{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,6]],"date-time":"2026-11-06T11:43:22Z","timestamp":1793965402115,"version":"4.8.0"},"reference-count":55,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2023,3,30]],"date-time":"2023-03-30T00:00:00Z","timestamp":1680134400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Deputyship for Research &amp; Innovation, Ministry of Education in Saudi Arabia","award":["IFKSURG-2-490"],"award-info":[{"award-number":["IFKSURG-2-490"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["TropicalMed"],"abstract":"<jats:p>Increasing rates of serious multi-drug resistant (MDR) Pseudomonas aeruginosa infections have been reported globally, including in Saudi Arabia. This retrospective study investigates the epidemiological, microbiological, and clinical characteristics of multi-resistant P. aeruginosa (n3579 clinical isolates) in King Fahad Medical City, Riyadh, Saudi Arabia (2019\u20132021). Information on antimicrobial susceptibility and medical history was collected from the hospital database. P. aeruginosa infections occurred in 55.6% of males and 44.4% of females, and P. aeruginosa was more prevalent in children than in adults. Our analysis showed that P. aeruginosa had the highest sensitivity to amikacin (92.6%) and greatest resistance to aztreonam (29.8%), imipenem (29.5%), ceftazidime (26.1%), meropenem (25.6%), and cefepime (24.3%). MDR and extensively drug resistant (XDR) strains were more prevalent in male than female patients. Female patients showed higher rates of infection with pan-drug resistant (PDR) strains. Respiratory samples contained the majority of resistant isolates. Septic shock and liver disease were strongly correlated with mortality in the ICU patient group after analysing the relative risk associated with mortality. Our study emphasises the threat of multi-resistant P. aeruginosa in Saudi Arabia (and potentially the Middle East) and highlights important sources and contexts of infection that inhibit its effective control and clinical management.<\/jats:p>","DOI":"10.3390\/tropicalmed8040205","type":"journal-article","created":{"date-parts":[[2023,3,30]],"date-time":"2023-03-30T01:05:26Z","timestamp":1680138326000},"page":"205","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":42,"title":["Epidemiological, Microbiological, and Clinical Characteristics of Multi-Resistant Pseudomonas aeruginosa Isolates in King Fahad Medical City, Riyadh, Saudi Arabia"],"prefix":"10.3390","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0001-8594-215X","authenticated-orcid":false,"given":"Taghreed A.","family":"Hafiz","sequence":"first","affiliation":[{"name":"Clinical Laboratory Sciences Department, College of Applied Medical Sciences, King Saud University, Riyadh 12372, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Eman A.","family":"Bin Essa","sequence":"additional","affiliation":[{"name":"Clinical Laboratory Sciences Department, College of Applied Medical Sciences, King Saud University, Riyadh 12372, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah R.","family":"Alharbi","sequence":"additional","affiliation":[{"name":"Clinical Laboratory Sciences Department, College of Applied Medical Sciences, King Saud University, Riyadh 12372, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ahmed S.","family":"Alyami","sequence":"additional","affiliation":[{"name":"Pathology and Clinical Laboratory Medicine, King Fahad Medical City, Riyadh 11525, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zeina S.","family":"Alkudmani","sequence":"additional","affiliation":[{"name":"Clinical Laboratory Sciences Department, College of Applied Medical Sciences, King Saud University, Riyadh 12372, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Murad A.","family":"Mubaraki","sequence":"additional","affiliation":[{"name":"Clinical Laboratory Sciences Department, College of Applied Medical Sciences, King Saud University, Riyadh 12372, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-0608-4797","authenticated-orcid":false,"given":"Norah A.","family":"Alturki","sequence":"additional","affiliation":[{"name":"Clinical Laboratory Sciences Department, College of Applied Medical Sciences, King Saud University, Riyadh 12372, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fawzia","family":"Alotaibi","sequence":"additional","affiliation":[{"name":"Pathology