vaccinated against TBE at least once, which is more than the 7–8% reported for the general public in Slovenia in 2014 (National Public Health Institute of the Republic Slovenia, 2020b). The majority of the respondents engage in outdoor education once or several times a week, which is in line with findings of Kos and Jerman (2013). Special attention should be paid to this topic in the spring and early summer months, when outdoor activities are in full swing. Although tick activity

Fig. 2. Children during the tick-hunting activity. Fig. 3. Finding a “tick” on a child’s body.

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generally peaks from April to July throughout Europe (Mansfield et al., 2009), teachers do not report higher tick bite incidence among children in July (Fig. 1), which is due to the fact that educational programs are less intensive during the summer months because many preschool children and preschool teachers are on summer vacation. Preschool children are even more exposed to ticks and tick-borne diseases due to their playfulness and body height. This also emerges from the data collected on the occurrence of ticks on various parts of the body, including the head. Ticks mainly attach to children’s necks and heads (Christen et al., 1993; Berglund et al., 1995). Ticks, especially the adult stage, can be found high in shrubs, in tall grass, and in dense forests (Mansfield et al., 2009). Preschool teachers generally remove ticks from children’s bodies in a professional manner. Nevertheless, additional attention should be given to teacher training, including how to remove ticks properly with tweezers. Above all, the importance of immediate action (removal of ticks) upon detection should be emphasized. The shorter the time between the tick bite and tick removal, the lower the risk of infection, especially for LB (Hayes and Piesman, 2003).

Measures for tick prevention are critical (Pearson, 2015; Slunge et al., 2019; National Public Health Institute of the Republic Slovenia, 2020b; Weisshaar et al., 2006), as is good communication with parents and guardians (Prezza et al., 2005), which was the focus of our second and third research questions. More than four-fifths of those surveyed carry out some tick bite-prevention measures, most frequently the use of repellents before the children go outdoors. What teachers should emphasize even more or when applying preventive measures is appropriate clothing for children (long trousers, long-sleeved shirts, socks pulled up over long trousers, closed shoes, etc.) and an appropriate choice of natural play and educational areas where there are no compact areas with tall grass or shrubs. Two-thirds of the teachers report that they inform parents or guardians about tick bite-prevention measures before engaging in outdoor activities, which is very important in order to minimize the risk of tick-borne diseases and to ensure positive communication and cooperation with parents and guardians. Fortu- nately, respondents reported few individual cases in which they encountered resistance from parents and guardians to outdoor education due to tick-borne diseases. The respondents’ answers also give us optimism about the importance of outdoor education because they know how to build a cooperative relationship with parents and guardians, and they justify the importance of outdoor education. In a study among Slovenian preschool teachers and parents about safety issues of play and learning outdoors (Kos and Jerman, 2013) it was revealed that, similarly to preschool teachers, nearly half of parents stated that they accepted risk as a component of outdoor play and learning. In fact, preschool teachers were more concerned than parents; considerably fewer parents than preschool teachers felt that all activities must be subordinate to safety. A systematic review (Richardson et al., 2019) suggests that personal protective strategies that limit exposure to ticks should continue to be recommended, as should education to encourage the adoption of personal protective strategies. Further investigation of educational measures for children is necessary because the findings of Richardson

et al. (2019) were mixed.

The last part of the discussion focused on teachers’ attitudes toward ticks and tick-borne diseases, and some of the factors that influence them. The attitudes of preschool teachers toward ticks and tick-borne diseases did not significantly correlate with the frequency with which they engage in outdoor activities in preschools. Outdoor education has an important place in the Slovenian preschool curriculum (Kos and Jerman, 2013; Torkar, 2014). Therefore, any negative correlation between these two variables would negatively affect preschool children’s outdoor experience. An interesting result is that respondents with a more positive attitude toward the important natural role of ticks also expressed a more positive attitude toward learning about ticks and were less afraid of ticks. Vaccination is an important intervention for pre- venting TBE (Steffen, 2019). The results suggest that preschool teachers that were vaccinated against TBE expressed a more positive attitude toward the important natural role of ticks. This means that they accept the intrinsic value of these animals more and reduce their TBE risk with vaccination. The potential Lyme disease vaccine VLA15, currently in development (Eisen, 2021), could further improve teacher attitudes and potentially contribute to the advancement of outdoor education. Sur- prisingly, respondents who knew someone personally that had had a tick-borne disease showed less fear of ticks and tick-borne diseases. This should be addressed in the future studies.

5. Conclusion

This study concludes that, despite the objective risks associated with LB and TBE, there is still broad consensus among educators and parents on the importance of outdoor education in the early years. Nevertheless, research has shown that there is still some potential for improvement in education of preschool teachers and consistent implementation of tick bite-prevention measures in preschools.

Author statement

Gregor Torkar - roles: conceptualization, data curation, formal analysis, methodology, validation; supervision, review & editing. Mar- janca Kos - roles: writing - original draft, review & editing; visualization.

Acknowledgements

We would like to thank all preschool teachers who participated in the research, Nika Stradovnik for helping us collect the data, and the Uni- versity of Ljubljana Faculty of Education for received financial support.

We would also like to thank the two reviewers for their constructive comments. The article is dedicated to Ela Sofija, the daughter of the first author, who overcame LB during the research and continues to enjoy being outdoors.

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