Antimicrobial resistance (AMR) is one of the biggest threats to human health worldwide. The World Health Organization (WHO, Geneva, Switzerland) has launched the "One-Health" approach, which encourages assessment of antibiotic-resistant genes (ARGs) within environments shared by human-animals-plants-microbes to constrain and alleviate the development of AMR. Aerosols as a medium to disseminate ARGs, have received minimal attention. In the present study, we investigated the distribution and abundance of ARGs in indoor and outdoor aerosols collected from an urban location in Kuwait and the interior of three hospitals. The high throughput quantitative polymerase chain reaction (HT-qPCR) approach was used for this purpose. The results demonstrate the presence of aminoglycoside, beta-lactam, fluoroquinolone, tetracycline, macrolide-lincosamide-streptogramin B (MLSB), multidrug-resistant (MDR) and vancomycin-resistant genes in the aerosols. The most dominant drug class was beta-lactam and the genes were IMP-2-group (0.85), Per-2 group (0.65), OXA-54 (0.57), QnrS (0.50) and OXA-55 (0.55) in the urban non-clinical settings. The indoor aerosols possessed a richer diversity (Observed, Chao1, Shannon's and Pielou's evenness) of ARGs compared to the outdoors. Seasonal variations (autumn vs. winter) in relative abundances and types of ARGs were also recorded (R2 of 0.132 at p < 0.08). The presence of ARGs was found in both the inhalable (2.1 µm, 1.1 µm, 0.7 µm and < 0.3 µm) and respirable (>9.0 µm, 5.8 µm, 4.7 µm and 3.3 µm) size fractions within hospital aerosols. All the ARGs are of pathogenic bacterial origin and are hosted by pathogenic forms. The findings present baseline data and underpin the need for detailed investigations looking at aerosol as a vehicle for ARG dissemination among human and non-human terrestrial biota.
Keywords: HT-qPCR; antibiotic-resistant bacteria; antibiotics; human pathogens; molecular methods.
Shen C, Zhang JH, Liu JL, Han XN, Shang TH, Dai JX.Huan Jing Ke Xue. 2022 Aug 8;43(8):4166-4178. doi: 10.13227/j.hjkx.202111088.PMID: 35971714 Chinese.
Szekeres E, Chiriac CM, Baricz A, Szőke-Nagy T, Lung I, Soran ML, Rudi K, Dragos N, Coman C.Environ Pollut. 2018 May;236:734-744. doi: 10.1016/j.envpol.2018.01.107. Epub 2018 Feb 15.PMID: 29454283
Wei N, Lu J, Dong Y, Li S.mSystems. 2022 Aug 30;7(4):e0003722. doi: 10.1128/msystems.00037-22. Epub 2022 Aug 1.PMID: 35913190 Free PMC article. Review.
Kim D.-W., Cha C.-J. Antibiotic resistome from the One-Health perspective: Understanding and controlling antimicrobial resistance transmission. Exp. Mol. Med. 2021;53:301–309. doi: 10.1038/s12276-021-00569-z. - DOI - PMC - PubMed
Zhou Z.-C., Shuai X.-Y., Lin Z.-J., Liu Y., Zhu L., Chen H. Prevalence of multi-resistant plasmids in hospital inhalable particulate matter (PM) and its impact on horizontal gene transfer. Environ. Pollut. 2021;270:116296. doi: 10.1016/j.envpol.2020.116296. - DOI - PubMed
Desai B.H. 14. United Nations Environment Program (UNEP) Yearb. Int. Environ. Law. 2017;28:498–505. doi: 10.1093/yiel/yvy072. - DOI
World Health Organization . Antimicrobial Resistance: Global Report on Surveillance. World Health Organization; Geneva, Switzerland: 2014.
