Skip to main content
Log in

Epithelial morphometric alterations and mucosecretory responses in the nasal cavity of mice chronically exposed to hydrothermal emissions

  • Original Paper
  • Published:
Environmental Geochemistry and Health Aims and scope Submit manuscript

Abstract

Air pollutants (either of natural or anthropogenic origin) represent a considerable environmental risk to human health by affecting the respiratory system and causing respiratory disorders. In this study, we investigate the effects of chronic exposure to hydrothermal emissions on the nasal cavity of mice since it is the first and the most exposed region of the respiratory system. This study, carried in S. Miguel Island, Azores—Portugal, used Mus musculus as a bioindicator species. Mice were captured in an area with non-eruptive active volcanism (Furnas Village) and another area without volcanism (Rabo de Peixe, reference site). The hydrothermal emissions present at Furnas Village are characterized by the continuous release of several gases (CO2, H2S, 222Rn) along with metals (e.g. Hg, Cd, Zn, Al) and particulate matter into the environment. We test the hypothesis whether chronic exposure to this specific type of pollution causes epithelial morphometric, mucosecretory and neuronal alterations on the nasal cavity. Thickness measurements were taken in the squamous, respiratory and olfactory epithelia. The relative density of cell types (basal, support and neurons) was also assessed in the olfactory epithelium and the mucosecretory activity was determined in the lateral nasal glands, Bowman’s gland and goblet cells. Mice chronically exposed to hydrothermal emissions presented thinner olfactory epithelia and lesser mucous production, which could result in loss of olfactory capabilities as well as a decrease in the protective function provided by the mucous to the lower respiratory tract. For the first time, it is demonstrated that, in mice, this specific type of non-eruptive active volcanism causes epithelial and mucosecretory alterations, leading to the loss of olfactory capabilities.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data availability

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Abbreviations

AB/PAS:

Alcian Blue (2.5 pH)/ Periodic Acid Schiff

GEM:

Gaseous Elemental Mercury

BowGl:

Bowman’s Gland

GobCell:

Goblet Cell

H&E:

Haematoxylin and Eosin

LaNaGl:

Lateral Nasal Gland

OlfEpi:

Olfactory Epithelium

ResEpi:

Respiratory Epithelium

SquEpi:

Squamous Epithelium

VomOrg:

Vomeronasal Organ

FOI:

Functional Olfactory Index

FR:

Furnas (Figures only)

RP:

Rabo de Peixe (Figures only)

References

  • Amaral, A. F. S., Arruda, M., Cabral, S., & Rodrigues, A. S. (2008). Essential and non-essential trace metals in scalp hair of men chronically exposed to volcanogenic metals in the Azores. Portugal. Environment International, 34(8), 1104–1108. https://doi.org/10.1016/j.envint.2008.03.013

    Article  CAS  Google Scholar 

  • Amaral, A., Cabral, C., Guedes, C., & Rodrigues, A. (2007). Apoptosis, metallothionein, and bioavailable metals in domestic mice (Mus musculus L.) from a human-inhabited volcanic area. Ecotoxicology, 16, 475–482. https://doi.org/10.1007/s10646-007-0156-y

    Article  CAS  Google Scholar 

  • Amaral, A. F. S., & Rodrigues, A. S. (2007). Chronic exposure to volcanic environments and chronic bronchitis incidence in the Azores. Portugal. Environmental Research, 103(3), 419–423. https://doi.org/10.1016/j.envres.2006.06.016

    Article  CAS  Google Scholar 

  • Amaral, A. F. S., & Rodrigues, A. S. (2011). Volcanogenic contaminants: Chronic exposure. In J. Nriagu (Ed.), Encyclopedia on Environmental Health (pp. 681–689). Elsevier B.V.

    Chapter  Google Scholar 

  • Amaral, A., Rodrigues, V., Oliveira, J., Pinto, C., Carneiro, V., Sanbento, R., Cunha, R., & Rodrigues, A. (2006). Chronic exposure to volcanic environments and cancer incidence in the Azores, Portugal. Science of the Total Environment, 367, 123–128. https://doi.org/10.1016/j.scitotenv.2006.01.024

    Article  CAS  Google Scholar 

  • Bagnato, E., Viveiros, F., Pacheco, J. E., D’Agostino, F., Silva, C., & Zanon, V. (2018). Hg and CO2 emissions from soil diffuse degassing and fumaroles at Furnas Volcano (São Miguel Island, Azores): Gas flux and thermal energy output. Journal of Geochemical Exploration, 190, 39–57.

