Skip to main content

Advertisement

SpringerLink
Log in

Chemical signature and antimicrobial activity of Central Portuguese Natural Mineral Waters against selected skin pathogens

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

Abstract

The common therapeutic indications of Portuguese Natural Mineral Waters (NMWs) are primarily for respiratory, rheumatic and musculoskeletal systems. However, these NMWs have been increasingly sought for dermatologic purposes. Opposing to what is observed in the major European Thermal Centres, there are few scientific evidences supporting the use of Portuguese NMWs for clinical applications. The aim of this study was to characterize the antimicrobial profile of individual NMWs from the central region of Portugal and correlate the results with their physicochemical characterization. An extensive multivariate analysis (principal component analysis) was also performed to further investigate this possible correlation. Six collection strains representing skin microbiota, namely Staphylococcus aureus, Escherichia coli, Corynebacterium amycolatum, Candida albicans, Staphylococcus epidermidis and Cutibacterium acnes, were analysed, and their antimicrobial profile was determined using Clinical and Laboratory Standards Institute M07-A10, M45-A2, M11-A6 and M27-A3 microdilution methods. Different NMWs presented different antimicrobial profiles against the strains used; the physicochemical composition of NMWs seemed to be correlated with the different susceptibility profiles. Cutibacterium acnes showed a particularly high susceptibility to all NMWs belonging sulphurous/bicarbonated/sodic ionic profile, exhibiting microbial reductions up to 65%. However, due to the complex physicochemical composition of each water an overall conclusion regarding the effect of a specific ion on the growth of different microorganisms is yet to be known.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abu-Ghazaleh, B. (2016). Effect of sodium chloride on subsequent survival of Staphylococcus aureus in various preservatives. Food and Nutrition Sciences,07, 955–963.

    Article  CAS  Google Scholar 

  • Achermann, Y., Goldstein, E. J. C., Coenye, T., & Shirtliffa, M. E. (2014). Propionibacterium acnes: From commensal to opportunistic biofilm-associated implant pathogen. Clinical Microbiology Reviews,27, 419–440. https://doi.org/10.1128/CMR.00092-13.

    Article  CAS  Google Scholar 

  • Akiyama, H., Yamasaki, O., Tada, J., Kubota, K., & Arata, J. (2000). Antimicrobial effects of acidic hot-spring water on Staphylococcus aureus strains isolated from atopic dermatitis patients. Journal of Dermatological Science,24, 112–118. https://doi.org/10.1016/S0923-1811(00)00091-8.

    Article  CAS  Google Scholar 

  • APHA. (2005). Standard methods for the examination of water and wastewater (21st ed.). Washington, DC: American Public Health Association.

    Google Scholar 

  • Araujo, A. R. T. S., Sarraguça, M. C., Ribeiro, M. P., & Coutinho, P. (2017). Physicochemical fingerprinting of thermal waters of Beira Interior region of Portugal. Environmental Geochemistry and Health,39, 483–496. https://doi.org/10.1007/s10653-016-9829-x.

    Article  CAS  Google Scholar 

  • Belmares, J., Detterline, S., Pak, J. B., & Parada, J. P. (2007). Corynebacterium endocarditis species-specific risk factors and outcomes. BMC Infectious Diseases,7, 4. https://doi.org/10.1186/1471-2334-7-4.

    Article  Google Scholar 

  • Braga, P. C., Ceci, C., Marabini, L., & Nappi, G. (2013). The antioxidant activity of sulphurous thermal water protects against oxidative DNA damage: A comet assay investigation. Drug Res (Stuttg),63, 198–202. https://doi.org/10.1055/s-0033-1334894.

    Article  CAS  Google Scholar 

  • Brown, S. K., & Shalita, A. R. (1998). Acne vulgaris. Lancet,351, 1871–1876.

    Article  CAS  Google Scholar 

  • Cantista, P. (2008). O termalismo em Portugal. An Hidrol Medica,3, 79–107.

    Google Scholar 

  • Carbajo, J. M., & Maraver, F. (2017). Sulphurous mineral waters: New applications for health. Evidence-Based Complementary and Alternative Medicine. https://doi.org/10.1155/2017/8034084.

    Article  Google Scholar 

  • Child, Dennis. (2006). The essentials of factor analysis (3rd ed.). New York, NY: Continuum International Publishing Group.

    Google Scholar 

  • CLSI. (2004). Methods for antimicrobial susceptibility testing of anaerobic bacteria (6th ed). CLSI Standard M11-A6. Wayne, PA: Clinical and Laboratory Standards Institute.

  • CLSI. (2008). Reference method for broth dilution antifungal susceptibility testing of yeasts (3rd ed). CLSI Standard M27-A3. Wayne, PA: Clinical and Laboratory Standards Institute.

