Gypsy moth-induced dermatitis: a hospital review and community survey

ARTICLE

ejd.2012.1722

Auteur(s) : Takayuki Kikuchi¹ tptakayuki@yahoo.co.jp, Ken Kobayashi¹, Kiyomi Sakata², Toshihide Akasaka³

¹ Kuzumaki Hospital, 16-1-1, Kuzumaki-cho, Iwate-gun, 028-5402, Japan

² Department of Hygiene and Preventive Medicine

³ Department of Dermatology, Iwate Medical University Iwate, Japan

Reprints: T. Kikuchi

Among the order Lepidoptera, which is estimated to comprise between 125,000 and 150,000 species, only a handful of species are known to cause adverse effects in humans [1, 2]. Despite the diversity and nearly worldwide distribution of Lepidoptera, documentation of adverse effects in humans due to the species is scarce in the medical literature [3]. Most of the effects are mild and self-limiting; therefore, the true incidence is difficult to quantify, and the numbers are likely to be underestimated [3]. Adverse events typically occur in only one or a few exposed individuals; however, several Lepidoptera species are prone to natural abundance, leading to increased exposure frequency and “epidemics” of cutaneous or systemic symptoms [3]. An additional problem is that some species have the ability to disseminate themselves widely [3]. The gypsy moth (GM), Lymantria dispar, combines both these factors: the species can sometimes appear in large numbers, and newly hatched caterpillars can be dispersed by the wind [4, 5].

The native range of GM extends over most of the temperate forests [6]. The Asian strain is native to Japan, Russia, and other Asian countries; the European strain is native to Europe. Around 1869, the European strain was accidentally introduced in United States, where it has been gradually expanding its range [7]. Cyclic infestation has been recorded and is well known as a serious defoliator of broad-leaved forests [8]. GM infestation usually starts in larch plantations and spreads to natural broad-leaved forests in the second year of infestation in Japan. Most infestations collapse 2 or 3 years later due to natural enemies [9-11].

GM caterpillar dermatitis is a pruritic, papular, urticarial eruption that is usually associated with exposure to larva of the first developmental stage (instar) [12]. The condition can persist for several days to 2 weeks and may be sufficiently severe to cause the affected individual to seek medical attention [12-15]. Non-cutaneous symptoms including eye and respiratory irritation have also been reported [12, 16-18]. Human exposure can occur via direct contact with a caterpillar or through contact with associated airborne materials such as setae, silken threads, and shed skins [19]. Outbreaks of GM caterpillar dermatitis have been reported in parts of the northeastern United States [13, 14, 19]. Young children have been shown to be especially at risk from effects of GM exposure [19], although it is not clear whether children are inherently more sensitive than adults to the effects of exposure or whether they have a greater incidence of response because they spend more time outdoors than do adults and thus have greater potential for exposure to larvae [20]. The pathologic mechanism of GM caterpillar dermatitis has not been fully clarified; however, some studies have suggested hypersensitivity to insect antigen [12, 17-19].

Since 2007, GM infestations have occurred in and around Kuzumaki town, Iwate Prefecture, Japan. We first became aware of an outbreak of GM caterpillar dermatitis in the spring of 2008 [21]. Then, in the summer of 2008, massive numbers of adult moths appeared, and the females laid eggs. Egg mass counts in Kuzumaki ranged from 2,100 to 30,000 per hectare at the 5 forest sampling sites (Iwate Prefectural Forestry Research Center). Consequently, in the spring of 2009, copious numbers of larvae – far more than in 2008 –hatched, and the rash problem expanded. The purpose of the present study was to identify the clinical features of GM caterpillar-induced health problems and to investigate the incidence of GM caterpillar dermatitis in the general population during the 2009 outbreak.

Methods

The study protocol was approved by our institutional review board.

Hospital review of caterpillar dermatitis patients

We reviewed the records of 229 patients who had received a clinical diagnosis of GM caterpillar dermatitis at Kuzumaki Hospital from April to June 2009. The inclusion criteria for GM caterpillar dermatitis were as follows:

• –. pruritic, erythematous, papular, and occasionally vesicular eruption within 24 h following known exposure to the larvae or its appendages,
• –. characteristic distribution of the eruption on the body,
• –. presence of eruption developed only during the first-instar larval stage of the insect (most larvae that hatch from the end of April to early May).

