Resistance Pattern of Klebsiella pneumoniae in Aseer Region, Saudi Arabia: A Ten-Year Hospital-Based Study
Abstract
:1. Introduction
2. Methods
2.1. Study Design
2.2. Sample Collection
2.3. Bacterial Identification
2.4. Antibiotic Susceptibility Testing
2.5. Data Collection
2.6. Ethical Considerations
3. Data Analysis
4. Results
5. Discussion
6. Conclusions and Recommendations
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Perween, N.; Prakash, S.K.; Siddiqui, O. Multi drug resistant Klebsiella isolates in burn patients: A comparative study. J. Clin. Diagn. Res. 2015, 9, DC14. [Google Scholar]
- Abayneh, M.; Tesfaw, G.; Abdissa, A. Isolation of extended-spectrum β-lactamase-(ESBL-) producing Escherichia coli and K. pneumoniae from patients with community-onset urinary tract infections in Jimma University Specialized Hospital, Southwest Ethiopia. Can. J. Infect. Dis. Med. Microbiol. 2018, 2018, 4846159. [Google Scholar] [CrossRef]
- Ameshe, A.; Engda, T.; Gizachew, M. Prevalence, antibiotic susceptibility patterns, including ESBL production and associated risk factors of Klebsiella species among UTI suspected patients at Bahir-dar town. Northwest Ethiop. 2020, 10. [Google Scholar] [CrossRef]
- Xu, L.; Sun, X.; Ma, X. Systematic review and meta-analysis of mortality of patients infected with carbapenem-resistant Klebsiella pneumoniae. Ann. Clin. Microbiol. Antimicrob. 2017, 16, 18. [Google Scholar] [CrossRef]
- Lam, M.M.C.; Wyres, K.L.; Duchêne, S.; Wick, R.R.; Judd, L.M.; Gan, Y.-H.; Hoh, C.-H.; Archuleta, S.; Molton, J.S.; Kalimuddin, S.; et al. Population genomics of hypervirulent K. pneumoniae clonal-group 23 reveals early emergence and rapid global dissemination. Nat. Commun. 2018, 9, 2703. [Google Scholar] [CrossRef] [PubMed]
- Ballén, V.; Gabasa, Y.; Ratia, C.; Ortega, R.; Tejero, M.; Soto, S. Antibiotic resistance and virulence profiles of klebsiella pneumoniae strains isolated from different clinical sources. Front. Cell. Infect. Microbiol. 2021, 11, 738223. [Google Scholar] [CrossRef] [PubMed]
- Al-Zalabani, A.; A AlThobyane, O.; Alshehri, A.H.; O Alrehaili, A.; O Namankani, M.; Aljafri, O.H. Prevalence of klebsiella pneumoniae antibiotic resistance in Medina, Saudi Arabia, 2014–2018. Cureus 2020, 12, e9714. [Google Scholar] [CrossRef]
- Oliveira, R.; Castro, J.; Silva, S.; Oliveira, H.; Saavedra, M.J.; Azevedo, N.F.; Almeida, C. Exploring the antibiotic resistance profile of clinical K. pneumoniae isolates in Portugal. Antibiotics 2022, 11, 1613. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Zhong, H.; Han, X.; Wang, N.; Cai, Y.; Wang, H.; Yu, J.; Zhang, X.; Zhang, K. Impact of antibiotic prescription on the resistance of K. pneumoniae at a tertiary hospital in China, 2012–2019. Am. J. Infect. Control 2021, 49, 65–69. [Google Scholar] [CrossRef]
