Next Article in Journal
Molecular Docking and Molecular Dynamics Simulations in Related to Leishmania donovani: An Update and Literature Review
Next Article in Special Issue
The Effectiveness of Topical Dimethicone Together with a One Health Approach for the Control of Tungiasis in the Sanumás Communities, Yanomami Territory, Amazon Rainforest: A Real-World Study
Previous Article in Journal
Schistosoma Infection Burden and Risk Factors among School-Aged Children in a Rural Area of the Democratic Republic of the Congo
Previous Article in Special Issue
High Level of Knowledge about Tungiasis but Little Translation into Control Practices in Karamoja, Northeastern Uganda
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
TropicalMed
Volume 8
Issue 10
10.3390/tropicalmed8100456
tropicalmed-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Tungiasis: Participation of Cats and Chickens in the Dispersion and Maintenance of the Disease in an Endemic Tourist Area in Brazil

by
Jamille Bispo de Carvalho Teixeira
1,
Katharine Costa dos Santos
1,
Paula Elisa Brandão Guedes
1,
Rebeca Costa Vitor
1,
Thammy Vieira Bitar
2,
Tatiani Vitor Harvey
3,
Anaiá da Paixão Sevá
1 and
Renata Santiago Alberto Carlos
1,*
1
Programa de Pós-Graduação em Ciência Animal—PPGCA, Departamento de Ciências Agrárias e Ambientais (DCAA), Universidade Estadual de Santa Cruz (UESC), Ilhéus 45662-900, Bahia, Brazil
2
Departamento de Ciências Agrárias e Ambientais (DCAA), Curso de Medicina Veterinária, Universidade Estadual de Santa Cruz (UESC), Ilhéus 45662-900, Bahia, Brazil
3
Veterinarian, College Station, TX 77845, USA
*
Author to whom correspondence should be addressed.
Trop. Med. Infect. Dis. 2023, 8(10), 456; https://doi.org/10.3390/tropicalmed8100456
Submission received: 28 June 2023 / Revised: 18 August 2023 / Accepted: 2 September 2023 / Published: 25 September 2023
(This article belongs to the Special Issue New Insights into Tungiasis: Morbidity, Epidemiology, and Control)
Browse Figures
Versions Notes

Abstract

:
Tunga spp. are fleas commonly found in impoverished tropical regions. In Vila Juerana, a tourist community in Ilheus, Bahia, Brazil, where tungiasis is endemic, dogs are the main host of fleas during their life cycle. However, there is no information about the role of cats and chickens in tungiasis in the village. Of the 272 households investigated, 112 had domestic animals, 48 had only dogs, 28 had only cats, and nine had only chickens. Of the 27 households with cohabitation among species, 16 had cats and dogs, eight had chickens and dogs, and three had dogs, cats, and chickens. The injuries due to tungiasis were ranked according to the Fortaleza classification, considering stages I, II, and III as viable lesions. The paws/feet of 71/111 (63.9%) cats and 173/439 (39.4%) chickens were inspected. Dogs that lived with positive cats and chickens also were inspected. Among the 38% (27/7; 95% IC 26.74–49.32) positive cats, 16 cohabited houses with infected dogs but none lived with positive chickens. Of the chickens, 2.3% (4/173; 95% IC 0.07–4.5) had lesions caused by tungiasis. In each household where a cat was infected, the dog was also positive. Two chickens cohabited with an infected dog and the other two did not coexist with other species. Cohabitation with infected dogs and the absence of house confinement restrictions in Vila Juerana make cats important carriers that spread tungiasis in this community. Chickens had a low frequency of tungiasis lesions despite living in proximity to infected dogs and cats.

1. Introduction

Tungiasis is a zoonotic disease that mainly affects socially vulnerable populations in slums, rural and coastal settlements, and fishing and indigenous villages [1,2,3,4,5,6]. Despite the low mortality rate of the disease, the morbidity rate is high, due largely to the negligence of public health authorities in addressing the infection [7,8,9,10,11,12,13,14].
In Brazil, the main species associated with the disease in humans and animals is T. penetrans [15,16]. The gravid female flea initially penetrates the epidermis (usually of the feet or paws) of its host, seeks a blood source in the tissue for its food, and, after fertilization, undergoes body hypertrophy, increasing five to ten-fold in size and reaching up to 1 cm in diameter. The enlarged fleas are called neosomes [10,11,12,13,14]. Subsequently, the fleas begin oviposition for a period of approximately 21 days, after this period they die [15,16]. The lesions that occur after the flea penetrates a host can cause clinical complications such as pain, swelling, and itching, which can progress to tissue necrosis, secondary bacterial infection, sepsis, loss of digits, or tetanus [3,17,18,19]. Infection in humans is associated with the contact of T. penetrans dispersed in the soil with the skin, especially in people living with infected domestic animals such as dogs, pigs, goats, cats, and chickens [10,20,21].
To rank the stage of flea penetration lesions, the Fortaleza classification is used [22], which was created based on observation of the disease in humans and later applied in studies of tungiasis in dogs [6,23].
In sub-Saharan Africa, pigs, dogs, and goats are of great importance in the epidemiological chain of the disease, with pigs being identified as the main hosts and reservoirs of the epidemiological cycle of Tunga spp. [24,25,26,27,28,29]. Among Brazilian studies, dogs were identified as the main hosts of Tunga spp. in various regions of the country [6,30,31]. Studies carried out in the northeast region also observed the presence of Tunga spp. in cats [32,33] and rodents [32]. Cattle [34] and wild animals [35,36] were also reported as suffering from tungiasis in South America.
Depending on the region studied, other animal species may act as reservoirs for Tunga spp., as previously reported. For this reason, it is necessary to elucidate the composition of the epidemiological chain in endemic areas in order to contribute to improvements in mitigation strategies for preventing and controlling human infection. In this type of environment, the infection of different animal species can be one of the main obstacles to controlling human and domestic animal infections.
This article analyzes the co-participation of cats and chickens cohabiting with each other and with other animals as maintainers and dispersers of tungiasis in an endemic tourist community in the municipality of Ilheus, Bahia, Brazil.