    Article  CAS  Google Scholar 

  • Camargo Pires-Neto, R., Júlia Lichtenfels, A., Regina Soares, S., Macchione, M., Saldiva, H. N., & P., Dolhnikoff, M. . (2006). Effects of São Paulo air pollution on the upper airways of mice. Environmental Research, 101(3), 356–361. https://doi.org/10.1016/j.envres.2005.12.018

    Article  CAS  Google Scholar 

  • Camarinho, R., Garcia, P. V., Choi, H., & Rodrigues, A. S. (2019a). Chronic exposure to non-eruptive volcanic activity as cause of bronchiolar histomorphological alteration and inflammation in mice. Environmental Pollution, 253, 864–871. https://doi.org/10.1016/j.envpol.2019.07.056

    Article  CAS  Google Scholar 

  • Camarinho, R., Garcia, P. V., Choi, H., & Rodrigues, A. S. (2019b). Overproduction of TNF-α and lung structural remodelling due to chronic exposure to volcanogenic air pollution. Chemosphere, 222, 227–234.

    Article  CAS  Google Scholar 

  • Camarinho, R., Garcia, P. V., & Rodrigues, A. S. (2013). Chronic exposure to volcanogenic air pollution as cause of lung injury. Environmental Pollution, 181, 24–30. https://doi.org/10.1016/j.envpol.2013.05.052

    Article  CAS  Google Scholar 

  • Camarinho, R., Navarro-Sempere, A., Garcia, P. V., García, M., Segovia, Y., & Rodrigues, A. S. (2021). Chronic exposure to volcanic gaseous elemental mercury: Using wild Mus musculus to unveil its uptake and fate. Environmental Geochemistry and Health. https://doi.org/10.1007/s10653-021-00924-z

    Article  Google Scholar 

  • Chamanza, R., & Wright, J. A. (2015). A review of the comparative anatomy, histology, physiology and pathology of the nasal cavity of rats, mice, dogs and non-human primates. Relevance to inhalation toxicology and human health risk assessment. Journal of Comparative Pathology, 153(4), 287–314.

    Article  CAS  Google Scholar 

  • Coakley, R. J., Taggart, C., Greene, C., McElvaney, N. G., & O’Neill, S. J. (2002). Ambient pCO2 modulates intracellular pH, intracellular oxidant generation, and interleukin-8 secretion in human neutrophils. Journal of Leukocyte Biology, 71, 603–610.

    CAS  Google Scholar 

  • Corps, K. N., Islam, Z., Pestka, J. J., & Harkema, J. R. (2010). Neurotoxic, inflammatory, and mucosecretory responses in the nasal airways of mice repeatedly exposed to the macrocyclic trichothecene mycotoxin Roridin A: dose-response and persistence of injury. Toxicologic Pathology, 38(3), 429–451. https://doi.org/10.1177/0192623310364026

    Article  CAS  Google Scholar 

  • Fukuda, N., Shirasu, M., Sato, K., Ebisui, E., Touhara, K., & Mikoshiba, K. (2008). Decreased olfactory mucus secretion and nasal abnormality in mice lacking type 2 and type 3 IP3 receptors. European Journal of Neuroscience, 27(10), 2665–2675. https://doi.org/10.1111/j.1460-9568.2008.06240.x

    Article  Google Scholar 

  • Guest, J. E., Gaspar, J. L., Cole, P. D., Queiroz, G., Duncan, A. M., Wallenstein, N., Ferreira, T., & Pacheco, J. M. (1999). Volcanic geology of Furnas volcano, São Miguel, Azores. Journal of Volcanology and Geothermal Research, 92(1–2), 1–29.

