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Exposure to Bat Droppings Among Tourists Visiting Caves in the Brazilian Amazon: A Risk for Disease Transmission

      To the Editor:
      Bats harbor diverse pathogens and are considered as a source of zoonotic diseases, in particular those caused by viruses. Large-scale epidemics that have occurred since the end of the 20th century have been associated with viruses of bat origin, such as Hendra virus, Nipah virus, and SARS-CoV virus. The etiology of the coronavirus disease 2019 pandemic is a betacoronavirus of probable bat origin.
      • Zhou P.
      • Yang X.
      • Wang X.
      • Hu B.
      • Zhang L.
      • Zhang W.
      • et al.
      A pneumonia outbreak associated with a new coronavirus of probable bat origin.
      The reason why these mammals carry numerous viruses is under debate, with strong evidence suggesting unique immunologic features. In several animal species including bats, pathogens are shed via saliva, feces, and urine. Infections from these secretions can occur via direct contact or indirectly through contaminated soil, water, food, and aerosols. Thus, places with high concentrations of excreta, such as caves, mines, tunnels, and bridges, may be the origin of zoonotic infections.

      Tourists Highly Exposed to Bat Droppings in Amazon Caves—

      The facts presented refer to 2 d of field observations carried out in July 2018 in Presidente Figueiredo (PF), a small tourist town in Amazonas state, Brazil. PF has approximately 36,000 inhabitants and is 128 km away from the Manaus urban center. The city is located within the dense Amazon rainforest in a region with low deforestation levels. The Maroaga and Onça caves (2°3’3.31”S 59°58’14.61”W and 1°59’13.94”S 60°3’35.30”, respectively) are among the most visited tourist destinations of Amazonas state. Both of these caves lacked safety measures to support tourist activities, such as handrails, stairs, signposts, and artificial lighting. In Maroaga, approximately 50 m after the cave entrance, there were copious amounts of bat excreta covering extensive areas of the ground (Figure 1), and it was virtually impossible to avoid stepping on it. Most of the tourists present on that occasion had their feet unprotected and inevitably stepped in soil moistened with droppings or stepped into the small stream that started inside the cave. Few bats were observed, but most presumably inhabited the deeper interior of the cave, where tourist access was prohibited. The tour guide reported that the cave was visited daily by several tourists, who had free access regardless of the guide’s presence. She mentioned having no concern regarding the risks of exposure to bat feces.
      Figure 1
      Figure 1Interior of Maroaga cave, Presidente Figueiredo, Amazonas state, Brazil (July 2018). A thick, brownish layer of bat droppings can be observed covering the ground surface, except for the middle path of the cave where a small stream runs toward the exterior. The image was captured approximately 50 m inside the cave, where tourists access frequently.
      The geologic structure of the Onça cave was relatively small and more open than Maroaga. It featured abundant bat droppings in areas accessed by tourists (Figure 2). Numerous bats were observed, and it was possible to be in close proximity owing to the low height of the cave. The tour guide here also declared no concerns about the exposure to bats and their droppings and was constantly encouraging tourists to get close to these mammals to observe them and take pictures. The events witnessed in PF presumably reflect daily tourist activities in Maroaga and Onça caves.
      Figure 2
      Figure 2Onça cave, Presidente Figueiredo, Amazonas state, Brazil (July 2018). Large amounts of bat droppings were present in the areas accessed by tourists, with various spots featuring a reddish color due to ingestion of açaí (Euterpe oleracea), a purple fruit highly consumed by insectivorous bats (numerous seeds of açaí discarded by bats were present over their excreta).