- Mohammed, A.; Seid, M.E.; Gebrecherkos, T.; Tiruneh, M.; Moges, F. Bacterial isolates and their antimicrobial susceptibility patterns of wound infections among inpatients and outpatients attending the University of Gondar Referral Hospital, Northwest Ethiopia. Int. J. Microbiol. 2017, 2017, 8953829. [Google Scholar] [CrossRef]
- Sakkas, H.; Bozidis, P.; Ilia, A.; Mpekoulis, G.; Papadopoulou, C. Antimicrobial Resistance in bacterial pathogens and detection of Carbapenemases in K. pneumoniae isolates from Hospital Wastewater. Antibiotics 2019, 8, 85. [Google Scholar] [CrossRef] [PubMed]
- Effah, C.Y.; Sun, T.; Liu, S.; Wu, Y. Klebsiella pneumoniae: An increasing threat to public health. Ann. Clin. Microbiol. Antimicrob. 2020, 19, 1. [Google Scholar] [CrossRef] [PubMed]
- Navon-Venezia, S.; Kondratyeva, K.; Carattoli, A. Klebsiella pneumoniae: A major worldwide source and shuttle for antibiotic resistance. FEMS Microbiol. Rev. 2017, 41, 252–275. [Google Scholar] [CrossRef] [PubMed]
- Heidary, M.; Goudarzi, H.; Hashemi, A.; Eslami, G.; Goudarzi, M.; Chirani, A.; Amraei, S. The prevalence of genes that encode quinolone resistance in K. pneumoniae strains isolated from hospitalized patients during 2013–2014. Arch. Pediatr. Infect. Dis. 2016, 5, e38343. [Google Scholar]
- Hassuna, N.A.; AbdelAziz, R.A.; Zakaria, A.; Abdelhakeem, M. Extensively-Drug Resistant Klebsiella pneumoniae Recovered From Neonatal Sepsis Cases From a Major NICU in Egypt. Front. Microbiol. 2020, 11, 1375. [Google Scholar] [CrossRef] [PubMed]
- Hu, F.P.; Guo, Y.; Zhu, D.M.; Wang, F.; Jiang, X.F.; Xu, Y.C.; Shen, J.L.; Sun, Z.Y.; Chen, Z.J.; Ni, Y.X.; et al. Resistance trends among clinical isolates in China reported from CHINET surveillance of bacterial resistance, 2005–2014. Clin. Microbiol. Infect. 2016, 22, S9–S14. [Google Scholar] [CrossRef] [PubMed]
- Trepanier, P.; Mallard, K.; Meunier, D.; Pike, R.; Brown, D.; Ashby, J.P.; Donaldson, H.; Awad-El-Kariem, F.M.; Balakrishnan, I.; Cubbon, M.; et al. Carbapenemase-producing Enterobacteriaceae in the UK: A national study (EuSCAPE-UK) on prevalence, incidence, laboratory detection methods and infection control measures. J. Antimicrob. Chemother. 2016, 72, 596–603. [Google Scholar] [CrossRef]
- Sleiman, A.; Awada, B.; Mocadie, M.; Sherri, N.; Haraoui, L.-P.; Baby, V.; Araj, G.F.; Kanj, S.S.; Rizk, N.; Matar, G.M.; et al. An unequivocal superbug: PDR Klebsiella pneumoniae with an arsenal of resistance and virulence factor genes. J. Infect. Dev. Ctries. 2021, 15, 404–414. [Google Scholar] [CrossRef]
- Al-Zahrani, I.A.; Alsiri, B.A. The emergence of carbapenem-resistant Klebsiella pneumoniae isolates producing OXA-48 and NDM in the Southern (Asir) province, Saudi Arabia. Saudi Med. J. 2018, 39, 23–30. [Google Scholar] [CrossRef]
