Supramolecular coordination platinum metallacycle–based multilevel wound dressing for bacteria sensing and wound healing

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Non-healing wounds induced by antibiotic resistance have emerged as serious threats to human health. As promising candidates for the treatment of bacterial infections, metal-organic cycles/cages (MOCs) exhibit excellent antibacterial properties. However, the rational application of nanoscale MOCs has been limited due to difficulties in processability and transferability. To address these problems, a centimeter-scale Pt MOC film was constructed via multistage assembly and improved by coating it on N,N′-dimethylated dipyridinium thiazolo[5,4-d]thiazole (MPT)-stained silk fabric for bacterial sensing and wound healing. The as-prepared multilevel wound dressing enabled the monitoring of wound infection in real time and timely treatment with high spatiotemporal precision.

Abstract

The exploitation of novel wound healing methods with real-time infection sensing and high spatiotemporal precision is highly important for human health. Pt-based metal-organic cycles/cages (MOCs) have been employed as multifunctional antibacterial agents due to their superior Pt-related therapeutic efficiency, various functional subunits and specific geometries. However, how to rationally apply these nanoscale MOCs on the macroscale with controllable therapeutic output is still challenging. Here, a centimeter-scale Pt MOC film was constructed via multistage assembly and subsequently coated on a N,N′-dimethylated dipyridinium thiazolo[5,4-d]thiazole (MPT)-stained silk fabric to form a smart wound dressing for bacterial sensing and wound healing. The MPT on silk fabric could be used to monitor wound infection in real-time through the bacteria-mediated reduction of MPT to its radical form via a color change. The MPT radical also exhibited an excellent photothermal effect under 660 nm light irradiation, which could not only be applied for photothermal therapy but also induce the disassembly of the Pt MOC film suprastructure. The highly ordered Pt MOC film suprastructure exhibited high biosafety, while it also showed improved antibacterial efficiency after thermally induced disassembly. In vitro and in vivo studies revealed that the combination of the Pt MOC film and MPT-stained silk can provide real-time information on wound infection for timely treatment through noninvasive techniques. This study paves the way for bacterial sensing and wound healing with centimeter-scale metal-organic materials.

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Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis

(2022)

Summary Background Antimicrobial resistance (AMR) poses a major threat to human health around the world. Previous publications have estimated the effect of AMR on incidence, deaths, hospital length of stay, and health-care costs for specific pathogen–drug combinations in select locations. To our knowledge, this study presents the most comprehensive estimates of AMR burden to date. Methods We estimated deaths and disability-adjusted life-years (DALYs) attributable to and associated with bacterial AMR for 23 pathogens and 88 pathogen–drug combinations in 204 countries and territories in 2019. We obtained data from systematic literature reviews, hospital systems, surveillance systems, and other sources, covering 471 million individual records or isolates and 7585 study-location-years. We used predictive statistical modelling to produce estimates of AMR burden for all locations, including for locations with no data. Our approach can be divided into five broad components: number of deaths where infection played a role, proportion of infectious deaths attributable to a given infectious syndrome, proportion of infectious syndrome deaths attributable to a given pathogen, the percentage of a given pathogen resistant to an antibiotic of interest, and the excess risk of death or duration of an infection associated with this resistance. Using these components, we estimated disease burden based on two counterfactuals: deaths attributable to AMR (based on an alternative scenario in which all drug-resistant infections were replaced by drug-susceptible infections), and deaths associated with AMR (based on an alternative scenario in which all drug-resistant infections were replaced by no infection). We generated 95% uncertainty intervals (UIs) for final estimates as the 25th and 975th ordered values across 1000 posterior draws, and models were cross-validated for out-of-sample predictive validity. We present final estimates aggregated to the global and regional level. Findings On the basis of our predictive statistical models, there were an estimated 4·95 million (3·62–6·57) deaths associated with bacterial AMR in 2019, including 1·27 million (95% UI 0·911–1·71) deaths attributable to bacterial AMR. At the regional level, we estimated the all-age death rate attributable to resistance to be highest in western sub-Saharan Africa, at 27·3 deaths per 100 000 (20·9–35·3), and lowest in Australasia, at 6·5 deaths (4·3–9·4) per 100 000. Lower respiratory infections accounted for more than 1·5 million deaths associated with resistance in 2019, making it the most burdensome infectious syndrome. The six leading pathogens for deaths associated with resistance (Escherichia coli, followed by Staphylococcus aureus, Klebsiella pneumoniae, Streptococcus pneumoniae, Acinetobacter baumannii, and Pseudomonas aeruginosa) were responsible for 929 000 (660 000–1 270 000) deaths attributable to AMR and 3·57 million (2·62–4·78) deaths associated with AMR in 2019. One pathogen–drug combination, meticillin-resistant S aureus, caused more than 100 000 deaths attributable to AMR in 2019, while six more each caused 50 000–100 000 deaths: multidrug-resistant excluding extensively drug-resistant tuberculosis, third-generation cephalosporin-resistant E coli, carbapenem-resistant A baumannii, fluoroquinolone-resistant E coli, carbapenem-resistant K pneumoniae, and third-generation cephalosporin-resistant K pneumoniae. Interpretation To our knowledge, this study provides the first comprehensive assessment of the global burden of AMR, as well as an evaluation of the availability of data. AMR is a leading cause of death around the world, with the highest burdens in low-resource settings. Understanding the burden of AMR and the leading pathogen–drug combinations contributing to it is crucial to making informed and location-specific policy decisions, particularly about infection prevention and control programmes, access to essential antibiotics, and research and development of new vaccines and antibiotics. There are serious data gaps in many low-income settings, emphasising the need to expand microbiology laboratory capacity and data collection systems to improve our understanding of this important human health threat. Funding Bill & Melinda Gates Foundation, Wellcome Trust, and Department of Health and Social Care using UK aid funding managed by the Fleming Fund.

