Mosquito Bite-Avoidance Attitudes and Behaviors in Travelers at Risk of Malaria

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1 I S T M 33 ORIGINAL ARTICLE Mosquito Bite-Avoidance Attitudes and Behaviors in Travelers at Risk of Malaria Larry Goodyer, PhD and John Song, PhD Leicester School of Pharmacy; School of Applied Social Sciences, De Montfort University, Leicester, UK DOI: /jtm Introduction. Mosquito bite prevention is an important strategy to reduce the risk of contracting malaria and advice on the methods available should be offered in pre-travel consultations. This study examines the attitudes of a cohort of UK travelers to the various bite-avoidance strategies and the extent to which they are practiced when visiting malaria-endemic areas. Method. This was a retrospective cohort study of UK travelers above 18 years of age returning from malaria-endemic areas. Those who agreed to participate were ed a Web-based questionnaire on their return to the UK. The questionnaire consisted of items relating to attitudes to bite-avoidance measures and malaria and the use of bite-avoidance measures while away. Results. One hundred and thirty-two travelers completed the questionnaire representing a 51% response rate. Frequent use of repellents (69%) was higher than covering the arms (49%) and legs (56%), or using insecticide vaporizers (16%), sprays (24%), and bed nets (32%). Those under the age of 30 tended to use bite avoidance less frequently. Gender, purpose, and duration of travel were also found to influence the use of particular measures. A reliable 17-point attitude to the bite-avoidance questionnaire (Cronbach s alpha = 0.70) was constructed and a subscale score indicated that attitudes influenced the use of repellents. Conclusion. The use of measures to avoid mosquito bites on retiring and covering arms and legs needs to be further emphasized to travelers. The attitude scales described could be a useful tool in practice and research into this area. In the last 30 years there has been an increasing trend of travel from the UK to tropical destinations where mosquito-borne diseases such as malaria and dengue are endemic. 1 Approximately 1,500 to 2,000 travelers return to the UK annually having contracted malaria 2 and this can result in severe morbidity and in some cases death. Apart from malaria chemoprophylaxis the key strategy advised for travelers is to adopt methods that protect against bites. UK guidelines give the following advice to all travelers visiting malaria-endemic areas: 2 Cover up all exposed skin when outside between dusk and dawn, eg, wear long sleeves and trousers. Clothing can also be treated with insecticide. Apply a repellent containing 50% diethyltoluamide (DEET) to exposed skin following manufacturer s instructions. Reapplication may be necessary throughout the evening. Alternatives to DEET are available if this is not acceptable to the traveler. Corresponding Author: Prof. Larry Goodyer, PhD, Leicester School of Pharmacy, Faculty of Health and Life Sciences, De Montfort University, The Gateway, Leicester LE1 9BH, UK. lgoodyer@dmu.ac.uk On retiring, ensure the room is clear of mosquitoes by the use of a plug-in insecticide vaporizer or knockdown spray. Sleep in an air-conditioned or well-screened room where possible. In some situations, when out of doors or sleeping in poorly screened rooms, use an insecticide-treated mosquito net. The various repellents and other modes of bite avoidance for travelers have recently been the subject of an evidence-based review. 3 There has been surprisingly little research conducted on the way that travelers follow bite-avoidance advice or use repellents in practice. It could be argued that bite avoidance is viewed in the same way as any chemoprophylactic agent to protect against malaria; it is only effective if the individual adheres to the regimen prescribed. Yet although work has been conducted defining levels of adherence, attitudes, and behaviors regarding antimalarials, 4 6 this is not the case for bite avoidance. There is also little data available concerning compliance to insect repellent use, although it has been stated that it is generally less than to malaria chemoprophylaxis. 7 In retrospective questionnairebased studies of travelers 8 and field studies in 2013 International Society of Travel Medicine, Journal of Travel Medicine 2014; Volume 21 (Issue 1): 33 38

