Issue
Distribution of blaTEM, blaSHV, blaCTX-M, blaOXA, and blaDHA in Proteus mirabilis Isolated from Diabetic Foot Infections in Erbil, Iraq
Corresponding Author(s) : Samira Fattah Hamid
Cellular and Molecular Biology,
Vol. 66 No. 1: Issue 1
Abstract
Diabetic foot infection is considered to be one of the most important medical, economic, and social problems and a major cause of morbidity and mortality. Proteus mirabilis is a common etiologic agent of diabetic foot infections. This study aimed to determine the prevalence of beta-lactamase genes in P. mirabilis recovered from patients with diabetic foot wounds in Erbil, Iraq. Eighteen P. mirabilis isolated from 84 patients with diabetic foot ulcers were first phenotypically examined for the existence of extended-spectrum beta-lactamases by combined disc method and double-disc synergy method that all isolates showed positive results by both methods. The results were confirmed genetically by PCR to detect beta-lactamase-encoding genes (blaTEM, blaSHV, blaCTX-M, blaOXA, and blaDHA). The results revealed that all isolates contained extended-spectrum beta-lactamase and that 80% of the P. mirabilis isolates contained blaDHA, 60% had blaTEM, 53.3% had blaOXA, and 26.7% had blaCTX-M, whereas no isolates harbored blaSHV. The coexistence of two or more beta-lactamase genes in one isolate was observed. The existence of four genes (blaTEM + blaCTX-M + blaOXA + blaDHA) in the same isolate was documented in two isolates. In conclusion, this is the first study that reports a high prevalence of blaDHA and the coexistence of four resistance genes in the same organism in P. mirabilis isolated from diabetic foot patients in Iraq.
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- Kaimkhani GM, Siddiqui AA, Rasheed N, Rajput MI, Kumar J, Khan MH, Nisar S, Mustafa S, Yaqoob U. Pattern of infecting microorganisms and their susceptibility to antimicrobial drugs in patients with diabetic foot infections in a tertiary care hospital in karachi, pakistan. Cureus 2018; 10:6.
- Miyan Z, Fawwad A, Sabir R, Basit A. Microbiological pattern of diabetic foot infections at a tertiary care center in a developing country. Age 2017; 53: 10.20.
- Thurber EG, Kisuule F, Humbyrd C, Townsend J. Inpatient management of diabetic foot infections: a review of the guidelines for hospitalists. J Hosp Med 2017; 12: 994-1000.
- Shankar E, Mohan V, Premalatha G, Srinivasan R, Usha A. Bacterial etiology of diabetic foot infections in South India. Eur J Intern Med 2005; 16: 567-570.
- Noor S, Ahmad J, Parwez I, Ozair M. Culture-based screening of aerobic microbiome in diabetic foot subjects and developing non-healing ulcers. Front Microbiol 2016; 7: 1792.
- Hicks CW, Selvarajah S, Mathioudakis N, Sherman RL, Hines KF, Black III JH, Abularrage CJ. Burden of infected diabetic foot ulcers on hospital admissions and costs. Ann Vasc Surg 2016; 33: 149-158.
- Umadevi S, Kumar S, Joseph NM, Easow JM, Kandhakumari G, Srirangaraj S, Raj S, Stephen S. Microbiological study of diabetic foot infections. Indian. J .Med. Spec. 2011; 2;1.
- Kang WJ, Shi L, Shi Y, Cheng L, Ai HW, Zhao WJ. Analysis on distribution, drug resistance and risk factors of multi drug resistant bacteria in diabetic foot infection. Biomed Res 2017; 28: 10186-10190.
- Lipsky BA, Berendt AR, Cornia PB, Pile JC, Peters EJ, Armstrong DG, Deery HG, Embil JM, Joseph WS, Karchmer AW. 2012 Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis 2012; 54: 132-173.
- Zubair M, Malik A, Ahmad J. Clinico-bacteriology and risk factors for the diabetic foot infection with multidrug resistant microorganisms in north India. Biol Med. 2010; 2: 22-34.
