Human tick bite records in a United States Air Force population, : implications for tick-borne disease risk

Journal of Wilderness Medicine, 5,405-412 (1994) ORIGINAL ARTICLE Human tick bite records in a United States Air Force population, 1989-1992: implications for tick-borne disease risk BRIAN S. CAMPBELL, DO, MPH] and DAVID E. BOWLES, PhD2* IUS AirForce School ofaerospace Medicine. BrooksAFB, Texas, 78235, USA 2Air Force AnnstrongLaboratory, Occupational Medicine Division, Environmental Biology Branch, Brooks AFB, Texas, 78235, USA Reports of tick parasitism were recorded for US Air Force personnel (n = 410) from 30 states and the District of Columbia. Of 462 ticks involved in attacks on people, the lone star tick,amblyomma americanum, and the American dog tick, Dermacentor variabilis, were the most common species represented (34.2% and 34.0%, respectively). Two vectors of Lyme disease, Ixodes pacificus and Ixodes scapularis (including the former Ixodes dammini) also parasitized people but were less common (1.7% and 9.1%, respectively). In addition, 34 (7.3%) brown dog ticks, Rhipicephalus sanguineus, were identified from human hosts. Most ticks submitted for identification were adults (66.5%) and nymphs (29.1%). Larvae were submitted infrequently «5%). Of those specimens examined for feeding status, 50.0% had blood-fed to some degree. Patients from which ticks were removed were predominantly male (56.8%) and ranged in age from 1 to 76 years with 55.3% (n = 152) being under 20 years. The head and neck area and the lower extremities were the most common sites of attachment by ticks (37.7% and 24.3%, respectively), but ticks were found attached on other areas of the body also, including the trunk, upper extremities, buttocks, and groin. Most ticks (65.5%) bit their victims during May, June, or July, but parasitism occurred during all months of the year. Our data suggest that people from all age groups and from across the United States are vulnerable to parasitism by ticks and, potentially, tick-borne diseases. Key words: ticks, human parasitism, military population, United States Introduction In North America, ticks (Acari: Ixodoidea) are foremost among arthropods in transmitting disease to humans. They have been implicated in the transmission of several serious human diseases, including Lyme borreiiosis, tickborne typhus (Rocky Mountain spotted fever), tularemia, relapsing fever, Colorado tick fever, babesiosis, ehrlichiosis, and tickborne encephalitis (Powassanvirus) [1-9]. Feedingby some ticks can cause tick paralysis, a progressive and ascending flaccid paralysis triggered by a neurotoxic substance in tick saliva [9]. Moreover, the parasiticbehaviorofticks can produce considerable psychological distress among affected individuals [10,11]. Ticks and tick-borne diseases sometimes are associated with the outdoor recreational and vocational activities of urbanized humans. Hiking, camping, hunting, fishing, and 'To whom correspondence should be addressed. Present address: Texas Parks & Wildlife Department, Resource Protection Office, 300 em. Allen Parkway, Building B, San Marcos, Texas 78666. 0953-9859 1994 Chapman & Hall

406 Campbell and Bowles other sports, as well as job requirements that place individuals in outdoor settings, increase the risk of being attacked by ticks and contracting tick-borne diseases. Clinical suspicion of a tick-borne disease often is based on exposure to ticks or tick habitat. However, not all species of ticks can transmit disease to humans, and tran'smission of particular pathogens can be restricted to a given species or groups of species. Therefore, identification of ticks removed from people aids in differential diagnosis and treatment. Previous studies have evaluated parasitism by ticks to determine which species of ticks most commonly attack people. However, these studies have been largely limited to small geographic areas [10-14] or have involved a limited number of tick species [15,16]. In an effort to better understand the relative risk of tick attacks and tick-borne disease on people over a broad geographic area, we summarized tick parasitism over a 4-year period for US Air Force personnel stationed across the United States. Materials and methods US Air Force Regulation 161-1, Medical Entomology Program [17], directs health-care provider,s to remove ticks found on patients and submit them to the USAF Armstrong Laboratory, Medical Entomology Function for identification and disease risk assessment. Health-care workers also provide information on the age and sex of the victim, site of tick attachment, and collection date and locality. In turn, entomologists at the Armstrong Laboratory provide health-care workers with information on the tick's identity, life stage (larva, nymph, adult male or female), feeding status (fed or unfed) as determined through visual observation, and known disease associations. Although the Armstrong Laboratory receives ticks from a variety ofsources, such as those from pets and survey collections, only ticks that had bit humans are included here. Ticks included in this study were removed from persons from January 1989 through December 1992. The Air Force population considered here includes active-duty members and their families, visiting retirees, and civilian employees. The data contained herein are subject to a strong selection bias in that we received ticks from only those victims of tick bites who sought medical attention and, of those, only from patients of health-care providers who were aware of, and willing to comply with, the regulations. Undoubtedly, many cases of tick parasitism go unreported, in part because some people never realize they are being parasitized, as when the specimens are small. Because of these strong biases, we only present a summary analysis of the data. Results Our study sample included ticks from widely distributed areas within the continental United States (Fig. 1). Areas not showing ticks means that no specimens from those locations were submitted during this study and should not be construed to mean that ticks do not occur there. Individual collection localities are too numerous to be shown but included both military installations and civilian locations within the indicated states. Many of the states represented in this study have at least two tick species that commonly attacked people. Seven states (Delaware, Florida, North Carolina, Ohio, Oklahoma, South Carolina, Texas) each yielded three tick species that parasitized people. California, New Jersey, and New York each reported four tick species that bit humans. A single unidentified nymphal Ixodes recorded from Wisconsin is not indicated in Fig. 1.