  • CLSI. (2010). Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria (2nd ed). CLSI Standard M45-A2. Wayne, PA: Clinical and Laboratory Standards Institute.

  • CLSI. (2015). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically (10th ed). CLSI Standard M07-A10. Wayne, PA: Clinical and Laboratory Standards Institute.

  • Cogen, A. L., Nizet, V., & Gallo, R. L. (2008). Skin microbiota: A source of disease or defence? British Journal of Dermatology,158, 442–455. https://doi.org/10.1111/j.1365-2133.2008.08437.x.

    Article  CAS  Google Scholar 

  • Cross, J. H., Bradbury, R. S., Fulford, A. J., Jallow, A. T., Wegmüller, R., Prentice, A. M., et al. (2015). Oral iron acutely elevates bacterial growth in human serum. Scientific Reports,5, 16670. https://doi.org/10.1038/srep16670.

    Article  CAS  Google Scholar 

  • Direção Geral de Energia e Geologia. (2017). Frequência Termal em 2017. In: Direcção Geral de Energia e Geologia. Retrieved January 4, 2019, from http://www.dgeg.gov.pt/

  • Direção-Geral da Saúde. (1989). Indicações Terapêuticas dos Estabelecimentos Termais Portugueses. In: Diário da Republica, 2a série, 23 Maio 1989. Retrieved January 9, 2019, https://www.dgs.pt/saude-ambiental/areas-de-intervencao/estabelecimentos-termais/legislacao-indicacoes-terapeuticas.aspx

  • dos Santos, A. L., Santos, D. O., de Freitas, C. C., Ferreira, B. L. A., Afonso, I. F., Rodrigues, C. R., et al. (2007). Staphylococcus aureus: Visiting a strain of clinical importance. Jornal Brasileiro de Patologia e Medicina Laboratorial,43, 413–423. https://doi.org/10.1021/ed067p473.

    Article  Google Scholar 

  • Duguid, I. G., Evans, E., Brown, M. R. W., & Gilbert, P. (1992). Growth-rate-independent killing by ciprofloxacin of biofilm-derived staphylococcus epidermidis evidence for cell-cycle dependency. Journal of Antimicrobial Chemotherapy,30, 791–802. https://doi.org/10.1093/jac/30.6.791.

    Article  CAS  Google Scholar 

  • Faga, A., Nicoletti, G., Gregotti, C., Finotti, V., Nitto, A., & Gioglio, L. (2012). Effects of thermal water on skin regeneration. International Journal of Molecular Medicine,29, 732–740. https://doi.org/10.3892/ijmm.2012.917.

    Article  Google Scholar 

  • Ferreira, M. O., Costa, P. C., & Bahia, M. F. (2010). Effect of São Pedro do sul thermal water on skin irritation. International Journal of Cosmetic Science,32, 205–210. https://doi.org/10.1111/j.1468-2494.2010.00527.x.

    Article  CAS  Google Scholar 

  • Gomes, C., Carretero, M. I., Pozo, M., Maraver, F., Cantista, P., Armijo, F., et al. (2013). Peloids and pelotherapy: Historical evolution, classification and glossary. Applied Clay Science,75–76, 28–38. https://doi.org/10.1016/j.clay.2013.02.008.

    Article  CAS  Google Scholar 

  • Gomes, C., Rocha, F., Silva, E., Patinha, C., Forjaz, V., Terroso, D. (2010). Benefits of mud/clay and thermal spring water in the. In Environment 2010: Situation and Perspectives for the European Union (pp 1–5)

  • Hercogova, J., Stanghellini, E., Tsoureli-Nikita, E., & Menchini, G. (2002). Inhibitory effects of Leopoldine spa water on inflammation caused by sodium lauryl sulphate. Journal of the European Academy of Dermatology and Venereology,16, 263–266. https://doi.org/10.1046/j.1468-3083.2002.00451.x.

    Article  CAS  Google Scholar 

  • Hernández Torres, A., et al. (2006). Técnicas y tecnologías en hidrología médica e hidroterapia . Informe de Evaluación de Tecnologías Sanitarias, 50, Agencia de Evaluación de Tecnologías Sanitarias (AETS), Instituto de Salud Carlos III, Ministerio de Sanidad y Consumo. Madrid.  

  • INFARMED - Instituto Nacional da Farmácia e do Medicamento. (2009). Farmacopeia portuguesa 9: edição oficial (9th ed.). Fundação Calouste Gulbenkian: Lisboa.

    Google Scholar 

  • Inoue, T., Inoue, S., & Kubota, K. (1999). Bactericidal activity of manganese and iodide ions against staphylococcus aureus: A possible treatment for acute atopic dermatitis. Acta Dermato Venereologica,79, 360–362. https://doi.org/10.1080/000155599750010265.

