Introduction
Tungiasis (sand flea disease) is a parasitic skin disease with origins in South America.
It was introduced into sub-Saharan Africa in the 19th century [1]–[3]. Sand flea disease
is a zoonosis caused by the penetration of female sand fleas into the skin. In humans,
tungiasis predominantly affects marginalized populations. Children and elderly people
are especially susceptible to severe disease. Sand flea disease is the most frequent
parasitic infection in many resource-poor communities. In animals like dogs, pigs,
or ruminants, the infection has severe consequences with, for example, reduced milk
production when the skin of the udder is affected.
Despite the substantial disease burden caused by embedded sand fleas, tungiasis is
basically neglected by health care providers, policy makers, the scientific community,
the pharmaceutical industry, and funding institutions [4]. Although not included in
WHO's list of neglected tropical diseases (NTDs), tungiasis bears all the hallmarks
of an NTD to merit apprehension from the public health sector [5]–[7]. It occurs in
resource-poor communities, causing considerable morbidity and loss of quality of life.
Systematic data on disease occurrence are not available.
Medical History
Reports in colonial documents and travel reports from the early 20th century indicate
that tungiasis caused severe morbidity among indigenous populations such as grave
inflammation in the feet, deep ulcers, gangrene, lymphangitis, and septicaemia [1].
The suffering was so intense that affected individuals cut off their inflamed toes
in sheer desperation. It is also reported that military operations sometimes had to
be stopped because the feet of the indigenous soldiers, who did not wear shoes, were
so sore and mutilated that they could not walk [8], [9]. Decle reported in 1898:
“… I was met by a man who came to show me his foot. The little toe was enormously
swollen and full of matter (pus). I dressed it, and in a few moments a dozen others
had collected, with their feet in an awful condition from the jiggers. Half of them
had removed the parts attacked, cutting themselves to the bone. All these sores were
most dreadful, and all I would do was to dress them.”
Decle also noted that tungiasis perpetuated poverty:
“….In some villages of Uduhu, I found the people starving, as they were so rotten
with ulcers from jiggers that they had been unable to work in their fields, and could
not even go to cut the few bananas that had been growing.”
Mutilation of the feet was so common that it caused a characteristic gait alteration:
“A knowing eye may always perceive when the feet of negros are the abode of the chigoe
[chigoe = jiggers; designation of tungiasis in the Caribbean]. They dare not place
their feet firmly on the ground, on account of the pain such a position would give
them, but they hobble along with their toes turned up. And by this you know that they
are not suffering from tubboes [local designation of yaws], but from the actual depredations
of the chigoes.” [10].
Biology and Transmission of an Intriguing Parasite
Tunga penetrans and Tunga trimamillata belong to the genus Tunga of the order Siphonaptera
and are unique within the realm of fleas in such a way that nonfertilized females
penetrate into the skin and remain there until they die in situ after 4 to 6 weeks
[11], [12]. By its last abdominal segments, which form a kind of cone, the parasite
remains in contact with the environment to breathe, defecate, copulate, and expel
eggs, offering an opening of 250 to 500 µm in the skin as a possible entry point for
pathogenic microorganisms [13].
The off-host part of the sand flea cycle is similar to other Siphonaptera species.
Expelled eggs fall to the ground and develop into larvae, pupae, and adults in the
immediate surroundings. Larvae hatch after 1 to 6 days (mean 3–4 days) and pupation
takes place after another 5–7 days [12]. The formation of adult fleas inside the puparium
needs 9–15 days [12]. Under favorable conditions, an adult sand flea will emerge about
20 days after an egg has “touched down” [14].
Three life cycles of the sand flea coexist in a tropical environment: a human, a domestic
animal, and a sylvatic cycle (Figure 1). These cycles overlap, partially or totally,
depending on the context (Figure 2). In rural South America, e.g., dogs and cats will
be around in and out of the house during the day, whereas small rodents enter during
the night. In Uganda, pigs, sheep, and goats inhabit the house with their owners during
the night to prevent them from being stolen. Local patterns of cohabitation between
humans and animals thus explain why different animal species will act as reservoirs
for tungiasis in different settings [15]–[17].
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Figure 1
Life cycle of T. penetrans in a tropical environment.
The human, domestic, and sylvatic cycles are linked but without close overlap.
10.1371/journal.pntd.0003133.g002
Figure 2
Life cycle of T. penetrans in a tropical environment.
