COLLEMBOLIASIS: YET ANOTHER EMERGING ZOONOSIS? A PRELIMINARY REPORT

Frederic L. Frye, DVM, MSc, CBiol, FIBiol,
Davis, California

It has been known for over a century that springtail insects (Apterygota) can live freely or in association with a variety of biological systems that include terrestrial, freshwater- and shoreline-marine aquatic. Once believed to be entirely saprophagous and/or phytophagous facultative (or obligate) detritovores, springtails have been found in the following circumstances: feeding upon nesting ants, flies, and conspecific dead springtails (Dasgupta and Dasgupta, 1995); infesting bumblebees (Husband and Brown, 1976); infesting insect eggs (Tosi, 1977; Tosi and Sartini, 1983; Waldorf 1971); parasitizing cabbage moth larvae (Griffiths, 1985); infesting hermit crabs (Van Goetham and Hanssens, 1982); living in the gut of an avian ectoparasitic insect, Myrsidea sp., which is a Mallophagan louse (Oniki and Butler, 1990); parasitizing salamanders and toads (Dasgupta and Dasgupta, 1990); associated with nesting mammals (Dasgupta and Dasgupta, 1995; Hrivnak, 1981; 1983; Nosek and Vysotskaya, 1976; Roy and Dasgupta, 1971; Szabo, 1977); and attracted to and actively feeding on moist blood films from red pandas, Ailurus fulgens, (Dasgupta and Dasgupta, 1995). There have been a few reports of springtails infesting humans (Dasgupta and Dasgupta, 1995; Hunter, Frye and Schwartzwelder, 1960; Scott, Wiseman, and Stojanovich, 1962). Collembola can utilize phoresy as a means for transporting themselves from one habitat (or host) to another, particularly from birdnest to birdnest (Oniki and Butler, 1990). Thus, mounting evidence supports the contention that, although they usually are thought to be merely ubiquitous and harmless saprophytes, springtails can alter their behavior and become parasitic without undergoing evolutionary structural alterations to their feeding anatomy. While not limited to springtails, a change in fundamental feeding behavior is unusual and noteworthy.

Recently, I was contacted by an official of the National Pediculosis Society who was investigating the possibility that all members of a family that was living in Iowa and suffering from very sever and intensely pruritic mutifocal head, trunk, and pubic dermatitis were infested with parasitic collembolan (springtail) insects. After extensive diagnosis and treatment of their intese pruritis, each was told that he/she was suffering from "delusional parasitosis" and was referred for psychiatric evaluation. The adult female in the family is a registered obstetrical nurse and perceived that these lesions could be attributed to an organic rather than a psychological aetiology. She then commenced a search for "unconventional" professional assistance to help determine the cause for this condition. Interestingly, the rationale for contacting me may have been erroneous because: (1) although I am the senior author of a paper documenting the parasitism of a dog by human crab lice, Phthirus pubis, (Frye and Furman, 1968), I possess no special knowledge of springtails; and (2) although there is a textbook on tropical medicine edited by someone with an identical surname as mine, I am not the author. However, this approach was serendipitous because I began my veterinary career as a chronic disease epidemiologist and I am now a comparative pathologist with an admittedly ecclectic curiousity.

Affected patients complained of slightly raised rec, black, and/or white lesions that itched, and it felt as if something was crawling beneath the skin. When scraped or rubbed with vinegar or antifungal cream, some areas produced short red or white "fibres" that moved. In a few instances, entire creatures with "scorpion-like tails that curved downward" were teased out. In some instances, the patients reported seeing small, round, white "nit"-like objects adhering to their head hairs.

Routine tests and biopsies were negative for the presence of Herpesviral dermatitis, mite infestation (scabies), and head- and bodylouse infestation (pediculosis). However, the white nit-like objects that adhered to individual head hairs probably were the eggs of headlice. Some skin biopsies revealed the presence of arthropod insects that were characterized as collembolas. Because of their similar small size, it is unlikely that the springtails used the headlice as phoretic transport vehicles to move between hosts. Therefore, it appears that some patients were simultaneously infested with both springtails and headlice.