Department, College of Medicine, King Saud University, Riyadh 12372, Saudi Arabia"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,3,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"217","DOI":"10.3390\/life4020217","article-title":"Horizontal gene transfer among bacteria and its role in biological evolution","volume":"4","author":"Arber","year":"2014","journal-title":"Life"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1475","DOI":"10.1513\/AnnalsATS.201906-459OC","article-title":"Definitive and indeterminate Pseudomonas aeruginosa infection in adults with community-acquired pneumonia: A prospective observational study","volume":"18","author":"Sando","year":"2021","journal-title":"Ann. Am. Thorac. Soc."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1701190","DOI":"10.1183\/13993003.01190-2017","article-title":"Burden and risk factors for Pseudomonas aeruginosa community-acquired pneumonia: A multinational point prevalence study of hospitalised patients","volume":"52","author":"Restrepo","year":"2018","journal-title":"Eur. Respir.J."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"242","DOI":"10.1186\/cc11421","article-title":"Year in review 2011: Critical care\u2013infection","volume":"16","author":"Afshari","year":"2012","journal-title":"Crit. Care"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"39","DOI":"10.3389\/fcimb.2017.00039","article-title":"Pseudomonas aeruginosa Lifestyle: A Paradigm for Adaptation, Survival, and Persistence","volume":"7","author":"Moradali","year":"2017","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e00031-19","DOI":"10.1128\/CMR.00031-19","article-title":"Epidemiology and Treatment of Multidrug-Resistant and Extensively Drug-Resistant Pseudomonas aeruginosa Infections","volume":"32","author":"Horcajada","year":"2019","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"de Sousa, T., H\u00e9braud, M., Dapkevicius, M.L., Maltez, L., Pereira, J.E., Capita, R., Alonso-Calleja, C., Igrejas, G., and Poeta, P. (2021). Genomic and Metabolic Characteristics of the Pathogenicity in Pseudomonas aeruginosa. Int. J. Mol. Sci., 22.","DOI":"10.3390\/ijms222312892"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1038\/s41598-018-37422-9","article-title":"Virulence characteristics and an action mode of antibiotic resistance in multidrug-resistant Pseudomonas aeruginosa","volume":"9","author":"Hwang","year":"2019","journal-title":"Sci. Rep."},{"key":"ref_9","unstructured":"European Centre for Disease Prevention and Control (2022). Antimicrobial Resistance in the EU\/EEA (EARS-Net)\u2014Annual Epidemiological Report 2021."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"155","DOI":"10.4103\/0974-777X.192962","article-title":"Prevalence of multidrug-resistant, extensively drug-resistant, and pandrug-resistant Pseudomonas aeruginosa from a tertiary level intensive care unit","volume":"8","author":"Gill","year":"2016","journal-title":"J. Glob. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","unstructured":"Morales, E., Cots, F., Sala, M., Comas, M., Belvis, F., Riu, M., Salvad\u00f3, M., Grau, S., Horcajada, J.P., and Montero, M.M. (2012). Hospital costs of nosocomial multi-drug resistant Pseudomonas aeruginosa acquisition. BMC Health Serv. Res., 12.","DOI":"10.1186\/1472-6963-12-122"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"949","DOI":"10.1002\/phar.1636","article-title":"Infections caused by resistant gram-negative bacteria: Epidemiology and management","volume":"35","author":"Kaye","year":"2015","journal-title":"Pharmacother. J. Hum. Pharmacol. Drug Ther."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"152","DOI":"10.1016\/j.jiph.2020.11.010","article-title":"Risk factors, antimicrobial susceptibility pattern and patient outcomes of Pseudomonas aeruginosa infection: A matched case-control study","volume":"14","author":"Alhussain","year":"2021","journal-title":"J. Infect. Public Health"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1035","DOI":"10.15537\/smj.2018.10.22944","article-title":"High antimicrobial resistant rates among gram-negative pathogens in intensive care units: A retrospective study at a tertiary care hospital in Southwest Saudi Arabia","volume":"39","author":"Ibrahim","year":"2018","journal-title":"Saudi Med.J."