    Article  CAS  Google Scholar 

  • Ki, V., & Rotstein, C. (2008). Bacterial skin and soft tissue infections in adults: A review of their epidemiology, pathogenesis, diagnosis, treatment and site of care. Canadian Journal of Infectious Diseases and Medical Microbiology,19, 173–184.

    Article  Google Scholar 

  • Ko, H. H. T., Lareu, R. R., Dix, B. R., & Hughes, J. D. (2018). In vitro antibacterial effects of statins against bacterial pathogens causing skin infections. European Journal of Clinical Microbiology and Infectious Diseases,37, 1125–1135. https://doi.org/10.1007/s10096-018-3227-5.

    Article  CAS  Google Scholar 

  • Kühbacher, A., Burger-Kentischer, A., & Rupp, S. (2017). Interaction of Candida Species with the skin. Microorganisms,5, 32. https://doi.org/10.3390/microorganisms5020032.

    Article  CAS  Google Scholar 

  • Lee, H. P., Choi, Y. J., Cho, K. A., Woo, S. Y., Yun, S. T., Lee, J. T., et al. (2012). Effect of spa spring water on cytokine expression in human keratinocyte HaCaT cells and on differentiation of CD4+ T cells. Annals of Dermatology,24, 324–336. https://doi.org/10.5021/ad.2012.24.3.324.

    Article  CAS  Google Scholar 

  • Matz, H., Orion, E., & Wolf, R. (2003). Balneotherapy in dermatology. Dermatologic Therapy,16, 132–140. https://doi.org/10.1046/j.1529-8019.2003.01622.x.

    Article  Google Scholar 

  • McCaig, L. F., McDonald, L. C., Mandal, S., & Jernigan, D. B. (2006). Staphylococcus aureus-associated skin and soft tissue infections in ambulatory care. Emerging Infectious Diseases,12, 1715–1723. https://doi.org/10.3201/eid1211.060190.

    Article  Google Scholar 

  • Meylan, P., Lang, C., Mermoud, S., Johannsen, A., Norrenberg, S., Hohl, D., et al. (2017). Skin colonization by Staphylococcus aureus precedes the clinical diagnosis of atopic dermatitis in infancy. J Invest Dermatol,137, 2497–2504. https://doi.org/10.1016/j.jid.2017.07.834.

    Article  CAS  Google Scholar 

  • Nicoletti, G., Saler, M., Pellegatta, T., Tresoldi, M., Bonfanti, V., Malovini, A., et al. (2017). Ex vivo regenerative effects of a spring water. Biomed Reports,7, 508–514. https://doi.org/10.3892/br.2017.1002.

    Article  CAS  Google Scholar 

  • Nouri, M., & Titley, K. (2003). Paediatrics—A review of the antibacterial effect of fluoride. Oral Health,93, 8–12.

    Google Scholar 

  • Nunes, S., & Tamura, B. (2012). Revisão histórica das águas termais. Surgical & Cosmetic Dermatology,3, 252–258.

    Google Scholar 

  • Otto, M. (2009). Staphylococcus epidermidis—the ‘accidental’ pathogen. Nature Reviews Microbiology,7, 555–567. https://doi.org/10.1038/nrmicro2182.Staphylococcus.

    Article  CAS  Google Scholar 

  • Patruta, S. I., & Hörl, W. H. (1999). Iron and infection. Kidney International,55, S125–S130. https://doi.org/10.1046/J.1523-1755.1999.055SUPPL.69125.X.

    Article  Google Scholar 

  • Petkovšek, Ž., Eleršič, K., Gubina, M., Žgur-Bertok, D., & Erjavec, M. S. (2009). Virulence potential of Escherichia coli isolates from skin and soft tissue infections. Journal of Clinical Microbiology,47, 1811–1817. https://doi.org/10.1128/JCM.01421-08.

    Article  CAS  Google Scholar 

  • Quattrini, S., Pampaloni, B., & Brandi, M. L. (2016). Natural mineral waters: Chemical characteristics and health effects. Clinical Cases in Mineral and Bone Metabolism,13, 173–180. https://doi.org/10.11138/ccmbm/2016.13.3.173.

    Article  Google Scholar 

  • Rebelo, M., da Silva, E. F., & Rocha, F. (2015). Characterization of Portuguese thermo-mineral waters to be applied in peloids maturation. Environmental Earth Sciences,73, 2843–2862. https://doi.org/10.1007/s12665-014-3670-2.