- Grayson ML. Diabetic foot infections: antimicrobial therapy. Infect. Dis Clin North Am 1995; 9: 143-161.
- Lipsky BA. Diabetic foot infections: current treatment and delaying the ‘post"antibiotic era'. Diabetes. Metab Res Rev 2016; 32: 246-253.
- Citron DM, Goldstein EJ, Merriam CV, Lipsky BA, Abramson MA. Bacteriology of moderate-to-severe diabetic foot infections and in vitro activity of antimicrobial agents. J Clin Microbiol 2007; 45: 2819-2828.
- Shanmugam P, Jeya M. The bacteriology of diabetic foot ulcers, with a special reference to multidrug resistant strains. J Clin Diagn Res 2013; 7: 441.
- Caubey M, Suchitra M. Occurrence of TEM, SHV and CTX-M β lactamases in clinical isolates of Proteus species in a tertiary care center. Infect. Disord. Drug .Targets 2018; 18: 68-71.
- Hegazy W. Diclofenac inhibits virulence of Proteus mirabilis isolated from diabetic foot ulcer. Afr J Microbiol Res 2016; 10: 733-743.
- Tom IM, Agbo E, Faruk UA, Umoru AM, Ibrahim MM, Umar JB, Haruna AB, Aliyu A. Implication of Proteus spp in the pathology of nosocomial wound infection in northeastern nigeria. IJPR 2018; 9: 1-8.
- Mordi R, Momoh M. Incidence of Proteus species in wound infections and their sensitivity pattern in the University of Benin Teaching Hospital. Afr J Biotechnol 2009; 8:5.
- Huang Y, Cao Y, Zou M, Luo X, Jiang Y, Xue Y, Gao F. A comparison of tissue versus swab culturing of infected diabetic foot wounds. Int J Endocrinol 2016; 2016.
- CLSI C. Performance standards for antimicrobial susceptibility testing. Clinical Lab Standards Institute 2016.
- Yaykasli KO, Kayıkçı MA, Yamak N, Soguktas H, Duzenli S, Arslan AO, Metin A, Kaya E, Hatipoglu OF. Polymorphisms in MMP-2 and TIMP-2 in Turkish patients with prostate cancer, Turk J Med Sci 2014; 44:839-843
- Yamak N, Yaykasli KO, Yilmaz U, Eroz R, Uzunlar AK, Ankaralı H, Sahiner C, Baltaci D. Association between survivin gene polymorphisms and the susceptibility to colon cancer development in turkish population, Asian Pac J Cancer Prev 2014; 15:8963-8967.
- Zhang W, Niu Z, Yin K, Liu P, Chen L. Quick identification and quantification of Proteus mirabilis by polymerase chain reaction (PCR) assays. Ann Microbiol 2013; 63: 683-689.
- Kaftandzieva A, Trajkovska-Dokic E, Panovski N. Prevalence and molecular characterization of extended spectrum beta-lactamases (ESBLs) producing Escherichia coli and Klebsiella pneumoniae. Prilozi 2011; 32: 129-141.
- Ahmed OB, Asghar AH, Bahwerth FS. Prevalence of ESBL genes of Pseudomonas aeruginosa strains isolated from Makkah Hospitals, Saudi Arabia. Euro J Biol Med Sci Res 2015; 3: 12-18.
- Perim MC, Borges JDC, Celeste SR, Orsolin Ede F, Mendes RR, Mendes GO, Ferreira RL, Carreiro SC, Pranchevicius MC. Aerobic bacterial profile and antibiotic resistance in patients with diabetic foot infections. Rev Soc Bras Med Trop 2015; 48: 546-554.
- Rampal SRL, Devaraj NK, Yoganathan PR, Mahusin MA, Teh SW, Kumar SS. Distribution and prevalence of microorganisms causing diabetic foot infection in Hospital Serdang and Hospital Ampang for the year 2010 to 2014. Biocatal Agric Biotechnol 2019; 17: 256-260.
