Hostname: page-component-848d4c4894-sjtt6 Total loading time: 0 Render date: 2024-06-23T09:48:19.612Z Has data issue: false hasContentIssue false
  • English
  • Français

Natural Antibacterial Clays: Historical Uses and Modern Advances

Published online by Cambridge University Press:  01 January 2024

Lynda B. Williams
Lynda B. Williams*
Affiliation:
School of Earth & Space Exploration, Arizona State University, Tempe, AZ 85287-1404, USA
*
*lynda.williams@asu.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Antibacterial clays in nature include a variety of clay mineral assemblages that are capable of killing certain human pathogens. Although clays have been used for medicinal applications historically, only in the last decade have analytical methods and instrumentation been developed that allow researchers to evaluate the antibacterial mechanisms of various clays applied medicinally. Comparisons of the mineralogical and chemical compositions of natural clays that kill bacteria have promoted a better understanding of the mineral properties that are toxic to a broad-spectrum of human pathogens, including bacteria that have developed resistance to antibiotics. Popular literature is filled with reports of ‘healing’ clays, that, when tested against pathogens in vitro and compared to controls, do not appear to have bactericidal properties. It is important, however, to differentiate what properties make a clay ‘healing,’ versus what makes a clay ‘antibacterial.’ Most antibacterial clays identified to date buffer pH conditions of a hydrated clay outside the range of conditions in which human pathogens thrive (circum-neutral pH) and require oxidation reactions to occur. It is the change in oxidation state and pH imposed by the hydrated clay, applied topically, that leads to a chemical attack of the bacteria. Healing clays, on the other hand, may not kill bacteria but have soothing effects that are palliative. This article reviews some of the historical uses of clays in medicine but focuses primarily on the common characteristics of natural antibacterial clays and early studies of their antibacterial mechanisms. In this era of bacterial resistance to antibiotics, mimicking the antibacterial mechanisms exhibited by natural clays could be advantageous in the development of new antimicrobial agents.

Keywords

Antibacterial ClayBactericideBentonitesFenton MetalsHealingHydrothermal ClayMedical GeologyMedicinal ClayMetal ToxicityReactive Oxygen SpeciesReduced Iron Clay
Type
Research Article
Information
Clays and Clay Minerals , Volume 67 , Issue 1 , 15 February 2019 , pp. 7 - 24
Copyright
Copyright © Clay Minerals Society 2019

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Alba, B. M., & Gross, C. A. (2004). Regulation of the Escherichia coli sigma-dependent envelope stress response. Molecular Microbiology, 52, 613–619.CrossRefGoogle ScholarPubMed
Awad, M. E., López-Galindo, A., Setti, M., El-Rahmany, M. M., & Iborra, C. V. (2017). Kaolinite in pharmaceutics and biomedicine. International Journal of Pharmacology, 533, 34–48.CrossRefGoogle ScholarPubMed
Baker, S. E., Sawvel, A. M., Zheng, N., & Stucky, G. D. (2007). Controlling bioprocesses with inorganic surfaces: Layered clay hemostatic agents. Chemistry of Materials, 19, 4390–4392.CrossRefGoogle Scholar
Bauer, A. W., Kirby, W. M. M., Sherris, J. C., & Turck, M. (1966). Antibiotic susceptibility testing by a standardized single disk method. American Journal of Clinical Pathology, 45, 493–496.CrossRefGoogle ScholarPubMed