Xu H., Chen Z., Huang R., Cui Y., Li Q., Zhao Y., Wang X., Mao D., Luo Y., Ren H. Antibiotic resistance gene-carrying plasmid spreads into the plant endophytic bacteria using soil bacteria as carriers. Environ. Sci. Technol. 2021;55:10462–10470. doi: 10.1021/acs.est.1c01615. - DOI - PubMed
Xu Y., Li H., Shao Z., Li X., Zheng X., Xu J. Fate of antibiotic resistance genes in farmland soil applied with three different fertilizers during the growth cycle of pakchoi and after harvesting. J. Environ. Manag. 2021;289:112576. doi: 10.1016/j.jenvman.2021.112576. - DOI - PubMed
Wu J., Wang J., Li Z., Guo S., Li K., Xu P., Ok Y.S., Jones D.L., Zou J. Antibiotics and antibiotic resistance genes in agricultural soils: A systematic analysis. Crit. Rev. Environ. Sci. Technol. 2023;53:847–864. doi: 10.1080/10643389.2022.2094693. - DOI
Habibi N., Uddin S., Lyons B., Al-Sarawi H.A., Behbehani M., Shajan A., Razzack N.A., Zakir F., Alam F. Antibiotic resistance genes associated with marine surface sediments: A baseline from the shores of Kuwait. Sustainability. 2022;14:8029. doi: 10.3390/su14138029. - DOI
Habibi N., Uddin S., Al-Sarawi H., Aldhameer A., Shajan A., Zakir F., Abdul Razzack N., Alam F. Metagenomes from coastal sediments of Kuwait: Insights into the microbiome, metabolic functions and resistome. Microorganisms. 2023;11:531. doi: 10.3390/microorganisms11020531. - DOI - PMC - PubMed
Al-Sarawi H.A., Najem A.B., Lyons B.P., Uddin S., Al-Sarawi M.A. Antimicrobial resistance in Escherichia coli isolated from marine sediment samples from Kuwait bay. Sustainability. 2022;14:11325. doi: 10.3390/su141811325. - DOI
Amarasiri M., Sano D., Suzuki S. Understanding human health risks caused by antibiotic resistant bacteria (ARB) and antibiotic resistance genes (ARG) in water environments: Current knowledge and questions to be answered. Crit. Rev. Environ. Sci. Technol. 2020;50:2016–2059. doi: 10.1080/10643389.2019.1692611. - DOI
Al-Sarawi H.A., Jha A.N., Al-Sarawi M.A., Lyons B.P. Historic and contemporary contamination in the marine environment of Kuwait: An overview. Mar. Pollut. Bull. 2015;100:621–628. doi: 10.1016/j.marpolbul.2015.07.052. - DOI - PubMed
Al-Sarawi H.A., Jha A.N., Baker-Austin C., Al-Sarawi M.A., Lyons B.P. Baseline screening for the presence of antimicrobial resistance in E. coli isolated from Kuwait’s marine environment. Mar. Pollut. Bull. 2018;129:893–898. doi: 10.1016/j.marpolbul.2017.10.044. - DOI - PubMed
Chakraborty J., Sapkale V., Rajput V., Shah M., Kamble S., Dharne M. Shotgun metagenome guided exploration of anthropogenically driven resistomic hotspots within Lonar soda lake of India. Ecotoxicol. Environ. Saf. 2020;194:110443. doi: 10.1016/j.ecoenv.2020.110443. - DOI - PubMed
Yang X., Yan L., Yang Y., Zhou H., Cao Y., Wang S., Xue B., Li C., Zhao C., Zhang X. The occurrence and distribution pattern of antibiotic resistance genes and bacterial community in the Ili river. Front. Environ. Sci. 2022;212:840428. doi: 10.3389/fenvs.2022.840428. - DOI
Chen P., Guo X., Li F. Antibiotic resistance genes in bioaerosols: Emerging, non-ignorable and pernicious pollutants. J. Clean. Prod. 2022;348:131094. doi: 10.1016/j.jclepro.2022.131094. - DOI
Habibi N., Uddin S., Al Salameen F., Behbehani M., Shirshikhar F., Abdul Razzack N., Shajan A., Hussain F.Z. Collection of bacterial community associated with size fractionated aerosols from Kuwait. Data. 2021;6:123. doi: 10.3390/data6120123. - DOI
Habibi N., Uddin S., Al Salameen F., Al Amad S., Kumar V., Al Otaibi M. Identification and Characterization of Novel Corona and Associated Respiratory Viruses in Aerosols. Kuwait Institute for Scientific Research; Safat, Kuwait: 2021. Final Report FB157C.