2. Materials and Methods

2.1. Ethical Considerations and Study Area

This study was carried out after approval by the Ethics Committee on Animal Use (CEUA) of the State University of Santa Cruz (UESC) under numbers 015/21 and 027/21, and after written consent from the owners of the animals included in this study.
The project was developed in a semi-rural endemic coastal community frequented by tourists (Figure 1), Vila Juerana, located in the district of Aritagua, part of the municipality of Ilheus, Bahia, Brazil (S 14.96767°, W 039.32436°) [37]. The predominant vegetation type is Atlantic Forest, with the presence of beaches and mangrove forests. The climate is classified as humid tropical. This area was previously studied [6,23,37,38] and found to be an endemic zone for tungiasis, with a prevalence of 62.3% (95% CI: 52.7–71.2%) Tunga spp. in dogs, causing large numbers of lesions [23].

2.2. Clinical Study

A census was conducted that included all residences in Vila Juerana, which were visited to check for the presence of cats, chickens, and any other domestic or wild animals cohabiting with each other and with dogs. During a visit, the owner of the residence was questioned about the presence and description of animal species in their residence. After this stage, houses that had cats, chickens, ducks, tortoises, and parakeets were inspected, and if there were also dogs in these houses, they were also inspected. Each animal (cat or chicken) was considered as a sample unit. Cats, chickens, dogs, ducks, tortoises, and parakeets were physically restrained and inspected to identify lesions caused by Tunga penetrans. Animals that did not allow restraint were not inspected. Each visited dwelling included in this study was georeferenced using a Garmin® GPS map device with the UTM system.
Chickens for examination were selected by the owners, who used docility as a criterion, which facilitated manual restraint. Many chickens also had free access to yards and streets, making their capture impossible.
Lesions were counted and staged according to the Fortaleza classification [22] as follows: (a) stage I: penetration of Tunga spp., indicated by a red-brown spot approximately 1 mm in size; (b) stage II: full penetration, denoted by a central brownish or black dot and an expanding mother-of-pearl-like halo of 0.5–2.0 mm with indistinct edges and a zone of perilesional erythema; (c) stage III: hypertrophy of the yellowish-white halo with distinct edges and a central black dot; (d) stage IV: involution phase, characterized by a dark-brownish discoloration or black crust with a deceased parasite, with or without necrosis in the surrounding area; and (e) stage V: residual circular scarring [22]. Animals with active parasites in stages I, II, and III were considered positive. Animals with only stage IV and V inactive lesions were considered negative. The animals were also evaluated for acute clinical signs related to tungiasis lesions, such as hyperemia, pain, suppuration, clustering (three or more nearby lesions), fissure, ulcer, mutilation, lameness, and ectopic lesions.

2.3. Statistical Analysis

The factors associated with infection by T. penetrans were evaluated using a multivariate analysis. The cats were categorized by age range, sex, and coat length. These independent variables were compared with the dependent variable denoting the presence or absence of tungiasis, where stages I to III were considered positive (active lesions) and stages IV and V negative (inactive lesions), according to the Fortaleza classification. The respective data were submitted to multivariate regression analysis using the generalized multivariate model. For the selection of the independent variables, backward approximation was used. The best model was defined as having the lowest value of the Akaike information criterion, and variables were considered significant with a p-value < 0.05. For variables not included in the best model, a univariate analysis was performed. All statistical analyses were carried out with R software (version 3.6.1) using the stats (GLM function) and epiDisplay (logistic.display function) packages.
Cat coat length was determined with visual inspection based on cats of the defined breeds British Shorthair for short hair and British Longhair for long hair, according to the standard of the Fédération Internacionale Féline (FIFe) [39]. Age was categorized based on existing guidelines for standardizing the age range of felines: kitten, animals up to one year; junior, from one year to two years; prime, from three to six years; and mature, seven years or older [40,41]. The number of lesions of stages I to III by age range was also compared. For this, the normality test of the number of lesions was performed. Since the resulting distribution was not normal, the nonparametric Kruskal–Wallis test followed by the Wilcoxon post hoc test with Bonferroni correction for the p-value was performed. The result was considered significant with a p-value < 0.05. All analyses were performed with the R program (version 3.5) using the epiDisplay and rstatix packages. For chickens, a descriptive analysis was used.

3. Results

3.1. House Visits and Geolocation

A total of 272 houses were counted and visited. Of these, 41.6% (113/272) were closed because they were used only for tourism at certain times of the year, known locally as “summer houses”, so there were no animals.
Of the houses that had permanent residents, 29.5% (47/159) had no animals, while 30.1% (48/159) only had dogs, and 40.6% (64/159) had cats and chickens cohabiting with dogs. In 9 of the 64 residences, the cats could not be evaluated since they had feral behavior, with excessive aggression, making rendering and inspection impossible (not even the owners could approach them).
Regarding spatial distribution, the residences with chickens were more frequently located in the central region of the community, but residences with cats were homogeneously distributed in space (Figure 2).
Of the remaining 55 houses that had domestic animals, 34.5% (19/55) had only cats, while in 29.1% (16/55) of these houses, cats and dogs lived together. In 16.3% (9/55) of these residences had only chickens, while 14.5% (8/55) of these residences, chickens cohabited only with dogs. Only 5.5% (3/55) of these residences had dogs, cats, and chickens lived together (Figure 3).
In 7.3% (4/55) of these houses, other types of animals (six ducks, six tortoises, and one parakeet) were found living with cats, dogs, and/or chickens. There were no other animal species in the residences or in the neighborhood.