Behroozian, S., Svensson, S. L., & Davies, J. (2016). Kisameet clay exhibits potent antibacterial activity against the ESKAPE pathogens. mBio, 7, e01842-01815.CrossRefGoogle ScholarPubMed
Caflisch, K. M., Schmidt-Malan, S. M., Mandrekar, J. N., Karau, M. J., Kicklas, J. P., Williams, L. B., & Patel, R. (2018). Antimicrobial activity of reduced iron clay against pathogenic biofilms from wound infections. International Journal of Antimicrobial Agents, 52, 692–696.CrossRefGoogle ScholarPubMed
Carretero, M. I. (2002). Clay minerals and their beneficial effects upon human health: a review. Applied Clay Science, 21, 155–163.CrossRefGoogle Scholar
Carretero, M. I., Gomes, C. S. F., & Tateo, F. (2006). Clays and human health. In Bergaya, F., Theng, B. K. G., & Lagaly, G. (Eds.), Handbook of Clay Science (Vol. 1, pp. 717–741). Developments in Clay Science, Elsevier Ltd.CrossRefGoogle Scholar
Cervini-Silva, J., Nieto-Camacho, A., Palacios, E., Montoya, J. A., Gómez-Vidales, V., & Ramirez-Apán, M. T. (2013). Anti-inflammatory and anti-bacterial activity, and cytotoxicity of halloysite surfaces. Colloids and Surfaces B, 111, 651–655.CrossRefGoogle ScholarPubMed
Cervini-Silva, J., Nieto-Camacho, A., Kaufhold, S., Ufer, K., Palacios, E., Montoya, A., & Dathe, W. (2016). Antiphlogistic effect by zeolite as determined by a murine inflammation model. Microporous and Mesoporous Materials, 228, 207–214.CrossRefGoogle Scholar
CLSI, [formerly National Committee for Clinical Laboratory Standards: NCCLS] (1999). Methods for Determining Bactericidal Activity of Antimicrobial Agents: Approved Guideline. NCCLS document M26-A, 19(18), 32pp.Google Scholar
CLSI, [Clinical and Laboratory Standards Institute] (2012). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically: Approved Standard, 9th edition. M07-A9, 32(2), 69 pp.Google Scholar
Cunningham, T. M., Koehl, J. L., Summers, J. S., & Haydel, S. E. (2010). pH-dependent metal ion toxicity influences the antibacterial activity of two natural mineral mixtures. Public Library of Science One, 5, e9456.Google ScholarPubMed
Cygan, R. T., Ho, C. K., & Weiss, C. J. (2002). Linking the Geosciences to Emerging Bio-engineering Technologies. Sandia National Laboratories Report SAND2002–3690, 59 pp.CrossRefGoogle Scholar
Dong, H. L., Fredrickson, J. K., Kennedy, D. W., Zachara, J. M., Kukkadappu, R. K., & Onstott, T. C. (2000). Mineral transformation associated with the microbial reduction of magnetite. Chemical Geology, 169, 299–318.CrossRefGoogle Scholar
Eberl, D. D. (2003). Users guide to RockJock: A program for determining quantitative mineralogy from powder X-ray diffraction data. USGS Open file Report 03-78. USGS.Google Scholar
Ernstsen, V., Gates, W. P., & Stucki, J. W. (1998). Microbial reduction of structural iron in clays – A renewable source of reduction capacity. Journal of Environmental Quality, 27, 761–766.CrossRefGoogle Scholar
Exley, C. (2004). The pro-oxidant activity of aluminum. Free Radical Biology in Medicine, 36, 380–387.CrossRefGoogle ScholarPubMed
Fein, J., Daughney, C., Yee, N., & Davis, T. A. (1997). A chemical equilibrium model for metal adsorption onto bacterial surfaces. Geochimica et Cosmochimica Acta, 67, 3319–3328.CrossRefGoogle Scholar
Fenton, H. J. H. (1894). Oxidation of tartaric acid in the presence or iron. Journal of the Chemical Society, 65, 899–910.CrossRefGoogle Scholar