Habibi N., Uddin S., Al-Salameen F., Al-Amad S., Kumar V., Al-Otaibi M., Razzack N.A., Shajan A., Shirshikar F. SARS-CoV-2, other respiratory viruses and bacteria in aerosols: Report from Kuwait’s hospitals. Indoor Air. 2021;31:1815–1825. doi: 10.1111/ina.12871. - DOI - PMC - PubMed
Habibi N., Uddin S., Behbehani M., Al Salameen F., Razzack N.A., Zakir F., Shajan A., Alam F. Bacterial and fungal communities in indoor aerosols from two Kuwaiti hospitals. Front. Microbiol. 2022;13:955913. doi: 10.3389/fmicb.2022.955913. - DOI - PMC - PubMed
Habibi N., Uddin S., Behbehani M., Abdul Razzack N., Hussain F.Z., Shajan A. SARS-CoV-2 in hospital air as revealed by comprehensive respiratory viral panel sequencing. Infect. Prev. Pract. 2022;4:100199. doi: 10.1016/j.infpip.2021.100199. - DOI - PMC - PubMed
Xie J., Jin L., He T., Chen B., Luo X., Feng B., Huang W., Li J., Fu P., Li X. Bacteria and antibiotic resistance genes (ARGs) in PM2. 5 from China: Implications for human exposure. Environ. Sci. Technol. 2018;53:963–972. doi: 10.1021/acs.est.8b04630. - DOI - PubMed
He P., Wu Y., Huang W., Wu X., Lv J., Liu P., Bu L., Bai Z., Chen S., Feng W. Characteristics of and variation in airborne ARGs among urban hospitals and adjacent urban and suburban communities: A metagenomic approach. Environ. Int. 2020;139:105625. doi: 10.1016/j.envint.2020.105625. - DOI - PubMed
Li L., Wang Q., Bi W., Hou J., Xue Y., Mao D., Das R., Luo Y., Li X. Municipal solid waste treatment system increases ambient airborne bacteria and antibiotic resistance genes. Environ. Sci. Technol. 2020;54:3900–3908. doi: 10.1021/acs.est.9b07641. - DOI - PubMed
McEachran A.D., Blackwell B.R., Hanson J.D., Wooten K.J., Mayer G.D., Cox S.B., Smith P.N. Antibiotics, bacteria, and antibiotic resistance genes: Aerial transport from cattle feed yards via particulate matter. Environ. Health Perspect. 2015;123:337–343. doi: 10.1289/ehp.1408555. - DOI - PMC - PubMed
Jin L., Xie J., He T., Wu D., Li X. Airborne transmission as an integral environmental dimension of antimicrobial resistance through the “One Health” lens. Crit. Rev. Environ. Sci. Technol. 2022;52:4172–4193. doi: 10.1080/10643389.2021.2006537. - DOI
Ginn O., Lowry S., Brown J. A systematic review of enteric pathogens and antibiotic resistance genes in outdoor urban aerosols. Environ. Res. 2022;212:113097. doi: 10.1016/j.envres.2022.113097. - DOI - PubMed
Rocha-Melogno L., Crank K.C., Ginn O., Bergin M.H., Brown J., Gray G.C., Hamilton K.A., Bibby K., Deshusses M.A. Quantitative microbial risk assessment of outdoor aerosolized pathogens in cities with poor sanitation. Sci. Total Environ. 2022;827:154233. doi: 10.1016/j.scitotenv.2022.154233. - DOI - PubMed
Liang Z., Yu Y., Ye Z., Li G., Wang W., An T. Pollution profiles of antibiotic resistance genes associated with airborne opportunistic pathogens from typical area, Pearl River Estuary and their exposure risk to human. Environ. Int. 2020;143:105934. doi: 10.1016/j.envint.2020.105934. - DOI - PubMed
Gat D., Mazar Y., Cytryn E., Rudich Y. Origin-dependent variations in the atmospheric microbiome community in Eastern Mediterranean dust storms. Environ. Sci. Technol. 2017;51:6709–6718. doi: 10.1021/acs.est.7b00362. - DOI - PubMed
