Review

For reprint orders, please contact [email protected]

Revision on tungiasis:
treatment options and prevention
Jorg Heukelbach

The parasitic skin disease tungiasis occurs in many resource-poor communities in Latin
America, the Caribbean and sub-Saharan Africa. The sand flea, Tunga penetrans, most
commonly penetrates into the skin of the feet. Many individuals harbor a large number of
embedded parasites and show significant morbidity. Standard treatment consists of
surgical extraction of the flea and application of a topical antibiotic. There are no drugs
available with proven effectiveness. Clinical trials performed in the last few years did not
show very promising results. Thus, surgical extraction still remains the treatment of choice
CONTENTS
in patients with a low parasite load, such as tourists returning from endemic areas.
Epidemiology
Probably the best approach to reduce tungiasis-associated morbidity in heavily affected
Diagnosis individuals is the application of a repellent to prevent the penetration of sand fleas. In the
Therapy & prevention future, we should see new exciting data on the biology, epidemiology, therapy and control
of tungiasis of tungiasis.
Conclusion
Expert Rev. Anti Infect. Ther. 4(1), 151–157 (2006)
Expert commentary
Tungiasis (also known as sand flea disease) precarious [1,7]. Bacterial superinfection is
Five-year view
occurs in Latin America and sub-Saharan almost invariably present, and pustules,
Key issues Africa, and causes considerable morbidity in abscesses and ulcers are commonly seen [8].
References affected communities [1]. This parasitic skin Pain, inflammation and fissures hinder
Affiliation disease is characterized by the penetration of individuals from walking normally [9].
the female sand flea Tunga penetrans Sequelae include deformation and loss of
(Linnaeus, 1758) into the skin of its host. toenails, as well as deformation of digits. In
After penetration, the flea undergoes nonvaccinated individuals, tungiasis lesions
hypertrophy. Some days later the parasite may be a port of entry of clostridiae leading
enlarges up to 1 cm in diameter, producing a to tetanus [10–13].
large number of eggs during a period of In this article, an overview on tungiasis is
2–3 weeks [2,3]. Eggs are expelled from the given, possible therapeutic and preventive
rear opening of the flea, which is visible as a measures are discussed and a future outlook
black dot in the center of the lesion. is presented.
Several weeks after penetration, the fleas die
and are later sloughed from the epidermis by Epidemiology
Federal University of Ceará, skin-repair mechanisms [2]. Both male and T. penetrans is one of the few parasites that
Department of Community Health, female T. penetrans are blood feeding [4]. spread from the neotropical to the afro-
School of Medicine, Rua Prof. Penetration most commonly occurs on the tropical region. It occurred originally on the
Costa Mendes 1608, 5° andar,
feet, but may occur anywhere on the body, American continent, and the first reports of
Fortaleza 60430–140, Brazil
Tel.: +55 854 009 8045 such as the hands, elbows, neck, buttocks the disease date back to the years of the
Fax: +55 854 009 8050 and genital region [5,6]. Typically, T. penetrans discovery of the Americas [14–18]. The first
[email protected] affects the periungual area of the toes, the scientific description was made by Aleixo de
heels and the soles. Abreu from Brazil in the 17th century [19]. In
KEYWORDS:
chigoe, ectoparasite, jigger flea, Severe complications are common in areas the 19th century, the parasite was dispersed
prevention, sand flea, therapy, where people suffer from constant reinfec- by humans to many parts of sub-Saharan
treatment, Tunga penetrans,
tungiasis tion, and where hygiene conditions are Africa [15,16,20,21], and at the end of the

www.future-drugs.com 10.1586/14787210.4.1.151 © 2006 Future Drugs Ltd ISSN 1478-7210 151