Also, if the inclusion criteria were met fully, GM caterpillar dermatitis was diagnosed even when the patients did not report direct contact with the larvae. A patient was counted only once in this analysis, that is, during their initial visit. We assessed the following information: age, gender, date of onset of dermatitis, affected areas, recognition of direct contact with larvae on the affected area, non-cutaneous symptoms, allergy history, experience of similar dermatitis in the spring of 2008, and possible precipitating activities that involved exposure to caterpillars or their associated materials. In addition, we investigated the association between the daily number of patients and weather conditions by using data from the Japan Meteorological Agency [22].

Questionnaire survey in Kuzumaki town

We conducted a questionnaire survey covering all 2,891 households (7,770 residents) in Kuzumaki, a rural mountain town. An anonymous self-administered questionnaire was distributed to each household in 1 June 2009 and was collected two weeks later regardless of whether affected people were present in the household. The questionnaire was devised to obtain the following information: gender, age, affected or not affected by suspected GM caterpillar dermatitis in the spring of 2009, sought or did not seek medical attention when affected in 2009, and affected or not affected by similar dermatitis in the spring of 2008. Because heavy infestations of newly hatched larvae were expected in 2009, we conducted a public relations campaign widely through media in order to spread awareness about the GM caterpillar-induced health problems using characteristic clinical pictures before the hatching. Based on these instructions, the self-diagnosis for GM caterpillar dermatitis according to a community survey was “pruritic, erythematous eruption thought to be induced by GM caterpillars developed after hatching of GM larvae.”

Statistical analyses

All analyses were performed using SPSS (version 12.0J SPSS Inc., Chicago, IL) and STATA (version 10.0 Stata-Corp LP, College Station, TX) software packages. The Mann-Whitney U-test and Fisher's exact test were used to compare the group of patients with direct contact with larvae and those without direct contact. The Basic Resident Register of Kuzumaki was used to obtain population statistics. The χ² test was used to analyze the difference in response rate and affected rates. With Poisson regression analysis adjusted by age, gender and age, differences in the incidence of dermatitis were examined. The strength of the relationship between incidences in 2008 and in 2009 was assessed by odds ratio (OR). P values<0.05 were considered to be significant for all statistical analyses.

Results

Hospital review of caterpillar dermatitis patients

Of the 229 patients surveyed, 80 (35%) were male and 149 (65%) were female, with an age range from 3 to 90 years and a median age of 67 years. Affected areas were located primarily on the neck and arms (figures 1A, B). Twenty-two patients (10%) developed non-cutaneous symptoms. Sixty-three patients (28%) had a history of allergy. One hundred and twenty-two patients (53%) reported having experienced similar dermatitis in the spring of 2008 (table 1). The association between the date of onset of dermatitis and the daily maximum temperature in Kuzumaki is depicted in figure 2. One hundred and eighty patients (79%) did not notice direct contact with larvae on their affected areas. There was no significant difference between the group of patients with direct contact and those without direct contact (p>0.05). All patients were treated as outpatients with topical and/or oral antihistamines and/or steroids, depending on the severity of their symptoms.

Table 1 Hospital review of GM dermatitis patients and comparison of the patients with direct contact with larvae and those without direct contact.

SD, standard deviation

^*Mann-Whitney U-test

^** Fisher's exact test

^∘Multiple options possible

^∘∘Possible precipitating activities that involved exposure to caterpillars or their appendages