2 34 Goodyer and Song servicemen, 9 adherence to bite recommendations does appear to be low. Further, the attitudes of travelers to the recommended bite-avoidance measures have not been rigorously investigated to date. This study will describe an often neglected but central area to the success of bite-avoidance methods: the extent to which the user will apply bite-avoidance measures. An aim of this study is to investigate the use of an attitude toward bite-avoidance measures questionnaire and explore how these attitudes might influence behavior. Method This study was designed as a multicenter retrospective questionnaire-based survey. The inclusion criteria were that participants planned to visit a malaria-endemic area and could complete the survey within 2 months of return. They also needed to have a permanent personal address that they would access on return from travel and were above 18 years of age. Prior to travel, all participants attended a travel clinic run by a nurse or physician with a particular interest in travel medicine. To this end, the participating clinics were drawn from the membership of the British Global and Travel Health Association who were running clinics and had agreed to participate following an to all members. Two further general practices where there was a well-established travel clinic in operation were also recruited. The study period ran from October 2011 to October All travelers who attended the clinics and met the broad inclusion criteria were offered an information sheet inviting them to participate in the study, which was supplemented by verbal information from the clinic nurse if they agreed to take part. If they agreed to participate at that point they were only asked to supply their first name, address, and month of return from the malaria-endemic area, be that to the UK or other country of origin. On the last day of their month of return participants were sent an containing a link to an online questionnaire (SurveyMonkey) and again asked for their consent before completing. An reminder was sent to all participants 1 month later. The project was approved by the Nottingham 1 Ethics Committee, and separate UK National Health Service Research and Development approval was obtained for each of the individual sites. Questionnaire Design The questionnaire was developed and assessed as previously reported. 10 Items were constructed based on information obtained through in-depth interviews with a variety of individuals identified through travel clinics; those who had previously traveled to malariaendemic areas, individuals planning to travel to malariaendemic areas for the first time, and those who had no experience of or planning to travel to malariaendemic areas. From the themes that emerged from the interviews, a questionnaire was constructed using closed question and Likert-type scales. Face validity of the questionnaire was assessed and subsequently confirmed through review of the questionnaire by practitioners (a nurse, pharmacist, and physician) in travel medicine. The test retest method with a 2-week interval was employed to examine the questionnaire reliability. Usability was further investigated through pilot studies. In total the questionnaire consisted of: 7 Questions relating to traveler details, eg, age, gender, and itinerary 8 Questions on specific use of bite-avoidance measures, eg, repellents and whether they were frequently, sometimes, or never used 3 Questions relating to experience while away, eg, whether many, few, or no mosquito bites were experienced 17 Attitude statements exploring attitudes toward different methods of bite avoidance on a 1 to 5 Likert scale indicating level of agreement to the statement. Examples of items include, Repellents are unpleasant to use, and Using insecticide sprays on clothes reduces mosquito bites. Further four statements relate to attitudes toward malaria measured on a 1 to 5 Likert scale. An example includes, Malaria is a severe condition. The total score of the attitude scale was calculated by reversing selected negatively worded items and summing them. Analysis Data were analyzed using ibm spss version 20 for Windows. Prior to detailed analysis of the data, the total score for the attitude scale was obtained by first reverse-scoring the relevant items such that higher scores indicate a positive attitude and then summing all scores for the attitude scale items. In addition, various subscales were constructed based on categories of bite-avoidance measures. Reliability was measured by calculating the Cronbach s alpha. 11 Categorical relationships were examined using Chi-square test of independence with Pearson Chi-square being used where expected counts were less than five in more than three cells. Other relationships were explored by linear regression. Multinomial logistic regression was employed to examine the predictive relationship between the attitude scale scores and the behavioral outcome of bite-avoidance measures undertaken. Results In total, 255 participants were sent an invitation and 132 completed the questionnaire representing a good 51% response rate. 12 A private travel clinic chain of eight individual and geographically diverse clinics recruited the largest number (60) and one single travel clinic in a general practice (GP) surgery the second