Ferrell, R. E. Jr. (2008). Medicinal clay and spiritual healing. Clays and Clay Minerals, 56, 751–760.CrossRefGoogle Scholar
Ferris, F. G., Fyfe, W. S., & Beveridge, T. J. (1987). Bacteria as nucleation sites for authigenic minerals in a metal-contaminated lake sediment. Chemical Geology, 63, 225–232.CrossRefGoogle Scholar
Finkelman, R. B. (2006). Health benefits of geologic materials and geologic processes. International Journal of Environmental Research and Public Health, 3, 338–342.CrossRefGoogle ScholarPubMed
Finkelman, R. B. (2019). The influence of clays on human health: A medical geology perspective. Clays and Clay Minerals, 67.CrossRefGoogle Scholar
Fortin, D., & Beveridge, T. J. (1997). Role of the bacterium Thiobacillus in the formation of silicates in acid mine tailings. Chemical Geology, 141, 235–250.CrossRefGoogle Scholar
George, K. M., Chatterjee, D., Gunawardana, G., Welty, D., Hayman, J., Lee, R., & Small, P. L. C. (2002). Mycolactone: A polyketide toxin from Mycobacterium ulcerans, required for virulence. Science, 283(5403), 854–857.CrossRefGoogle Scholar
Gomes, C. (2013). Naturotherapies based on minerals. Geomaterials, 3, 1–14.CrossRefGoogle Scholar
Haack, E. A., & Warren, L. A. (2003). Biofilm hydrous manganese oxyhydroxides and metal dynamics in acid rock drainage. Environmental Science & Technology, 37, 4138–4147.CrossRefGoogle ScholarPubMed
Harrison, J. J., Turner, R. J., & Ceri, H. (2005). High-throughput metal susceptibility testing of microbial biofilms. BMC Microbiology, 5, 1–11.CrossRefGoogle ScholarPubMed
Haydel, S. E., Remenih, C. M., & Williams, L. B. (2008). Broad-spectrum in vitro antibacterial activities of clay minerals against antibiotic-susceptible and antibiotic-resistant bacterial pathogens. Journal of Antimicrobial Chemotherapy, 61, 353–361.CrossRefGoogle ScholarPubMed
Hedges, A. J. (2002). Estimating the precision of serial dilutions and viable bacterial counts. International Journal of Food Microbiology, 76, 207–214.CrossRefGoogle ScholarPubMed
Høiby, N., Bjarnsholt, T., Givskov, M., Molin, S., & Coifu, O. (2010). Antibiotic resistance of bacterial biofilms. International Journal of Antimicrobial Agents, 35, 322–332.CrossRefGoogle ScholarPubMed
Hoorn, C. (1994). Fluvial palaeoenvironments in the intracratonic Amazonas Basin (Early Miocene-early Middle Miocene, Colombia). Palaeogeography, Palaeoclimatology, Palaeoecology, 109, 1–54.CrossRefGoogle Scholar
Honty, M., De Craen, M., Wang, L., Madejova, J., Czimerova, A., Pentrak, M., Stricek, I., & Van Geet, M. (2010). The effect of high pH alkaline solutions on the mineral stability of the Boom Clay – Batch experiments at 60°C. Applied Geochemistry, 25, 825–840.CrossRefGoogle Scholar
Huisman, O., D'Ari, R., & Gottesman, S. (1984). Cell-division control in Escherichia coli: Specific induction of the SOS function SfiA protein is sufficient to block septation. Proceedings of the National Academy of Science USA, 81, 4490–4494.CrossRefGoogle ScholarPubMed
Imlay, J. A., Chin, S. M., & Linn, S. (1988). Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science, 240, 640–642.Google ScholarPubMed
Jackson, M. L. (1979). Soil Chemical Analysis Advanced course. 2nd edition. Madison: Published by the author. 895 pp.Google Scholar
Keyer, K., & Imlay, J. A. (1996). Superoxide accelerates DNA damage by elevating free-iron levels. Proceedings of the National Academy of Science USA, 93, 13635–13640.CrossRefGoogle ScholarPubMed