Human tick bite records, 1989-1992 407 Amblyomma amerlcanum c Dermacentor andersonl.0.. :ili!1abl1l.i t.lx2.dn~ oj.~ 4 J. scapularls '" RhIpicephalus sangylneus Fig. 1. Geographic distribution of tick parasitism among US Air Force personnel, 1989-1992. Of the 462 ticks we examined, the lone star tick, Amblyomma americanum, and the American dog tick, Dermacentor variabilis, were the most common, comprising 34.2% (n = 158) and 34.0% (n = 157), respectively, of all specimens submitted (Table 1). Dermacentor variabilis is the most widely distributed of the species found in this study, but Table 1. Species and life stages of ticks removed from a US Air Force population, 1989-1992* Species n % Larvae Nymphs Adults Male Female Amblyomma americanum 158 34.2 10 68 38 41 Amblyomma spp. 22 4.8 2 15 3 1 Dennacentor andersoni 16 3.5 0 0 7 8 D. variabilis 157 34.0 0 6 70 79 Dennacentor spp. 11 2.4 4 4 0 1 Ixodes cookei 3 0.6 1 2 0 0 I. pacificus 8 1.7 0 0 0 7 I. scapularis 42 9.1 2 10 0 28 Ixodes spp. 11 2.4 0 5 0 6 Rhipicephalus sanguineus 34 7.3 1 21 6 6 TOTAL 462 100.0 20 132 124 177 *Life stage could not be determined for all specimens.

408 Campbell and Bowles Table 2. The seasonal distribution ofticks attacking US Air Force personnel, 1989-1992 Species Month ofcollection J F M A M J J A S 0 N D Amblyomma americanum 1 5 23 35 46 24 11 10 1 2 Amblyomma spp. 1 5 6 1 4 1 4 Dermacentor variabilis 2 1 11 51 40 41 11 Dermacentor andersoni 1 7 7 1 Dermacentor spp. 1 2 6 1 1 Ixodes scapularis 4 2 5 8 3 3 4 2 2 1 2 6 Ixodes pacificus 2 1 3 2 Ixodes cookei 1 2 Ixodes spp. 3 2 1 3 1 1 Rhipicephalus sanquineus 1 2 1 4 8 4 5 7 1 1 TOTAL 4 7 16 49 106 111 86 35 20 14 3 11 lone star ticks were most common despite being primarily distributed in the southeastern quadrant of the contiguous 48 states. The eastern black-legged tick, Ixodes scapularis (n = 42,9.1%) (includes the former Ixodes dammini; see Oliver et al. [18]), and the brown dog tick, Rhipicephalus sanguineus (n = 34, 7.3%), also were submitted routinely but were less common. All other species, and specimens that could not be identified to species because they were damaged following removal, were submitted infrequently «5%). Adult (n = 301, 65.0%) and nymphal ticks (n = 132, 28.5%) were the most common life stages received. Only 20 (4.3%) larval ticks were submitted for identification during the study interval. Most bites over the 4 years of this study occurred during May, June, and July (Table 2), but ticks were active during all months of the year. Feeding status was determined for 65.2% (n = 302) of all ticks, and 50.0% of these had taken at least a partial blood meal. However, only 18.5% (n = 28) appeared to be fully engorged with blood. Most specimens were removed from the head and neck (n = 101, 37.7%) and the lower extremities (n = 65, 24.3%). In addition, ticks were detected on the trunk (n = 58, 21.6%), groin (n = 19, 7.1 %), upper extremities (n = 13,4.9%), and buttocks (n = 12,4.5%). Multiple ticks were removed from 7.8% of patients (n = 32, X = 2.7, range = 2 to 7). Age and sex were reported for 275 of the individuals (Table 3). Patient age ranged from 1 to 76 years (n = 275), with 48.0% (n = 132) being 10 years or under; adults primarily between the ages of 21 and 40 years accounted for the remainder. Males were parasitized more frequently than females (n = 154,56.8%, and n = 117,43.2%, respectively). Discussion All ticks examined in this study are capable of transmitting diseases to humans (Table 4). In addition, most of these species have broad distributions in North America [5], which clearly was reflected in this study. Although the lone star tick was found to be the most common species parasitizing humans, it generally is not considered to be a major vector of human disease. However, this species can effectively transmit tularemia [9], and it is a