3 Bite-Avoidance Attitude and Behavior 35 Table 1 Participant details Table 2 Use of bite-avoidance measures n (%)* Gender Male 55 (41.7) Female 75 (56.8) Age (38.6) (15.9) (15.2) (18.2) (12.1) Destination South Asia 15 (11.4) Sub-Saharan Africa 78 (59.1) S America 9 (6.8) SE Asia 19 (14.4) Other 7 (5.3) Reason for travel Tourist (package holiday or hotel single destination) 39 (29.5) Business 26 (19.7) Backpack or trek 38 (28.8) Visiting friends and relatives 10 (7.6) Charity, volunteer, nongovernment organizations 15 (11.4) Cruise 1 (0.8) Expedition 2 (1.5) Length of trip <1 month 107 (81.1) 1 3 months 20 (15.2) >3 months 5 (3.8) Advice on bite avoidance A lot 73 (55.7) Some 56 (42.7) None 2 (1.5) Previously visited area with risk of malaria 83 (62.9) Number of bites Many 13 (9.8) Few 63 (47.7) None 55 (41.7) Used more bite-avoidance measures if bitten 40 (30.3) Prescribed anti-malarial medication 107 (81.1) *The sample size, n = 132; however, missing values were excluded. largest (50) number of participants. The remainder were recruited through seven other travel clinics located in GP surgeries, occupational health centers, and student University health services. Traveler Characteristics These are described in Table 1. Younger people tended to travel for more than 1 month (68% vs < 20% in other age groups, p = 0.01). Also, 44% of those in 18 to 30 age group were backpacking compared to <20% in any other age group. Gender and regions visited were significantly related (p = 0.01) although the strength of association was weak. Length of stay was found to be associated with the region visited (p = 0.04) and the reason for traveling (p = 0.001). The extent to which travelers reported following the various bite-avoidance measures is shown in Frequently (%) Sometimes (%) Never (%) Air-conditioned room 64 (48.5) 34 (25.8) 33 (25.0) Used net 43 (32.6) 31 (23.5) 57 (43.2) Covered arms 65 (49.2) 54 (40.9) 12 (9.1) Treated clothing 21 (15.9) 20 (15.2) 82 (62.1) Wore trousers 74 (56.1) 45 (34.1) 11 (8.3) Used repellent 91 (68.9) 21 (15.9) 18 (13.6) Used insecticide spray 32 (24.2) 29 (22.0) 70 (53.0) Used vaporizers 21 (15.9) 21 (15.9) 88 (66.7) Missing data were excluded in the calculation of the percentages. Figure 1 Use of bite-avoidance measures by age group. Table 2. A number of relationships between traveler characteristics and the bite-avoidance measures were observed (p < 0.05, Chi-squared). Women tended to sleep more frequently in air-conditioned rooms but wore long trousers less frequently than men. Those staying less than a month tended to sleep less in airconditioned rooms. Age was correlated to a number of measures (Figure 1). Those visiting sub-saharan Africa used bed nets and those visiting South Asia wore long trousers more compared to other regions. Reason for travel also influenced behavior; backpackers more frequently used repellents and tourists were more likely to use methods to clear the room of mosquitoes. Experience of Mosquito Bites Thirteen (9.8%) travelers reported receiving many bites while away, 63 (47.7%) a few bites, and 55 (41.7%) no bites. Forty (30.3%) said that they used more bite-avoidance measures if bitten and 107 (81.1%) were taking prophylactic antimalarials. A multiple regression analysis was conducted to investigate the relationship between the level of bites reported and the degree to each of the various bite-avoidance advice was followed. More frequently covering arms, wearing long trousers, and sleeping in an air-conditioned room were associated with reporting fewer bites, but more

4 36 Goodyer and Song frequently using repellent was associated with reporting a greater frequency of bites (p < 0.05). Of those who received many bites, 69% reported using more bite-avoidance measures whereas 47% of those receiving a few bites used more measures (p = 0.002). Females reported bites more frequently than males though this failed to reach significance (p = 0.07). Spending a longer time away was associated with reporting more bites (p < 0.001). Those aged between 18 and 30 reported more bites than other ages (p < 0.05) although this must be considered in the light of the finding that younger travelers tended to be backpackers who also would be spending a longer time away. Traveler s Attitudes to Bite-Avoidance Methods The mean score of the 21-point scale was (SD = 8.37). The attitude scale potentially comprised of five subscales which assessed the attitudes toward the use of mosquito nets, insect repellents, clothing, sleep-related bite-avoidance methods, and attitudes toward malaria. Reliability of the 21-item scale was assessed using Cronbach s alpha (0.696), indicating an acceptable level of reliability of the scale. Due to the different natures of the four items relating to attitudes toward malaria these were excluded