Kibanova, D., Nieto-Camacho, A., & Cervini-Silva, J. (2009). Lipid peroxidation induced by expandable clay minerals. Environmental Science & Technology, 43, 7550–7555.CrossRefGoogle ScholarPubMed
Kim, J., Dong, H., Seabaugh, J., Newell, S. W., & Eberl, D. D. (2004). Role of microbes in the smectite-to-illite reaction. Science, 203, 830–832.CrossRefGoogle Scholar
Kogel, J. E. (2014). Mining and processing kaolin. Elements, 10, 189–193.CrossRefGoogle Scholar
Kohanski, M. A., Dwyer, D. J., Hayete, B., Lawrence, C. A., & Collins, J. J. (2007). A common mechanism of cellular death induced by bactericidal antibiotics. Cell, 130, 797–810.CrossRefGoogle ScholarPubMed
Konhauser, K. O. (2007). Introduction to Geomicrobiology (425 p). Oxford: Blackwell Publishing.Google Scholar
Konhauser, K. O., & Urrutia, M. M. (1999). Bacterial clay authigenesis: a common biogeochemical process. Chemical Geology, 161, 399–413.CrossRefGoogle Scholar
Kostka, J. E., Dalton, D. D., Skelton, H., Dollhopf, S., & Stucki, J. W. (2002). Growth of iron (III)-reducing bacteria on clay minerals as the sole electron acceptor and comparison of growth yields on a variety of oxidized iron forms. Applied Environmental Microbiology, 68, 6256–6262.CrossRefGoogle Scholar
Laufer, B. (1930). Geophagy. Field Museum of Natural History, Chicago, USA, Publication 280, 198 pp.CrossRefGoogle Scholar
Lawton, G., Granville-Chapman, J., & Parker, P. J. (2009). Novel haemostatic dressings. Journal of the Royal Army Medical Corps, 155, 309–314.CrossRefGoogle ScholarPubMed
Lemire, J. A., Harrison, J. J., & Turner, R. J. (2013). Antimicrobial activity of metals: mechanisms, molecular targets and applications. National Review of Microbiology, 11, 371–384.CrossRefGoogle ScholarPubMed
Londoño, S. C., & Williams, L. B. (2016). Unraveling the antibacterial mode of action of a clay from the Colombian Amazon. Environmental Geochemistry and Health, 38, 363–379.CrossRefGoogle ScholarPubMed
Londoño, S. C., Hartnett, H. E., & Williams, L. B. (2017). Antibacterial activity of aluminum in clay from the Colombian Amazon. Environmental Science & Technology, 51, 2401–2408.CrossRefGoogle ScholarPubMed
Ma'or, Z., Henis, Y., Alon, Y., Orlov, E., Sørensen, K. B., & Oren, A. (2006). Antimicrobial properties of Dead Sea black mineral mud. International Journal of Dermatology, 45, 504–511.CrossRefGoogle ScholarPubMed
Maurice, P. A., & Warren, L. A. (2006). Introduction to geomicrobiology: microbial interactions with minerals. In Maurice, P. A. & Warren, L. A. (Eds.), Methods for Study of Microbe-mineral Interactions (Vol. 14, pp. 2–35). Clay Minerals Society Workshop Lectures.Google Scholar
Moore, D. M., & Reynolds, R. C. (1997). X-ray Diffraction and the Identification and Analysis of Clay Minerals (2nd ed. 378 pp). New York: Oxford University Press.Google Scholar
Morrison, K. D., Underwood, J. C., Metge, D. W., Eberl, D. D., & Williams, L. B. (2014). Mineralogical variables that control the antibacterial effectiveness of a natural clay deposit. Environmental Geochemistry and Health, 36, 613–631.CrossRefGoogle ScholarPubMed
Morrison, K. D., Misra, R., & Williams, L. B. (2016). Unearthing the antibacterial mechanismofmedicinal clay: A geochemical approach to combating antibiotic resistance. Nature Scientific Reports, 6, 19043.CrossRefGoogle Scholar
Morrison, K. D., Williams, S. N., & Williams, L. B. (2017). The anatomy of an antibacterial clay deposit: A new economic geology. Economic Geology, 112, 1551–1570.CrossRefGoogle Scholar