    Article  CAS  Google Scholar 

  • Richard, M. J., Guiraud, P., Arnaud, J., Cadi, R., Monjo, A. M., Richard, A., et al. (2010). Pouvoir antioxydant d’une eau thermale séléniée sur des fibroblastes cutanés humains diploides. Journal français d’hydrologie,22, 119–125. https://doi.org/10.1051/water/19912201119.

    Article  Google Scholar 

  • Ridaura, V. K., Bouladoux, N., Claesen, J., Chen, Y. E., Byrd, A. L., Constantinides, M. G., et al. (2018). Contextual control of skin immunity and inflammation by Corynebacterium. Journal of Experimental Medicine,215, 785–799. https://doi.org/10.1084/jem.20171079.

    Article  CAS  Google Scholar 

  • Tabachnick, B. G., & Fidell, L. S. (2007). Using multivariate statistics (5th ed.). Boston, MA: Allyn & Bacon/Pearson Education.

    Google Scholar 

  • Underhill, D. M., & Iliev, I. D. (2014). The mycobiota: Interactions between commensal fungi and the host immune system. Nature Reviews Immunology,14, 405–416.

    Article  CAS  Google Scholar 

  • Van Loveren, C. (2001). Antimicrobial activity of fluoride and its in vivo importance: Identification of research questions. Caries Research,35, 65–70. https://doi.org/10.1159/000049114.

    Article  Google Scholar 

  • Zalas, P., Mikucka, A., & Gospodarek, E. (2004). Antibiotic sensitivity of Corynebacterium amycolatum. Medycyna Doswiadczalna I Mikrobiologia,56, 327–334.

    CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to acknowledge all Thermal Centres involved in the project and the financial support provided by FEDER funds through the POCI—COMPETE 2020—Operational Programme Competitiveness and Internationalisation in Axis I—Strengthening research, technological development and innovation (Project POCI-01-0145-FEDER-007491) and National Funds by FCT—Foundation for Science and Technology (Project UID/Multi/00709/2013), Provere Termas Centro—Projeto Âncora de Inovação, co-funded by Centro 2020, Portugal 2020 and European Union funds.

Author information

Authors and Affiliations

  1. Health Sciences Research Centre (CICS-UBI), University of Beira Interior, Av. Infante D. Henrique, 6200-506, Covilhã, Portugal

    Ana Sofia Oliveira, Cátia Vicente Vaz, Sara Correia, Raquel Ferreira, Luiza Breitenfeld, José Martinez-de-Oliveira, Rita Palmeira-de-Oliveira & Ana Palmeira-de-Oliveira

  2. Center for Neuroscience and Cell Biology, University of Coimbra, Rua Larga, 3004-504, Coimbra, Portugal

    Ana Silva, Rita Palmeira-de-Oliveira, Cláudia Pereira & Maria Teresa Cruz

  3. Department of Mathematics and Center of Mathematics and Applications, University of Beira Interior, Rua Marquês D’Ávila e Bolama, 6201-001, Covilhã, Portugal

    Sandra Saraiva Ferreira

  4. Faculty of Health Sciences, University of Beira Interior, Av. Infante D. Henrique, 6200-506, Covilhã, Portugal

    Raquel Ferreira, Luiza Breitenfeld, José Martinez-de-Oliveira & Ana Palmeira-de-Oliveira

  5. Child and Woman’s Health Department, Cova da Beira Hospital Centre, Quinta do Alvito, 6200-251, Covilhã, Portugal

    José Martinez-de-Oliveira

  6. Labfit–Health Products Research and Development Lda, UBImedical, Estrada Nacional 506, 6200-284, Covilhã, Portugal

    Rita Palmeira-de-Oliveira & Ana Palmeira-de-Oliveira

  7. Faculty of Medicine, University of Coimbra, Pólo das Ciências da Saúde, Azinhaga de Santa Comba, 3000-548, Coimbra, Portugal

    Cláudia Pereira

  8. Faculty of Pharmacy, University of Coimbra, Pólo das Ciências da Saúde, Azinhaga de Santa Comba, 3000-548, Coimbra, Portugal

    Maria Teresa Cruz

Authors
  1. Ana Sofia Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cátia Vicente Vaz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ana Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sandra Saraiva Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Sara Correia
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Raquel Ferreira
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Luiza Breitenfeld
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. José Martinez-de-Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Rita Palmeira-de-Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Cláudia Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Maria Teresa Cruz
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Ana Palmeira-de-Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ana Palmeira-de-Oliveira.

Additional information

Publisher's Note

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

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 58 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Oliveira, A.S., Vaz, C.V., Silva, A. et al. Chemical signature and antimicrobial activity of Central Portuguese Natural Mineral Waters against selected skin pathogens. Environ Geochem Health 42, 2039–2057 (2020). https://doi.org/10.1007/s10653-019-00473-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10653-019-00473-6

Keywords

Search

Navigation