to form a 17-item attitude toward bite-avoidance measures scale and the reliability was marginally higher (0.702). The Cronbach s alpha of the four subscales was low, the highest being that to repellents (0.58). Analysis of variance indicated that total score (21-point questionnaire) was related to age (p < 0.001) and reason for travel (p < 0.01), those under 30 years achieving lower scores and tourists higher scores. A series multinomial logistic regression was conducted to examine whether the use of various biteavoidance measures can be predicted by the scores on the attitude toward bite-avoidance measures scale. Only the 17-item attitude scale scores (ie, excluding the 4 attitude toward malaria items) used as the predictor of bite-avoidance measures, showed significant finding related to the wearing of trousers (p = 0.036). To further explore a specific bite-avoidance behavior, the repellent attitude subscale was used to predict the use of repellent while recognizing that by using the subscale, the reliability of the scales was limited by the fewer number of items. The other subscales were not analyzed for this relationship because of their lower reliability. The use of repellent was significantly predicted by the attitude toward repellent subscale scores in Table 3. More specifically, the attitude toward repellent significantly predicted the Use of repellent frequently. However, Cronbach s alpha for the attitude toward repellent subscale is not ideal (α = 0.58), and therefore this will require further examination. Table 3 Logistic regression for attitude and behavior repellent subscale B (SE) 95% CI for odds ratio Lower Odds ratio Upper Frequently vs never Intercept (1.942) Repellent score (0.108)* Sometimes vs never Intercept (2.296) Repellent score (0.129) *p <.05. Discussion Participant Characteristics The population in the study is derived from those attending a number of travel clinics before departure and is a relatively small sample compared to, for instance, those derived from the airport departure/arrival surveys. 13 However, besides examining the bite-avoidance behaviors of travelers, a primary aim was to test a new attitude questionnaire and in this case could be viewed as the first pilot study. Further there have been no studies to date that have specifically focused on the bite-avoidance behaviors of UK travelers. The clinics are mainly run by nurses who have developed a particular interest in travel medicine and would not themselves be representative of the majority of nurses based in a GP surgery offering travel health services. It is possible that there was a selection bias in that those clinics volunteering to take part are the most committed to the provision of travel health services. No attempt was made here to identify the type or level of advice on bite avoidance given by these clinics although they have a special interest in travel medicine, and taking part in this study may result in better levels of advice than might be usually given to those attending other travel health services in the UK. Due to the number of centers involved, the level of advice would be quite diverse, but it was known that the travel clinic chain which took part in this study offered standardized verbal and written information. It has been reported that up to one third of travelers who are going overseas do not seek pre-travel health advice when this would have been recommended. 13 It would therefore be reasonable to assume that travelers in this study have a better knowledge and attitude toward biteavoidance measures. The study population also tends to be of a younger age group and traveling for less than 3 months. Of relevance to the findings in this study is that the younger travelers tended to be on a backpacking trip and spending more than 1 month away. It should also be noted that the cohort is predominantly traveling to malaria-endemic areas of sub-saharan Africa rather than those areas where dengue is of greater risk. In

5 Bite-Avoidance Attitude and Behavior 37 summary, although the findings are limited by the relatively small sample size, the specialist nature of the clinics, that the travelers attracted to such clinics may have a different awareness of travel health issues to the general population, and that the level of advice given regarding bite avoidance may also not reflect that of the general traveling public, this exploratory study is one of the first in attempting to investigate various aspects of bite-avoidance attitudes and behaviors using a relatively long and in-depth questionnaire. Adherence to Bite-Avoidance Measures Advice regarding the covering of exposed skin seems to be followed less regularly than other methods. Compared to the other methods there is a higher rate of sometimes wearing long sleeves and trousers, which probably reflects behavior