Nealson, K. H., Belz, A., & McKee, B. (2002). Breathing metals as a way of life: geobiology in action. Antonie Van Leeuwenhoek International Journal of General and Molecular Microbiology, 81, 215–222.Google Scholar
Nies, D. H. (1999). Microbial heavy-metal resistance. Applied Microbiology and Biotechnology, 51, 730–750.CrossRefGoogle ScholarPubMed
Nunez, J., Renslow, R., Cliff, J. B. III, & Anderton, C. R. (2018). NanoSIMS for biological applications: Current practices and analyses. Biointerphases 03B301, 13, 1–26.Google Scholar
Pearson, R. G. (1966). Acids and bases. Science, 151, 172–177.CrossRefGoogle ScholarPubMed
Potts, R., Behrensmeyer, A. K., Faith, J. T., Tryon, C. A., Brooks, A.S., Yellen, J. E., Deino, A. L., Kinyanjui, R., Clark, J. B., Haradon, C., Levin, N. E., Jeijer, H. H. M., Veatch, E. G., Owen, R. B., & Renaut, R. W. (2018). Environmental dynamics during the onset of the Middle Stone Age in eastern Africa. Science. https://doi.org/10.1126/science.aao2200.CrossRefGoogle Scholar
Radomski, A., Jurasz, P., Alonso-Escolano, D., Drews, M., Morandi, M., Malinski, T., & Radomski, M. W. (2005). Nanoparticle-induced platelet aggregation and vascular thrombosis. British Journal of Pharmacology, 146, 882–893.CrossRefGoogle ScholarPubMed
Raivio, T. L. (2005). Envelope stress responses and Gram-negative bacterial pathogenesis. Molecular Microbiology, 56, 1119–1128.CrossRefGoogle ScholarPubMed
Reinbacher, W. R. (2003). Healing Earths; The Third Leg of Medicine (244 pp). Toronto, Canada: 1st Books Library, York University.Google Scholar
Schoonen, M. A. A., Cohn, C. A., Roemer, E., Laffers, R., Simon, S. R., & O'Riordan, T. (2006). Mineral-induced formation of reactive oxygen species. In Sahai, N. & Schoonen, M. A. A. (Eds.), Medical Mineralogy and Geochemistry (pp. 179–221). Chantilly: Reviews in Mineralogy and Geochemistry, 64, Mineralogical Society of America and Geochemical Society.CrossRefGoogle Scholar
Schoonen, M. A. A., Harrington, A. D., Laffers, R. A., & Strongin, D. R. (2010). Role of hydrogen peroxide and hydroxyl radical in pyrite oxidation by molecular oxygen. Geochimica et Cosmochimica Acta, 74, 4971–4987.CrossRefGoogle Scholar
Sezonov, G., Joseleau-Petit, D., & D'Ari, R. (2007). Escherichia coli physiology in Luria-Bertani broth. Journal of Bacteriology, 189, 8746–8749.CrossRefGoogle ScholarPubMed
Sposito, G. (1980). The operational definition of the zero point of charge in soils. Soil Science Society of America Journal, 45, 292–297.CrossRefGoogle Scholar
Środoń, J., & McCarty, D. K. (2008). Surface area and layer charge of smectite from CEC and EGME/H2O-retention measurements. Clays and Clay Minerals, 56, 155–174.CrossRefGoogle Scholar
Stephens, C. (2002). Microbiology: Breaking down biofilms. Current Biology, 12, R132–R134.CrossRefGoogle ScholarPubMed
Svensson, S. L., Behroozian, S., Xu, W., Surette, M. G., Li, L., & Davies, J. (2017). Kisameet glacial clay: an unexpected source of bacterial diversity. American Society of Microbiology mBio, 8, e00590–e00517.Google ScholarPubMed
Takeno, N. (2005). Atlas of Eh-pH diagrams: Intercomparison of thermodynamic databases. Geological Survey of Japan Open File Report No., 419, 285 pp.Google Scholar
Tateo, F., Ravaglioli, A., Andreoli, C., Bonina, F., Coiro, V., Degetto, S., Giaretta, A., Orsini, A. M., Puglia, C., & Summa, V. (2009). The in-vitro percutaneous migration of chemical elements from a thermal mud for healing use. Applied Clay Science, 44, 83–94.CrossRefGoogle Scholar