Human tick bite records, 1989-1992 409 Table 3. A summary of patient information included in this study* Age group n % No./Sex (%) (years) Male Female 1-10 132 48.0 62 (48.4) 66 (51.6) 11-20 20 7.3 13 (65.0) 7 (35.0) 21-30 37 13.4 25 (67.6) 12 (32.4) 31-40 29 10.6 20 (69.0) 9 (31.0) 41-50 27 9.8 16 (59.3) 11 (40.7) 51-60 15 5.5 9 (60.0) 6 (40.0) 61-70 11 4.0 6 (54.5) 5 (45.5) 71-76 4 1.4 3 (75.0) 1 (25.0) TOTAL 275 100.0 154 (56.8) 117 (43.2) 'Patient data were incomplete for 135 of 410 patients included in this study. Gender was not reported for some representatives of the 1-10-year age group. suspected vector of Lyme borreliosis [19] and ehrlichiosis [9]. Because the lone star tick is active and feeds on a broad range of hosts, it should not be dismissed as insignificant when, involved in attacks on people. Lone star ticks can occur also in enormous population' densities, which may produce psychological distress in some individuals [10]. Table 4. Species of ticks removed from members of a US Air force population from 1989-1992, including human diseases known to be transmitted by the respective species* Species DiseaseSf Amblyomma americanum (lone star tick) Dermacentor variabilis (American dog tick) D. andersoni (Rocky Mountain wood tick) Ixodes scapularis (eastern black-legged tick) l. pacificus (western black-legged tick) l. cookei (Cooke's black-legged tick) Rhipicephalus sanguineus (brown dog tick) Tularemia, Bullis fever, (tickborne typhus, Lyme borreliosis, ehrlichiosis, tick paralysis) tularemia, tickborne typhus, tick paralysis, (ehrlichiosis) Colorado tick fever, tickborne typhus, tick paralysis Babesiosis, Lyme borreliosis, tick paralysis Lyme borreliosis Tick-borne encephalitis,** (Lyme borreliosis) Boutonneuse fever [Africa, Europe], tickborne typhus [Mexico], Mediterranean spotted fever [Israel], tickborne encephalitis [Africa], (ehrlichiosis) Note: Diseases for which the ticks are only suspected vectors are shown in parentheses. *Disease data modified from Goddard [5] and Spach et ai. [9]. *Diseases occurred in North America unless indicated by country or region in brackets. Rocky Mountain spotted fever. *'Powassan virus.

410 Campbell and Bowles Dermacentor variabilis is among the most medically important ticks in North America because of its broad geographic range, high vector potential for tick-borne typhus, tularemia, tick paralysis [5,9], and propensity for using humans as hosts. In addition, the American dog tick also may be a vector of ehrlichiosis [9]. Therefore, the American dog tick must be considered to be a significant and realistic threat to the health of people who participate in outdoor activities. Other researchers also have shown D. variabilis to be among the most common species attacking humans [11,12,14]. A related species, Dermacentor andersoni (Rocky Mountainwood tick), is the primaryvectorofcolorado tick fever and tick-borne typhus in western North America. Although we found that this species parasitized humans in 5 western states (Fig. 1), only 16 specimens were submitted to us for identification. However, the low number of D. andersoni records we received may be a result of the lower human population densities in the western states and, hence, reduced the incidence of tick parasitism. The species ofixodes reported in this study are either confirmed or suspected vectors of Lyme borreliosis and/or human babesiosis. As such, the feeding of these ticks on humans should always present cause for concern. The eastern black-legged tick, Ixodes scapularis, is particularly common in the eastern, northeastern, and midwestern United States where Lyme borreliosis is most prevalent. Moreover, this species readily parasitizes humans. A related species, the western black-legged tick (I. pacificus), also was found in this study, and it is considered to be a primary vector of Lyme borreliosis in the western states. In our study, nymphs and adult females of the black-legged ticks accounted for 90% of the attacks by these two species. Nymphal and adult females ofi. scapularis are the primary life stages responsible for transmitting Borrelia burgdorferi (Lyme disease causative agent) to humans [20]. The brown dog tick, R. sanguineus, generally is not considered to be a significant parasite of humans in the United States. This cosmopolitan species is primarily a pest of pets, especially dogs. However, in other areas of the world, the brown dog tick has a broad host range, including humans [21]. The increase in reported attacks on humans by brown dog ticks in the United States in recent years [14,15,22,23] shows this species parasitizes humans more commonly than previously reported. The brown dog tick is a vector of tick-borne typhus in Mexico, and it also may be involved in the transmission of human ehrlichiosis [5]. In Europe, Africa and Asia, the brown dog tick has been reported to transmit boutonneuse fever, Mediterranean spotted fever, tick paralysis, and tick-borne encephalitis [5,24], thus implying a potentially significant public health concern when involved in attacks on humans. In addition, because of its association with pets, the brown dog tick can be the most common tick species in some urban environments, especially in the southeastern United States. Our finding that adult and nymphal ticks were the most common life stages parasitizing humans is consistent with previous reports [5,12,14,25]. The low number of larval or "seed" ticks submitted in this study may relate to their host preference (e.g., rodents, birds) and small size. Depending on the species, larval ticks may go unnoticed until the specimen becomes fully blood-engorged. The time required for engorgement and pathogen transmission varies considerably among tick species, life stages, and the type of pathogens being transmitted. However, half the ticks in this study were at least partially fed. A large proportion of these specimens probably had ample opportunity to transmit pathogens. Our finding that the head and neck were the preferred feeding sites is consistent with previous reports on tick parasitism

