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Preliminary Evaluation of Natural Antibacterial Clays for Treating Wound Infections

Published online by Cambridge University Press:  01 January 2024

Lynda B. Williams Open the ORCID record for Lynda B. Williams [Opens in a new window] ,
Suzannah M. Schmidt-Malan  and
Robin Patel
Lynda B. Williams*
Affiliation:
School of Earth and Space Exploration, Arizona State University, Tempe, AZ 85287, USA
Suzannah M. Schmidt-Malan
Affiliation:
Division of Clinical Microbiology, Dept. of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN 55905, USA
Robin Patel
Affiliation:
Division of Clinical Microbiology, Dept. of Laboratory Medicine and Pathology, Mayo Clinic, Rochester, MN 55905, USA Division of Infectious Diseases, Dept. of Medicine, Mayo Clinic, Rochester, MN 55905, USA
*
*E-mail address of corresponding author: lynda.williams@asu.edu
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Abstract

The overuse of antibiotics in medicine has led to concerns over management of wound infections where antibiotic-resistant bacteria are involved. Wound infections exhibit both acquired and biofilm-associated antibiotic resistance; innovative non-antibiotic therapeutic and preventive treatments are needed to limit emergence of conventional antimicrobial resistance and to address biofilm-associated resistance. Toward this goal, natural antibacterial clays have been identified that are effective at killing drug-resistant human pathogens in planktonic and biofilm states, in vitro. To move toward clinical testing of antibacterial clays, the present study was conducted to evaluate the topical application of a natural antibacterial clay to wounds in mice experimentally infected with methicillin-resistant Staphylococcus aureus (MRSA). Five preliminary animal trials were conducted to test various methods of applying hydrated antibacterial clay to infected wounds. None of the experiments yielded significantly reduced MRSA infection in vivo, compared to controls. Several hypotheses were tested to explore the diminished clay antibacterial activity in vivo including: (1) pH and Eh of mineral-bacterial suspensions may differ in wound fluids compared to growth media; (2) antibacterial reactants may complex with components of the wound; (3) hydrated clays may dry out in the wound; and (4) limited dissolved oxygen may reduce Fenton reactions. Ancillary in vitro tests were performed to explore these hypotheses. Results indicate that the clay application to wounds may require enhanced oxidation and possibly a longer treatment regimen. The experimental results foster understanding of the natural clay–bacterial interactions in wounds and may improve designs for medicinal applications.

Keywords

Animal testingAntibacterial clayMRSAReduced iron mineralsWound infections
Type
Article
Information
Clays and Clay Minerals , Volume 69 , Issue 5: Clay Minerals in Health Applications , October 2021 , pp. 589 - 602
Copyright
Copyright © The Clay Minerals Society 2021

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Footnotes

This paper belongs to a special issue on ‘Clay Minerals in Health Applications’