Li N., Liu C., Zhang Z., Li H., Song T., Liang T., Li B., Li L., Feng S., Su Q. Research and technological advances regarding the study of the spread of antimicrobial resistance genes and antimicrobial-resistant bacteria related to animal husbandry. Int. J. Environ. Res. Public Health. 2019;16:4896. doi: 10.3390/ijerph16244896. - DOI - PMC - PubMed
Brooks J., McLaughlin M., Scheffler B., Miles D. Microbial and antibiotic resistant constituents associated with biological aerosols and poultry litter within a commercial poultry house. Sci. Total Environ. 2010;408:4770–4777. doi: 10.1016/j.scitotenv.2010.06.038. - DOI - PubMed
Xie J., Jin L., Wu D., Pruden A., Li X. Inhalable antibiotic resistome from wastewater treatment plants to urban areas: Bacterial hosts, dissemination risks, and source contributions. Environ. Sci. Technol. 2022;56:7040–7051. doi: 10.1021/acs.est.1c07023. - DOI - PubMed
Zhou Z.-C., Liu Y., Lin Z.-J., Shuai X.-Y., Zhu L., Xu L., Meng L.-X., Sun Y.-J., Chen H. Spread of antibiotic resistance genes and microbiota in airborne particulate matter, dust, and human airways in the urban hospital. Environ. Int. 2021;153:106501. doi: 10.1016/j.envint.2021.106501. - DOI - PubMed
Zhang T., Li X., Wang M., Chen H., Yang Y., Chen Q.-l., Yao M. Time-resolved spread of antibiotic resistance genes in highly polluted air. Environ. Int. 2019;127:333–339. doi: 10.1016/j.envint.2019.03.006. - DOI - PubMed
Zhen Q., Deng Y., Wang Y., Wang X., Zhang H., Sun X., Ouyang Z. Meteorological factors had more impact on airborne bacterial communities than air pollutants. Sci. Total Environ. 2017;601:703–712. doi: 10.1016/j.scitotenv.2017.05.049. - DOI - PubMed
Lee G., Yoo K. A review of the emergence of antibiotic resistance in bioaerosols and its monitoring methods. Rev. Environ. Sci. Bio/Technol. 2022;21:799–827. doi: 10.1007/s11157-022-09622-3. - DOI - PMC - PubMed
Franklin A., Brinkman N., Jahne M., Keely S. Twenty-first century molecular methods for analyzing antimicrobial resistance in surface waters to support One Health assessments. J. Microbiol. Methods. 2021;184:106174. doi: 10.1016/j.mimet.2021.106174. - DOI - PMC - PubMed
Yadav B., Tyagi R. Current Developments in Biotechnology and Bioengineering. Elsevier; Amsterdam, The Netherlands: 2020. Development of molecular methods to detect and control emerging drug-resistance pathogens; pp. 377–419.
Luby E., Ibekwe A.M., Zilles J., Pruden A. Molecular methods for assessment of antibiotic resistance in agricultural ecosystems: Prospects and challenges. J. Environ. Qual. 2016;45:441–453. doi: 10.2134/jeq2015.07.0367. - DOI - PubMed
Waseem H., Jameel S., Ali J., Saleem Ur Rehman H., Tauseef I., Farooq U., Jamal A., Ali M.I. Contributions and challenges of high throughput qPCR for determining antimicrobial resistance in the environment: A critical review. Molecules. 2019;24:163. doi: 10.3390/molecules24010163. - DOI - PMC - PubMed
Waseem H., ur Rehman H.S., Ali J., Iqbal M.J., Ali M.I. Antibiotics and Antimicrobial Resistance Genes in the Environment. Elsevier; Amsterdam, The Netherlands: 2020. Global trends in ARGs measured by HT-qPCR platforms; pp. 206–222.