3.2. Evaluation of Cats in Vila Juerana

In total, 111 cats were counted, and 63.9% (71/111) were inspected. All cats were semi-domiciled and had free access to the street. Of these, 49.8% (35/71) were male and 50.2% (36/71) were female. Due to their feral behavior, as described above, the other 36.1% (40/111) of the cats could not be evaluated.
Of the cats evaluated, 38% (27/71; 95% 26.74–49.32) were positive for tungiasis lesions (stages I, II, and III), while 12.7% (9/71) had lesion stages IV or V and were considered negative, and 49.3% (35/71) had no lesions suggestive of tungiasis. The number of lesions per cat and the total number of lesions are listed in Table 1. The evaluation of neosomes using stereo microscopy revealed that the species affecting cats in Vila Juerana was T. penetrans [34].
Lesions (Table 1 and Figure 4) resulting from all stages of development of T. penetrans were found, totaling 192 lesions. Mutilation was the most observed clinical sign in cats (Table 1 and Figure 5). All lesions in cats were in the periungual region and pads. No ectopic lesions were observed. A total of 77.7% (21/27) cats had more than one stage of injury, while 59.3% (16/27) showed no clinical signs, 40.7% (11/27) had clinical signs, and six had more than one associated clinical sign.
Regarding the acute and chronic clinical signs related to T. penetrans infection, signs of hyperemia, clustering, fissures, ulceration, and mutilation were found (Figure 5 and Figure 6). Other clinical signs such as lameness and suppuration were not observed in the animals.
Among the three variables related to the characteristics of the cats, only age and sex were included in the multivariate analysis, and coat length was included in the univariate analysis. There was only one animal in the mature category, so it was removed from all regression analyses. In these analyses (Table 2), 51.4% (18/35) of males and only 25.7% (9/36) of females had tungiasis, meaning that males were 3.75 times more likely to become infected than females, with a significant difference (p = 0.016; Table 2). Kittens and prime cats had a lower infection prevalence (22.1% and 26.7%, respectively) than juniors (47.6%), but there was no significant difference between these groups (p = 0.055). Similarly, long-haired animals had a higher infection prevalence (42.9%; 3/7) than short-haired animals but without statistical significance (p = 0.806).

3.3. Evaluation of Chickens in Vila Juerana

The houses in Vila Juerana had a total of 439 chickens, of which 173 were inspected. Among these 173 chickens, 2.31% (4/173; 95% IC 0.07–4.5) had lesions caused by Tunga spp. (Figure 7).
None of the chicken coops had bedding. An investigation of the type of floor in the coops indicated the predominance of sandy floors, except in one house, where the chicken coop floor was made of cement (Figure 8). All chickens with T. penetrans were kept in coops with sandy floors.

3.4. The Evaluation of Other Animals

Six ducks, six tortoises, and one parakeet were also inspected. In the residences where ducks were found, they coexisted with dogs and chickens. The tortoises coexisted with cats, dogs, and chickens, and the parakeet lived with dogs and chickens. None of them were infected.

3.5. Assessment of Cohabitation in the Dwellings with Infected Cats and Chickens

Of the 27 positive cats, 66.6% (18/27) cohabited with positive dogs and 33.3% (8/27) did not cohabit with any other positive animal. Of the four positive chickens, 50% (2/4) cohabited with positive dogs and the rest did not cohabit with any other species (Figure 9).

4. Discussion

Several studies have identified the participation of domestic cats in the epidemiological chain of tungiasis in Brazil [16,32,33,42,43,44,45]. In Fortaleza, state of Ceara, also located in the northeast region of the country, high infection rates were found in cats from a shanty town (slum) (49.6%) and from a fishing community (32.4%) [32]. This high prevalence was expected in our study (36.62%) due to similarity in the environmental, structural, and sanitary characteristics of the communities investigated. We also emphasize that in the studies cited above, none of the authors investigated stages of infection and clinical signs in domestic cats, which is essential for understanding the role of these animals in maintaining the endemic profile in communities since they act as egg dispersers.
In this respect, the previous reports of feline tungiasis [23,33] combined with the high prevalence and high number of active lesions found in this study indicate that domestic cats are important reservoirs of the parasite. Mutilation was the most commonly observed clinical sign in the cats from Vila Juerana, which was also observed in the community’s dogs [23]. This finding can be explained by feline hygiene and grooming habits to relieve itching and remove the parasite with repeated licking/biting [46], which can lead to the loss of nails or phalanges.
The prevalence of infection was higher in male cats. The natural behavior of semi-domesticated animals such as hunting [47], associated with searching for females in estrus and territory marking [47,48], leads male cats to travel greater distances and explore a wider variety of habitats, creating a higher probability of exposure to fleas. In turn, this increases the risk of infection and spreading flea eggs inside and outside residences [49].
A relevant factor for the high prevalence of tungiasis in felines in this study is the fact there are many feral cats in the village, which are not accessible for evaluation and treatment. The lack of adequate treatment for tungiasis in cats associated with the large feral population makes these animals important vectors of tungiasis, equal to or even greater than dogs. Even with tungiasis control in dogs, this cat population contributes to the spread of T. penetrans in the environment [50]. We suppose that this same factor may be associated with the lack of seasonality in the disease in the region, considering there is no treatment for cats and that dogs are rarely treated in the community. Thus, the absence of tungiasis control in cats and cohabitation with dogs in residences may be a limiting factor for canine prevention of human tungiasis [6,23,33,38,51].
Chickens have a less relevant role in tungiasis as incidental hosts in Vila Juerana. However, inspection of these animals is recommended since they live in the same environment as pigs, dogs, cats, and humans in endemic areas [44,50]. In a study that inspected chickens in Rio de Janeiro, Brazil, none were found to be infected with tungiasis [30]. Studies in Kenya have associated Tunga spp. infection in humans with the presence of chickens and other domestic animals, mainly dogs [26,52]. In the present study, one of the houses with positive chickens also had positive dogs. There were no dogs in the other residence with infected chickens. However, the sandy soil in the chicken coops and the habit of raising semi-domesticated animals in the village, allows for an interaction between positive dogs and chickens, increasing the risk of transmission and dissemination of T. penetrans between species [53]. Based on our field observation, we believe this low incidence of tungiasis in chickens can be explained by the fact that chickens normally scratch the sandy ground looking for food (foraging behavior) [53], and consequently, may ingest some reproductive forms of parasites directly from the soil. Another important factor is that their feet are made of thick keratin plates [54], which makes it difficult for the flea to penetrate. In some feet, lesions like mutilations by pecking were found, and we believe this possibly indicates the elimination of the neosomes by the animals’ beaks.
Although dogs are considered the main reservoirs of Tunga spp. in Brazil [23], there is a need for further investigation regarding felines and other animal species and their potential epidemiological risks [16,30,32,42] since these species have constant interactions. Additionally, since semi-domesticated or feral cats can cover large geographical areas and promote the dissemination of eggs, it is important to understand how cats contribute to the renewal of the life cycle and maintenance of this zoonosis in endemic areas. Furthermore, the spread of T. penetrans by reservoir animals like cats may be a risk factor for accidental infections of tourists who carry the disease back to their home regions [19,55].
Urgent government actions aimed at educating cat owners regarding management guidelines to control the population of feral cats are necessary for the control of diseases such as tungiasis. Rigorous sanitary control of animals living in the same environment is also necessary to combat the spread of fleas between species.