The human, domestic, and sylvatic cycles overlap closely.
In dwellings without a solid floor—common in resource-poor settings in South America
and sub-Saharan Africa—the sand flea's whole life cycle may be completed indoors [14].
T. penetrans is one of the few parasites that can maintain its whole life cycle in
a person's sleeping quarter. Eggs expelled when a person sleeps will fall directly
down to the floor or fall later, when the bed is made. The eggs may then be transferred
to crevices and holes when the floor is swept. The larvae feed on the ever-present
organic material. Eventually, adults emerging from pupae adhere to and penetrate into
the skin, when a person places his or her naked feet on the ground. If people have
to sleep on the floor, sand fleas will also penetrate parts of the body other than
the feet. Ectopic penetration sites are common in the poorest of the poor, in those
who do not even have a bed [18].
Similarly, classrooms in rural Africa with floors containing holes, cracks, and flaked
mortar constitute ideal breeding and transmission places. Children, who often do not
wear closed shoes, put their feet (many hosting a dozen viable sand fleas) on the
ground, exposing their skin for many hours (Hermann Feldmeier, unpublished observation,
2013). The number of feet is high in a classroom, which means many potential carriers
of the parasite and also a substantial amount of organic material on the ground.
The Pathogenesis Explains the Morbidity and the Consequences for Public Health
The inflammatory response around burrowed viable, dead, or decaying sand fleas is
the basis for the clinical and pathological manifestations. Acute inflammation—characterized
by erythema, edema, pain, and itching—is caused by the growth of a biologically active
foreign body within the epidermis, exerting pressure on the surrounding tissue [11].
A bacterial superinfection will increase the inflammatory response. In endemic areas,
this is almost always the case. Aerobic and anaerobic bacteria (Clostridia included)
have been isolated from embedded sand fleas [13]. It is not far-fetched to assume
that bacteria present on the ground may adhere to adult fleas. The bacteria are then
carried into the host's epidermis, eventually reaching the dermis when the parasite
penetrates the basal membrane of the epidermis and inserts its proboscis into dermal
capillaries. Pathogens could, of course, also be actively introduced underneath the
skin through scratching [13].
Another inflammatory pathway seems to be related to the presence of endosymbiotic
Wolbachia bacteria regularly present in burrowed sand fleas [19]. When the parasite
dies in situ, Wolbachia-derived lipopolysaccharides are released in the surrounding
tissue, which will result in an inflammatory response.
In resource-poor settings with a low coverage of tetanus vaccination, circumstantial
evidence even points to a causal relationship between tungiasis and tetanus [20]–[22].
This is not surprising; Clostridium tetani is a soil pathogen. Adult sand fleas may
passively pick up spores of the bacteria and carry them into the human skin. Alternatively,
scratching of the lesion with soil-contaminated fingers may introduce the pathogen
in a lesion.
These various patho-physiological mechanisms may cause suppuration, abscess formation,
ulcers, lymphangitis, tissue necrosis, and gangrene. The result will be chronic pain,
disability, and disfigurement, ending in mutilated feet responsible for the characteristic
gait seen in individuals living in endemic areas [10]. In Brazil, all heavily infected
children were observed to have walking difficulties [23]. Children with tungiasis
are said to have disproportionately high absenteeism from school and to perform worse
in school than unaffected pupils, since constant itching and pain make it difficult
to concentrate [24].
The chronic sequels are debilitating and incapacitating [25]–[27]. Disfigurement and
mutilation of the feet will impair mobility, hinder normal day-to-day activities,
and have a detrimental effect on household economics, which are much dependent on
the physical fitness of the adult household members.
The pathogenesis of the chronic manifestations of tungiasis, such as desquamation,
hyperkeratosis, formation of fissures and ulcers, hypertrophy of nail rims, deformation
of toes, and deformation and loss of nails, is presently not understood.
In an act of desperation, affected individuals often try to get rid of the parasites
by using sharp instruments such as safety pins, needles, scissors, a knife, a thorn,
or a sharply pointed piece of wood. These instruments are usually not disinfected
and are also used by and for several household members and neighbors (Hermann Feldmeier,
unpublished observation, 2013). Since a burrowed sand flea cannot be extracted without
causing hemorrhage, this traditional treatment of tungiasis has to be considered as
a possible way to transmit blood-borne pathogens such as hepatitis B and C virus and,
perhaps, also HIV, from one person to another. Theoretically, the extremely high prevalence
of hepatitis B virus infection in children in many countries in sub-Saharan Africa
could be partially attributed to this treatment of tungiasis [28], [29].