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Recent Developments in the Preparation and Chemistry of Metallacycles and Metallacages via Coordination.

Timothy R. Cook, Peter Stang (2015)

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Nanomaterial-based therapeutics for antibiotic-resistant bacterial infections

Jessa Marie V. Makabenta, Ahmed Nabawy, Cheng-Hsuan Li … (2020)

Antibiotic-resistant bacterial infections arising from acquired resistance and/or through biofilm formation necessitate the development of innovative 'outside of the box' therapeutics. Nanomaterial-based therapies are promising tools to combat bacterial infections that are difficult to treat, featuring the capacity to evade existing mechanisms associated with acquired drug resistance. In addition, the unique size and physical properties of nanomaterials give them the capability to target biofilms, overcoming recalcitrant infections. In this Review, we highlight the general mechanisms by which nanomaterials can be used to target bacterial infections associated with acquired antibiotic resistance and biofilms. We emphasize design elements and properties of nanomaterials that can be engineered to enhance potency. Lastly, we present recent progress and remaining challenges for widespread clinical implementation of nanomaterials as antimicrobial therapeutics.

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Author and article information

Contributors

Xiao-Qiang Wang

Yao Sun

Peter J. Stang:

ORCID: https://orcid.org/0000-0002-2307-0576

Yan Sun

Journal

Journal ID (nlm-ta): Proc Natl Acad Sci U S A

Journal ID (iso-abbrev): Proc Natl Acad Sci U S A

Journal ID (publisher-id): PNAS

Title: Proceedings of the National Academy of Sciences of the United States of America

Publisher: National Academy of Sciences

ISSN (Print): 0027-8424

ISSN (Electronic): 1091-6490

Publication date (Electronic, pub): 25 March 2024

Publication date (Print, pub): 2 April 2024

Publication date PMC-release: 25 March 2024

Volume: 121

Issue: 14

Electronic Location Identifier: e2318391121

Affiliations

[1] ^aInterdisciplinary Institute of NMR and Molecular Sciences, Key Laboratory of Coal Conversion and New Carbon Materials of Hubei Province, School of Chemistry and Chemical Engineering, Wuhan University of Science and Technology , Wuhan 430081, China

[2] ^bKey Laboratory for Special Functional Materials of Ministry of Education, School of Materials Science and Engineering, Collaborative Innovation Center of Nano Functional Materials and Applications, Henan University , Zhengzhou 450046, China

[3] ^cResearch School of Polymeric Materials, School of Materials Science and Engineering, Jiangsu University , Zhenjiang 212013, China

[4] ^dDepartment of Paediatrics, Ruijin Hospital, School of Medicine, Shanghai Jiao Tong University , Shanghai 200240, China

[5] ^eKey Laboratory of Pesticides and Chemical Biology, Ministry of Education, College of Chemistry, Central China Normal University , Wuhan 430079, China

[6] ^fDepartment of Chemistry, University of Utah , Salt Lake City, UT 84112

Author notes

²To whom correspondence may be addressed. Email: wangxq@ 123456wust.edu.cn , sunyaogbasp@ 123456ccnu.edu.cn , stang@ 123456chem.utah.edu , or elaine.sun@ 123456henu.edu.cn .

Contributed by Peter J. Stang; received November 7, 2023; accepted February 16, 2024; reviewed by Samuel H. Gellman and Karen L. Wooley

¹W.-Z.L., Xiao-Qiang Wang, and L.-R.L. contributed equally to this work.

Author information

Peter J. Stang https://orcid.org/0000-0002-2307-0576

Article

Publisher ID: 202318391

DOI: 10.1073/pnas.2318391121

PMC ID: 10998585

PubMed ID: 38527207

SO-VID: 108c6d25-083d-4b28-ac00-a61338bd0662

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This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY).

History

Date received : 07 November 2023

Date accepted : 16 February 2024

Page count

Pages: 8, Words: 3490

Funding

Funded by: National Natural Science Foundation of China;

Award ID: 51903195

Award Recipient : Xiao Qiang Wang Award Recipient : Yan Sun

Funded by: National Natural Science Foundation of China;

Award ID: 22372055

Award Recipient : Xiao Qiang Wang Award Recipient : Yan Sun

Supramolecular coordination platinum metallacycle–based multilevel wound dressing for bacteria sensing and wound healing

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Most cited references 48

Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis

Recent Developments in the Preparation and Chemistry of Metallacycles and Metallacages via Coordination.

Nanomaterial-based therapeutics for antibiotic-resistant bacterial infections

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