5. Conclusions

In the region of Vila Juerana, Bahia, Brazil, cats have a high incidence of tungiasis, constituting the second most important host of T. penetrans in the region. With regard to chickens, although they are part of the same environment where infected dogs and cats circulate and spend most of their time on sandy soil, the results of this study suggest they play a less important role in the dissemination of T. penetrans and are thus accidental hosts in the region studied.

Author Contributions

Conceptualization, J.B.d.C.T., K.C.d.S., P.E.B.G., T.V.B., R.C.V., T.V.H. and R.S.A.C.; investigation, J.B.d.C.T., K.C.d.S., P.E.B.G., R.C.V., T.V.B. and R.S.A.C.; writing—preparation of original draft, J.B.d.C.T.; writing—proofreading and editing, J.B.d.C.T., K.C.d.S., P.E.B.G., R.C.V., T.V.B., T.V.H., A.d.P.S., T.V.H. and R.S.A.C.; formal analysis A.d.P.S.; visualization, T.V.H. and R.S.A.C.; supervision R.S.A.C. All authors have read and agreed to the published version of the manuscript.

Funding

This study received financial support from the State University of Santa Cruz (UESC) through granting of scholarships. The authors thank the Bahia State Research Support Foundation (FAPESB) and the Coordination for the Improvement of Higher Education Personnel—Brazil (CAPES)—Financial Code 001 for granting the scholarships. Renata Santiago Alberto Carlos is a PQ2 CNPq researcher.

Institutional Review Board Statement

This work was approved by the Ethics in Animal Use Committee of the State University of Santa Cruz (CEUA-UESC) under numbers 015/21 and 027/21.

Informed Consent Statement

Adherence to project activities was voluntary. The methodology as well as the purpose of this study were explained to the participants in the local language, and time was given for them to answer questions, clarify, and make decisions. All participants were over 18 years old and signed an informed consent form in Portuguese. Anyone could withdraw from the study at any time without further explanation.