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13756-018-0370-9","article-title":"Risk factors for hospitalized patients with resistant or multidrug-resistant Pseudomonas aeruginosa infections: A systematic review and meta-analysis","volume":"7","author":"Raman","year":"2018","journal-title":"Antimicrob. Resist. Infect. Control"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1244","DOI":"10.1093\/jac\/dkz030","article-title":"High incidence of MDR and XDR Pseudomonas aeruginosa isolates obtained from patients with ventilator-associated pneumonia in Greece, Italy and Spain as part of the MagicBullet clinical trial","volume":"74","author":"Gato","year":"2019","journal-title":"J. Antimicrob.Chemother."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"154149","DOI":"10.1016\/j.jcrc.2022.154149","article-title":"Risk factors for mortality in ICU patients in 10 middle eastern countries: The role of healthcare-associated infections","volume":"72","author":"Rosenthal","year":"2022","journal-title":"J. Crit. Care"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"2506","DOI":"10.3390\/microorganisms10122506","article-title":"Stenotrophomonas maltophilia Epidemiology, Resistance Characteristics, and Clinical Outcomes: Understanding of the Recent Three Years&rsquo; Trends","volume":"10","author":"Hafiz","year":"2022","journal-title":"Microorganisms"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1111\/j.1469-0691.2011.03570.x","article-title":"Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance","volume":"18","author":"Magiorakos","year":"2012","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1186\/s13054-015-0926-5","article-title":"An international multicenter retrospective study of Pseudomonas aeruginosa nosocomial pneumonia: Impact of multidrug resistance","volume":"19","author":"Micek","year":"2015","journal-title":"Crit. Care"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1179\/1973947814Y.0000000185","article-title":"Prevalence and antimicrobial resistance among Gram-negative pathogens in Saudi Arabia","volume":"26","author":"Yezli","year":"2014","journal-title":"J. Chemother."},{"key":"ref_22","first-page":"2","article-title":"Incidence and antibiotic susceptibility pattern of pseudomonas aeruginosa isolated from inpatients in two Tertiary Hospitals","volume":"5","author":"Ahmed","year":"2016","journal-title":"Clin. Microbiol. Open Access"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"e00202-21","DOI":"10.1128\/mSphere.00202-21","article-title":"Epidemiology of Multidrug-Resistant Pseudomonas aeruginosa in the Middle East and North Africa Region","volume":"6","author":"Hadi","year":"2021","journal-title":"Msphere"},{"key":"ref_24","doi-asserted-by":"crossref","unstructured":"Tiri, B., Sensi, E., Marsiliani, V., Cantarini, M., Priante, G., Vernelli, C., Martella, L.A., Costantini, M., Mariottini, A., and Andreani, P. (2020). Antimicrobial Stewardship Program, COVID-19, and Infection Control: Spread of Carbapenem-Resistant Klebsiella Pneumoniae Colonization in ICU COVID-19 Patients. What Did Not Work?. J. Clin. Med., 9.","DOI":"10.3390\/jcm9092744"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"31","DOI":"10.24018\/ejmed.2021.3.5.1047","article-title":"Prevalence of Antimicrobial Resistance of Common Bacterial Isolates before and during COVID-19 Pandemic in Armed Forces Hospital Jazan, Saudi Arabia","volume":"3","author":"AlDiba","year":"2021","journal-title":"Eur. J. Med. Health Sci."},{"key":"ref_26","unstructured":"Centers for Disease, National Center for Emerging and Zoonotic Infectious Diseases, and Division of Healthcare Quality Promotion (2022). COVID-19: U.S. Impact on Antimicrobial Resistance, Special Report 2022."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1556\/EuJMI.1.2011.3.2","article-title":"Taking stock of infections and antibiotic resistance in the elderly and long-term care facilities: A survey of existing and upcoming challenges","volume":"1","author":"Augustine","year":"2011","journal-title":"Eur. J. Microbiol. Immunol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"e00283-22","DOI":"10.1128\/iai.00283-22","article-title":"Sex and Gender Differences in Bacterial Infections","volume":"90","author":"Dias","year":"2022","journal-title":"Infect. Immun."