Lai F.Y., Muziasari W., Virta M., Wiberg K., Ahrens L. Profiles of environmental antibiotic resistomes in the urban aquatic recipients of Sweden using high-throughput quantitative PCR analysis. Environ. Pollut. 2021;287:117651. doi: 10.1016/j.envpol.2021.117651. - DOI - PubMed
Muziasari W.I., Pitkänen L.K., Sørum H., Stedtfeld R.D., Tiedje J.M., Virta M. Corrigendum: The resistome of farmed fish feces contributes to the enrichment of antibiotic resistance genes in sediments below Baltic Sea fish farms. Front. Microbiol. 2017;8:1491. doi: 10.3389/fmicb.2017.01491. - DOI - PMC - PubMed
Owayed A.F., Husain E.H., Al-Khabaz A., Al-Qattan H.Y., Al-Shammari N. Epidemiology and clinical presentation of pandemic influenza A (H1N1) among hospitalized children in Kuwait. Med. Princ. Pract. 2012;21:254–258. doi: 10.1159/000333771. - DOI - PubMed
Gupta M., Lee S., Bisesi M., Lee J. Indoor microbiome and antibiotic resistance on floor surfaces: An exploratory study in three different building types. Int. J. Environ. Res. Public Health. 2019;16:4160. doi: 10.3390/ijerph16214160. - DOI - PMC - PubMed
Perkins S.D., Mayfield J., Fraser V., Angenent L.T. Potentially pathogenic bacteria in shower water and air of a stem cell transplant unit. Appl. Environ. Microbiol. 2009;75:5363–5372. doi: 10.1128/AEM.00658-09. - DOI - PMC - PubMed
Prussin A.J., Garcia E.B., Marr L.C. Total concentrations of virus and bacteria in indoor and outdoor air. Environ. Sci. Technol. Lett. 2015;2:84–88. doi: 10.1021/acs.estlett.5b00050. - DOI - PMC - PubMed
Habibi N., Behbehani M., Uddin S., AL Salameen F., Shajan A., Zakir F. A safe and effective sample collection method for assessment of SARS-CoV-2 in aerosol samples. In: Ramanathan A.L., Chidambaram S., Jonathan M.P., Munoz-Arriola F., Prasanna M.V., Kumar P., editors. Environmental Resilience and Transformation in Times of COVID-19. Elsevier; Amsterdam, The Netherlands: 2021.
Uddin S., Habibi N., Fowler S.W., Behbehani M., Gevao B., Faizuddin M., Gorgun A.U. Aerosols as vectors for contaminants: A perspective based on outdoor aerosol data from Kuwait. Atmosphere. 2023;14:470. doi: 10.3390/atmos14030470. - DOI
Ma L., Yabo S.D., Lu L., Jiang J., Meng F., Qi H. Seasonal variation characteristics of inhalable bacteria in bioaerosols and antibiotic resistance genes in Harbin. J. Hazard. Mater. 2023;446:130597. doi: 10.1016/j.jhazmat.2022.130597. - DOI - PubMed
Behbehani M., Uddin S., Habibi N., Al Salameen F., Sajid S., Abdulrazzack N., Zakir F., Shirshikhar F. 210Po in Ultrafine Aerosol Particles and Its Likelihood to Mutate the Microbial Community. Kuwait Institute for Scientific Research; Safat, Kuwait: 2021. Final Report FB160C.