- Ahmadi, M.; Ranjbar, R.; Behzadi, P.; Mohammadian, T. Virulence factors, antibiotic resistance patterns, and molecular types of clinical isolates of Klebsiella Pneumoniae. Expert Rev. Anti-Infect. Ther. 2022, 20, 463–472. [Google Scholar] [CrossRef]
- Montravers, P.; Grall, N.; Kantor, E.; Augustin, P.; Boussion, K.; Zappella, N. Microbiological profile of patients treated for postoperative peritonitis: Temporal trends 1999–2019. World J. Emerg. Surg. 2023, 18, 58. [Google Scholar] [CrossRef] [PubMed]
- Zhang, W.X.; Chen, H.Y.; Chen, C.; Chen, J.H.; Wan, F.S.; Li, L.X.; Chen, M.; Zhang, J. Resistance phenotype and molecular epidemiology of carbapenem-resistant K. pneumoniae isolates in Shanghai. Microb. Drug Resist. 2021, 27, 1312–1318. [Google Scholar] [CrossRef] [PubMed]
- Mirzaie, A.; Ranjbar, R. Antibiotic resistance, virulence-associated genes analysis and molecular typing of K. pneumoniae strains recovered from clinical samples. AMB Express 2021, 11, 122. [Google Scholar] [CrossRef] [PubMed]
- Ferraro, M.J. Performance Standards for Antimicrobial Susceptibility Testing; NCCLS: Orlando, FL, USA, 2001. [Google Scholar]
- Moradigaravand, D.; Martin, V.; Peacock, S.J.; Parkhill, J. Evolution and epidemiology of multidrug-resistant K. pneumoniae in the United Kingdom and Ireland. MBio 2017, 8, 10–128. [Google Scholar] [CrossRef] [PubMed]
- Mohd Asri, N.A.; Ahmad, S.; Mohamud, R.; Mohd Hanafi, N.; Mohd Zaidi, N.F.; Irekeola, A.A.; Shueb, R.H.; Yee, L.C.; Mohd Noor, N.; Mustafa, F.H.; et al. Global prevalence of nosocomial multidrug-resistant Klebsiella pneumoniae: A systematic review and meta-analysis. Antibiotics 2021, 10, 1508. [Google Scholar] [CrossRef] [PubMed]
- Jalal, N.A.; Al-Ghamdi, A.M.; Momenah, A.M.; Ashgar, S.S.; Bantun, F.; Bahwerth, F.S.; Hariri, S.H.; Johargy, A.K.; Barhameen, A.A.; Al-Said, H.M.; et al. Prevalence and Antibiogram Pattern of K. pneumoniae in a Tertiary Care Hospital in Makkah, Saudi Arabia: An 11-Year Experience. Antibiotics 2023, 12, 164. [Google Scholar] [CrossRef] [PubMed]
- Ficik, J.; Andrezál, M.; Drahovská, H.; Böhmer, M.; Szemes, T.; Liptáková, A.; Slobodníková, L. Carbapenem-Resistant Klebsiella pneumoniae in COVID-19 Era—Challenges and Solutions. Antibiotics 2023, 12, 1285. [Google Scholar] [CrossRef] [PubMed]
- Al Bshabshe, A.; Al-Hakami, A.; Alshehri, B.; A Al-Shahrani, K.; A Alshehri, A.; Al Shahrani, M.B.; Assiry, I.; Joseph, M.R.; Alkahtani, A.M.; E Hamid, M. Rising K. pneumoniae Infections and Its Expanding Drug Resistance in the Intensive Care Unit of a Tertiary Healthcare Hospital, Saudi Arabia. Cureus 2020, 12, e10060. [Google Scholar] [CrossRef] [PubMed]
- Ibrahim, M.E. High antimicrobial resistant rates among Gram-negative pathogens in intensive care units. A retrospective study at a tertiary care hospital in Southwest Saudi Arabia. Saudi Med. J. 2018, 39, 1035–1043. [Google Scholar] [CrossRef] [PubMed]