Heukelbach

century had already reached Zanzibar and Madagascar [20,22]. characterized by the penetration of the female flea. The
In those days, severe pathology caused by tungiasis, such as hypertrophy of the parasite’s abdomen begins in stage II, and
intense inflammation leading commonly to suppuration, the parasite becomes more obvious as a growing whitish
ulcer, gangrene and difficulties in walking, were reported by nodule (1–2 days after penetration). At this stage, the
travelers to endemic areas in South America, Africa and the anal–genital opening of the flea appears as a black dot in the
Caribbean [20,23–27]. center of the lesion. In stage III (2 days to several weeks after
The sand flea now occurs in Latin America (from Mexico penetration), the hypertrophy becomes macroscopically
in the north to Argentina in the south) on several Caribbean visible. Expulsion of eggs and feces are typical. The lesions
islands, as well as throughout sub-Saharan Africa [1,28–33]. In are usually painful and produce the sensation of foreign
the endemic area, the disease is concentrated in resource- bodies expanding under the skin. In stage IV, a black crust
poor communities, where prevalence may exceed covers an involuted lesion with a dead parasite. A residual
50% [31,33–40]. In these communities, waste is not collected scar is characteristic of stage V.
(and consequently is abundant in the neighborhood), people
live close to infested rats and domestic animals (dogs and Therapy & prevention of tungiasis
cats) that contribute to high attack rates, and houses often do As severe pathology caused by tungiasis almost exclusively
not have concrete floors. In fact, families living in houses occurs in resource-poor settings, the disease is still neglected,
with floors of sand are most vulnerable for tungiasis [41]. The and clinical efficacy/effectiveness of only a few topical and
presence of dogs and waste on the compound have also been oral compounds has been adequately tested. There is no drug
identified as risk factors; the population attributable fraction on the market with satisfactory effectiveness.
(i.e., the fraction of cases which would not have occurred if Consequently, standard treatment consists of surgical
the exposure had been avoided) of these two variables has extraction of the flea under sterile conditions [1]. In a setting
been estimated to be greater than 50% [41]. where the attack rate is not very high, daily inspection of the
The parasite load is high in these areas, and commonly feet and immediate extraction of embedded fleas is the best
individuals harbor dozens – even hundreds – of fleas [7,35]. approach and protects against complications. The opening in
During the year, attack rates vary significantly with relatively the epidermis has to be carefully widened with a sterile
few cases occurring during the rainy season, and a higher needle or a similar instrument to enable the extraction of the
incidence and prevalence during the dry season [42]. entire flea without rupturing. This is not easy and requires a
A variety of animals may serve as reservoirs for T. penetrans. skilled hand. Thus, the flea is often torn during extraction,
Especially dogs and cats, but also pigs and rats are important and parasite parts are left in the wound. In addition, in
reservoirs [43–48]. For example, in a resource-poor community resource-poor settings, hygiene is often not applied, and
in northeast Brazil, 67% of dogs, 50% of cats and 59% of severe inflammation and bacterial superinfection are a
captured rats were found infested and contributed to a high common result. After extraction, the wound should be
attack rate in humans [48]. treated with a topical antibiotic. Fleas should be extracted as
early as possible to reduce the risk of secondary infections [8].
Diagnosis Tungiasis lesions may also serve as an entry point for
The diagnosis of tungiasis is easy and made by clinical tetanus [10–13], and immune status has to be verified; in the
inspection [1]. Patients often complain about itching, pain case of insufficient protection vaccination is indicated.
and the sensation of a foreign body. Most lesions occur on Extraction of embedded fleas is simply not feasible in
the nail rim. Eggs attached to the skin and the release of fecal situations where people live in a highly affected community,
coils are pathognomonic. In the presence of a fully suffering from dozens or even hundreds of penetrated sand
developed, reproductively active female flea, a round, watch fleas, and with attack rates of ten or more new fleas per
glass-like patch appears, frequently accompanied by inflam- individual per day. This is exemplified by a historical report
mation, hyperkeratosis and desquamation of the surrounding from Africa where 280 sand fleas were extracted on 1 day
skin. In late-stage lesions, a black crust covers a dead parasite. from a boy who had been infested at feet, knees, hands,
A biopsy of the lesion is usually not indicated. In single elbows and the back [24].
cases of atypical tungiasis, diagnosis can be difficult, and a Different compounds have been evaluated for their
biopsy may be indicated, for example, when lesions have a efficacy on tungiasis in a number of clinical trials. In 1982,
pseudoepitheliomatous appearance at ectopic sites [6]. Parts good efficacy of the antischistosomal agent niridazole
of the female flea and eggs in its abdomen are evident in (Ambilhar®), a nitrothioimidazole, was achieved in a clinical
histological sections [28,49–55]. trial in Nigeria [56]. The authors had observed that treatment
Infestation with T. penetrans is a dynamic process, and the of children with this agent for schistosomiasis resulted in the
aspects of the lesions change with time. The natural history death of the embedded sand fleas, so they conducted a
of tungiasis was described in 2003 in detail by Eisele and double-blind, randomized controlled trial in 155 school
colleagues [2]. The disease undergoes five stages: stage I lasts children with tungiasis. One dose of 30 mg/kg body weight
approximately half an hour to several hours, and is was compared with two doses given 1 week apart, and a