Valko, M., Morris, H., & Cronin, M. T. D. (2005). Metals, toxicity and oxidative stress. Current Medicinal Chemistry, 12, 1161–1208.CrossRefGoogle ScholarPubMed
Vermeer, D. E., & Ferrell, R. E. Jr. (1985). Nigerian geophagical clay: a traditional antidiarrheal pharmaceutical. Science, 227, 634–636.CrossRefGoogle Scholar
Walker, S., Flemming, C., Ferris, F., Beveridge, T., & Bailey, G. (1989). Physicochemical interaction of Escherichia coli cell envelopes and Bacillus subtilis cell walls with two clays and ability of the composite to immobilize heavy metals from solution. Applied and Environmental Microbiology, 55, 2976–2984.CrossRefGoogle Scholar
Wang, X., Dong, H., Zeng, Q., Xia, Q., Zhang, L., & Zhou, Z. (2017). Reduced iron-containing clay minerals as antibacterial agents. Environmental Science & Technology, 51, 7639–7647.CrossRefGoogle ScholarPubMed
Williams, R. J. (1999). What is wrong with aluminum? Journal of Inorganic Biochemistry, 76, 81–88.CrossRefGoogle Scholar
Williams, L. B. (2017). Geomimicry: Harnessing the antibacterial action of clays. Clay Minerals, 52, 1–24.CrossRefGoogle Scholar
Williams, L. B., & Haydel, S. E. (2010). Evaluation of the medicinal use of clay minerals as antibacterial agents. International Geology Reviews, 52, 745–770.CrossRefGoogle ScholarPubMed
Williams, L. B., & Hillier, S. (2014). Kaolins and Health: from first grade to first aid. Elements, 10, 207–211.CrossRefGoogle Scholar
Williams, L. B., Holland, M., Eberl, D. D., Brunet, T., & Brunet de Courrsou, L. B. (2004). Killer clays! Natural antibacterial clay minerals. Mineralogical Society Bulletin, 139, 3–8.Google Scholar
Williams, L. B., Haydel, S. E., Giese, R. F., & Eberl, D. D. (2008). Chemical and mineralogical characteristics of French green clays used for healing. Clays and Clay Minerals, 56, 437–452.CrossRefGoogle ScholarPubMed
Williams, L. B., Metge, D. W., Eberl, D. D., Harvey, R. W., Turner, A. G., Prapaipong, P., & Poret-Peterson, A. T. (2011). What makes a natural clay antibacterial? Environmental Science & Technology, 45, 3768–3773.CrossRefGoogle ScholarPubMed
Wilson, M. J. (2003). Clay mineralogical and related characteristics of geophagic materials. Journal of Chemical Ecology, 29, 1525–1547.CrossRefGoogle ScholarPubMed
Wilson, E., Henry, D. A., & Smith, J. A. (1990). Disk elution method for MICs and MBCs. Antimicrobial Agents and Chemotherapy, 34, 2128–2132.CrossRefGoogle ScholarPubMed
Winterbourn, C. C. (1995). Toxicity of iron and hydrogen peroxide: the Fenton reaction. Toxicology Letters, 82-83, 969–974.CrossRefGoogle ScholarPubMed
Winterbourn, C. C. (2008). Reconciling the chemistry and biology of reactive oxygen species. Nature Chemical Biology, 4, 278–286.CrossRefGoogle ScholarPubMed
Young, S. L. (2011). Craving Earth (228 pp). New York: Columbia University Press.CrossRefGoogle ScholarPubMed
Zarate-Reyes, L., Nieto-Camacho, A., Palacios, E., Gomaz-Vidales, V., Kaufhold, S., Ufer, K., Garcia-Zepeda, E., & Cervini-Silva, J. (2017). Antibacterial clay against Gram-negative antibiotic resistant bacteria. Journal of Hazardous Materials, 342, 625–632.CrossRefGoogle ScholarPubMed
Zastawny, T. H., Altman, S. A., Randerseichhorn, L., Madurawe, R., Lumpkin, J. A., Dizdaroglu, M., & Rao, G. (1995). DNA base modifications and membrane damage in cultured mammalian cells treated with iron ions. Free Radical Biology in Medicine, 18, 1013–1022.CrossRefGoogle ScholarPubMed