- Chang, D.; Sharma, L.; Dela Cruz, C.S.; Zhang, D. Clinical Epidemiology, Risk Factors, and Control Strategies of K. pneumoniae Infection. Front. Microbiol. 2021, 12, 750662. [Google Scholar]
- Nirwati, H.; Sinanjung, K.; Fahrunissa, F.; Wijaya, F.; Napitupulu, S.; Hati, V.P.; Hakim, M.S.; Meliala, A.; Aman, A.T.; Nuryastuti, T. Biofilm formation and antibiotic resistance of K. pneumoniae isolated from clinical samples in a tertiary care hospital, Klaten, Indonesia. BMC Proc. 2019, 13, 20. [Google Scholar] [CrossRef] [PubMed]
- Claassen-Weitz, S.; Lim, K.Y.; Mullally, C.; Zar, H.J.; Nicol, M.P. The association between bacteria colonizing the upper respiratory tract and lower respiratory tract infection in young children: A systematic review and meta-analysis. Clin. Microbiol. Infect. 2021, 27, 1262–1270. [Google Scholar] [CrossRef] [PubMed]
- Kern, W.; Rieg, S. Burden of bacterial bloodstream infection—A brief update on epidemiology and significance of multidrug-resistant pathogens. Clin. Microbiol. Infect. 2020, 26, 151–157. [Google Scholar] [CrossRef] [PubMed]
- Gebremeskel, L.; Teklu, T.; Kasahun, G.G.; Tuem, K.B. Antimicrobial resistance pattern of Klebsiella isolated from various clinical samples in Ethiopia: A systematic review and meta-analysis. BMC Infect. Dis. 2023, 23, 643. [Google Scholar] [CrossRef] [PubMed]
- Pei, N.; Liu, Q.; Cheng, X.; Liang, T.; Jian, Z.; Wang, S.; Zhong, Y.; He, J.; Zhou, M.; Kristiansen, K.; et al. Longitudinal Study of the Drug Resistance in K. pneumoniae of a Tertiary Hospital, China: Phenotypic Epidemiology Analysis (2013–2018). Infect. Drug Resist. 2021, 14, 613–626. [Google Scholar] [CrossRef] [PubMed]
- Sharma, A.; Thakur, A.; Thakur, N.; Kumar, V.; Chauhan, A.; Bhardwaj, N. Changing Trend in the Antibiotic Resistance Pattern of Klebsiella pneumonia Isolated from Endotracheal Aspirate Samples of ICU Patients of a Tertiary Care Hospital in North India. Cureus 2023, 15, e36317. [Google Scholar] [CrossRef] [PubMed]
- Hansen, G.T. Continuous Evolution: Perspective on the Epidemiology of Carbapenemase Resistance among Enterobacterales and Other Gram-Negative Bacteria. Infect. Dis. Ther. 2021, 10, 75–92. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Sun, Q.L.; Shen, Y.; Zhang, Y.; Yang, J.W.; Shu, L.B.; Zhou, H.W.; Wang, Y.; Wang, B.; Zhang, R.; et al. Rapid Increase in Prevalence of Carbapenem-Resistant Enterobacteriaceae (CRE) and Emergence of Colistin Resistance Gene mcr-1 in CRE in a Hospital in Henan, China. J. Clin. Microbiol. 2018, 56, e01932-17. [Google Scholar] [CrossRef]
Year | Total | Ward | Gender | |||||||
---|---|---|---|---|---|---|---|---|---|---|
GW | ICU | Male | Female | |||||||
No | % | No | % | No | % | No | % | No | % | |