Al Salameen F., Habibi N., Uddin S., Al Mataqi K., Kumar V., Al Doaij B., Al Amad S., Al Ali E., Shirshikhar F. Spatio-temporal variations in bacterial and fungal community associated with dust aerosol in Kuwait. PLoS ONE. 2020;15:e0241283. doi: 10.1371/journal.pone.0241283. - DOI - PMC - PubMed
Al-Salameen F., Habibi N., Uddin S., Al-Mataqi K., Al-Doaij B., Al-Amad S., Al-Ali E. Characterization and Identification of Microorganisms Associated with Airborne Dust in Kuwait. Kuwait Institute for Scientific Research; Safat, Kuwait: 2021. Final Report EM075C.
Behbehani M., Carvalho F.P., Uddin S., Habibi N. Enhanced polonium concentrations in aerosols from the Gulf oil producing region and the role of microorganisms. Int. J. Environ. Res. Public Health. 2021;18:13309. doi: 10.3390/ijerph182413309. - DOI - PMC - PubMed
Cao C., Jiang W., Wang B., Fang J., Lang J., Tian G., Jiang J., Zhu T.F. Inhalable microorganisms in Beijing’s PM2. 5 and PM10 pollutants during a severe smog event. Environ. Sci. Technol. 2014;48:1499–1507. doi: 10.1021/es4048472. - DOI - PMC - PubMed
Prussin A.J., Marr L.C. Sources of airborne microorganisms in the built environment. Microbiome. 2015;3:78. doi: 10.1186/s40168-015-0144-z. - DOI - PMC - PubMed
Zhao Y., Wang Q., Chen Z., Mao D., Luo Y. Significant higher airborne antibiotic resistance genes and the associated inhalation risk in the indoor than the outdoor. Environ. Pollut. 2021;268:115620. doi: 10.1016/j.envpol.2020.115620. - DOI - PubMed
Adams R.I., Bateman A.C., Bik H.M., Meadow J.F. Microbiota of the indoor environment: A meta-analysis. Microbiome. 2015;3:49. doi: 10.1186/s40168-015-0108-3. - DOI - PMC - PubMed
Gilbert Y., Veillette M., Duchaine C. Airborne bacteria and antibiotic resistance genes in hospital rooms. Aerobiologia. 2010;26:185–194. doi: 10.1007/s10453-010-9155-1. - DOI
Miletto M., Lindow S.E. Relative and contextual contribution of different sources to the composition and abundance of indoor air bacteria in residences. Microbiome. 2015;3:61. doi: 10.1186/s40168-015-0128-z. - DOI - PMC - PubMed
Chen M., Qiu T., Sun Y., Song Y., Wang X., Gao M. Diversity of tetracycline-and erythromycin-resistant bacteria in aerosols and manures from four types of animal farms in China. Environ. Sci. Pollut. Res. 2019;26:24213–24222. doi: 10.1007/s11356-019-05672-3. - DOI - PubMed
Gevao B., Uddin S., Krishnan D., Rajagopalan S., Habibi N. Antibiotics in wastewater: Baseline of the influent and effluent Streams in Kuwait. Toxics. 2022;10:174. doi: 10.3390/toxics10040174. - DOI - PMC - PubMed
Yang T., Jiang L., Bi X., Cheng L., Zheng X., Wang X., Zhou X. Submicron aerosols share potential pathogens and antibiotic resistomes with wastewater or sludge. Sci. Total Environ. 2022;821:153521. doi: 10.1016/j.scitotenv.2022.153521. - DOI - PubMed