- Seyedjavadi SS, Goudarzi M, Sabzehali F. Relation between blaTEM, blaSHV and blaCTX-M genes and acute urinary tract infections. J Acute Dis 2016; 5: 71-76.
- Datta P, Chander J, Gupta V, Mohi GK, Attri AK. Evaluation of various risk factors associated with multidrug-resistant organisms isolated from diabetic foot ulcer patients. J Lab Physicians 2019; 11: 58.
- Pal N, Hooja S, Sharma R, Maheshwari R. Phenotypic detection and antibiogram of β"‘lactamase"‘producing Proteus species in a Tertiary Care Hospital, India. Ann Med Health Sci Res 2016; 6: 267-279.
- Datta P, Gupta V, Arora S, Garg S, Chander J. Epidemiology of extended-spectrum β-lactamase, AmpC, and carbapenemase production in Proteus mirabilis. Jpn J Infect Dis 2014; 67: 44-46.
- Adeyemo AT, Kolawole B, Rotimi VO, Aboderin AO. Multicenter study of the burden of multidrug-resistant bacteria in the etiology of infected diabetic foot ulcers. BioRxiv 2019: 625012.
- Anvarinejad M, Pouladfar G, Japoni A, Bolandparvaz S, Satiary Z, Abbasi P, Mardaneh J. Isolation and antibiotic susceptibility of the microorganisms isolated from diabetic foot infections in Nemazee Hospital, Southern Iran. J Pathog 2015; 2015.
- Chaudhry WN, Badar R, Jamal M, Jeong J, Zafar J, Andleeb S. Clinico"‘microbiological study and antibiotic resistance profile of mecA and ESBL gene prevalence in patients with diabetic foot infections. Exp Ther Med 2016; 11: 1031-1038.
- Chen CM, Lai CH, Wu HJ, Wu LT. Genetic characteristic of class 1 integrons in Proteus mirabilis isolates from urine samples. Bio Med 2017; 7(2).
- Alabi OS, Mendonça N, Adeleke OE, da Silva GJ. Molecular screening of antibiotic-resistant determinants among multidrug-resistant clinical isolates of Proteus mirabilis from Southwest Nigeria. Afr Health Sci 2017; 17: 356-365.
- Saffar H, Niaraki NA, Tali AG, Baseri Z, Abdollahi A, Yalfani R. Prevalence of AmpC β-lactamase in clinical isolates of Escherichia coli, Klebsiella spp., and Proteus mirabilis in a Tertiary Hospital in Tehran, Iran. Jundishapur J Microbiol 2016; 9:12.
- Helmy MM, Wasfi R. Phenotypic and molecular characterization of plasmid mediated AmpC β-lactamases among Escherichia coli, Klebsiella spp., and Proteus mirabilis isolated from urinary tract infections in Egyptian hospitals. Biomed. Res Int 2014; 2014.
- Lin MF, Liou M-L, Kuo CH, Lin YY, Chen JY, Kuo HY. Antimicrobial susceptibility and molecular epidemiology of Proteus mirabilis isolates from three hospitals in Northern Taiwan. Microb Drug Resist 2019.
- Shabeeb BT, Alghanimi YK, Ahmed MM. Molecular and Bacteriologic study of β-lactam resistance Proteus mirabilis associated with urinary tract infection in Holy Karbala province, Iraq. JPSR 2018; 10: 549-555.
- Song W, Kim J, Bae IK, Jeong SH, Seo YH, Shin JH, Jang SJ, Uh Y, Shin JH, Lee MK. Chromosome-encoded AmpC and CTX-M extended-spectrum β-lactamases in clinical isolates of Proteus mirabilis from Korea. Antimicrob Agents Chemother 2011; 55: 1414-1419.
- Bidet P, Verdet C, Gautier V, Bingen E, Arlet G. First description of DHA-1 ampC β-lactamase in Proteus mirabilis. Clin Microbiol Infect 2005; 11: 591-592.