2013 | 442 | 11.3% | 252 | 57.0% | 190 | 43.0% | 298 | 67.4% | 144 | 32.6% |
2014 | 249 | 6.4% | 154 | 61.8% | 95 | 38.2% | 168 | 67.5% | 81 | 32.5% |
2015 | 238 | 6.1% | 167 | 70.2% | 71 | 29.8% | 168 | 70.6% | 70 | 29.4% |
2016 | 294 | 7.5% | 190 | 64.6% | 104 | 35.4% | 196 | 66.7% | 98 | 33.3% |
2017 | 270 | 6.9% | 178 | 65.9% | 92 | 34.1% | 170 | 63.0% | 100 | 37.0% |
2018 | 275 | 7.0% | 192 | 69.8% | 83 | 30.2% | 170 | 61.8% | 105 | 38.2% |
2019 | 543 | 13.8% | 311 | 57.3% | 232 | 42.7% | 355 | 65.4% | 188 | 34.6% |
2020 | 471 | 12.0% | 206 | 43.7% | 265 | 56.3% | 341 | 72.4% | 130 | 27.6% |
2021 | 639 | 16.3% | 323 | 50.5% | 316 | 49.5% | 412 | 64.5% | 227 | 35.5% |
2022 | 500 | 12.8% | 259 | 51.8% | 241 | 48.2% | 307 | 61.4% | 193 | 38.6% |
Total | 3921 | 100.0% | 2232 | 56.9% | 1689 | 43.1% | 2585 | 65.9% | 1336 | 34.1% |
Source | Ward | p-Value | |||
---|---|---|---|---|---|
GW | ICU | ||||
No | % | No | % | ||
Urine | 677 | 30.3% | 253 | 15.0% | 0.004 * |
Sputum | 373 | 16.7% | 372 | 22.0% | 0.036 * |
Wound | 337 | 15.1% | 213 | 12.6% | 0.048 * |
Blood | 129 | 5.8% | 330 | 19.5% | 0.001 * |
ETT | 154 | 6.9% | 272 | 16.1% | 0.039 * |
Abscess | 214 | 9.6% | 28 | 1.7% | 0.069 |
Aspirated fluid | 72 | 3.2% | 12 | 0.7% | 0.534 |
Nasooropharyngeal (NOP) | 145 | 6.5% | 60 | 3.6% | 0.339 |
Respiratory secretions and BAL (except sputum) | 49 | 2.2% | 117 | 6.9% | 0.417 |
Skin and soft tissue | 47 | 2.1% | 12 | 0.7% | 0.661 |
Vaginal swab | 11 | 0.5% | 3 | 0.2% | 0.886 |
Bone | 18 | 0.8% | 1 | 0.1% | 0.869 |
CSF | 5 | 0.2% | 14 | 0.8% | 0.874 |
Others | 1 | 0.0% | 2 | 0.1% | 0.996 |
Antibiotics | Year-Wise Prevalence (%) of Resistant K. pneumoniae | Overall | p-Value for Trend | ||||||||||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
2013 | 2014 | 2015 | 2016 | 2017 | 2018 | 2019 | 2020 | 2021 | 2022 | ||||||||||||||
No | % | No | % | No | % | No | % | No | % | No | % | No | % | No | % | No | % | No | % | No | % | ||
Ciprofloxacin | 261 | 59.0% | 115 | 46.2% | 109 | 45.8% | 140 | 47.6% | 132 | 48.9% | 140 | 50.9% | 301 | 55.4% | 349 | 74.1% | 482 | 75.4% | 289 | 57.8% | 2318 | 59.1% | 0.058 |
Bactrim | 174 | 39.4% | 68 | 27.3% | 96 | 40.3% | 108 | 36.7% | 131 | 48.5% | 169 | 61.5% | 317 | 58.4% | 325 | 69.0% | 434 | 67.9% | 230 | 46.0% | 2052 | 52.3% | 0.049 * |
Cefepime | 136 | 30.8% | 107 | 43.0% | 101 | 42.4% | 107 | 36.4% | 74 | 27.4% | 107 | 38.9% | 329 | 60.6% | 316 | 67.1% | 435 | 68.1% | 242 | 48.4% | 1954 | 49.8% | 0.046 * |
Piperacillin/tazobactam | 80 | 18.1% | 55 | 22.1% | 88 | 37.0% | 105 | 35.7% | 79 | 29.3% | 113 | 41.1% | 290 | 53.4% | 319 | 67.7% | 453 | 70.9% | 269 | 53.8% | 1851 | 47.2% | 0.043 * |
Amoxicillin/clavulanate | 219 | 49.5% | 81 | 32.5% | 78 | 32.8% | 61 | 20.7% | 79 | 29.3% | 59 | 21.5% | 265 | 48.8% | 306 | 65.0% | 415 | 64.9% | 218 | 43.6% | 1781 | 45.4% | 0.058 |