152 Expert Rev. Anti Infect. Ther. 4(1), (2006)

 Treatment and prevention of tungiasis

placebo group. The single-dose and two-dose regimen with affected sites [43,44,68]. However, these reports have not been
niridazole resulted in complete healing of all tungiasis lesions adequately controlled or documented and are of anecdotal
in 3 weeks in all subjects as compared with 0% healing of nature. Metrifonate is an organophosphorous compound
ulcers in the control group. However, the outcome measures used in human medicine as an antischistosomal drug due to
were not well defined, and there were other methodological its activity against Schistosoma haematobium.
problems which limit the interpretation of results. For In historical reports, topical gamma benzene hexachloride
example, after 3 weeks, it is expected that most sand fleas (Lindane, Gammatox®) was also claimed to be effective in
have died anyway, and reinfection rate has to be evaluated, killing embedded T. penetrans in humans, pigs and
which was not the case in this trial. It is also not clear cattle [45,69]. However, there are no appropriate data
whether the results were due to an antiparasiticidal or anti- verifying these observations. There are also anecdotal reports
inflammatory/bactericidal effect of niridazole. This anti- of topical application of petroleum, kerosene and
schistosomal agent is now known to cause cancer and is a dichlordiphenyltrichloroethane, or bathing the feet in
suspected gastrointestinal, liver and kidney toxicant [57–60]. formalin solution [16,56,70]. Obviously, these measures are not
Thus, the drug has become obsolete and clearly cannot be acceptable today.
recommended for use in tungiasis. Wearing shoes has been considered as a possible means to
In the last 10 years, dermatologists have claimed that the protect individuals against sand fleas [1]. However, for most
anthelminthic agent ivermectin has been efficacious in people affected by tungiasis, conventional shoes are simply
Brazil, where the oral drug is registered for the treatment of not affordable and flip-flops are worn instead. Additionally,
other parasitic skin diseases (scabies and pediculosis) [61]. In closed shoes and socks seem to prevent tungiasis to a certain
Argentina, oral treatment with ivermectin (one dose of degree, but complete protection cannot be achieved.
200 µg/kg body weight) was suggested to be effective in a In severely affected communities, reinfestation may occur
patient with tungiasis [62]. However, as sand fleas die daily, and the sand fleas remain embedded in the host, even if
naturally several weeks after penetration, uncontrolled they have been killed by a chemotherapeutic agent. Thus, the
studies are difficult to interpret. In fact, a recent randomized port of entry of bacterial pathogens and the causal agent for
controlled trial with oral ivermectin at a relatively high dose inflammatory reaction persist. Consequently, the use of an
(300 µg/kg body weight given in two doses on consecutive effective repellent would probably be a better approach to
days) did not show any efficacy as compared with a reduce tungiasis-associated morbidity than treatment after
placebo [61]. infestation in areas where socioeconomic conditions are
Other authors suggested treatment with oral thiabendazole precarious and where attack rates are high.
(50 mg/kg/day for 15–18 days). As these studies have not A natural repellent based on coconut, jojoba (Simmondsia
been controlled, the effectiveness of oral thiabendazole chinensis) oil and Aloe vera (Zanzarin®), which is
remains speculative [63–65]. Thiabendazole is often not well recommended against biting insects and ticks, showed an
tolerated by patients, causing nausea and other gastro- impressive regression of clinical pathology in heavily
intestinal side effects, thus it may not offer a suitable infested patients [71]. In a controlled crossover study
treatment in any case. conducted in an area with extremely high transmission,
Some efficacy of topical 0.8% ivermectin, 0.2% twice-daily application onto the feet reduced the infestation
metrifonate and 5% thiabendazole lotions were reported in a rate by more than 90% (FELDMEIER AND COLLEAGUES, UNPUB-
trial compared with a topical placebo lotion and a control LISHED OBSERVATIONS). Interestingly, application of the
group without treatment [66]. It remains speculative if higher repellent for a period of 4 weeks reduced the clinical pathol-
concentrations of these compounds will result in better cure ogy to an insignificant level. This finding is of particular
rates, and appropriate studies are indicated. interest, as prevention of tungiasis-associated pathology is an
In a controlled field trial on dogs, the topical application important achievement. A study is currently being under-
of a combination of 10% imidacloprid and 50% permethrin taken to determine the optimal intermittent application
(Advantix®) provided a good efficacy against embedded regimen of the repellent.
sand fleas [67]. Presumably, the reduction of the animal Interestingly, the use of a repellent to reduce severe infesta-
reservoir in a community will reduce the attack rate in the tion was proposed more than 50 years ago [72]. There are
human population. Thus, the treatment of dogs with these several other promising compounds used in traditional
compounds could be an effective approach to reduce the medicine to prevent sand fleas from penetrating, such as
prevalence of human tungiasis at the community level. In a castor plant oil and cassava extract which need to be tested by
similar way, appropriate campaigns to reduce the rat in vitro and in vivo studies.
population will probably increase the effectiveness of An epidemiological study has recently suggested that
control measures. exposure takes place outside and inside houses [41]. Off-host
To kill embedded fleas from dogs and cattle, some authors life cycle can be interrupted intradomiciliary by cementing
recommended foot bathing with 0.2% metrifonate solution floors of houses. However, there are no reliable data on
and topical application of 4% metrifonate solution at intervention studies published.