Wei K., Zou Z., Zheng Y., Li J., Shen F., Wu C.-Y., Wu Y., Hu M., Yao M. Ambient bioaerosol particle dynamics observed during haze and sunny days in Beijing. Sci. Total Environ. 2016;550:751–759. doi: 10.1016/j.scitotenv.2016.01.137. - DOI - PubMed
Waśko I., Kozińska A., Kotlarska E., Baraniak A. Clinically Relevant β-Lactam Resistance Genes in Wastewater Treatment Plants. Int. J. Environ. Res. Public Health. 2022;19:13829. doi: 10.3390/ijerph192113829. - DOI - PMC - PubMed
Tooke C.L., Hinchliffe P., Bragginton E.C., Colenso C.K., Hirvonen V.H., Takebayashi Y., Spencer J. β-Lactamases and β-Lactamase Inhibitors in the 21st Century. J. Mol. Biol. 2019;431:3472–3500. doi: 10.1016/j.jmb.2019.04.002. - DOI - PMC - PubMed
Pongchaikul P., Mongkolsuk P. Comprehensive Analysis of Imipenemase (IMP)-Type Metallo-β-Lactamase: A global distribution threatening Asia. Antibiotics. 2022;11:236. doi: 10.3390/antibiotics11020236. - DOI - PMC - PubMed
Philippon A., Slama P., Dény P., Labia R. A structure-based classification of class A β-lactamases, a broadly diverse family of enzymes. Clin. Microbiol. Rev. 2016;29:29–57. doi: 10.1128/CMR.00019-15. - DOI - PMC - PubMed
Kunhikannan S., Thomas C.J., Franks A.E., Mahadevaiah S., Kumar S., Petrovski S. Environmental hotspots for antibiotic resistance genes. Microbiologyopen. 2021;10:e1197. doi: 10.1002/mbo3.1197. - DOI - PMC - PubMed
Lautenbach E., Marsicano R., Tolomeo P., Heard M., Serrano S., Stieritz D.D. Epidemiology of Gram-negative antimicrobial resistance in a multi-state network of long-term care facilities. Infect. Control Hosp. Epidemiol. Off. J. Soc. Hosp. Epidemiol. Am. 2009;30:790. doi: 10.1086/599070. - DOI - PMC - PubMed
Habibi N., Mustafa A.S., Khan M.W. Composition of nasal bacterial community and its seasonal variation in health care workers stationed in a clinical research laboratory. PLoS ONE. 2021;16:e0260314. doi: 10.1371/journal.pone.0260314. - DOI - PMC - PubMed
Verhoeven P.O., Gagnaire J., Botelho-Nevers E., Grattard F., Carricajo A., Lucht F., Pozzetto B., Berthelot P. Detection and clinical relevance of Staphylococcus aureus nasal carriage: An update. Expert Rev. Anti-Infect. Ther. 2014;12:75–89. doi: 10.1586/14787210.2014.859985. - DOI - PubMed
Reyes N., Montes O., Figueroa S., Tiwari R., Sollecito C.C., Emmerich R., Usyk M., Geliebter J., Burk R.D. Staphylococcus aureus nasal carriage and microbiome composition among medical students from Colombia: A cross-sectional study. F1000Research. 2020;9:78. doi: 10.12688/f1000research.22035.1. - DOI - PMC - PubMed
Habibi N., Uddin S., Fowler S.W., Behbehani M. Microplastics in the atmosphere: A review. J. Environ. Expo. Assess. 2022;1:6. doi: 10.20517/jeea.2021.07. - DOI
Habibi N., Uddin S., Al-Salameen F., Al-Amad S., Abdul Razzack N., Shajan A. Proceedings of the Scientific Poster Day 2020–2021. Kuwait University; Kuwait City, Kuwait: 2021. Evidences of airborne spread of SARS CoV2 in indoor air.