    Article  CAS  Google Scholar 

  • Hansell, A., & Oppenheimer, C. (2004). Health hazards from volcanic gases: A systematic literature review. Archives of Environmental Health, 59, 628–639. https://doi.org/10.1080/00039890409602947

    Article  CAS  Google Scholar 

  • Harkema, J. R., Carey, S. A., & Wagner, J. G. (2006). The nose revisited: A brief review of the comparative structure, function, and toxicologic pathology of the nasal epithelium. Toxicologic Pathology, 34(3), 252–269. https://doi.org/10.1080/01926230600713475

    Article  CAS  Google Scholar 

  • Hendry, J. H., Simon, S. L., Wojcik, A., Sohrabi, M., Burkart, W., Cardis, E., Laurier, D., Timarche, M., & Hayata, I. (2009). Human exposure to high natural background radiation: What can it teach us about radiation risks? Journal of Radiological Protection, 29, A29–A42.

    Article  CAS  Google Scholar 

  • International Agency for Research on Cancer Monographs on the evaluation of the carcinogenic risks to Humans (IARC). (1988). Man-made mineral fibres and radon. Lyon, France: IARC Press, 43, 33–171.

    Google Scholar 

  • Islam, Z., Harkema, J. R., & Pestka, J. J. (2006). Satratoxin G from the black mold Stachybotrys chartarum evokes olfactory sensory neuron loss and inflammation in the murine nose and brain. Environmental Health Perspectives, 114(7), 1099–1107. https://doi.org/10.1289/ehp.8854

    Article  CAS  Google Scholar 

  • Jafari, F.H., Minhas, L.A., Shoro, A.A., Tahir, M. (2010). A histological study of bowman’s glands in humans olfactory Mucosa. Pakistan Armed Forces Medical Journal, 60(1), 3–8. Available from: https://www.researchgate.net/publication/271509372_A_HISTOLOGICAL_STUDY_OF_BOWMAN'S_GLANDS_IN_HUMAN_OLFACTORY_MUCOSA

  • Jaramillo, A. M., Azzegagh, Z., Tuvim, M. J., & Dickey, B. F. (2018). Airway mucin secretion. Annals of the American Thoracic Society, 15, 164–170. https://doi.org/10.1513/AnnalsATS.201806-371AW

    Article  Google Scholar 

  • Kristbjornsdottir, A., & Rafnsson, V. (2013). Cancer incidence among population utilizing geothermal hot water: A census-based cohort study. International Journal of Cancer, 133, 2944–2952.

    CAS  Google Scholar 

  • Linhares, D., Garcia, P. V., Garcia, F., Ferreira, T., Rodrigues, A. D. S. (2015). Air pollution by hydrothermal volcanism and human pulmonary function. BioMed Research International, 2015, 326794. https://doi.org/10.1155/2015/326794.

    Article  CAS  Google Scholar 

  • Linhares, D., Garcia, P., Rodrigues, A. (2017). Radon exposure and human health: What happens in volcanic environments? In F. Adrovic (Ed.). Radon. doi: https://doi.org/10.5772/intechopen.71073.

  • Linhares, D., Garcia, P. V., Silva, C., Barroso, J., Kazachkova, N., Pereira, R., Lima, M., Camarinho, R., Ferreira, T., & Rodrigues, A. (2018). DNA damage in oral epithelial cells of individuals chronically exposed to indoor Radon (222Rn) in a hydrothermal área. Environmental Geochemistry and Health, 40(5), 1713–1724.

    Article  CAS  Google Scholar 

  • Martoja, R., Martoja-Pierson, M., Grumbles, L. C., Moncanut, M. E., & Coll, M. D. (1970). Técnicas de histologia animal (1st ed.). Toray-Masson.

    Google Scholar 

  • Maynard, R., Krzyzanowski, M., Vilahur, N., Héroux, M.-E. (2017). Evolution of WHO air quality guidelines: past, present and future. Copenhagen: WHO Regional Office for Europe. Available from: http://www.euro.who.int/en/health-topics/environment-and-health/air-quality/publications/2017/evolution-of-who-air-quality-guidelines-past,-present-and-future-2017

  • Murdoch, B., & Roskams, A. J. (2007). Olfactory epithelium progenitors: Insights from transgenic mice and in vitro biology. Journal of Molecular Histology, 38(6), 581–599. https://doi.org/10.1007/s10735-007-9141-2

    Article  CAS  Google Scholar 

  • Navarro-Sempere, A., Segovia, Y., Rodrigues, A. S., Garcia, P. V., Camarinho, R., & García, M. (2020). First record on mercury accumulation in mice brain living in active volcanic environments: a cytochemical approach. Environmental Geochemistry and Health., 43(1), 171–183. https://doi.org/10.1007/s10653-020-00690-4