},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"McGregor, J.C., Elman, M.R., Bearden, D.T., and Smith, D.H. (2013). Sex- and age-specific trends in antibiotic resistance patterns of Escherichia coli urinary isolates from outpatients. BMC Fam. Pract., 14.","DOI":"10.1186\/1471-2296-14-25"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"201","DOI":"10.22207\/JPAM.13.1.21","article-title":"Prevalence and Antibiotic Susceptibility among Gram Negative Bacteria Isolated from Intensive Care Units at a Tertiary Care Hospital in Riyadh, Saudi Arabia","volume":"13","author":"Azim","year":"2019","journal-title":"J. Pure Appl. Microbiol."},{"key":"ref_31","first-page":"2164","article-title":"In vitro activity of ceftolozane\/tazobactam alone and in combination with amikacin against MDR\/XDR Pseudomonas aeruginosa isolates from Greece","volume":"75","author":"Galani","year":"2020","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1825","DOI":"10.1093\/jac\/dkz147","article-title":"Spanish nationwide survey on Pseudomonas aeruginosa antimicrobial resistance mechanisms and epidemiology","volume":"74","author":"Zamorano","year":"2019","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_33","first-page":"3","article-title":"Surveillance of antimicrobial resistance among clinical isolates recovered from a tertiary care hospital in Al Qassim, Saudi Arabia","volume":"8","author":"Said","year":"2014","journal-title":"Int. J. Health Sci."},{"key":"ref_34","first-page":"2276","article-title":"Public knowledge, attitude and practice towards antibiotics use and antimicrobial resistance in Saudi Arabia: A web-based cross-sectional survey","volume":"10","author":"Albrahim","year":"2021","journal-title":"J. Public Health Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"4155","DOI":"10.3389\/fmicb.2021.765113","article-title":"Genomic Characterization of Carbapenem-Non-susceptible Pseudomonas aeruginosa Clinical Isolates From Saudi Arabia Revealed a Global Dissemination of GES-5-Producing ST235 and VIM-2-Producing ST233 Sub-Lineages","volume":"12","author":"Doumith","year":"2022","journal-title":"Front. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"3386","DOI":"10.1093\/jac\/dkaa326","article-title":"Antibiotic use in patients with COVID-19: A \u2018snapshot\u2019 Infectious Diseases International Research Initiative (ID-IRI) survey","volume":"75","author":"Nadrah","year":"2020","journal-title":"J. Antimicrob. Chemother."},{"key":"ref_37","doi-asserted-by":"crossref","unstructured":"Codjoe, F.S., and Donkor, E.S. (2018). Carbapenem Resistance: A Review. Med.Sci., 6.","DOI":"10.3390\/medsci6010001"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"e379","DOI":"10.1016\/S1473-3099(18)30414-6","article-title":"Epidemiology of common resistant bacterial pathogens in the countries of the Arab League","volume":"18","author":"Moghnieh","year":"2018","journal-title":"Lancet Infect. Dis."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"465","DOI":"10.1016\/j.jiph.2019.03.024","article-title":"Carbapenem-Resistant Enterobacteriaceae: An update narrative review from Saudi Arabia","volume":"12","author":"Alotaibi","year":"2019","journal-title":"J. Infect. Public Health"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1086\/429323","article-title":"Colistin: The revival of polymyxins for the management of multidrug-resistant gram-negative bacterial infections","volume":"40","author":"Falagas","year":"2005","journal-title":"Clin. Infect. Dis."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1261","DOI":"10.2147\/IDR.S170233","article-title":"Carbapenem-resistant Acinetobacter baumannii and Pseudomonas aeruginosa: Characterization of carbapenemase genes and E-test evaluation of colistin-based combinations","volume":"11","author":"Ramadan","year":"2018","journal-title":"Infect. Drug Resist."},{"key":"ref_42","first-page":"1341","article-title":"Antimicrobial-resistant bacteria in a general intensive care unit in Saudi Arabia","volume":"31","author":"Saeed","year":"2010","journal-title":"Saudi Med. J."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"103227","DOI":"10.1016\/j.iccn.2022.103227","article-title":"Healthcare-associated infections in adult intensive care unit patients: Changes in epidemiology, diagnosis, prevention and contributions of new technologies","volume":"70","author":"Blot","year":"2022","journal-title":"Intensive Crit. Care Nurs."