- Yong D, Lim Y, Song W, Choi YS, Park DY, Lee H, Yum JH, Lee K, Kim JM, Chong Y. Plasmid-mediated, inducible AmpC β-lactamase (DHA-1)-producing Enterobacteriaceae at a Korean hospital: wide dissemination in Klebsiella pneumoniae and Klebsiella oxytoca and emergence in Proteus mirabilis. Diagn Microbiol Infect Dis 2005; 53: 65-70.
- Fam N, Gamal D, El Said M, El Defrawy I, El Dadei E, El Attar S, Sorur A, Ahmed S, Klena J. Prevalence of plasmid-mediated ampC genes in clinical isolates of Enterobacteriaceae from Cairo, Egypt. Microbiol. Res J Int 2013: 525-537.
- Park SD, Uh Y, Lee G, Lim K, Kim JB, Jeong SH. Prevalence and resistance patterns of extended"spectrum and AmpC β"lactamase in Escherichia coli, Klebsiella pneumoniae, Proteus mirabilis, and Salmonella serovar Stanley in a Korean tertiary hospital. Apmis 2010; 118: 801-808.
- Ibrahimagić A, Uzunović S, Bedenić B. Prevalence of co-existence genes and clonal spread of ESBL-producing isolates causing hospital and community-acquired infections in Zenica-Doboj Canton, Bosnia and Herzegovina. J Health Sci 2017; 7: 80-90.
- Pokhrel RH, Thapa B, Kafle R, Shah PK, Tribuddharat C. Co-existence of beta-lactamases in clinical isolates of Escherichia coli from Kathmandu, Nepal. BMC Res Notes 2014; 7: 694.
References
Kaimkhani GM, Siddiqui AA, Rasheed N, Rajput MI, Kumar J, Khan MH, Nisar S, Mustafa S, Yaqoob U. Pattern of infecting microorganisms and their susceptibility to antimicrobial drugs in patients with diabetic foot infections in a tertiary care hospital in karachi, pakistan. Cureus 2018; 10:6.
Miyan Z, Fawwad A, Sabir R, Basit A. Microbiological pattern of diabetic foot infections at a tertiary care center in a developing country. Age 2017; 53: 10.20.
Thurber EG, Kisuule F, Humbyrd C, Townsend J. Inpatient management of diabetic foot infections: a review of the guidelines for hospitalists. J Hosp Med 2017; 12: 994-1000.
Shankar E, Mohan V, Premalatha G, Srinivasan R, Usha A. Bacterial etiology of diabetic foot infections in South India. Eur J Intern Med 2005; 16: 567-570.
Noor S, Ahmad J, Parwez I, Ozair M. Culture-based screening of aerobic microbiome in diabetic foot subjects and developing non-healing ulcers. Front Microbiol 2016; 7: 1792.
Hicks CW, Selvarajah S, Mathioudakis N, Sherman RL, Hines KF, Black III JH, Abularrage CJ. Burden of infected diabetic foot ulcers on hospital admissions and costs. Ann Vasc Surg 2016; 33: 149-158.
Umadevi S, Kumar S, Joseph NM, Easow JM, Kandhakumari G, Srirangaraj S, Raj S, Stephen S. Microbiological study of diabetic foot infections. Indian. J .Med. Spec. 2011; 2;1.
Kang WJ, Shi L, Shi Y, Cheng L, Ai HW, Zhao WJ. Analysis on distribution, drug resistance and risk factors of multi drug resistant bacteria in diabetic foot infection. Biomed Res 2017; 28: 10186-10190.
Lipsky BA, Berendt AR, Cornia PB, Pile JC, Peters EJ, Armstrong DG, Deery HG, Embil JM, Joseph WS, Karchmer AW. 2012 Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis 2012; 54: 132-173.
Zubair M, Malik A, Ahmad J. Clinico-bacteriology and risk factors for the diabetic foot infection with multidrug resistant microorganisms in north India. Biol Med. 2010; 2: 22-34.