modification due to environmental conditions, eg, heat and humidity. Following advice on retiring is less well practiced in relation to clearing the bedroom of mosquitoes. Sleeping in air-conditioned rooms and using nets would be a function of the type of travel, ie, backpackers sleeping in budget hotels or those sleeping outside. Treating clothing with an insecticide was the least performed measure and this could be a reflection of the low availability of suitable products (only one licensed in the UK currently) as well as poor knowledge of the technique by health professionals. Those under the age of 30 had the poorest levels of adherence and this age group has been shown to have a lower uptake of pre-travel health advice. 14 Other studies have shown similar rates of repellent use. 15,16 The uptake of adherence to methods other than use of repellents has not been widely reported. A study of participants with a comparable age range described similar levels in the use of long clothing. 17 Use of repellents in expatriates 18 and travelers from some countries has been shown to be much lower. 19 A limitation of these findings is that travelers self assessment of adherence is quite frequently higher than actual reported adherence, as for instance has been found in studies on malaria chemoprophylaxis. 20 It is also possible that the knowledge that the participant would be questioned on their bite-avoidance behaviors on return, albeit anonymously, may have altered their behavior, ie, a Hawthorne effect. However, a study specifically investigating the Hawthorne effect in UK health services settings showed that only minimal amounts of behavioral changes were accounted for by participation in research, concluding that the Hawthorne effect is negligible in health services research. 21 Even if the Hawthorne effect was to have occurred, it is likely to be weak and in a positive direction of utilizing bite-avoidance measures. Given the relatively low use of bite-avoidance measures generally, it is unlikely that the Hawthorne effect was a major contributor to this study. Level of Bites Reported It would be anticipated that those adhering to the recommended bite-avoidance measures would report receiving fewer bites. The regression analysis did indicate a significant effect of bite-avoidance measures on the reported biting rates although only a small proportion of the variance was explained by the model. There are likely to be a number of other variables not captured, such as local mosquito density and the likely variation of mosquito bite reaction, which would influence perceived bite rates. The largest contribution to the model in receiving fewer bites is in the wearing of trousers (beta standardized coefficient value 0.209) which could be anticipated considering the tendency of certain species to bite around the ankles. It might be surprising that the more frequently repellent is used, the higher the biting frequency reported. This could be explained by a behavioral change in that those experiencing more bites then apply repellent more regularly; 70% of those who received many bites and 40% who received a few bites stated they would have used more measures if bitten. It may have been worthwhile to ask specifically if more regular repellent application was employed if experiencing more bites to address this question. Attitude Scales The total attitude score exhibited a reasonable reliability and could be employed in assessing the general attitudes of travelers to bite-avoidance measures, in particular the 17-point scale. The high mean score might be expected in those who have visited travel clinics run by expert nurses. The scale should be investigated on other populations of travelers, eg, those who have had no or little travel health advice. A correlation between attitudes and use of the measures might be expected, eg, a poor attitude would influence low uptake of the measures. This was demonstrated for the subscales examining the important areas of repellents and appropriate use clothing. The wearing of long trousers was the factor most influenced by attitudes and it is also the behavior associated with the lowest reporting of mosquito bites. The attitude scores were the lowest in the 18 to 30 age group, as might be expected in this age group. 12 The repellent subscale correlated to the use of repellents (Table 3) and could be useful in screening those less likely to use bite-avoidance measures. The attitude scale and some of the subscales overall show potential for application in assessing the factors influencing bite-avoidance behavior although further refinement to improve their psychometric properties would be warranted. This first exploratory study can be used to modify the questionnaire and apply it to wider and different cohorts of travelers, leading to more fully validated scales.