Data Availability Statement

All data are available within the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Feldmeier, H.; Kehr, J.D.; Heukelbach, J. A plant-based repellent protects against Tunga penetrans infestation and sand flea disease. Acta. Trop. 2006, 99, 126–136. [Google Scholar] [CrossRef]
  2. Muehlen, M.; Feldmeier, H.; Wilcke, T.; Winter, B.; Heukelbach, J. Identifying risk factors for tungiasis and heavy infestation in a resource-poor community in northeast Brazil. Trans. R. Soc. Trop. Med. Hyg. 2006, 100, 371–380. [Google Scholar] [CrossRef] [PubMed]
  3. Ariza, L.; Seidenschwang, M.; Buckendahl, J.; Gomide, M.; Feldmeier, H.; Heukelbach, J. Tungíase: Doença negligenciada causando patologia grave em uma favela de Fortaleza, Ceará. Rev. Soc. Bras. Med. Trop. 2007, 40, 63–67. [Google Scholar] [CrossRef]
  4. Lefebvre, M.; Capito, C.; Durant, C.; Hervier, B.; Grossi, O. Tungiasis: A poorly documented tropical dermatosis. Médecine Mal. Infect. 2011, 41, 465–468. [Google Scholar] [CrossRef] [PubMed]
  5. Nyangacha, R.M.; Odongo, D.; Oyieke, F.; Bii, C.; Muniu, E.; Chasia, S.; Ochwoto, M. Spatial distribution, prevalence and potential risk factors of Tungiasis in Vihiga County, Kenya. PLoS Negl. Trop. Dis. 2018, 13, e0007244. [Google Scholar] [CrossRef]
  6. Harvey, T.V.; Heukelbach, J.; Assunção, M.S.; Fernandes, T.M.; da Rocha, C.M.B.M.; Carlos, R.S.A. Seasonal variation and persistence of tungiasis infestation in dogs in an endemic community, Bahia State (Brazil): Longitudinal study. Parasitol. Res. 2019, 118, 1711–1718. [Google Scholar] [CrossRef] [PubMed]
  7. Heukelbach, J.; Sales De Oliveira, F.A.; Hesse, G.; Feldmeier, H. Tungiasis: A neglected health problem of poor communities. Trop. Med. Int. Health 2001, 6, 267–272. [Google Scholar] [CrossRef]
  8. Wilcke, T.; Heukelbach, J.; Moura, R.C.S.; Kerr-Pontes, L.R.S.; Feldmeier, H. High prevalence of tungiasis in a poor neighbourhood in Fortaleza, Northeast Brazil. Acta Trop. 2002, 83, 255–258. [Google Scholar] [CrossRef]
  9. Feldmeier, H.; Eisele, M.; Van Marck, E.; Mehlhorn, H.; Ribeiro, R.; Heukelbach, J. Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil: IV. Clinical and histopathology. Parasitol. Res. 2004, 94, 275–282. [Google Scholar] [CrossRef]
  10. Heukelbach, J.; Wilcke, T.; Harms, G.; Feldmeier, H. Seasonal variation of tungiasis in an endemic community. Am. J. Trop. Med. Hyg. 2005, 72, 145–149. [Google Scholar] [CrossRef]
  11. Hotez, P.; Ottesen, E.; Fenwick, A.; Molyneux, D. The neglected tropical diseases: The ancient afflictions of stigma and poverty and the prospects for their control and elimination. In Hot Topics in Infection and Immunity in Children; Pollard, A.J., Finn, A., Eds.; Springer: New York, NY, USA, 2006; pp. 23–33. [Google Scholar]
  12. Feldmeier, H.; Kehr, J.D.; Poggensee, G.; Heukelbach, J. High exposure to Tunga penetrans (Linnaeus, 1758) correlates with intensity of infestation. Mem. Inst. Oswaldo Cruz. 2006, 101, 65–69. [Google Scholar] [CrossRef] [PubMed]
  13. Pampiglione, S.; Fioravanti, M.L.; Gustinelli, A.; Onore, G.; Mantovani, B.; Luchetti, A.; Trentini, M. Sand flea (Tunga spp.) infections in humans and domestic animals: State of the art. Med. Vet. Entomol. 2009, 23, 172–186. [Google Scholar] [CrossRef]
  14. Mutebi, F.; Krücken, J.; Feldmeier, H.; von Samsom-Himmelstjerna, G. Clinical implications and treatment options of tungiasis in domestic animals. Parasitol. Res. 2021, 120, 4113–4123. [Google Scholar] [CrossRef] [PubMed]
  15. Feldmeier, H.; Eisele, M.; Sabóia-Moura, R.C.; Heukelbach, J. Severe tungiasis in underprivileged communities: Case series from Brazil. Emerg. Infect. Dis. 2003, 9, 949–955. [Google Scholar] [CrossRef]
  16. Bonfim, W.M.; Cardoso, M.D.; Cardoso, V.A.; Andreazze, R. Tungíase em uma área de aglomerado subnormal de Natal-RN: Prevalência e fatores associados. Epidemiol. Serviços Saúde 2010, 19, 379–388. [Google Scholar] [CrossRef]
  17. Fabián, M.B. Tungiosis y Tunga penetrans. Rev. Peru. Med. Exp. Salud Publica 2005, 22, 323–324. [Google Scholar]
  18. Feldmeier, H.; Heukelbach, J.; Ugbomoiko, U.S.; Sentongo, E.; Mbabazi, P.; von Samson-Himmelstjerna, G.; Krantz, I. Tungiasis—A Neglected Disease with Many Challenges for Global Public Health. PLoS Negl. Trop. Dis. 2014, 8, e3133. [Google Scholar] [CrossRef]
  19. Palicelli, A.; Boldorini, R.; Campisi, P.; Disanto, M.G.; Gatti, L.; Portigliotti, L.; Tosoni, A.; Rivasi, F. Tungiasis in Italy: An imported case of Tunga penetrans and review of the literature. Pathol. Res. Pract. 2016, 212, 475–483. [Google Scholar] [CrossRef]
  20. Mutebi, F.; Krücken, J.; von Samson-Himmelstjerna, G.; Waiswa, C.; Mencke, N.; Eneku, W.; Andrew, T.; Feldmeier, H. Animal and human tungiasis-related knowledge and treatment practices among animal keeping households in Bugiri District, South-Eastern Uganda. Acta Trop. 2018, 177, 81–88. [Google Scholar] [CrossRef] [PubMed]