    Article  CAS  Google Scholar 

  • Quéré, J. P., & Vincent, J. P. (1989). Détermination de l’âge chez le mulot gris (Apodemus sylvaticus L., 1758) par la pesée des cristallins. Mammalia, 53, 287–294. https://doi.org/10.1515/mamm.1989.53.2.287

    Article  Google Scholar 

  • Rodrigues, A. S., Arruda, M. S. C., & Garcia, P. V. (2012). Evidence of DNA damage in humans inhabiting a volcanically active environment: A useful tool for biomonitoring. Environment International, 49, 51–56. https://doi.org/10.1016/j.envint.2012.08.008

    Article  CAS  Google Scholar 

  • Rogers, D.F. (2007). Physiology of airway mucus secretion and pathophysiology of hypersecretion. Respiratory Care, 52(9), 1134–1146. Available from: http://rc.rcjournal.com/content/52/9/1134.

  • Searle, R. (1980). Tectonic pattern of the Azores spreading centre and triple junction. Earth and Planetary Science Letters, 51(2), 415–434.

    Article  Google Scholar 

  • Silva, C., Ferreira, T., Viveiros, F., & Allard, P. (2015). Soil radon (222Rn) monitoring at Furnas Volcano (São Miguel, Azores): Applications and challenges. European Physics Journal - Special Topics, 224, 659–686.

    Article  CAS  Google Scholar 

  • Tam, E., Miike, R., Labrenz, S., Sutton, A. J., Elias, T., Davis, J., Chen, Y. L., Tantisira, K., Dockery, D., & Avol, E. (2016). Volcanic air pollution over the Island of Hawai’i: Emissions, dispersal, and composition. Association with respiratory symptoms and lung function in Hawai’i Island school children. Environment International, 92–93, 543–552. https://doi.org/10.1016/j.envint.2016.03.025

    Article  CAS  Google Scholar 

  • Thornton, D. J., Rousseau, K., & McGuckin, A. (2008). Structure and function of the polymeric mucins in airways mucus. Annual Review of Physiology, 70(1), 459–486.

    Article  CAS  Google Scholar 

  • Viveiros, F., Cardellini, C., Ferreira, T., Caliro, S., Chiodini, G., & Silva, C. (2010). Soil CO2 emissions at Furnas volcano, São Miguel Island, Azores archipelago: Volcano monitoring perspectives, geomorphologic studies, and land use planning application. Journal of Geophysical Research: Solid Earth, 115(12), 1–17.

    Google Scholar 

  • Widdicombe, J. H., & Wine, J. J. (2015). Airway gland structure and function. Physiological Reviews, 95(4), 1241–1319. https://doi.org/10.1152/physrev.00039.2014

    Article  CAS  Google Scholar 

  • Young, J. T. (1981). Histopathological examination of the rat nasal cavity. Fundamental and Applied Toxicology, 1, 309–312. https://doi.org/10.1016/S0272-0590(81)80037-1

    Article  CAS  Google Scholar 

Download references

Acknowlegements

The authors would like to thank Paulo Melo for the field assistance in the capture of Mus musculus. Ricardo Camarinho is currently supported by a Ph.D. fellowship grant (M3.1.a/F/048/2015) from Fundo Regional da Ciência (Regional Government of the Azores).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A. S. Rodrigues.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflicts of interest.

Ethical Approval

All the procedures were carried out in strict accordance with the European Convention for the protection of vertebrate animals used in experimental and other scientific purposes (ETS123), directive 2010/63/EU and Portuguese law decree (DL 113/2013), and approved by the Ethics committee of the University of Azores (project 10/2020). All efforts were made to minimize animal suffering.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Capsule

Chronic exposure to hydrothermal emissions causes epithelial and mucosecretory alterations in the nasal cavity.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Camarinho, R., Pardo, A.M., Garcia, P.V. et al. Epithelial morphometric alterations and mucosecretory responses in the nasal cavity of mice chronically exposed to hydrothermal emissions. Environ Geochem Health 44, 2783–2797 (2022). https://doi.org/10.1007/s10653-021-01067-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-021-01067-x

Keywords

Navigation