Uddin S., Al-Ghadban A., Gevao B., Al-Shamroukh D., Al-Khabbaz A. Estimation of suspended particulate matter in Gulf using MODIS data. Aquat. Ecosyst. Health Manag. 2012;15:41–44. doi: 10.1080/14634988.2012.668114. - DOI
Uddin S., Fowler S.W., Habibi N., Sajid S., Dupont S., Behbehani M. A preliminary assessment of size-fractionated microplastics in indoor aerosol—Kuwait’s baseline. Toxics. 2022;10:71. doi: 10.3390/toxics10020071. - DOI - PMC - PubMed
Gevao B., Al-Bahloul M., Zafar J., Al-Matrouk K., Helaleh M. Polycyclic aromatic hydrocarbons in indoor air and dust in Kuwait: Implications for sources and nondietary human exposure. Arch. Environ. Contam. Toxicol. 2007;53:503–512. doi: 10.1007/s00244-006-0261-6. - DOI - PubMed
Gevao B., Uddin S., Al-Bahloul M., Al-Mutairi A. Persistent organic pollutants on human and sheep hair and comparison with POPs in indoor and outdoor air. J. Environ. Expo. Assess. 2022;1:5. doi: 10.20517/jeea.2021.06. - DOI
Madi N., Al-Nakib W., Mustafa A.S., Habibi N. Metagenomic analysis of viral diversity in respiratory samples from patients with respiratory tract infections in Kuwait. J. Med. Virol. 2018;90:412–420. doi: 10.1002/jmv.24984. - DOI - PMC - PubMed
Zaheer R., Noyes N., Ortega Polo R., Cook S.R., Marinier E., Van Domselaar G., Belk K.E., Morley P.S., McAllister T.A. Impact of sequencing depth on the characterization of the microbiome and resistome. Sci. Rep. 2018;8:5890. doi: 10.1038/s41598-018-24280-8. - DOI - PMC - PubMed
Núñez A., de Paz G.A., Rastrojo A., Ferencova Z., Gutiérrez-Bustillo A.M., Alcamí A., Moreno D.A., Guantes R. Temporal patterns of variability for prokaryotic and eukaryotic diversity in the urban air of Madrid (Spain) Atmos. Environ. 2019;217:116972. doi: 10.1016/j.atmosenv.2019.116972. - DOI
Tignat-Perrier R., Dommergue A., Thollot A., Magand O., Amato P., Joly M., Sellegri K., Vogel T.M., Larose C. Seasonal shift in airborne microbial communities. Sci. Total Environ. 2020;716:137129. doi: 10.1016/j.scitotenv.2020.137129. - DOI - PubMed
Gevao B., Uddin S., Dupont S. Baseline concentrations of pharmaceuticals in Kuwait’s coastal marine environment. Mar. Pollut. Bull. 2021;173:113040. doi: 10.1016/j.marpolbul.2021.113040. - DOI - PubMed
Alper E., Elkilani A., Bouhamra W. Estimation of air exchange rates in Kuwaiti residential buildings; Proceedings of the 20th AIVC and Indoor Air 99 Conference “Ventilation and Indoor Air Quality in Buildings; Edinburgh, Scotland. 9–13 August 1999.
Gaviria-Figueroa A., Preisner E.C., Hoque S., Feigley C.E., Norman R.S. Emission and dispersal of antibiotic resistance genes through bioaerosols generated during the treatment of municipal sewage. Sci. Total Environ. 2019;686:402–412. doi: 10.1016/j.scitotenv.2019.05.454. - DOI - PubMed
Dhariwal A., Junges R., Chen T., Petersen F.C. ResistoXplorer: A web-based tool for visual, statistical and exploratory data analysis of resistome data. NAR Genom. Bioinform. 2021;3:lqab018. doi: 10.1093/nargab/lqab018. - DOI - PMC - PubMed
Schauberger P., Walker A., Braglia L., Sturm J., Garbuszus J.M., Barbone J.M. Openxlsx: Read, Write and Edit XLSX Files. R Package Rersion 4.1.0. 2018. [(accessed on 25 March 2023)]. Available online: https://CRAN.R-project.org/package=openxlsx.
Cohen I., Huang Y., Chen J., Benesty J. Noise Reduction in Speech Processing. Springer; Berlin/Heidelberg, Germany: 2009. Pearson correlation coefficient; pp. 1–4.
Bengtsson-Palme J. The diversity of uncharacterized antibiotic resistance genes can be predicted from known gene variants—But not always. Microbiome. 2018;6:125. doi: 10.1186/s40168-018-0508-2. - DOI - PMC - PubMed
Anderson M.J., Walsh D.C. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol. Monogr. 2013;83:557–574. doi: 10.1890/12-2010.1. - DOI
Love M.I., Huber W., Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550. doi: 10.1186/s13059-014-0550-8. - DOI - PMC - PubMed