  21. Elson, L.; Wright, K.; Swift, J.; Feldmeier, H. Control of tungiasis in absence of a roadmap: Grassroots and global approaches. Trop. Med. Infect. Dis. 2017, 2, 33. [Google Scholar] [CrossRef]
  22. Eisele, M.; Heukelbach, J.; Van Marck, E.; Mehlhorn, H.; Meckes, O.; Franck, S.; Feldmeier, H. Investigations on the biology, epidemiology, pathology and control of Tunga penetrans in Brazil: I. Natural history of tungiasis in man. Parasitol. Res. 2003, 90, 87–99. [Google Scholar] [CrossRef]
  23. Harvey, T.V.; dos Santos Freire, Z.; dos Santos, K.C.; de Jesus, A.V.; Guedes, P.E.B.; da Paixão Sevá, A.; de Almeida Borges, F.; Carlos, R.S.A. Clinical and macroscopic morphological features of canine tungiasis. Parasitol. Res. 2021, 120, 807–818. [Google Scholar] [CrossRef]
  24. Ugbomoiko, U.S.; Ofoezie, I.E.; Heukelbach, J. Tungiasis in Lagos State, Nigeria ropical medicine rounds Ugbomoiko, Ofoezie, and Heukelbach Tungiasis: High prevalence parasite load, and morbidity in a rural community in Lagos State, Nigeria. Int. J. Dermatol. 2007, 46, 475–481. [Google Scholar] [CrossRef] [PubMed]
  25. Mwangi, J.N.; Ozwara, H.S.; Motiso, J.M.; Gicheru, M.M. Characterization of Tunga penetrans Antigens in Selected Epidemic Areas in Murang’a County in Kenya. PLoS Negl. Trop. Dis. 2015, 9, 1–6. [Google Scholar] [CrossRef] [PubMed]
  26. Mwangi, J.N.; Ozwara, H.S.; Gicheru, M.M. Epidemiology of Tunga penetrans infestation in selected areas in Kiharu constituency, Murang’a County, Kenya. Trop. Dis. Travel Med. Vaccines 2015, 1, 13. [Google Scholar] [CrossRef]
  27. Mutebi, F.; Krücken, J.; Feldmeier, H.; Waiswa, C.; Mencke, N.; Von Samson-Himmelstjerna, G. Tungiasis-associated morbidity in pigs and dogs in endemic villages of Uganda. Parasites Vectors 2016, 9, 1–9. [Google Scholar] [CrossRef]
  28. Mutebi, F.; Krücken, J.; Feldmeier, H.; Waiswa, C.; Mencke, N.; Eneku, W.; von Samson-Himmelstjerna, G. High intensity of Tunga penetrans infection causing severe disease among pigs in Busoga, South Eastern Uganda. BMC Vet. Res. 2017, 13, 206. [Google Scholar] [CrossRef]
  29. Deka, M.A. Mapping the geographic distribution of tungiasis in sub-Saharan Africa. Trop. Med. Infect. Dis. 2020, 5, 122. [Google Scholar] [CrossRef]
  30. De Carvalho, R.W.; De Almeida, A.B.; Barbosa-Silva, S.C.; Amorim, M.; Ribeiro, P.C.; Serra-Freire, N.M. The Patterns of Tungiasis in Araruama Township, State of Rio de Janeiro, Brazil. Mem. Inst. Oswaldo Cruz 2003, 98, 31–36. [Google Scholar] [CrossRef]
  31. Linardi, P.M.; Calheiros, C.M.L.; Campelo-Junior, E.B.; Duarte, E.M.; Heukelbach, J.; Feldmeier, H. Occurrence of the off-host life stages of Tunga penetrans (Siphonaptera) in various environments in Brazil. Ann. Trop. Med. Parasitol. 2010, 104, 337–345. [Google Scholar] [CrossRef] [PubMed]
  32. Heukelbach, J.; Costa, A.M.L.; Wilcke, T.; Mencke, N.; Feldmeier, H. The animal reservoir of Tunga penetrans in severely affected communities of north-east Brazil. Med. Vet. Entomol. 2004, 18, 329–335. [Google Scholar] [CrossRef]
  33. Harvey, T.V.; Linardi, P.M.; Carlos, R.S.A.; Heukelbach, J. Tungiasis in domestic, wild, and synanthropic animals in Brazil. Acta Trop. 2021, 222, 106068. [Google Scholar] [CrossRef]
  34. Linardi, P.M.; De Avelar, D.M.; Facury Filho, E.J. Establishment of Tunga trimamillata (Siphonaptera: Tungidae) in Brazil. Parasitol. Res. 2013, 112, 3239–3242. [Google Scholar] [CrossRef]
  35. Di Nucci, D.L.; Ezquiaga, M.C.; Abba, A.M. Tunga penetrans in Giant anteater (Myrmecophaga tridactyla) from Argentina. Vet. Parasitol. Reg. Stud. Rep. 2017, 10, 82–84. [Google Scholar] [CrossRef]
  36. Schott, D.; Ribeiro, P.R.; Souza, V.K.; Surita, L.E.; Amorim, D.B.; Bianchi, M.V.; Anicet, M.Z.; Alievi, M.M.; Pavarini, S.P.; Carvalho, R.W.; et al. Clinical and pathological aspects of first report of Tunga penetrans infestation on southern brown howler monkey (Alouatta guariba clamitans) in Rio Grande do Sul, Brazil. J. Med. Primatol. 2020, 49, 315–321. [Google Scholar] [CrossRef]
  37. Harvey, T.V.; Campos Júnior, D.A.; Cardoso, T.P. Estudo descritivo da população rural canina da Vila Juerana, Distrito de Aritaguá, Município de Ilhéus -Ba. Pubvet 2013, 224, 0001–0108. [Google Scholar]
  38. Harvey, T.V.; Heukelbach, J.; Assunção, M.S.; Fernandes, T.M.; da Rocha, C.M.B.M.; Carlos, R.S.A. Canine tungiasis: High prevalence in a tourist region in Bahia state, Brazil. Prev. Vet. Med. 2017, 139, 76–81. [Google Scholar] [CrossRef]
  39. Fédération Internationale Féline. Available online: http://www1.fifeweb.org/dnld/std/BLH-BSH.pdf (accessed on 10 August 2023).
  40. Öhlund, M.; Palmgren, M.; Holst, B.S. Overweight in adult cats: A cross-sectional study. Acta Vet. Scand. 2018, 60, 1–10. [Google Scholar] [CrossRef]