www.future-drugs.com 153
Heukelbach

Conclusion for the off-host stages (larvae and pupae) of the flea will be
Tungiasis has been a neglected disease for a long time. The known in detail, which will help to identify where trans-
disease is highly prevalent in many urban shantytowns and mission occurs most commonly, and to focus control
rural communities in the endemic area. There is not a single measures on these areas. The limited information on these
drug on the market with proven satisfactory effectiveness for aspects has hampered control of tungiasis at the community
tungiasis. It is also questionable if an effective antiparasitic level. Intervention studies will show the efficacy and
compound would be of great benefit for the affected popula- effectiveness of various control measures.
tions, as the attack rate in these communities is usually very Sand fleas harbor bacteria of the genus Wolbachia in large
high, and people may get infested daily by several female sand numbers [74,75]. These endobacteria are known obligatory
fleas that newly penetrate into the skin. As killing of the symbionts in other parasites, such as filaria, and have been
embedded parasite does not reduce the risk of superinfection, considered as targets for chemotherapy with antibiotics (e.g.,
the use of chemotherapy seems not to be useful in these doxycycline) [76]. The role in the biology of T. penetrans is not
settings. A better approach of individual protection would known; it is possible that Wolbachia of T. penetrans are also
probably be the prevention of infestation by the means of an obligatory symbionts. It is furthermore possible that the endo-
effective repellent that is applied daily on the feet. To reduce bacteria of sand fleas contribute to the severe inflammation
the tungiasis-associated morbidity, an intermittent application constantly found in human tungiasis [75]. Future studies will
during the high transmission period (dry season) would have to show whether antigens released from parasites actually
probably be sufficient. Additionally, the repellent could also be play a role in the intense inflammatory reaction. Wolbachia may
applied on animals such as dogs. However, to control tungiasis also be a target for chemotherapy, if they can be proven to be
at the community level, an integrated approach is necessary to obligatory for reproduction and survival of T. penetrans. There-
reduce all reservoirs (human and animal) and the off-host fore, the presence of Wolbachia in the sand flea offers new and
premature stages [73]. Tungiasis is a disease of the very poor, and exciting perspectives for therapy and control.
improvement of housing and hygiene conditions will be the The disease has been neglected in the past by healthcare
most effective approach not only to control tungiasis, but also providers and policy makers. However, this situation is
other parasitic diseases associated with poverty. changing, and it is expected that in the next few years inter-
vention measures will be implemented to reduce the attack
Expert commentary rate in high-risk communities. These will have to focus on
Treatment of choice of tungiasis consists of the surgical health education, improvement of housing conditions and
extraction of embedded parasites under sterile conditions the prevention of infestation. Natural remedies used
and application of a topical antibiotic. However, this is only traditionally by affected populations may serve as effective
feasible in individuals with few parasites, such as tourists repellents against tungiasis in the near future. The inter-
having visited an endemic area. ventions will not eradicate the disease, but may reduce the
There is a clear need for more trials on the effectiveness of parasite burden from most heavily infested individuals,
possible antiparasitic compounds. As there are currently no thereby preventing severe pathology. With the raising aware-
effective chemotherapeutic approaches at hand, prevention ness of tungiasis as a public health problem, new vulnerable
of newly penetrating fleas is an option to reduce severe groups such as indigenous populations will be identified, and
morbidity. On the individual level this may be reached by epidemiologic studies and control measures performed in
using a repellent. On the community level, control of these populations.
tungiasis is a complex issue and needs an integrated approach Authorities in areas where the environmental and climatic
including clinicians, public health specialists, veterinarians conditions are favorable for the spread of the parasite have to
and biologists, considering also the animal reservoirs. be aware of the risk of introduction of tungiasis into areas
where the parasite has not yet been observed. For example,
Five-year view some years ago, single autochthonous cases of tungiasis have
Many aspects of the parasite and the disease are still not been described from southern Italy [77] and India [78], areas
understood. As awareness of the disease has been rising in the where the disease is currently not endemic. Recently, some
scientific community, it can be assumed that in the next few children coming from a refugee camp in Tanzania to
years knowledge on tungiasis will increase significantly. The Australia were heavily infested with tungiasis, and concerns
epidemiology and morbidity in resource-poor settings and have been raised about the risk of the introduction onto the
factors that contribute to extremely high parasite burden will Australian continent [79]. Tungiasis may also be introduced
be better understood. In the next few years, the life cycle of by returning tourists [28].
the parasite will probably be established in the laboratory, Recently, a new flea species, Tunga trimamillata, which
which will help to understand the biology of the parasite in parasitizes humans, has been described from Ecuador [80,81].
detail, especially the immature off-host stages of the flea, and It is possible that this parasite is prevalent in other areas, and
to identify adulticidal and larvicidal compounds in vitro to the lack of data on epidemiology and pathology of this spe-
be tested in the field. Additionally, the developmental sites cies calls for future studies.