References

Behroozian, S., Svensson, S. L., Li, L. Y., & Davies, J. E. (2020). Broad-spectrum antimicrobial and antibiofilm activity of a natural clay mineral from British Columbia. Canada. mBio, 11, e02350–e02320. https://doi.org/10.1128/mBio.02350-20Google ScholarPubMed
Caflisch, K.M., Schmidt-Malan, S.M., Mandrekar, J.N., Karau, M.J., Nicklas, J.P., Williams, L.B., & Patel, R. (2018). Antibacterial activity of reduced iron clay against pathogenic bacteria from wound infections. International Journal of Antimicrobial Agents, 52, 692–696.CrossRefGoogle ScholarPubMed
Cervini-Silva, J., Nieto-Camacho, A., Ramirez-Apan, M. T., Gomez-Vidales, V., Palacios, E., Montoya, A., & Ronquillo de Jesus, E. (2015). Anti-inflammatory, anti-bacterial and cytotoxic activity of fibrous clays. Colloids and Surfaces B: Biointerfaces, 129, 1–6.CrossRefGoogle ScholarPubMed
Darder, M., Colilla, M., & Ruiz-Hitzky, E. (2003). Biopolymer-clay nanocomposites based on chitosan intercalated in montmorillonite. Chemical Materials, 15, 3774–3780.CrossRefGoogle Scholar
Dong, H. (2012). Clay–microbe interactions and implications for environmental mitigation. Elements, 8, 113–118.CrossRefGoogle Scholar
Eberl, D.D. (2007). User's guide to RockJock: A program for determining quantitative mineralogy from powder X-ray diffraction data. U.S. Geological Survey, Open-file report 03–78. 48 pp.Google Scholar
Fomina, M., & Skorochod, I. (2020). Microbial interaction with clay minerals and its environmental and biotechnological implications. Minerals, 10, 861. https://doi.org/10.3390/min10100861CrossRefGoogle Scholar
Garcia-Villén, F., Souza, I. M. S., Barbosa, R. M., Borrego-Sánchez, A., Sámcjez-Espejo, R., Ojeda-Riascos, S., & Iborra, C. V. (2020). Natural inorganic ingredients in wound healing. Current Pharmaceutical Design, 26, 621–641.CrossRefGoogle ScholarPubMed
Gomes, C., Rautureau, M., Niel, J., & Gomes, J. (2021). Clay and clay mineral benefits and risks on human health from ancestral to current time: A synoptic overview. Clays and Clay Minerals (in press).CrossRefGoogle Scholar
Haque, S., Nasar, A., & Inamuddin, A. M. A. (2018). Montmorillonite clay nanocomposites for drug delivery. In Inamuddin, A. M. A. & Ali, M. (Eds.), Applications of Nanocomposite Materials in Drug Delivery. Woodhead Publishing Series in Biomaterials. https://doi.org/10.1016/B978-0-12-813741-3.00039-XGoogle Scholar
Haydel, S. E., Remenih, C. M., & Williams, L. B. (2008). Broadspectrum in vitro antibacterial activities of clay minerals against antibiotic-susceptible and antibiotic-resistant bacterial pathogens. Journal of Antimicrobial Chemotherapy, 61353–61361.Google Scholar
Imlay, J. A. (2019). Where in the world do bacteria experience oxidative stress? Environmental Microbiology, 21(2), 521–530.CrossRefGoogle Scholar
Jaisi, D. P., Dong, H., Kim, J. W., He, Z., & Morton, J. P. (2007). Nontronite particle aggregation induced by microbial Fe (III). reduction and exopolysaccharide production. Clays and Clay Minerals, 55, 96–107.CrossRefGoogle Scholar
Kim, C. K., Karau, M. J., Greenwood-Quaintance, K. E., Tilahun, A. Y., Krogman, A., David, C. S., Pritt, B. S., Patel, R., & Rajagopalan, G. (2015). Superantigen-producing Staphylococcus aureus elicits systemic immune activation in a murine wound colonization model. Toxins (Basel), 7, 5308–5319 PMCID: PMC 4690136.CrossRefGoogle Scholar
Komadel, P., Madejová, J., & Stucki, J. W. (1999). Partial stabilization of Fe (II) in reduced ferruginous smectite by Li fixation. Clays and Clay Minerals, 47, 458–465.CrossRefGoogle Scholar
Li, G. L., Zhou, C. H., Fiore, S., & Yu, W. H. (2019). Interactions between microorganisms and clay minerals: New insights and broader applications. Applied Clay Science, 177, 91–113.CrossRefGoogle Scholar
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(2), 363–379. https://doi.org/10.1007/s10653-015-9723-yCrossRefGoogle ScholarPubMed
Londoño, S. C., Hartnett, H., & Williams, L. B. (2017). The antibacterial activity of aluminum in clay from the Colombian Amazon. Environmental Science and Technology, 51, 2401–2408. https://doi.org/10.1021/acs.est.6b04670CrossRefGoogle ScholarPubMed
Marks, H., Bucknor, A., Roussakis, E., Nowell, N., Kamali, P., Cascales, J. P., Kazei, D., Lin, S. J., & Evans, C. L. (2020). A paintable phosphorescent bandage for postoperative tissue oxygen assessment in DIEP flap reconstruction. Science Advances, 6, eabd1061.CrossRefGoogle ScholarPubMed
Miller, M. B., & Bassler, B. L. (2001). Quorum sensing in bacteria. Annual Review of Microbiology, 55, 165–199. https://doi.org/10.1146/annurev.micro.55.1.165CrossRefGoogle ScholarPubMed
Moore, D. M., & Reynolds, R. C. (1997). X-ray Diffraction and the Identification and Analysis of Clay Minerals (2nd ed.). 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(4), 613–631.CrossRefGoogle ScholarPubMed