      Evidences of Zoonoses Transmitted Through Bat Droppings—

      Although various pathogens originate from bats, information on the transmission pathways to humans need further studies. Nonetheless, exposure to droppings has been demonstrated or proposed as an important source of zoonoses. Histoplasmosis, caused by the fungus Histoplasma capsulatum, is one of the most frequently observed diseases associated with bat excreta and is commonly referred to as “cave disease.” Although the majority of infected people present either no symptoms or mild illness, some individuals develop more severe clinical symptoms leading to mortality, such as acute pulmonary histoplasmosis, granulomatous mediastinitis, and disseminated histoplasmosis.
      • Kauffman C.A.
      Histoplasmosis: a clinical and laboratory update.
      Transmission to humans occurs mainly via inhalation of fungal spores from the feces of bats and birds; thus, places with high concentrations of excreta from these animals may be the origin of histoplasmosis outbreaks.
      • Ashford D.A.
      • Hajjeh R.A.
      • Kelley M.F.
      • Kaufman L.
      • Hutwagner L.
      • McNeil M.M.
      Outbreak of histoplasmosis among cavers attending the National Speleological Society Annual Convention, Texas, 1994.
      ,
      • Lyon G.M.
      • Bravo A.V.
      • Espino A.
      • Lindsley M.D.
      • Gutierrez R.E.
      • Rodriguez I.
      • et al.
      Histoplasmosis associated with exploring a bat-inhabited cave in Costa Rica, 1998–1999.
      Nipah virus is a highly virulent bat-borne paramyxovirus that emerged in Malaysia in 1998, causing outbreaks with high fatality rates in Asian countries. Infection occurs through contact with the secretions of infected pigs and via person-to-person transmission. Nipah virus infection in humans is likely to occur via consumption of date palm sap contaminated with bat excreta.
      • Islam M.S.
      • Sazzad H.M.S.
      • Satter S.M.
      • Sultana S.
      • Hossain M.J.
      • Hasan M.
      • et al.
      Nipah virus transmission from bats to humans associated with drinking traditional liquor made from date palm sap, Bangladesh, 2011–2014.
      The sap is traditionally collected in open pots placed at the top of palm trees, a procedure that enables bats to access the harvested sap to consume it and may allow contamination by bat excreta.
      Empirical evidence on the transmission routes from bats to humans for certain bat-transmitted diseases needs to be confirmed; however, available data suggest that high exposure to droppings is the most likely source of infection, as observed in the case of Marburg hemorrhagic fever (MHF). Since 1975, outbreaks of MHF have been associated with visits to caves and mines,
      • Amman B.R.
      • Carroll S.A.
      • Reed Z.D.
      • Sealy T.K.
      • Balinandi S.
      • Swanepoel R.
      • et al.
      Seasonal pulses of Marburg virus circulation in juvenile Rousettus aegyptiacus bats coincide with periods of increased risk of human infection.
      and the Egyptian fruit bat Rousettus aegyptiacus was later identified as the prime reservoir host for Marburg virus. Unprotected contact with infected bat feces or aerosols is considered to be the source of MHF infection,
      Centers for Disease Control and Prevention
      Marburg hemorrhagic fever (transmission).
      as successfully demonstrated via experimental respiratory infections in animal models.
      • Leffel E.K.
      • Reed D.S.
      Marburg and Ebola viruses as aerosol threats.
      Other human pathogens found in bats may be transmitted via exposure to bat droppings, such as Leptospira spp and Hantavirus, both of which are primarily transmitted to humans through rodent excreta.

      Final Considerations—

      The high level of exposure to bat droppings in PF needs greater attention from the public health perspective. Histoplasmosis is the most likely zoonosis to emerge from this scenario. Furthermore, exposure to bat droppings should be recognized as a risk for spillover events, with new and undiscovered pathogens (mainly viruses) emerging in human populations. Such risk is possibly enhanced by the proximity of PF to the city of Manaus and to the high biodiversity of the Amazon biome, as the emergence of zoonotic pathogens of wildlife origin correlates strongly with both human density and wildlife biodiversity, respectively.
      • Morse S.S.
      • Mazet J.A.K.
      • Woolhouse M.
      • Parrish C.R.
      • Carroll D.
      • Karesh W.B.
      • et al.
      Prediction and prevention of the next pandemic zoonosis.
      The development and operation of new strategies to mitigate the risks of disease transmission inside Maroaga and Onça caves are warranted. Briefly, such strategies should include specific protocols for personal protection (eg, the use of appropriate clothing, footwear, safety helmets, and safety instructions), professionalization of tour guides, and studies to characterize the risks of disease transmission during speleological tourism.

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