  41. Quimby, J.; Gowland, S.; Carney, H.C.; dePorter, T.; Plummer, P.; Westropp, J. 2021 AAHA/AAFP Feline Life Stage Guidelines. JFMS Clin. Pract. 2021, 23, 211–233. [Google Scholar]
  42. Pilger, D.; Schwalfenberg, S.; Heukelbach, J.; Witt, L.; Mehlhorn, H.; Mencke, N.; Khakban, A.; Feldmeier, H. Investigations on the biology, epidemiology, pathology, and control of Tunga penetrans in Brazil: VII. The importance of animal reservoirs for human infestation. Parasitol. Res. 2008, 102, 875–880. [Google Scholar] [CrossRef]
  43. Pilger, D.; Schwalfenberg, S.; Heukelbach, J.; Witt, L.; Mencke, N.; Khakban, A.; Feldmeier, H. Controlling tungiasis in an impoverished community: An intervention study. PLOS Negl. Trop. Dis. 2008, 2, e324. [Google Scholar] [CrossRef]
  44. Mutebi, F.; Krücken, J.; Feldmeier, H.; Waiswa, C.; Mencke, N.; Sentongo, E.; von Samson-Himmelstjerna, G. Animal Reservoirs of Zoonotic Tungiasis in Endemic Rural Villages of Uganda. PLoS Negl. Trop. Dis. 2015, 9, e0004126. [Google Scholar] [CrossRef]
  45. Wiese, S.; Elson, L.; Reichert, F.; Mambo, B.; Feldmeier, H. Prevalence, intensity and risk factors of tungiasis in Kilifi County, Kenya: I. Results from a community-based study. PLoS Negl. Trop. Dis. 2017, 11, e0005925. [Google Scholar] [CrossRef]
  46. Stelow, E. Behavior as an Ilness Indicator. Vet. Clin. Small Anim. 2020, 50, 695–706. [Google Scholar] [CrossRef] [PubMed]
  47. Escobar-Aguirre, S.; Alegría-Morán, R.A.; Calderon-Amor, J.; Tadich, T.A. Can Responsible Ownership Practices Influence Hunting Behavior of Owned Cats?: Results from a Survey of Cat Owners in Chile. Animals 2019, 9, 745. [Google Scholar] [CrossRef] [PubMed]
  48. Horwitz, D.F. Common feline problem behaviors- Urine Spraying. J. Feline Med. Surg. 2019, 21, 209–219. [Google Scholar] [CrossRef] [PubMed]
  49. Barrat, D.G. Home Range Size, Habitat Utilization and Movement Patterns of Suburban and Farm Cats Felis catus. Ecography 1997, 20, 271–280. [Google Scholar] [CrossRef]
  50. Mutebi, F.; McNeilly, H.; Thielecke, M.; Reichert, F.; Wiese, S.; Mukone, G.; Feldmeier, H. Prevalence and Infection Intensity of Human and Animal Tungiasis in Napak District, Karamoja, Northeastern Uganda. Trop. Med. Infect. Dis. 2023, 8, 111. [Google Scholar] [CrossRef] [PubMed]
  51. de Jesus, A.V.; Sevá, A.d.P.; Guedes, P.E.B.; dos Santos, K.C.; Harvey, T.V.; de Oliveira, G.M.S.; Bitar, T.V.; Ferreira, F.; Albuquerque, G.R.; Carlos, R.S.A. Spatial Distribution of Off-Host Stages of Tunga penetrans in the Soil within the Home Range of Nine Infected Dogs in An Endemic Tourist Area Brazil. Trop. Med. Infect. Dis. 2023, 8, 98. [Google Scholar] [CrossRef]
  52. Gitau, A.K.; Oyieke, F.A.; Mukabana, W.R. Assessment of the role played by domestic animals in jigger infection in Kandara sub-country, Kenya (case control study). PAMJ 2020, 39, 1–13. [Google Scholar]
  53. Zimmerman, P.H.; Buijs, S.A.F.; Bolhuis, J.E.; Keeling, L.J. Behaviour of domestic fowl in anticipation of positive and negative stimuli. Anim. Behav. 2011, 81, 569–577. [Google Scholar] [CrossRef]
  54. O’Malley, B. Avian anatomy and pshysiology. In Clinical Anatomy and Physiology of Exotic Species: Structure and Function of Mammals, Birds, Reptiles and Amphibians; Saunders, W.B., Ed.; Elsevier: Amsterdam, The Netherland, 2005; pp. 97–161. [Google Scholar]
  55. Santos, R.P.; Resende, R.; Duarte, d.L.; Brito, C. Tungiasis: A poorly-known diagnosis in Europe. Two paradigmatic cases from Portugal. Acta Dermatovenerol. APA 2017, 4, 115–117. [Google Scholar] [CrossRef] [PubMed]
Tropicalmed 08 00456 g001
Figure 1. Geolocation of Vila Juerana, Municipality of Ilheus, Bahia, Brazil.
Figure 1. Geolocation of Vila Juerana, Municipality of Ilheus, Bahia, Brazil.
Tropicalmed 08 00456 g001
Tropicalmed 08 00456 g002
Figure 2. Residences with evaluated cats, dogs, and chickens.
Figure 2. Residences with evaluated cats, dogs, and chickens.
Tropicalmed 08 00456 g002
Tropicalmed 08 00456 g003
Figure 3. Venn diagram showing the number of houses that had different combinations of cats, dogs, and chickens.
Figure 3. Venn diagram showing the number of houses that had different combinations of cats, dogs, and chickens.
Tropicalmed 08 00456 g003
Tropicalmed 08 00456 g004
Figure 4. (A) Cat paws with a stage I lesion (pink arrow), which is the exact moment when the Tunga penetrans female penetrates its host. (B) Cat paw with stage II lesions (red arrows) and a stage V lesion (yellow arrow). (C) Cat paw with a stage III lesion (black arrow) and stage IV (blue arrow) lesion according to the Fortaleza Classification [22].
Figure 4. (A) Cat paws with a stage I lesion (pink arrow), which is the exact moment when the Tunga penetrans female penetrates its host. (B) Cat paw with stage II lesions (red arrows) and a stage V lesion (yellow arrow). (C) Cat paw with a stage III lesion (black arrow) and stage IV (blue arrow) lesion according to the Fortaleza Classification [22].