Levofloxacin | 107 | 24.2% | 60 | 24.1% | 68 | 28.6% | 84 | 28.6% | 67 | 24.8% | 125 | 45.5% | 231 | 42.5% | 305 | 64.8% | 395 | 61.8% | 166 | 33.2% | 1608 | 41.0% | 0.047 * |
Meropenem | 23 | 5.2% | 13 | 5.2% | 32 | 13.4% | 61 | 20.7% | 58 | 21.5% | 84 | 30.5% | 268 | 49.4% | 318 | 67.5% | 445 | 69.6% | 257 | 51.4% | 1559 | 39.8% | 0.002 * |
Amikacin | 179 | 40.5% | 70 | 28.1% | 68 | 28.6% | 76 | 25.9% | 30 | 11.1% | 92 | 33.5% | 201 | 37.0% | 252 | 53.5% | 395 | 61.8% | 179 | 35.8% | 1542 | 39.3% | 0.158 |
Aztreonam | 187 | 42.3% | 24 | 9.6% | 0 | 0.0% | 2 | 0.7% | 10 | 3.7% | 100 | 36.4% | 241 | 44.4% | 276 | 58.6% | 356 | 55.7% | 149 | 29.8% | 1345 | 34.3% | 0.096 |
Ertapenem | 43 | 9.7% | 14 | 5.6% | 0 | 0.0% | 3 | 1.0% | 47 | 17.4% | 108 | 39.3% | 231 | 42.5% | 291 | 61.8% | 406 | 63.5% | 179 | 35.8% | 1322 | 33.7% | 0.006 * |
Ampicillin/sulbactam | 1 | 0.2% | 7 | 2.8% | 9 | 3.8% | 28 | 9.5% | 17 | 6.3% | 156 | 56.7% | 255 | 47.0% | 274 | 58.2% | 369 | 57.7% | 170 | 34.0% | 1286 | 32.8% | 0.001 * |
Moxifloxacin | 59 | 13.3% | 23 | 9.2% | 0 | 0.0% | 0 | 0.0% | 71 | 26.3% | 101 | 36.7% | 181 | 33.3% | 244 | 51.8% | 312 | 48.8% | 103 | 20.6% | 1094 | 27.9% | 0.039 * |
Cefotaxime | 42 | 9.5% | 76 | 30.5% | 55 | 23.1% | 10 | 3.4% | 37 | 13.7% | 47 | 17.1% | 148 | 27.3% | 236 | 50.1% | 294 | 46.0% | 137 | 27.4% | 1082 | 27.6% | 0.087 |
Imipenem | 34 | 7.7% | 20 | 8.0% | 40 | 16.8% | 59 | 20.1% | 54 | 20.0% | 52 | 18.9% | 147 | 27.1% | 154 | 32.7% | 334 | 52.3% | 177 | 35.4% | 1071 | 27.3% | 0.053 |
Colistin | 6 | 1.4% | 7 | 2.8% | 0 | 0.0% | 16 | 5.4% | 6 | 2.2% | 23 | 8.4% | 85 | 15.7% | 119 | 25.3% | 199 | 31.1% | 58 | 11.6% | 519 | 13.2% | 0.117 |
Tigecycline | 20 | 4.5% | 8 | 3.2% | 0 | 0.0% | 13 | 4.4% | 43 | 15.9% | 28 | 10.2% | 63 | 11.6% | 31 | 6.6% | 46 | 7.2% | 52 | 10.4% | 304 | 7.8% | 0.328 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2024 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Alshehri, S.M.; Abdullah, N.S.; Algarni, A.; AlZomia, A.S.; Assiry, M.M. Resistance Pattern of Klebsiella pneumoniae in Aseer Region, Saudi Arabia: A Ten-Year Hospital-Based Study. Medicina 2024, 60, 1344. https://doi.org/10.3390/medicina60081344
Alshehri SM, Abdullah NS, Algarni A, AlZomia AS, Assiry MM. Resistance Pattern of Klebsiella pneumoniae in Aseer Region, Saudi Arabia: A Ten-Year Hospital-Based Study. Medicina. 2024; 60(8):1344. https://doi.org/10.3390/medicina60081344
Chicago/Turabian StyleAlshehri, Saad Mohammed, Naif Saud Abdullah, Abdullah Algarni, Ahmed Saad AlZomia, and Mohammed Mushabub Assiry. 2024. "Resistance Pattern of Klebsiella pneumoniae in Aseer Region, Saudi Arabia: A Ten-Year Hospital-Based Study" Medicina 60, no. 8: 1344. https://doi.org/10.3390/medicina60081344