Human tick bite records, 1989-1992 411 [11,12,14]. We did not attempt to compare variation in attachment sites among or between species. Spring and summer months generally are the most popular for outdoor recreational activities in the United States, which may account for the increase in attacks by ticks we recorded during this time. The higher incidence of parasitism during the warmer months of the year most likely reflects the increased activity of ticks. Other studies have shown similar seasonal patterns of parasitism by ticks [5,12,25-27]. Our finding that ticks are active throughout the year shows that risk of infection from tickborne pathogens may be present at all times, particularly in warmer climates. However, the relative risk, even during warmer months, of getting a tick-borne disease is low, and the risks of contracting a given disease can vary considerably among geographic regions. The predominance of young «20 years) patients probably reflects the increased outdoor activity of this group in relation to more elder individuals, but the broad range in age of patients (1-76 years) clearly indicates that all age groups are vulnerable to parasitism by ticks. Although males outnumbered females in our study, the ratio of these two genders in relation to susceptibility to parasitism by ticks probably is nearly equal for the entire population. Although our data are derived from a military population, we believe that they represent a conservative estimate of the risk of tick infestation for all people in North America who engage in outdoor activities. Indeed, we found that ticks parasitizedvirtually all age groups and both sexes and that tick parasitism occurred throughout the continental United States. Given the emergence of serious tick-borne diseases, such as Lyme borreliosis and ehrlichiosis, and the continuing presence of tickborne typhus, Colorado tick fever, and babesiosis, people who participate in outdoor activities are at some risk of infection from tick-borne diseases. Individuals who engage in outdoor activities should be alert to tick bites and should use appropriate measuresfor avoiding ticks [6], and health-care providers certainly should include tick-borne illnesses in the differential diagnosis of patients with professions or hobbies that involve outdoor exposure. Acknowledgments We thank Armando Rosales for assisting with the literature search for this study. Dr. Chad McHugh, Dr. Jerome Goddard, Dr. Rich Robbins, and Dr. Durland Fish kindly reviewed earlier versions of the manuscript. References 1. Anderson, J.F., Mintz, E.D., Gadbaw, J.J. and Magnerelli, L.A. Babesia microti, human babesiosis, and Borrelia burgdorferi in Connecticut. 1 Clin Microbiol1991; 29, 2779-83. 2. Burgdorfer, W. A review of Rocky Mountain spotted fever (tick-borne typhus), its agent and its tick vectors in the United States. 1 Med Entomol1975; 12,269-78. 3. Emmons, R.W. Ecology of Colorado tick fever. Annu Rev Microbiol1988; 42, 49-64. 4. Eng, T.R., Harkess, J.R., Fishbein, D.B. et al. Epidemiologic, clinical, and laboratory findings of human ehrlichiosis in the United States, 1988.1Am MedAssoc 1990; 264, 2251-8. 5. Goddard, J. Ticks and tickborne diseases affecting military personnel. Brooks AFB (TX): USAF, School ofaerospace Medicine, 1989 Sept. Report No. USAFSAM-SR-89-2. 6. Hamilton, D.R. Avoiding Lyme disease. Postgrad Med 1990; 87, 167-76.

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