154 Expert Rev. Anti Infect. Ther. 4(1), (2006)

 Treatment and prevention of tungiasis

Key issues

• Tungiasis, caused by the penetration of the female sand flea Tunga penetrans, is a public health problem in many resource-poor
communities in its endemic areas.
• The disease causes considerable morbidity.
• Tungiasis has been neglected by the scientific community.
• Few therapeutic trials have been performed and there are no drugs on the market with proven clinically satisfactory effectiveness.
• The use of a repellent to minimize infestations is probably a better approach than chemotherapy to kill embedded sand fleas.
• Tungiasis is a disease of the very poor and control at the community level can only be achieved by an integrated approach.
• There is a risk of introduction of tungiasis into areas with suitable climatic conditions where the parasite is not yet endemic.
• Studies are needed to increase knowledge on epidemiology, therapy and control of tungiasis and on the off-host developmental
stages of the parasite.

References 9 Feldmeier H, Eisele M, van Marck E, 19 Guerra F. Aleixo de Abreu (1568–1630),

Papers of special note have been highlighted as: Ribeiro RA, Heukelbach J. Investigations on author of the earliest book on tropical
• of interest the biology, epidemiology, pathology and medicine describing amoebiasis, malaria,
•• of considerable interest control of Tunga penetrans in Brazil: IV. typhoid fever, scurvy, yellow fever,
Clinical and histopathology. Parasitol. Res. dracontiasis, trichuriasis and tungiasis in
1 Heukelbach J, de Oliveira FA, Hesse G,
94, 275–282 (2004). 1623. J. Trop. Med. Hyg. 71(3), 55–69
Feldmeier H. Tungiasis: a neglected health
10 Obengui. La tungose et le tétanos au C.H.U. (1968).
problem of poor communities. Trop. Med.
Int. Health 6(4), 267–272 (2001). de Brazzaville. Dakar Med. 34(1–4), 44–48 20 Hesse P. Die Ausbreitung des Sandflohs in
(1989). Afrika. Geogr. Z. 522–530 (1899).
2 Eisele M, Heukelbach J, van Marck E et al.
Investigations on the biology, epidemiology, 11 Tonge BL. Tetanus from chigger flea sores. 21 Henning G. Zur Geschichte des
pathology and control of Tunga penetrans in J. Trop. Pediatr. 35, 94 (1989). Sandflohs (Sarcopsylla penetrans L.) in
Brazil: I. Natural history of tungiasis in man. 12 Litvoc J, Leite RM, Katz G. Aspectos Afrika. Naturwissenschaftliche
Parasitol. Res. 90(2), 87–99 (2003). epidemiológicos do tétano no estado de São Wochenschrift 20, 310–312 (1904).
•• Detailed clinical and microscopic description Paulo (Brasil). Rev. Inst. Med. Trop. São Paulo 22 Blanchard RAE. Présence de la chique
of the natural history of tungiasis. 33(6), 477–484 (1991). (Sarcopsylla penetrans) à Madagascar. Arch.
3 Geigy R, Herbig A. Die Hypertrophie der 13 Greco JB, Sacramento E, Tavares-Neto J. Parasitol. 2, 627–630 (1899).
Organe beim Weibchen von Tunga penetrans. Chronic ulcers and myasis as ports of entry 23 Waterton C. Wanderings in South
Acta Trop. 6(3), 246–262 (1949). for Clostridium tetani. Braz. J. Infect. Dis. America the North-West of the United
4 Witt LH, Linardi PM, Meckes O et al. Blood- 5(6), 319–323 (2001). States and the Antilles, in the years 1812,
feeding of Tunga penetrans males. Med. Vet. 14 Guyon M. Note accompagnant la 1816, 1820 and 1824 with original
Entomol. 18(4), 439–441 (2004). présentation d’un ouvrage intitulé: histoire instruction for the perfect preservation of
naturelle et médicale de la Chique, birds and for cabinets of natural history.
5 Heukelbach J, Wilcke T, Eisele M, Feldmeier
Rhynchoprion penetrans (Oken). Compte Oxford University Press, UK, 108–109
H. Ectopic localization of tungiasis. Am. J.
Rendu de la Academie des Sciences 70, (1973).
Trop. Med. Hyg. 67(2), 214–216 (2002).
785–792 (1870). 24 Cotes EC. The jigger or chigoe pest. Ind.
6 Heukelbach J, Sahebali S, van Marck E,
15 Hoeppli R. Early references to the Med. Gaz. 4, 160–163 (1899).
Sabóia Moura RC, Feldmeier H.
Pseudoepitheliomatous hyperplasia in ectopic occurrence of Tunga penetrans in Tropical 25 Konczaki J. The Emin Pasha Relief
tungiasis: an unusual case. Braz. J. Infect. Dis. Africa. Acta Trop. 20(2), 143–152 (1963). Expedition (1887–1889): some
8(6), 465–468 (2004). • Comprehensive review on the comments on disease and hygiene. Can. J.
introduction of the sand flea into Africa in Afr. Stud. 19(3), 615–625 (1985).
7 Feldmeier H, Eisele M, Saboia-Moura RC,
the 19th century. 26 Grey G. The Kafue river and its
Heukelbach J. Severe tungiasis in
underprivileged communities: case series from 16 Gordon RM. The jigger flea. Lancet 2, headwaters. Geogr. J. 18(1), 62–77
Brazil. Emerg. Infect. Dis. 9(8), 949–955 47–49 (1941). (1901).
(2003). 17 Staden von Homberg zu Hessen H. 27 Bruce CO, Knigin TD, Yolles SF. A
8 Feldmeier H, Heukelbach J, Eisele M, Sousa Wahrhaftige Historia und Beschreibung discussion of the chigoe (Tunga penetrans)
AQ, Barbosa LM, Carvalho CB. Bacterial einer Landschaft der wilden, nacketen, based on experiences in British Guiana.
superinfection in human tungiasis. Trop. Med. grimmigen Menschenfresser Leuten, in der Mil. Surg. 82, 446–452 (1942).
Int. Health 7(7), 559–564 (2002). neuen Welt America gelegen. Frankfurt am 28 Franck S, Feldmeier H, Heukelbach J.
• Study shows that virtually all tungiasis Main: Weigand Hahn (1556). Tungiasis: more than an exotic nuisance.
lesions are superinfected with pathogenic 18 Tosti A. La Tunga ed i cannibali Travel Med. Infect. Dis. 1(3), 159–166
microorganisms in a severely Tupinamba. G. Ital. Dermatol. Venereol. (2003).
affected population. 135, 653–654 (2000). •• Comprehensive review on tungiasis.