Tropicalmed 08 00456 g004
Tropicalmed 08 00456 g005
Figure 5. Clinical signs related to Tunga penetrans infection in cat paws from Vila Juerana. (A) Hyperemia (black arrow); (B,C) ulcerations (red circle and blue arrow, respectively); and (D) fissures (yellow arrows).
Figure 5. Clinical signs related to Tunga penetrans infection in cat paws from Vila Juerana. (A) Hyperemia (black arrow); (B,C) ulcerations (red circle and blue arrow, respectively); and (D) fissures (yellow arrows).
Tropicalmed 08 00456 g005
Tropicalmed 08 00456 g006
Figure 6. (A) Cat with stage III lesions on paws (red arrow) and mutilation (tweezers). (B) Stage III lesion approximately 0.5 cm in diameter (black arrow), and the presence of a fissure resulting from the lesion (yellow arrow) [22].
Figure 6. (A) Cat with stage III lesions on paws (red arrow) and mutilation (tweezers). (B) Stage III lesion approximately 0.5 cm in diameter (black arrow), and the presence of a fissure resulting from the lesion (yellow arrow) [22].
Tropicalmed 08 00456 g006
Tropicalmed 08 00456 g007
Figure 7. Feet of chickens infected with T. penetrans. (A,B) Stage II lesions (tweezers). (C) Stage IV lesion (red arrow).
Figure 7. Feet of chickens infected with T. penetrans. (A,B) Stage II lesions (tweezers). (C) Stage IV lesion (red arrow).
Tropicalmed 08 00456 g007
Tropicalmed 08 00456 g008
Figure 8. Chicken coops in Vila Juerana, Ilheus Bahia, Brazil. In one chicken coop, the floor was made of cement (A), while the other chicken coops had sandy floors (B–D).
Figure 8. Chicken coops in Vila Juerana, Ilheus Bahia, Brazil. In one chicken coop, the floor was made of cement (A), while the other chicken coops had sandy floors (B–D).
Tropicalmed 08 00456 g008
Tropicalmed 08 00456 g009
Figure 9. Venn diagram showing the number of positive cats and chickens that cohabited with positive dogs.
Figure 9. Venn diagram showing the number of positive cats and chickens that cohabited with positive dogs.
Tropicalmed 08 00456 g009
Table 1. Staging (Fortaleza Classification) [22] and quantification of lesions associated with clinical signs in infected cats (n = 27) from Vila Juerana, Ilhéus, Bahia, Brazil.
Table 1. Staging (Fortaleza Classification) [22] and quantification of lesions associated with clinical signs in infected cats (n = 27) from Vila Juerana, Ilhéus, Bahia, Brazil.
CategoryInfected Animals
(n)		Total of Lesions
Lesion stagesI22
II2062
III2256
IV1431
V1722
Total 27 *173
Clinical signs **Mutilation67
Cluster55
Hyperemia44
Ulceration22
Fissure22
Total number of infected2720
Overall * 21 cats presented more than one lesion stage; ** 16 cats had no clinical signs; 11 cats had clinical signs; and 6 had more than one associated clinical sign.
Table 2. Number and percentage of positive and negative cats for each variable and their respective results of the univariate and multivariate regression analyses.
Table 2. Number and percentage of positive and negative cats for each variable and their respective results of the univariate and multivariate regression analyses.
Positiven%Negativen%TotalOR 95% IC p-ValueAnalyses
AgeKitten323.11070.9130.56 (0.08, 3.39)
Ref
0.41 (0.09, 1.49)		0.055
0.192		Multivariate
Junior2047.62252.442
Prime426.71173.315
SexFemale925.72674.335Ref
3.75 (1.32, 11.51)		0.016 *Multivariate
Male1851.41748.635
Coat lengthShort2437.153962.963Ref
1.22 (0.22, 5.99)		0.806Univariate
Long342.9457.17
* Significant p (p < 0.05); OR: odds ratio; n: number of animals in the category.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Teixeira, J.B.d.C.; dos Santos, K.C.; Guedes, P.E.B.; Vitor, R.C.; Bitar, T.V.; Harvey, T.V.; Sevá, A.d.P.; Carlos, R.S.A. Tungiasis: Participation of Cats and Chickens in the Dispersion and Maintenance of the Disease in an Endemic Tourist Area in Brazil. Trop. Med. Infect. Dis. 2023, 8, 456. https://doi.org/10.3390/tropicalmed8100456

AMA Style

Teixeira JBdC, dos Santos KC, Guedes PEB, Vitor RC, Bitar TV, Harvey TV, Sevá AdP, Carlos RSA. Tungiasis: Participation of Cats and Chickens in the Dispersion and Maintenance of the Disease in an Endemic Tourist Area in Brazil. Tropical Medicine and Infectious Disease. 2023; 8(10):456. https://doi.org/10.3390/tropicalmed8100456

Chicago/Turabian Style

Teixeira, Jamille Bispo de Carvalho, Katharine Costa dos Santos, Paula Elisa Brandão Guedes, Rebeca Costa Vitor, Thammy Vieira Bitar, Tatiani Vitor Harvey, Anaiá da Paixão Sevá, and Renata Santiago Alberto Carlos. 2023. "Tungiasis: Participation of Cats and Chickens in the Dispersion and Maintenance of the Disease in an Endemic Tourist Area in Brazil" Tropical Medicine and Infectious Disease 8, no. 10: 456. https://doi.org/10.3390/tropicalmed8100456

Article Metrics

Back to TopTop