6 38 Goodyer and Song Conclusion This study has indicated that there is variable use of mosquito bite-avoidance measures by UK travelers when visiting malaria-endemic areas. Covering up exposed skin when out of doors and taking measures to clear the room of mosquitoes before retiring are amongst the least frequently practiced. Those who are under 30 years of age generally displayed poorer bite-avoidance behaviors. A new scale for assessing attitudes to bite-avoidance measures has been piloted and appears to correlate to some behaviors. This could be further developed and applied in assessing the impact of educational strategies to improve adherence to biteavoidance measures. Acknowledgment We would like to thank the British Global and Travel Health Association for the support of this project. Declaration of Interests L. G. is a Director of Nomad Travel Store that produces and supplies bite-avoidance products. Otherwise the authors state they have no conflicts of interest to declare. References 1. Health Protection Agency. Foreign travel-associated illness in England, Wales and Northern Ireland. London: Health Protection Agency, Health Protection Agency. Guidelines for malaria prevention in travelers from the United Kingdom. London: Health Protection Agency, Goodyer LI, Croft AM, Frances SP, et al. Expert review of the evidence base for arthropod bite avoidance. J Travel Med 2010; 17: Goodyer L, Rice L, Martin A. Choice of and adherence to prophylactic anti-malarials. J Travel Med 2011; 18: Behrens RH, Taylor RB, Pryce DI, Low AS. Chemoprophylaxis compliance in travelers with malaria. J Travel Med 1998; 5: Huzly D, Schonfield C, Beuerle W, Bienzle U. Malaria chemoprophylaxis in German tourists: a prospective study on compliance and adverse reactions. J Travel Med 1996; 3: Schoepke A, Steffen R, Gratz N. Effectiveness of personal protection measures against mosquito bites for malaria prophylaxis in travelers. J Travel Med 1998; 5: Durrheim DN, Leggat PA. Prophylaxis against malaria: preventing mosquito bites is also effective. BMJ 1999; 318: Fai FY, Lee L. Perceptions and use of insect repellent amongst soldiers in the Singapore armed forces. Mil Med 1996; 161: Goodyer L, Shah J, Ropak K. Validation of a questionnaire to assess attitude to bite avoidance measure amongst travelers to malaria endemic areas. Northern European Travel Medicine Conference (NECTM), Helsinki, 2008: P4-06, 49. Available at: (Accessed 2013 Jun 30) 11. Field A. Discovering statistics using SPSS. London: Sage, Greenlaw C, Brown-Welty S. A comparison of web-based and paper-based survey methods: Testing assumptions of survey mode and response cost. Eval Rev 2009; 33: Herck K, Zuckerman J, Castelli F, et al. Travelers knowledge, attitudes, and practices on prevention of infectious diseases: results from a pilot study. J Travel Med 2003; 10: Haywood A, Haywood A, MacIntyre C, Seale H. Travel risk behaviors and uptake of pre-travel health preventions by university students in Australia. BMC Infect Dis 2012; 12:43. doi: / Piyaphanee W, Wattanagon Y, Silahamroon U, et al. Knowledge, attitudes and practices among foreign backpackers towards malaria risk in South East Asia. J Travel Med 2009; 16: Cobelens FG, Leentvaar-Kuijpers A. Compliance with malaria chemoprophylaxis and preventative measures against mosquito bites among Dutch travelers. Trop Med Int Health 1997; 2: Ropers G, Holle M, Wichman O, et al. Determinants of malaria prophylaxis among German tourists in Kenya, Senegal and Thailand. J Travel Med 2008; 15: Hamer D, Ruffing R, Callahan MV, et al. Knowledge and use of measures to reduce health risks by corporate expatriate employees in West Ghana. J Travel Med 2008; 15: Yoo YJ, Bae GO, Choi JH, et al. Korean travelers knowledge, attitudes and practices regarding the prevention of malaria: measures taken by travelers departing for India from Incheon International airport. J Travel Med 2007; 14: Landry P, Iorillo D, Darioli R, et al. Do travelers really take their mefloquine malaria chemoprophylaxis? Estimation of adherence by an electronic pillbox. J Travel Med 2006; 13: O Sullivan I, Orbell S, Rakow T, Parker R. Prospective research in health services settings: health psychology, science and the Hawthorne effect. J Health Psychol 2004; 9: