Tel.: 0039-51-792002or792063;Fax:0039-51-792039 Animale, UniversitàdiBologna,ViaTolara diSopra,40064OzzanoEmilia,Italia * Correspondingauthor:Dipartimentodi SanitàPubblicaVeterinariaePatologia 5. DepartmentofMorphologicalSciences, UniversityofModena,Italy of SãoToméandPríncipe 4. DirectionofVeterinaryServices,Ministry ofAgriculture,DemocraticRepublic 3. VeterinaryPractitioner,Padua,Italy 2. DepartmentofBiology,UniversityBologna,Italy 1. DepartmentofVeterinaryPublicHealth,UniversityBologna,Italy peculiar tothisgenus,whichhasbeenstudiedindetailsincethe hematophagous ectoparasites,pregnantfemales,byamechanism Whereas malesandnon-fertilizedfemalesbehave as regions ofAsia(11). from whichitspreadtoalmostallofAfrica,Madagascarandsome in manyregionsofLatinAmericawhereitoriginatedfrom,and various domesticandwildwarm-bloodedvertebrates.Itispresent flea, chigoeorchiggerisaninsectparasitizingmanand Tunga penetrans INTRODUCTION Tomé andPríncipe. conformation -EpidemiologySão Symptoms -HistopathologyBody Mankind -Swine Key words (Insecta: Siphonaptera),commonlycalledsand- Tunga penetrans - morphology oftheparasitearepresented. records oftheclinicalandhistologicalaspectslesions Tomé, aswasobservedinmanyvillagesofLatinAmerica.Photographic the parasite.ItcanbeassumedthatswineactasareservoirofchigoesinSão posing arealpublichealthproblem.Oneoftheauthors,too,wasaffectedby death ofwholelitters.Humancaseswerefrequentlyreportedontheisland economic damageduetoinabilitynursethesucking-pigs,resultingin the latterpresenceoffleasinsidetissuesteatscausedheavy (Insecta: Siphonaptera)localizedparticularlyinthelegs,snoutandudders.In of 100examinedwereaffectedbylesionsassociatedwith at thepublicslaughterhouseofcapitalhasascertainedthat28subjectsout Tomé andPríncipe.Asurveycarriedoutbytheauthorsonswineslaughtered Guinea, isnowadayspartofanindependentrepublic,theRepublicSão The islandofSãoTomé,aformerPortuguesecolony,locatedintheGulf Summary and histopathologicalaspects morphological Epidemiological, clinical, in SãoTomé (EquatorialAfrica): (Insecta: Siphonaptera)inpigs Tunga penetrans J.L.X. Mendes S. Pampiglione Retour aumenu

4 1* porco countries, e.g.Brazil,theparasite iscommonlycalled zoonosis withitsreservoirin swine(2,7,16,17)(insome 19) althoughithasbeenascertained thatthisdiseaseisatrue damage associatedwiththeparasite arehoweverscanty(1,4,6, Publications intheveterinarysectorandreportsonzootechnical non-endemic regionsinpersonscomingbackfromsuchareas. contracted inendemicareasautochthonouspopulationsor in The internationalliteraturefrequentlyreportshumancases completing thecycle. 10 to18days(10)ormore(9)andeventuallyintoadults,thus feeding ondecayingorganicmatterandtransformintopupaeafter released andfalltotheground,wherelarvalstageswilldevelop by (3). Oncemature,theeggs,morethan200perfemale(9,12),are represent aportalofentryforotherinfectionsincludingtetanus lesions, althoughofbenignnatureifproperlytreated,may inflammatory andulcerativeprocesses.Asarule,theparasite in abouttwoweeksandprovokemoreorlessinvalidating and thedevelopmentofeggs(12),enlargeuptosizeapea following thedilationofintestineandMalpighiantubules(9) last century(2,13,14,20),penetratethedepthofskinwhere, C. Pampiglione M. Trentini ) or,morerarely,inthedog(18). 2 F. MatteiGentili 2 F. Rivasi Tunga penetrans 5 3 201

Revue Élev.bicho de Méd. vét. Pays trop., 1998, 51 (3) : 201-205 PATHOLOGIE PARASITAIRE Retour au menu

Tunga penetrans in pigs in S?io Tomé

Having hadthe opportunityto seeseveral cases of the conditionin swine on the island of Sao Tomé and to collect substantial parasitologicalmaterial, the authorsthought it wasuseful to report the presenceof the parasitein a geographicarea not yet indicated as endemic and to illustrate its clinical, morphologicaland histopathologicalaspects. The Island of SaoTomé, alongwith the Island of Principeand a few other smallislands, is part of a little volcanic archipelagoin the Gulf of Guinea,west of the African toast (betweenl”44’ Lat. N and O”22’ Lat. S and between7”28’ and 6”28’ Long. E). It has beenan independentstate, the DemocraticRepublic of SaoTomé, since1975. It has a surfaceof 844 km2. The landscapeis exceedinglyvaried dependingon the diversity of its profile, with a mountainin its occidental half, 2024 m high and covered with luxuriant vegetationof equatorialtype, which leansabruptly to the seawhile in the eastempart the land slopesdown and becomesa plain with Figure 1: Pigs kept free to circulate among the houses in Si70 aspectsranging from Savannahto semi-aridareas. The climateof Tomé. the northern coastalstrip is characterizedby two seasons,wet from Septemberto May anddry from Juneto August. The restof the territory hasan equatorialclimate with rainfall throughoutthe The animals were first examined clinically, as a naked-eye year sometimesaveraging 7000 mmiyear. Relative humidity diagnosisis easy,due to the obviouslesions which, if present,are varies accordingto the different zonesfrom a minimumof 65.3% typical of the disease.Biopsy sampleswere takenboth to confirm to saturation. Average yearly temperature is 25.7”C with clinical diagnosisand to study the histopathologyof the lesions differencesof 3°C betweenthe hottest and coldestmonths (data and the parasite’smorphology in moredetail. This materialwas collectedat the Ministry of Agriculture of SaoTomé). fixed in buffered 10% formalin and histologicalsections were stainedwith hematoxilin-eosin,PAS and Trichromie Masson The populationnumbers 96,611 inhabitants (census of 1981)with Goldner. a meandensity of 97 inhabitants/km2,mainly farmers.The most widespreadculture is cacao(practically a monoculture),although coffee,coconut palms, pineapples, etc. are grown in smallplots of land. The populationlives in urban settlementsor in farms and n RESU LTS sparsesmall rural centers.Sanitary conditionsare very poor, due to the shortageof toilets and the strong fecal pollution of the environment(15), which consequentlyaffect the population’s Clinical and epidemiological findings health. Out of 100 pigs examined,28 (10 malesand 18 females)showed The livestockpopulation (1992) consistsof 500 cattle, 400 swine, typical lesionsof Tunga penetrans, always severalin number, 28,000 goats, 100 sheepand 12 horses.As to swine, a serious sometimesarranged in a carpet-likefashion, consisting of tens or outbreakof African swinefever occurredin 1986on the occasion hundredsof small protuberancesand crater-shapedulcerations of a project for the introduction of Large White pigs into the giving the skin surfacea pitted, warty or honeycomb-likeaspect. island.A stamping-outprogram was implementedwhich actually The mostaffected age class (60% of positivecases) was under one year old. No significant differenceswere seenbetween sexes affected only freshly-introducedpigs in state farms, whereas except for localization,which wasmore frequent in the uddersof small,family-run farmswere not involved at a11as the ownerslet females.The lesionswere sometimespresent in the snout(85.7%) their animalsrun to the forest in order not to have them killed. (figure 2) and teats (46.4%) (figure 3), the latter sometimes This seemsnot to have had a negativeimpact since no new cases showing necrotic processes with partial mutilation and of the diseasewere reported in subsequentyears and, after contemporarymammary obstruction and mastitis,but in a11cases recovering the pigs from the forest, the swine population was they were presentin the legs (figure 4). The occasionalpresence restoredfairly rapidly. Pigsin family farms are rearedfree range of T. penetrans was alsoobserved in the legsof a goat andin the and allowedto move aroundthe houses(figure 1) and sometimes foot-padof a cat aswell as in the solesand toes of somefarmers in the brushwoodSO that they cari feed on wasteand cooking andof one of the authorsof this paper. refuse or on edible vegetablesfound in the island’s forest environment. Morphological and histopathological aspects Cross-sectionsof the parasites(figure 5) showedthe external n MATERIALS AND METHODS cuticle with the hypodermadelimiting the enlargedabdomen, the anteriorend, muchsmaller than the restof the body, consistingof The pigs examined (100 head consistingof 66 males and 34 the headand thorax, and sometimesthe posteriorend with the last femalesaged 6 to 18 months)a11 came from smallherds of the abdominalsegments. Some sectionsof the head showed the family type sitedin the districtsof Agua Grande,Lobata, Mesoxi pigmentedeyes and a portion of the biting-suckling buccal and Lemba. They were a11crossbred and had been taken to the apparatusimmersed in the derma(figure 6). In the thoracic area public abattoir for slaughterfrom Januaryto March 1992.These sectionsof the legs were seen.Within the abdominalcuticle, in a were a11the pigs slaughteredduring this period under veterinary moreor lessenlarged body accordingto the stageof development, control. onecould observesome bundles of striated,hypertrophie muscular Retour au menu

Tunga penetrans à Sao Tomé chez le porc fibers (figure 7), which started from the thorax and penetrated the parasite in Africa (ll), that the condition has been present and abdomen joining the cuticle peripherally. Sections of the digestive probably spread in the island since the beginning of this century. tract were also seen containing amorphous material and At present, tungiasis is a serious public health problem in Sao granulocytes, as well as numerous small tracheae and sexual Tomé involving both swine and man. The parasite seems to be tubules containing eggs at different stages of maturation. frequent especially in children, as the fact, was mentioned by some Microscopic examination of the sections showed skin lesions school teachers. The pig farming methods which allow the animals around the chiggers according to different phases of penetration to move freely among the houses in search of waste, as well as the and development of the parasite. These were always ulcerated or very limited use of shoes by the inhabitants, especially children, microulcerated, with the presence of parts of well-preserved result in a large diffusion of the disease due to a wide insects or their residues more or less altered by regressive dissemination of eggs over the ground. It may be assumed that; processes. At the cutaneous level, there was usually a conspicuous inflammatory infiltration of the acute type, consisting prevailingly of eosinophilic granulocytes . Chronic inflammatory changes were also present with lymphocytes, plasmacells and fibroblasts. Newly formed capillary vessels were also seen with thin walls suggesting a pronounced congestion of the area. The presence of some hemorrhagic foci, edematous zones and microabscesses due to possible superimposed bacterial infections were also observed. The epithelial layer, frequently showing acanthosis and hyperkeratosis with a markedly irregular surface, was often ulcerated showing different evolutive stages. In some areas, the horny layer, considerably thinned, covered the parasite’s body almost completely, SOthat it was deeply inserted into the basa1 superficial layers of the host and communicated with the outside through a small foramen that had obviously allowed the parasite to breath .

Some fields showed larger cutaneous ulcers with walls containing Figure 3: Lesions by Tunga penetrans in the teats of a sow. a granulation tissue incorporating chitinous fragments of the insect’s exoskeleton and microsuppurative foci consisting of exudative-necrotic, fibrinous-leukocytary material. n DISCUSSION

Tungiasis in man has been reported in Sao Tomé since the beginning of this Century: Enderlein (8) reported a case in a foot of a Black person without indicating his information source. TO our knowledge, the literature consulted does not report investigations or descriptions of other cases in subsequent periods. We may, however, hypothesize on the basis of the first case and the frequent movements of the population between Sao Tomé and Angola, the latter being one of the first zones infested by the

Figure 2: Lesions by Tunga penetrans on the snout of a pig. Figure 4: A foot of swine seriously affected by Tunga penetrans.

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Tunga penetrans in pigs in SCo Tomé

Figure 5: Histological section showing 3 Tunga penetrans embedded into the skin of a swine (Trichromie Masson Figure 7: A detail of the head and thorax of Tunga penetrans Goldner, x 25). (PAS, x 725). E = eye, H = head, L = legs, Th = thorax.

In Sao Tomé, the disease in swine is strongly debilitating, with lameness and painful infestation of the snout in both sexes and, in females, painful lesions of the teats with frequent inflammatory or necrotic complications. Parasitism of the latter location often results in the mother’s inability to nurse the litter, leading to the death of a11piglets. This situation was shown to be one of the reasons why farmers have their sows slaughtered, as indicated by their own accounts . Four foci of tungiasis reported in swine in Africa in the literature were identical to those of Sao Tomé due to similar conditions of both the environment and farming methods with mass infestation and loss of litters. In another outbreak in a mode1 farm in Tanzania (4, 5), no animal exhibited extensive inflammatory processes or serious consequences thanks to a timely diagnosis and an immediate, successful treatment. It is obvious that the situation in Sao Tomé is due to the primitive type of farming, depressed socioeconomic conditions of the population and farmers’ ignorance of the parasite’s life cycle and the ways to interrupt it. No empirical treatment appeared to be utilized on the island. The control or even eradication of the condition on Sao Tomé might be noticeably improved by health authorities educating farmers to enable them to promptly diagnose and treat the disease in affected swine, as well as distributing antiparasitic ointments or lotions at low prices through veterinary services. A finding of this investigation contrasting with the reports of’other authors is that the pigs studied here were generally kept on muddy, damp soil, whereas since Blanchard’s studies in 1890 (2) it has always been stated that T. penetrans needs dry, sandy soils to develop into larval stages.

Acknowledgments Thanksare due to the Minister of Agriculture and the Minister of Figure 6: Histological section of Tunga penetrans (Trichromie Health of the Republicof Sao Tomé and Principefor supporting Masson Goldner, x 62). E = eye, H = head, M = muscle fibers, our researchand arrangingthe stay of someof the authorson the 0 = ovary, Th = thorax, Tr = tracheae. Island.Thanks are alsodue to the personnelof the Public Abattoir for their technicalassistance.

in the past, the condition was probably imported into the island by infected persons, but pigs are certainly now a reservoir of the REFERENCES disease. In fact, while the natives cari rely on self-treatment by 1. AVILA-CONZALEZ J., 1977. Reporte sobre un brote de niguasis en el immediately removing the parasite using a thom or a needle, thus ganado porcino de la poblacih de Yaxcaba, Yucath. Aspectos interrupting the parasite’s life cycle, swine passively undergo the zoon6ticos del mismo. Mem. / Simp. Intern. Lab. Diagn. Mexico, 3: establishment of hundreds of insects in their skin without defense, 776-779. and spread thousands of eggs over the ground with their 2. BLANCHARD R., 1890. Traité de zoologie médicale, tome II. Paris, movements among the houses. France, Baillère et Fils, p. 484-493. h

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Tunga penetrans à São Tomé chez le porc

3. BRUMPT E., 1949. Précis de parasitologie, 6e ed, tome II. Paris, 13. MANSON P., 1893. The chigger or sand-flea (Pulex penetrans). In: France, Masson, p. 1323-1325. Davidson’s Hygiene and diseases of warm climates. Edinburg, London, UK, Young J. Pentland Publ., p. 963-966. 4. COOPER J.E., 1967. An outbreak of Tunga penetrans in a pig herd. Vet. Rec., 80: 365-366. 14. MONIEZ R., 1889. Les parasites de l’homme (animaux et végétaux). Paris, France, Baillère et Fils, p. 251-256. 5. COOPER J.E., 1976. Tunga penetrans infestation in pigs. Vet. Rec., 98: 472. 15. PAMPIGLIONE S., VISCONTI S., PEZZINO G., 1987. Ricerche sui parassiti intestinali dell’uomo in Africa Subsahariana. II: São Tomé e 6. DIPEOLU O.O., 1975. Ectoparasites of local pigs in Western Nigeria. Príncipe. Parassitologia, 29: 15-25. Niger. J. Anim. Prod., 2: 222-226. 16. PATTON W.S., 1931. Insects, ticks, mites and venomous animals of 7. DURAN C., SOTO ALFARO J.M., PICADO C., 1916. Biologia de la medical and veterinary importance. Part II, Public Health. Croydon, UK, Nigua. An. Hosp. S. José Costa Rica: 1-17. Grubb Ltd, p. 653-657. 8. ENDERLEIN G., 1901. Zur Kenntniss der Flohe und Sanflohe. Zool. 17. PESSOA S.B., 1958. Parasitologia médica, 5a ed., Rio de Janeiro, Jahrb. Syst., 14: 549-557. Brasil, Guanabara Koogan, p. 902-903. 9. GEIGY R., HERBIG A., 1949. Die Hypertrophie der Organe beim 18. RIETSCHEL W., 1989. Beobachtungen zum Sandfloh (Tunga Weibchen von Tunga penetrans. Acta trop., 6: 246-262. penetrans) bei Mensch und Hund in Franzosisch Guayana. Tierarztl, 17: 10. HICKS E.P., 1931. The early stages of the Jigger, Tunga penetrans. 189-193. Ann. trop. Med. Parasitol., 24: 575-586. 19. VERHULST A., 1976. Tunga penetrans (Sarcopsylla penetrans) as a 11. HOEPPLI R., 1963. Early references to the occurrence of Tunga cause of agalactia in sows in the Republic of Zaire. Vet. Rec., 98: 384. penetrans in tropical Africa. Acta trop. (suppl.1), 20: 143-153. 20. WESTWOOD J.O., 1840. On the characters of the chigoe or jigger. 12. JORDAN K., 1956. Suctoria. I. Tungidae. In: Smart J. Ed., 3rd ed., A Trans. Entomol. Soc. London, 2: 199-203. handbook for the identification of insects of medical importance. London, UK, British Museum, p. 229-231. Reçu le 15.6.98, accepté le 21.10.98

Résumé Resumen

Pampiglione S., Trentini M., Mattei Gentili F., Mendes J.L.X., Pampiglione S., Trentini M., Mattei Gentili F., Mendes J.L.X., Pampiglione C., Rivasi F. Tunga penetrans (Insecta : Sipho- Pampiglione C., Rivasi F. Tunga penetrans (Insecta: Siphonap- naptera) chez le porc à São Tomé (Afrique équatoriale) : as- tera) en cerdos en Santo Tomé (Africa ecuatorial). Aspectos pects épidémiologiques, cliniques, morphologiques et histo- epidemiológicos, clínicos, morfológicos e histopatológicos pathologiques La isla de Santo Tomé, antigua colonia portuguesa, localizada L’île de São Tomé, une ancienne colonie portugaise située en el Golfo de Guinea, es actualmente parte de una república dans le Golfe de Guinée, fait partie aujourd’hui d’une répu- independiente, la República de Santo Tomé y Príncipe. Los blique indépendante, la République de São Tomé et Príncipe. autores realizaron un estudio sobre los suidos sacrificados en Une enquête réalisée sur des porcs abattus à l’abattoir public el matadero público de la capital, el cual demostró que 28 de de la capitale a établi que, sur 100 sujets examinés, 28 étaient los 100 individuos examinados se encontraron afectados por affectés par des lésions provoquées par Tunga penetrans (In- lesiones asociadas con Tunga penetrans (Insecta: Siphonap- secta: Siphonaptera), localisées particulièrement dans les tera), localizadas principalmente en las patas, hocico y ubres. pattes, le museau et les mamelles. La présence également de En esta última, la presencia de pulgas adentro de los tejidos puces dans l’épaisseur des mamelons a provoqué des pertes de los pezones causó unas fuertes pérdidas económicas, de- économiques importantes car ces conditions ont empêché bido a la incapacidad de alimentar a los lechones lactantes, l’allaitement des porcelets, entraînant ainsi la mort de nichées conduciendo a la muerte de toda la camada. Se reportaron entières. Des cas humains ont été reportés fréquemment dans frecuentemente casos en humanos en la isla, representando l’île, cette parasitose constituant un vrai problème de santé un verdadero problema para salud pública. Uno de los au- publique. Un des auteurs a été infecté lui même par le para- tores se encontró también afectado por los parásitos. Se site. Il semble que le porc représente un réservoir de T. pene- puede asumir que los suidos actúan como reservorio en Santo trans à São Tomé, comme cela a pu être observé dans de Tomé, tal y como se observó en varios pueblos de América nombreux villages d’Amérique latine. Les auteurs présentent latina. Se presentan estudios fotográficos de los aspectos clíni- les images photographiques des manifestations cliniques, du cos e histológicos de las lesiones y de la morfología del pará- tableau histologique des lésions et de la morphologie du para- sito. site. Palabras clave: Genero humano - Cerdo - Tunga penetrans - Mots-clés : Genre humain - Porcin - Tunga penetrans - Symp- Síntomas - Histopatología - Conformación animal - Epidemio- tômes - Histopathologie - Conformation animale - Epidémio- logía - Santo Tomé y Príncipe. logie - São Tomé et Príncipe. Revue Élev. Méd. vét. Pays trop., 1998, 51 (3) : 201-205 205