Severe Tungiasis in Underprivileged Communities: Case Series from Brazil

Hermann Feldmeier, Margit Eisele, Rômulo César Sabóia-Moura, Jôrg Heukelbach

Disclosures

Emerging Infectious Diseases. 2003;9(8) 

In This Article

Discussion

With a length of <1 mm, Tunga penetrans is the smallest known flea species.[27] Once burrowed in the skin of its host, the flea becomes hypertrophic, produces and releases eggs, and eventually dies. Microbiologically, the embedded flea behaves as a foreign body with a continuously enlarging surface.[8] The parasite remains buried in the epidermis, except for the posterior parts of the abdomen bearing the anus, the genital opening, and four pairs of large stigmata. The protruding hindquarters create a sore, connecting the surface of the skin to the epidermis and, through the proboscis of the flea, to the dermis. When the skin's surface is linked by means of a foreign body to underlying tissue layers, translocation of the normal microflora occurs, leading to a bacterial infection in the epidermis and presumably to the formation of a biofilm on the surface of the foreign body.[28] Thus, in the vertebrate host, the infection with T. penetrans is a self-limiting process, and the risk for infectious complications is obvious.

In fact, older literature abounds with observations on severe pathologic findings associated with tungiasis and mentions debilitating sequelae such as phagedenic ulcers, gangrene, auto-amputations of digits, and the loss of entire limbs.[19,29,30] Death resulting from infection with Clostridium tetani is not uncommon in nonvaccinated persons.[19,20,21,22] Such severe sequelae of tungiasis were not only observed in native South American populations by European travelers[2,15,31] but were also reported by military physicians responsible for local forces in West and East Africa.[15,16,29] In 1909, Decle[29] gave a vivid description of the havoc wrought by the ectoparasite on military personnel in Kenya: "At Ford Raymond the garrison consisted of 160 askaris (soldiers) and 70 porters; out of this men 72 soldiers and 30 porters were absolutely unfit for service through ulcers brought on by jiggers, and 30 more were lame." In another garrison, Fort Grant, severe tungiasis caused illness in 50% of the local soldiers.[29] During military operations in Cameroon in the first quarter of the 19th century, 5% of all septic admissions were due to complications of the ectoparasitosis.[15] These accounts show that severe tungiasis was an important health problem in the underdeveloped rural hinterlands of South America and Africa until the middle of the 20th century.

In the last 50 years, severe tungiasis seems to have disappeared as a disease entity. In current textbooks the ectoparasitosis is mainly mentioned as an exotic nuisance for the casual traveler in South America and sub-Saharan Africa.[6] Tourists seldom have more than one lesion and usually seek medical advice within 1 week of flea penetration, resulting in the extraction of the parasite at an early stage.[12] However, we observed persons living in a underdeveloped neighborhood in Fortaleza, northeast Brazil, where patients carried up to 145 sand fleas in all stages of development.

As parasites tend to accumulate at certain predilection sites, the pathologic findings should be particularly severe in these sites. In our patients and others in the community, many infected persons have lesions in the periungual region of the toes[9] which explains the high frequency (69%) of nail deformation or nail loss. Furthermore, as the sole of the feet and the heel were other predilection sites, difficulty in walking was also very common.

Various mechanisms exist by which embedded fleas could induce pathologic alterations of the skin in an early stage of development. Acute inflammation with erythema, edema, pain, and itching is conceivably due to tissue damage induced by a metabolically highly active and continuously enlarging parasite. As with other blood-sucking insects, T. penetrans releases proteolytic enzymes during penetration and growth, causing an inflammatory response of the skin. In comparison with other ectoparasites that frequently reinfect humans, the immune response of the host might contribute to the intense inflammation observed soon after penetration.

As the lesion develops, bacterial superinfection almost inevitably occurs.[8] During penetration, the flea breaks up the stratum corneum, allowing bacterial microcolonies on the skin surface to spread. In addition, pathogenic microorganisms on the outer surface of the flea may be actively carried into the epidermis.[8] As the continuously expanding body of the flea (the volume increases by a factor of roughly 2,000) consists of rather smooth intersegmental skin and newly formed chitinous clasps, the embedded flea fulfills the requirement of a structural matrix to which microorganisms could easily adhere.[32] In fact, scanning-electron microscopy of extracted fleas showed that pathogens such as streptococci and gram-negative rods formed a biofilm in the tiny grooves of newly built intersegmental skin as well as on the chitinous exoskeleton (Feldmeier and Meckes, unpub. data, 2002).

As the lesion itches immediately after the flea penetrates, patients usually start to scratch, which, in turn, promotes the entry of bacteria through the persistent sore in the epidermis. In fact, we invariably observed microabscesses in histologic sections of lesions only 2 days after penetration.[7]

In many of our patients, bacterial superinfection was also the result of an inappropriate manipulation of lesions with nonsterile instruments by the patient or caregiver (Figures 4 and 5). The remarkable desquamation of the skin observed around late-stage lesions (Figure 4) has its histopathologic correlates in hyperkeratosis and parakeratosis of the stratum corneum.[7]

Recently, Wolbachia species have been identified in the ovaries of T. penetrans.[33] As antigens of these bacterial endosymbionts have been associated with the pathologic immune response in some filarial diseases (e.g., onchocerciasis), part of the intense immune response in tungiasis might also be evoked by Wolbachia antigens being released from decaying fleas.[34] At present, a study is being undertaken to verify this assumption in experimentally infested rats.

Reports on severe tungiasis involve persons with particular risk factors, such as alcoholics or the mentally diseased, who are expected to have prolonged contact with the ground or are unable to care for themselves.[35,36] Our data clearly show that severe tungiasis also occurs in persons without such risk factors who live in an impoverished community, when environmental, socioeconomic, and behavioral factors coexist and make frequent reinfection likely or impede the extraction of penetrated fleas in the early stage. Recently, estimates show that in northeast Brazil alone, several million people who live in communities with similar environmental characteristics to those we studied are at risk of tungiasis.[2]

Although we cannot give an accurate estimate of severe tungiasis in the general population level, 16 (17%) of 86 patients arrived at the PHCC for reasons unrelated to the ectoparasitoses but showed important sequelae, which indicates that tungiasis is frequent on the community level. This assumption has been corroborated by a study performed in south of Brazil.

Thus, whereas severe tungiasis has disappeared from the underdeveloped rural hinterland where it formerly existed, this disease should be considered as a resurgent health problem of underdeveloped urban areas, where environmental conditions favor a high attack rate and social neglect is intricately linked to poverty and inadequate healthcare behavior. At least in Brazil, the medical profession wholly neglects this ectoparasitosis, and physicians do not diagnose tungiasis during consultation unless the condition is mentioned by the patient.[25,37]

Morse[38] has convincingly argued that a reemerging disease is rarely a purely microbiologic event but commonly has causative cofactors such as ecologic changes, changes in human demography, international travel, or breakdown of public health measures. The results of our study suggest that poverty, social neglect, and inappropriate healthcare behavior should be added to this list.

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