Questionnaire survey in Kuzumaki town

A total of 1,845 households (64%) responded. Of the 4,871 people who responded to the survey (63%), 2039 people (42%) reported having dermatitis in the spring of 2009 (table 2 table 2). There was no significant difference in response rate with respect to gender; however, there were significant differences among the age groups (p<0.001). The affected rate of males was slightly higher than that of females (p=0.029). There were significant differences in the affected rates by age groups in both males (p<0.001) and females (p<0.001). When the data were adjusted for age, gender was not associated with dermatitis (prevalence risk (PR)=1.03, 95% CI: 0.94-1.12, p=0.53). However, the age groups of 70-79 years and ≥80 years showed lower incidence of dermatitis (70-79 years: PR=0.68, 95% CI: 0.54-0.85, p=0.001) and (≥80 years: PR=0.47, 95% CI: 0.36-0.61, p<0.001). The relationship between 2008 and 2009 incidences among the affected population is depicted in (table 3). Those who had experienced similar dermatitis the previous year had a significantly higher occurrence of dermatitis the following year (OR=42.4, 95% CI: 33.48-53.60, p<0.001). Of those affected in 2009, 362 (18%) sought medical attention.

Table 2 Results of the questionnaire survey by gender and age bracket.

Table 3 Patients who were affected or not affected in 2008 and 2009.

Nine people who could not provide their status as of 2008 due to recent relocation and/or impending birth of a child were excluded.

Discussion

Hospital review of caterpillar dermatitis patients

GM larvae hatch from the overwintering egg mass starting in late April to early May [10]. They spend several days resting on or near the egg mass [23]. When the maximum temperature exceeds 18°C for several days, they climb vertically in response to light [4]. The larvae then spin silken threads and are widely dispersed by the wind [4]. The period from start to end of dispersal varies from 3 to 14 days, depending on temperature [23]. In our review, most of the patients started experiencing dermatitis during the same period when the first-instar larvae were being dispersed. The weather during the major dispersal period favored larval dispersal activity in the 2009 spring and these warm, pleasant days were also conducive to increased outdoor human activity, increasing the potential for contact with larvae and their associated airborne materials.

Aber et al. [13] reported that among school children, the affected area was located on the arms, neck, and legs of 75%, 23%, and 21% of patients, respectively, whereas in our review, the affected area was located on the arms, neck, and legs of 64%, 87%, and 11% of patients, respectively. This may be due to differences in the exposed areas of the body associated with the different age groups of patients. There has been no study comparing the affected area between children and adults in GM caterpillar dermatitis; however, in cutaneous reaction to Thaumetopoea pityocampa, Vaga et al. [24] mentioned that the most frequent affected area were the extremities in children and the neck in adults.

About 80% of our patients were unaware of direct contact with a caterpillar on the affected area. Two possible reasons can be given for this. First, the attached first-instar larvae are so small (3 mm long) that individuals might not recognize them. Second, invisible airborne setae or other materials may have been deposited on the skin and clothing. In caterpillar dermatitis caused by other species, it is suggested that the patient developed dermatitis even without direct contact with the larvae [25-30]. Similar tendency was noted for the GM in this survey as well. None of the manifestations of caterpillar dermatitis are absolutely specific, and the differential diagnosis may be broad [31]. Possible differential diagnoses include insect bite(s), seasonal allergies, contact dermatitis of other origin, atopic dermatitis and acute drug-induced eruption. Therefore, to clinical diagnose caterpillar dermatitis, clinical features, development situation, and surrounding environment will required to be considered.

Questionnaire survey in Kuzumaki town

Tuthill et al. [19] showed in an epidemiological study performed in Massachusetts that rash rates clearly declined with age; their findings showed that the affected rate by age was 19%, 10%, and 2% in age groups 0-12, 13-59, and ≥60, respectively. In our study, a high incidence was observed in adults as well as in children. Because of the characteristic dispersal behavior of GM larvae, any age group may be at risk for exposure by participating in outdoor activities. We think that the differences in incidence by generation in our study may be caused by differences in the frequency of outdoor activity participation and by the degree of skin exposure. In addition, the elderly are less likely to react to bed bug bites [32]. This phenomenon of “immunosenescence” may also explain the lower prevalence of GM dermatitis in the age groups 70-79 years and ≥80 years in this survey.

The following three theories for the pathologic mechanisms of GM dermatitis have been proposed:

• –. mechanical irritation of the skin,
• –. intracutaneous injection of toxic substance(s) through setae,
• –. hypersensitivity reaction to insect antigen [13].