},{"key":"ref_44","unstructured":"European Centre for Disease Prevention and Control (2019). Healthcare-Associated Infections Acquired in Intensive Care Units, ECDC. Annual Epidemiological Report for 2017."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"1134","DOI":"10.1016\/j.jiph.2020.03.012","article-title":"Six-year multicenter study on short-term peripheral venous catheters-related bloodstream infection rates in 246 intensive units of 83 hospitals in 52 cities of 14 countries of Middle East: Bahrain, Egypt, Iran, Jordan, Kingdom of Saudi Arabia, Kuwait, Lebanon, Morocco, Pakistan, Palestine, Sudan, Tunisia, Turkey, and United Arab Emirates-International Nosocomial Infection Control Consortium (INICC) findings","volume":"13","author":"Rosenthal","year":"2020","journal-title":"J. Infect. Public Health"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"e696","DOI":"10.1016\/j.ijid.2013.02.004","article-title":"Acinetobacter is the most common pathogen associated with late-onset and recurrent ventilator-associated pneumonia in an adult intensive care unit in Saudi Arabia","volume":"17","author":"Balkhy","year":"2013","journal-title":"Int. J. Infect. Dis."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e179","DOI":"10.1016\/S2666-5247(22)00355-X","article-title":"Antimicrobial resistance in patients with COVID-19: A systematic review and meta-analysis","volume":"4","author":"Langford","year":"2023","journal-title":"Lancet Microbe"},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Kabrah, A., Bahwerth, F., Alghamdi, S., Alkhotani, A., Alahmadi, A., Alhuzali, M., Aljerary, I., and Alsulami, A. (2022). Antibiotics Usage and Resistance among Patients with Severe Acute Respiratory Syndrome Coronavirus 2 in the Intensive Care Unit in Makkah, Saudi Arabia. Vaccines, 10.","DOI":"10.3390\/vaccines10122148"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1080\/14787210.2017.1367666","article-title":"Management of multidrug-resistant Pseudomonas aeruginosa in the intensive care unit: State of the art","volume":"15","author":"Maraolo","year":"2017","journal-title":"Expert Rev. Anti Infect. Ther."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"601","DOI":"10.1097\/01.ccm.0000435665.07446.50","article-title":"Prevalence, Risk Factors, and Mortality for Ventilator-Associated Pneumonia in Middle-Aged, Old, and Very Old Critically Ill Patients*","volume":"42","author":"Blot","year":"2014","journal-title":"Crit. Care Med."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"104","DOI":"10.4103\/1817-1737.128858","article-title":"Drug-resistant ventilator associated pneumonia in a tertiary care hospital in Saudi Arabia","volume":"9","author":"Balkhy","year":"2014","journal-title":"Ann. Thorac. Med."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1128\/AAC.50.1.43-48.2006","article-title":"Multidrug-resistant Pseudomonas aeruginosa: Risk factors and clinical impact","volume":"50","author":"Aloush","year":"2006","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"498","DOI":"10.3109\/08830185.2014.889129","article-title":"The role of the liver in sepsis","volume":"33","author":"Yan","year":"2014","journal-title":"Int. Rev. Immunol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1016\/j.cmi.2020.12.018","article-title":"Antibiotic prescribing in patients with COVID-19: Rapid review and meta-analysis","volume":"27","author":"Langford","year":"2021","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"101848","DOI":"10.1016\/j.eclinm.2023.101848","article-title":"Global antibiotic use during the COVID-19 pandemic: Analysis of pharmaceutical sales data from 71 countries, 2020\u20132022","volume":"57","author":"Nandi","year":"2023","journal-title":"Eclinicalmedicine"}],"container-title":["Tropical Medicine and Infectious Disease"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2414-6366\/8\/4\/205\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:06:39Z","timestamp":1760123199000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2414-6366\/8\/4\/205"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,30]]},"references-count":55,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["tropicalmed8040205"],"URL":"https:\/\/doi.org\/10.3390\/tropicalmed8040205","relation":{},"ISSN":["2414-6366"],"issn-type":[{"value":"2414-6366","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,3,30]]}}}