www.future-drugs.com 155
Heukelbach

29 González A, de Villalobos C, a resource-poor community in northeast 56 Ade-Serrano MA, Olomolehin OG,

Ranalletta MA, Coscarón MC. Aspectos Brazil. Trans. R. Soc. Trop. Med. Hyg. Adewunmi A. Treatment of human
adaptativos y biológicos de Tunga penetrans doi:10.1016/j.trstmh.2005.06.033 (2005). tungiasis with niridazole (Ambilhar): a
(Linné 1758). Epidemiología en • First adequately designed study on double-blind placebo-controlled trial. Ann.
comunidades aborígenes del norte risk factors on tungiasis and Trop. Med. Parasitol. 76(1), 89–92 (1982).
argentino. Arch. Argent. Dermatol. 54, heavy infestation. 57 Bulay O, Patil K, Wilson R, Shubik P.
119–123 (2004). 42 Heukelbach J, Wilcke T, Harms G, Kidney tumors induced in rats by the
30 Ibanez-Bernal S, Velasco-Castrejon O. Feldmeier H. Seasonal variation of tungiasis antischistosomal drug niridazole. Cancer
New records of human tungiasis in Mexico in an endemic community. Am. J. Trop. Res. 39(12), 4996–5002 (1979).
(Siphonaptera: Tungidae). J. Med. Entomol. Med. Hyg. 72(2), 145–149 (2005). 58 Bulay O, Clayson DB, Shubik P.
33(6), 988–989 (1996). 43 Rietschel W. Beobachtungen zum Sandfloh Carcinogenic effects of niridazole in rats.
31 Chadee DD. Tungiasis among five (Tunga penetrans) bei Mensch und Hund in Cancer Lett. 4(6), 305–310 (1978).
communities in south-western Trinidad, Französisch-Guayana. Tierärztl. Prax. 59 Urman HK, Bulay O, Clayson DB,
West Indies. Ann. Trop. Med. Parasitol. 17(2), 189–193 (1989). Shubik P. Carcinogenic effects of niridazole.
92(1), 107–113 (1998). 44 Franco da Silva LA, Teixeira Borges G, Cancer Lett. 1(2), 69–74 (1975).
32 Gibbs S. Skin disease and socio-economic Santana AP, Coelho Linhares GF, Soares 60 Knasmuller S, Szakmary A. Mutagenic
conditions in rural Africa: Tanzania. Int. J. Fioravanti MC, Romani AF. Alguns effects of niridazole in animal-mediated and
Dermatol. 35(9), 633–639 (1996). aspectos epidemiológicos e profiláticos da in liquid suspension assays using Escherichia
33 Carvalho RW, Almeida AB, tungíase em cães de Jataí, GO. Rev. Patol. coli K-12 as an indicator. Mutat. Res.
Barbosa-Silva SC, Amorim M, Ribeiro PC, Trop. 30(1), 69–73 (2001). 280(2), 93–101 (1992).
Serra-Freire NM. The patterns of tungiasis 45 Cooper JE. An outbreak of Tunga penetrans 61 Heukelbach J, Franck S, Feldmeier H.
in Araruama township, state of Rio de in a pig herd. Vet. Rec. 80(11), 365–366 Therapy of tungiasis: a double-blinded
Janeiro, Brazil. Mem. Inst. Oswaldo Cruz (1967). randomized controlled trial with oral
98(1), 31–36 (2003). 46 Cooper JE. Letter: Tunga penetrans ivermectin. Mem. Inst. Oswaldo Cruz 99(8),
34 Ade-Serrano MA, Ejezie GC. Prevalence of infestation in pigs. Vet. Rec. 98(23), 472 873–876 (2004).
tungiasis in Oto-Ijanikin village, Badagry, (1976). 62 Saraceno EF, Bazarra MLG, Calviello RC,
Lagos State, Nigeria. Ann. Trop. Med. 47 Verhulst A. Tunga penetrans (Sarcopsylla Quaranta MA, Mirarchi P, Sánchez GF.
Parasitol. 75(4), 471–472 (1981). penetrans) as a cause of agalactia in sows in Tungiasis: tratamiento de un caso con
35 Muehlen M, Heukelbach J, Wilcke T, the Republic of Zaire. Vet. Rec. 98(19), 384 ivermectina. Arch. Argent. Dermatol. 49,
Winter B, Mehlhorn H, Feldmeier H. (1976). 91–95 (1999).