Severely inflamed toes and mutilated feet cannot be hidden. Individuals with sand
flea disease feel ashamed as can be seen in other parasitic skin diseases with abhorrently
inflamed skin [30]. Children with tungiasis are teased and ridiculed in rural Kenya
[24]. In Brazil and Nigeria, patients with tungiasis suffer from social stigmatization
[4].
There Are No Reliable Data on Disease Occurrence
The broad array of symptoms and the social stigma associated with tungiasis do not
make the burden of disease easy to assess. Reliable data on disease occurrence are
available neither at national nor at regional levels. Tungiasis has a heterogeneous
distribution; most commonly and most severely affected are resource-poor strata of
tropical and subtropical populations [23], [28].
It is, however, known that T. penetrans is widespread in South America and sub-Saharan
Africa, and that it occurs on several Caribbean islands [25], [31]–[36]. In South
America, tungiasis is known in all countries with the exception of Chile. In sub-Saharan
Africa, all countries including Madagascar and the Comoro Islands seem to be affected.
As a rule of thumb, tungiasis thrives when living conditions are precarious, such
as in poor villages located near the beach, in rural communities in the hinterland,
in the periphery of small towns, and in slums of big cities [4], [25], [8], [37],
[38].
The incidence follows a distinct seasonal variation with peak transmission in the
dry season [39]. During the high transmission season, the prevalence in resource-poor
rural and urban communities in Brazil, Nigeria, and Madagascar may be up to 60% [4],
[31]–[33], [35], [36], [40]. Prevalence, intensity of infection, and morbidity are
closely related [41]. Reports in printed and electronic lay media indicate that tungiasis
has re-emerged in recent years in East Africa with several hundred thousand cases
in Uganda alone, of which many were associated with intense morbidity [42], [43].
Tungiasis is an important emerging infection in travelers returning from endemic areas
in South America and sub-Saharan Africa [44]. In travelers the morbidity is usually
low [45], [46].
Attack rates vary from setting to setting and may be as high as six newly penetrating
sand fleas per individual per 24 hours. In a slum in Northeast Brazil, all 47 individuals
returning to their households from a non-endemic area became infected within three
weeks [47]. The age-specific prevalence shows a characteristic s-shaped pattern with
a maximum prevalence in children between 5 and 14 years and elderly people [34]. Such
an age-specific prevalence curve may indicate that there is no development of a protective
immunity against penetrating sand fleas.
The question arises, why has sand flea disease re-emerged in such a dramatic way?
The explanation for this most probably lies in the complex interactions between the
parasite and the impoverished segments of various populations. After its introduction
to the African continent, tungiasis had been confined to people in the rural hinterland
[2]. With the construction of roads and an increasing mobility, the parasite could
easily extend its spatial distribution: if an infested individual does not wear closed
shoes and boards a bus or a pick-up taxi, expelled eggs will fall on the floor of
the vehicle and contaminate the soil when the floor of the vehicle is cleaned out
at its destination. Hence, today T. penetrans might easily travel hundreds of kilometers
a day. Since the off-host life cycle can take place wherever the soil is appropriate
and suitable animal hosts occur, the local propagation starts easily [28].
There is a general agreement that the occurrence of tungiasis is linked to poverty
[37], [38]. Poverty is in fact such a constant characteristic of sand flea disease
that the prevalence of tungiasis can be considered as a proxy for the economic development
of a community. Occurrence data of tungiasis are probably a better description of
what is going on in a community than economic averages and public health surveillance
indices [48].
We are convinced that the presence of a dozen or more viable sand fleas in the feet
of a child —a clear proxy of repeated and untreated infections—is a compelling indicator
of inattention to children's needs. A survey in a secondary school in the Busoga subregion,
north of Lake Victoria, Uganda, showed that less than 5% of the mothers regularly
inspected the feet of their children and attempted to remove embedded fleas (Hermann
Feldmeier, unpublished observation, 2013). Regular inspection of the feet and removal
of penetrated sand fleas are, for now, the optimal methods to keep clinical pathology
at bay.