Morrison, K. D., Misra, R., & Williams, L. B. (2016). Unearthing the antibacterial mechanism of medicinal clay: A geochemical approach to combating antibiotic resistance. Nature Scientific Reports, 5, 19043. https://doi.org/10.1038/srep19043CrossRefGoogle 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(7), 1551–1570. https://doi.org/10.5382/econgeo.2017.4521CrossRefGoogle Scholar
Müller, B. (2015). Experimental interactions between clay minerals and bacteria: A review. Pedosphere, 25(6), 799–810.CrossRefGoogle Scholar
Naik, S. P., Sjolin, J., Ching, S., Chi, F., & Herpfer, M. (2018). Quorum sensing disruption in Vibrio harveyi bacteria by clay minerals. Journal of Agricultural and Food Chemistry, 66, 40–44.CrossRefGoogle Scholar
Naylor, N. R., Atun, R., Zhu, N., Kulasabanathan, K., Silva, S., Chatterjee, A., Knight, G. M., & Robotham, J. V. (2018). Estimating the burden of antimicrobial resistance: A systematic literature review. Antimicrobial Resistance and Infection Control, 7, 58. https://doi.org/10.1186/s13756-018-0336-yCrossRefGoogle ScholarPubMed
Ochoa, M., Rahimi, R., Zhou, J., & others, many. (2020). Integrated sensing and delivery of oxygen for next-generation smart wound dressings. Microsystems & Nanoengineering, 6, 46. https://doi.org/10.1038/s41378-020-0141-7CrossRefGoogle ScholarPubMed
Otto, C. C., Kilbourne, J., & Haydel, S. E. (2016). Natural and ionexchanged illite clays reduce bacterial burden and inflammation in cutaneous methicillin-resistant Staphylococcus aureus infections in mice. Journal of Medical Microbiology, 65, 19–27.CrossRefGoogle ScholarPubMed
Photos-Jones, E., & Hall, A. J. (2011). Lemnian Earth and the earths of the Aegean, an archaeological guide to medicines, pigments and washing powders (p. 129). Potingair Press, Glasgow, UKGoogle Scholar
Silhavy, T. J., Kahne, D., & Walker, S. (2010). The bacterial cell envelope. Cold Springs Harbor. Perspectives in Biology, 2010(2), a000414.Google Scholar
Sirvio, L. M., & Grussing, D. M. (1989). The effect of gas permeability of film dressings on wound environment and healing. The Journal of Investigative Dermatology, 93(4), 528–531. https://doi.org/10.1016/B978-1-78242-456-7.00019-2CrossRefGoogle ScholarPubMed
Valko, M., Morris, H., & Cronin, M. T. D. (2005). Metals, toxicity, and oxidative stress. Current Medicinal Chemistry, 12, 1161–1208.CrossRefGoogle ScholarPubMed
Wang, X., Dong, H., Zeng, Q., Xia, Q., Zhang, L., & Zhou, Z. (2017). Reduced iron-containing clay minerals as antibacterial agents. Environmental Science and Technology, 51, 7639–7647.CrossRefGoogle ScholarPubMed
Werthén, M., Henriksson, L., Jensen, P., Sternberg, C., Givskov, M., & Bjarnholt, T. (2010). An in vitro model of bacterial infections in wounds and other soft tissues. Journal of Pathology, Microbiology and Immunology, 118, 156164. https://doi.org/10.1111/j.1600-0463.2009.02580.xGoogle Scholar
WHO (World Health Organization). (2019). IACG Interagency Coordination Group on Antimicrobial Resistance report to the Secretary General of the United Nations, No time to wait: Securing the future from drug-resistant infections. 25 pp. https://www.who.int/antimicrobial-resistance/interagency-coordination-group/final-report/en/Google Scholar
Williams, L. B. (2019). Natural antibacterial clays: Historical uses and modern advances. Clays and Clay Minerals, 67, 7–24.CrossRefGoogle Scholar
Williams, L. B. (2021). Antibacterial Clays: Scientific investigation of their practical applications in medicine. Chapter 20. In Finkelman, R., Seigel, M., & Selinus, O. (Eds.), Practical Applications of Medical Geology (pp. 671–696. ISBN 978-3-030-53892-7). Springer. https://doi.org/10.1007/978-3-030-53893-4_20CrossRefGoogle Scholar
Williams, L. B., & Haydel, S. E. (2010). Evaluation of the medicinal use of clay minerals as antibacterial agents. International Geology Review, 52(7/8), 745–770.CrossRefGoogle ScholarPubMed
Williams, L. B., Holland, M., Eberl, D. D., Brunet, T., & Brunet de Courssou, L. (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., Haydel, S. E., & Ferrell, R. E. (2009). Bentonites, bandaids and borborygmi. Elements, 5(2), 99–102.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 natural clays antibacterial? Environmental Science and Technology, 45, 3768–3773.CrossRefGoogle ScholarPubMed
Winterbourn, C. C. (2008). Reconciling the chemistry and biology of reactive oxygen species. Nature Chemical Biology, 4, 278–286.CrossRefGoogle ScholarPubMed
Xia, Q., Wang, X., Zeng, Q., Guo, D., Zhu, Z., Chen, H., & Dong, H. (2020). Mechanisms of enhanced antibacterial activity by reduced chitosan-intercalated nontronite. Environmental Science and Technology, 54, 5207–5217.CrossRefGoogle ScholarPubMed
Yuan, G., & Xiong, Y. (2017). Characterizing the surface charge of clay minerals with Atomic Force Microscopy (AFM). AIMS Materials Science, 4(3), 582–593. https://doi.org/10.3934/matersci.2017.3.582Google Scholar
Zhao, H., Bhattacharjee, S., Chow, R., Wallace, D., Maslinyah, J. H., & Xu, Z. (2008). Probing surface charge potentials of clay basal planes and edges by direct force measurements. Langmuir, 24, 12899–12910. https://doi.org/10.1021/la802112hCrossRefGoogle ScholarPubMed