Investigations on the biology, epidemiology, 48 Heukelbach J, Costa AM, Wilcke T, 63 Cardoso A. Generalized tungiasis treated
pathology and control of Tunga penetrans in Mencke N, Feldmeier H. The animal with thiabendazole. Arch. Dermatol. 117,
Brazil II. Prevalence, parasite load and reservoir of Tunga penetrans in severely 127 (1981).
topographic distribution of lesions in the affected communities of north-east Brazil. 64 Valença ZO, Cardoso AEC, Cardoso AS.
population of a traditional fishing village. Med. Vet. Entomol. 18(4), 329–335 (2004). Tunguiase generalizada: relato de dois casos
Parasitol. Res. 90, 449–455 (2003).
49 Fimiani M, Reimann R, Alessandrini C, tratados com thiabendazol. Dermatol. Iber.
36 Wilcke T, Heukelbach J, Cesar Saboia MR, Miracco C. Ultrastructural findings in Lat. Am. 3, 375–378 (1972).
Regina SK-P, Feldmeier H. High prevalence tungiasis. Int. J. Dermatol. 29(3), 220–222 65 Cardoso AEC. Tunguíase. An. Bras.
of tungiasis in a poor neighbourhood in (1990). Dermatol. 65(5a), 29S–33S (1990).
Fortaleza, Northeast Brazil. Acta Trop.
50 Douglas-Jones AG, Llewelyn MB, 66 Heukelbach J, Eisele M, Jackson A,
83(3), 255–258 (2002).
Mills CM. Cutaneous infection with Tunga Feldmeier H. Topical treatment of tungiasis:
37 Chadee DD. Distribution patterns of penetrans. Br. J. Dermatol. 133(1), 125–127 a randomized, controlled trial. Ann. Trop.
Tunga penetrans within a community in (1995). Med. Parasitol. 97(7), 743–749 (2003).
Trinidad, West Indies. J. Trop. Med. Hyg.
51 Burke WA, Jones BE, Park HK, Finley JL. 67 Klimpel S, Mehlhorn H, Heukelbach J,
97(3), 167–170 (1994).
Imported tungiasis. Int. J. Dermatol. Feldmeier H, Mencke N. Field trial of the
38 Chadee DD, Furlonge E, Naraynsingh C, 30(12), 881–883 (1991). efficacy of a combination of imidacloprid
Le Maitre A. Distribution and prevalence of
52 Reiss F. Tungiasis in New York City. Arch. and permethrin against Tunga penetrans
Tunga penetrans in coastal south Trinidad,
Dermatol. 93(4), 404–407 (1966). (sand flea, jigger flea) in dogs in Brazil.
West Indies. Trans. R. Soc. Trop. Med. Hyg.
53 Poppiti R Jr, Kambour M, Robinson MJ, Parasitol. Res. 97(Suppl. 1), S113–S119
85(4), 549 (1991).
Rywlin AM. Tunga penetrans in South (2005).
39 Nte AR, Eke FU. Jigger infestation in
Florida. South Med. J. 76(12), 1558–1560 68 Franco da Silva LA, Santana AP, Borges GT,
children in a rural area of Rivers State of
(1983). Coelho Linhares GF, Soares Fioravanti MC,
Nigeria. West Afr. J. Med. 14(1), 56–58
54 Macias PC, Sashida PM. Cutaneous Rabelo RE. Aspectos epidemiológicos e
(1995).
infestation by Tunga penetrans. Int. J. tratamento da tungíase bovina no
40 Ejezie GC. The parasitic diseases of school município de Jataí, Estado de Goiás. Ciência
Dermatol. 39(4), 296–298 (2000).
children in Lagos State, Nigeria. Acta Trop. Animal Brasil. 2(1), 65–67 (2001).
38(1), 79–84 (1981). 55 Smith MD, Procop GW. Typical histologic
features of Tunga penetrans in skin biopsies. 69 Campana CL, Guimaraes NA. Tungiasis:
41 Muehlen M, Feldmeier H, Wilcke T, considerations on a case with intense
Arch. Pathol. Lab Med. 126(6), 714–716
Winter B, Heukelbach J. Identifying risk infestation. Hospital Rio. J. 58, 711–719
(2002).
factors for tungiasis and heavy infestation in (1960).