A literature search revealed an expanding source of information that documents that springtails have become true parasites of a variety of animal hosts even though they lack specialized feeding structures. Once the Centers for Disease Control in Atlanta, Georgia began to investigate pruritic dermatitis of unknown pathogenicity, they found 123 cases. These cases included 122 people from 22 states in the U.S. and 1 person who was thought to have been infested in South Korea; all of these cases occurred from 1990 to 1995. The largest number were from California. Most were originally believed to be instances of scabies or pediculosis and, accordingly, were treated initially with prescription and/or over-the-counter proprietary insecticidal preparations. Most of these cases were traced to (or at least thought to be related to) a variety of outdoor occupations, contacts with domestic and wild animals, gardening activities, exposure to various fungi, etc. Patients ranged from young children to elderly adults. The sex ratio was 59% female:43% male. In one-third of the households, more than one inhabitant was affected by "atypical" pruritic dermatitis for which mites, lice, or other common arthropods could NOT be implicated as the aetiologic agent(s).

Whether the immune status of the affected individuals played a major role in promoting springtail parasitism or whether insecticide resistance was a component in these cases is entirely conjectural; however, both factors have been suggested as possibilities. In all of these cases, the patient's serological status with respect to HIV infection is unknown because of privacy protection; the liberal use of lindane and other potent organochlorine-containing acaricidal or insecticidal preparations was documented, but their actual role as promoters of immunoincompetence or chemical resistance is unknown.

To the date of this writing, the taxa that have been reported to induce intense pruritic dermatitis in man are: Entomobryo nivalis and E. tenuicauda (Hunter, et al, 1960; Scott, et al, 1962); Hypogastrura menubrialis and Sora buski (Megnin, 1839; Freche and Beille, 1896). In addition, Orchesella albosa var. oinslferi was recorded infesting humans without causing pruritis (Scott, et al, 1962).

In summary, these cases of collemboliasis may be only medical curiousities , or they may be the first "sentinel" instances of a significant emerging parasitism.

REFERENCES

Dasgupta, R. and Dasgupta, R. (1990). Collembolan Insects as Potential Parasites. Trans. R. Soc. Trop. Med. Hyg., 84:438.

Dasgupta, R. and Dasgupta, R. (1995). A Treatise on Zoophily in Collembola with a Summary of Knowledge on Origin and Evolution of Parasitism in Saprophagous Forms of Animals. J. Bengal Natural History (New Series) 1(2):53-60.

Freche, L. and Beille, L. (1896). Un Parasitisme Accidentale de L'Homme. Comp. Rend. Acad. Sci. Paris, 73-80.

Griffiths, G.C.D. (1985). Hypogastrurua succinea (Collembola:Hypogastruridae) Dispers by Adults of the Cabbot Maggot, Delia radicum (Diptera:Anthomytidae), Infected with the Parasitic Fungus Strongwellsea castrans (Zygomycetes:Entomophthoracea). Canadian Entomol., 8:1063-1064.

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Hunter, G.W., Frye, W.W. and Schwartzwelder, J.C. (1961). A MANUAL OF TROPICAL MEDICINE). Philadelphia, PA; W.B. Saunders Co. xxx+892 pp.

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Roy, P. and Dasgupta, B. (1971). Behavior of Chrysomys megacephala (Fahr) and Hemispyrellia ligurriens (Wied.) as Parasites of Living Animals under Experimental Conditions. S. Afr. J. Med. Sci., 36:85-91.

Scott, H.G., Wiseman, J.S.,, and Stojanovich, C.J. (1962). Collembola Infesting Man. Ann. Entomological Soc. America, 55(4):428-430.

Szabo, I. (1977). Examination of the Fauna in the Nests of Mammals and Birds in Hungary. Allantani Kozl., Budapest, 64(1-4):153-158.

Tosi, L. (1977). Alimenti Animali Neili Diete di Alcune Species di Collemboli, Richerce Preliminary sul Cannibalismo in Sinella caeca (Schott). Ateneo Paramense. Acta. Nat., 13:445-455.

Tosi, L. and Sartini, M. (1983). Interactions Between Social and Feeding Behaviour in Sinella caecs (Collembola). Boll. Zool. Naples, 50:189-195.