Morbidity Control Is Feasible
Sand flea disease is a zoonosis affecting a broad spectrum of domestic and sylvatic
animals; hence, control can only be achieved by a trans-disciplinary approach (Table
1). The “One Health” concept should be a suitable framework for this, since it means
that improvements of human and animal health are aimed for simultaneously [49]. A
small field trial in Brazil showed that a combination of 10% imidacloprid and 50%
permethrin temporarily reduced the parasite load [50].
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Table 1
Major goals and needs for achievements and control of tungiasis.
Goals
Needs
1. Assess the burden of disease and define regions and population groups that will
most benefit from effective control measures
• Perform systematic prevalence and morbidity studies in all countries in which tungiasis
occurs or is supposed to occur
• Establish geographical distribution of tungiasis in humans and animals in the Americas
and in sub-Saharan Africa
2. Understand the role which animal reservoirs play and describe characteristics of
local transmission dynamics (where, when and why people get infected)
• Determine the animal reservoir in different settings
• Design and implement methods of cooperation between the academic, the public health,
and the veterinary sectors
• Determine the duration of the transmission season(s) according to the climate characteristics
3. Assess the economic and societal impact of tungiasis in impoverished settings
• Establish animal models of tungiasis to evaluate the impact on livestock productivity
• Determine the impact tungiasis in humans and animals has on household economics,
performance in school, and access to local health and administrative infrastructure
• Quantify life quality impairment in patients with tungiasis
4. Eliminate health risks associated with the neglect of acute and chronic tungiasis-associated
morbidity and the treatment with inappropriate instruments
• Identify pathogens transmitted through inappropriate treatment with sharp instruments
• Provide simple, safe, effective, and sustainable means for self-treatment of tungiasis
• Screen locally available plants for repellent activity against sand fleas
• Prevent tungiasis through elimination of breeding sites and animal reservoirs
5. Raise awareness and create intersectional cooperation based on “One Health” principles
• Perform information, education, and communication campaigns—work on eliminating
the stigmatization associated with tungiasis (“It is nothing to be ashamed about!”)
• Create a community-led demand for community-based interventions: let local communities
speak for themselves
• Take advantage of flea control approaches in use for domestic animals
• Identify stakeholders on all levels from global to regional and from national to
local community
Up to now, no drug treatment has been found to be effective against burrowed sand
fleas in humans [51], [52]. Prevention is therefore the only available means to control
morbidity. Closed, solid shoes partially protect against invading sand fleas [53].
Confronted by the reality of resource-poor communities, however, protection by shoes
remains theoretical. Firstly, exposure frequently takes place inside houses, where
shoes usually are not worn. Secondly, shoes are considered as valuable assets and
will often not be used in schools, for walks, or playing around the house. Thirdly,
shoes have a tendency to perish rapidly, and sand fleas can easily reach the skin
through cracks and holes (Figure 3).
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Figure 3
Shoe of an adolescent from rural Kenya after 6 months of use.
A more realistic preventive approach is possible by application of a repellent based
on coconut oil (Zanzarin). Studies in Brazil and Madagascar show that a twice-daily
application of this repellent to the feet could reduce the attack rate by almost 100
percent [41], [53]–[55]. Existing tungiasis-associated morbidity was resolved within
a couple of weeks and mobility was regained. From these studies one could conclude
that acute—and to a lesser extent also chronic—pathology is reversible, if new penetrations
are prevented.
Final Considerations
Tungiasis has an important social dimension and affects human rights. Being a zoonosis
and considering its intricate links with poverty, it requires trans-disciplinary research
in which e.g., public health, social sciences, health education, and animal husbandry
need to interact. Obviously, tungiasis has the potential to trigger political anti-poverty
strategies by simultaneously addressing public health infrastructures in both humans
and animals at the community level.
Based on general characteristics used by WHO to determine which diseases are categorized
among the NTDs, there are compelling reasons for the inclusion of tungiasis in this
group. All countries where tungiasis is reported are low-income and lower middle-income
economies where this plague afflicts the same marginalized population segments and
communities affected by the already-recognized NTDs. The same inequity issues and
complex social determinants as in the field of the NTDs have perpetuated the transmission
of tungiasis in resource-poor communities in South America and sub-Saharan Africa.
The recent evidence of effective intervention measures against tungiasis should no
longer be ignored by global health organizations. WHO, through its regional offices
for the Americas and Africa, should work to raise awareness among NTD stakeholders
and formulate appropriate strategies to address this debilitating and mutilating parasitic
skin disease that has unnecessarily plagued disadvantaged communities for centuries.