In our survey, although 60% of people were not affected in either of the 2 years examined, almost everyone who had been affected by similar dermatitis in 2008 suffered dermatitis again in 2009, and some people were affected for the first time in 2009. We assume that susceptibility to antigens differs among individuals, and some individuals may develop an allergy to GM after repeated exposures over 1 or more years. Even though the results of this study do not contradict the first 2 theories, they do indicate the possibility that allergy reactions play a role in the onset of dermatitis, in addition to the other stimuli.

Our investigation has important limitations. All data were collected retrospectively and might have been subject to recall bias. None of the patients had a diagnosis of atopic dermatitis in their allergy history. One possible explanation is that Kuzumaki Hospital did not have a Department of Dermatology. Hence, patients with frequent skin troubles might have consulted their regular dermatologists. The prevalence of atopic dermatitis in school children in this region was reported to be 7.4%, which is lower than that of other districts [33]. In addition, a survey of prevalence in adults in Japan showed that the prevalence rates decrease with age: 10.9% for individuals in their 20s; 8.8% for those in their 30s; 3.9%, 40s; 2.4%, 50s and 60s [34]. The median age of our patients was 67 years, and there were fewer young people – 29 (10%) under 20 years of age –; this was also probably why none of the patients had a history of atopic dermatitis. In the questionnaire survey, we did not ascertain that dermatitis in all individuals was caused by GM caterpillars. Since the survey was based on self-diagnosis, false-positive cases can not entirely be excluded. In order to evaluate this selection bias, we conducted a supplementary survey at 2 elementary schools and found that 104/173 students (60%) in school A and 29/43 students (67%) in school B were affected by dermatitis. These 2 schools were in the area of high GM larvae density. Since we observed a relatively high affected rate among males and females younger than 10 years of age and in males aged 10-19 years, the results of the questionnaire survey seem to be consistent with the actual outbreak situation. In the study of this region, we aimed at simplifying questions, increasing the response rate, and evaluating actual damage. As a result, our study shows the difference in prevalence among gender and age groups, the relationship between the incidences among the affected population in 2 consecutive years, and the hospital consultation rates in a large population. However, other potential risk factors such as atopic status, which can predispose people to GM dermatitis, could not be identified. Further investigation will be required to identify other potential risk factors of GM induced dermatitis and to clarify the pathologic mechanisms of GM dermatitis.

When GM infestation occurs, it is necessary to provide information about this species to the residents. We need to consider that the possibility of contact with a caterpillar can increase with each insect generation due to increases in the number of newly hatched larvae. To avoid contact with insect antigen, individuals should take measures to minimize skin exposure. During infestation periods, efforts to eradicate the GM, including through application of pesticides and scraping off egg masses in residential areas, were performed on a broad scale. Nonetheless, removal of all egg masses that had been laid in sheltered locations or in forest trees was nearly impossible, and the larvae that hatched there were dispersed for long distances. Additionally, in a large number of patients, the association of dermatitis with caterpillar exposure was often not recognized. Therefore, it is likely that completely avoiding contact with the toxic substance(s) is rather difficult. Because the main dispersion occurs within 2 weeks [23], it would be better to avoid going outdoors unnecessarily during this period. In the questionnaire survey, only 18% of affected people sought medical attention, indicating that most of them treated and cured themselves at home. This result also suggests the importance of preventing undue anxiety and confusion among residents by informing them precisely on how to treat GM dermatitis and by educating them that such health problems are self-limiting and can be cured by an adequate response.

The GM has gone through many cycles of infestation in Japan. However, no community outbreaks of dermatitis were reported until after the recent infestation of 2008 [21]. In addition, there have been no reports of outbreaks from areas where GM exists as a native species. In these areas, it is possible that recognition of GM-related health problems is underestimated. Taken together, these observations indicate that physicians should pay more attention to this potential public health problem when GM infestations occur.

Disclosure

Acknowledgments: The authors would like to thank Kiyoko Terui and Kazuko Wakasa, school nurses, for participating in the elementary school survey. We are grateful to Professor Yasutomo Higashiura, Laboratory of Ecology, Tokyo University of Pharmacy and Life Sciences, for providing valuable information about GM. Financial support: none; Conflict of interest: none.

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