156 Expert Rev. Anti Infect. Ther. 4(1), (2006)

 Treatment and prevention of tungiasis

70 Vaz Z, Rocha UF. Tunga penetrans • First description of Wolbachia bacteria in 80 Pampiglione S, Trentini M,
(L., 1758), ‘bicho de pé’ em gado bovino. Tunga penetrans. Fioravanti ML, Gustinelli A. Differential
Livro de homenagem a R. F. Almeida 403, 75 Heukelbach J, Bonow I, Witt LH, diagnosis between Tunga penetrans
27–332 (1946). Feldmeier H, Fischer P. High infection (L., 1758) and T. trimamillata the two
71 Schwalfenberg S, Witt LH, Kehr JD, rate of Wolbachia endobacteria in the sand species of the genus Tunga parasitic in
Feldmeier H, Heukelbach J. Prevention of flea Tunga penetrans from Brazil. Acta man. Parasite 11(1), 51–57 (2004).
tungiasis using a biological repellent: a small Trop. 92, 225–230 (2004). 81 Fioravanti ML, Pampiglione S, Trentini M.
case series. Ann. Trop. Med. Parasitol. 98(1), 76 Hoerauf A, Adjei O, Buttner DW. A second species of Tunga (Insecta,
89–94 (2004). Antibiotics for the treatment of Siphonaptera) infecting man: Tunga
72 Soria MF, Capri JJ. Tetanos y ‘piques’. Prensa onchocerciasis and other filarial infections. trimamillata. Parasite 10(3), 282–283
Med. Argent. 40(1), 4–11 (1953). Curr. Opin. Investig. Drugs 3(4), 533–537 (2003).
(2002). • Recent description of a second Tunga spp.
73 Heukelbach J, Mencke N, Feldmeier H.
parasitizing humans.
Cutaneous larva migrans and tungiasis: the 77 Veraldi S, Carrera C, Schianchi R.
challenge to control zoonotic ectoparasitoses Tungiasis has reached Europe.
Affiliation
associated with poverty. Trop. Med. Int. Dermatology 201(4), 382 (2000).
Health 7(11), 907–910 (2002). • Jorg Heukelbach, MD, PhD
78 Sane SY, Satoskar RR. Tungiasis in
Professor of Epidemiology, Federal University of
74 Fischer P, Schmetz C, Bandi C et al. Tunga Maharashtra (a case report). J. Postgrad.
Ceará, Department of Community Health,
penetrans: molecular identification of Med. 31(2), 121–122 (1985).
School of Medicine, Rua Prof. Costa Mendes
Wolbachia endobacteria and their recognition 79 Swaminathan A, Gosbell IB, Zwar NA, 1608, 5° andar, Fortaleza 60430–140, Brazil
by antibodies against proteins of Douglas MW. Tungiasis in recently arrived Tel.: +55 854 009 8045
endobacteria from filarial parasites. Exp. African refugees. Med. J Aust. 183, 51 Fax: +55 854 009 8050
Parasitol. 102(3–4), 201–211 (2002). (2005). [email protected]

www.future-drugs.com 157