Grayson ML. Diabetic foot infections: antimicrobial therapy. Infect. Dis Clin North Am 1995; 9: 143-161.
Lipsky BA. Diabetic foot infections: current treatment and delaying the ‘post"antibiotic era'. Diabetes. Metab Res Rev 2016; 32: 246-253.
Citron DM, Goldstein EJ, Merriam CV, Lipsky BA, Abramson MA. Bacteriology of moderate-to-severe diabetic foot infections and in vitro activity of antimicrobial agents. J Clin Microbiol 2007; 45: 2819-2828.
Shanmugam P, Jeya M. The bacteriology of diabetic foot ulcers, with a special reference to multidrug resistant strains. J Clin Diagn Res 2013; 7: 441.
Caubey M, Suchitra M. Occurrence of TEM, SHV and CTX-M β lactamases in clinical isolates of Proteus species in a tertiary care center. Infect. Disord. Drug .Targets 2018; 18: 68-71.
Hegazy W. Diclofenac inhibits virulence of Proteus mirabilis isolated from diabetic foot ulcer. Afr J Microbiol Res 2016; 10: 733-743.
Tom IM, Agbo E, Faruk UA, Umoru AM, Ibrahim MM, Umar JB, Haruna AB, Aliyu A. Implication of Proteus spp in the pathology of nosocomial wound infection in northeastern nigeria. IJPR 2018; 9: 1-8.
Mordi R, Momoh M. Incidence of Proteus species in wound infections and their sensitivity pattern in the University of Benin Teaching Hospital. Afr J Biotechnol 2009; 8:5.
Huang Y, Cao Y, Zou M, Luo X, Jiang Y, Xue Y, Gao F. A comparison of tissue versus swab culturing of infected diabetic foot wounds. Int J Endocrinol 2016; 2016.
CLSI C. Performance standards for antimicrobial susceptibility testing. Clinical Lab Standards Institute 2016.
Yaykasli KO, Kayıkçı MA, Yamak N, Soguktas H, Duzenli S, Arslan AO, Metin A, Kaya E, Hatipoglu OF. Polymorphisms in MMP-2 and TIMP-2 in Turkish patients with prostate cancer, Turk J Med Sci 2014; 44:839-843
Yamak N, Yaykasli KO, Yilmaz U, Eroz R, Uzunlar AK, Ankaralı H, Sahiner C, Baltaci D. Association between survivin gene polymorphisms and the susceptibility to colon cancer development in turkish population, Asian Pac J Cancer Prev 2014; 15:8963-8967.
Zhang W, Niu Z, Yin K, Liu P, Chen L. Quick identification and quantification of Proteus mirabilis by polymerase chain reaction (PCR) assays. Ann Microbiol 2013; 63: 683-689.
Kaftandzieva A, Trajkovska-Dokic E, Panovski N. Prevalence and molecular characterization of extended spectrum beta-lactamases (ESBLs) producing Escherichia coli and Klebsiella pneumoniae. Prilozi 2011; 32: 129-141.
Ahmed OB, Asghar AH, Bahwerth FS. Prevalence of ESBL genes of Pseudomonas aeruginosa strains isolated from Makkah Hospitals, Saudi Arabia. Euro J Biol Med Sci Res 2015; 3: 12-18.
Perim MC, Borges JDC, Celeste SR, Orsolin Ede F, Mendes RR, Mendes GO, Ferreira RL, Carreiro SC, Pranchevicius MC. Aerobic bacterial profile and antibiotic resistance in patients with diabetic foot infections. Rev Soc Bras Med Trop 2015; 48: 546-554.
Rampal SRL, Devaraj NK, Yoganathan PR, Mahusin MA, Teh SW, Kumar SS. Distribution and prevalence of microorganisms causing diabetic foot infection in Hospital Serdang and Hospital Ampang for the year 2010 to 2014. Biocatal Agric Biotechnol 2019; 17: 256-260.
Seyedjavadi SS, Goudarzi M, Sabzehali F. Relation between blaTEM, blaSHV and blaCTX-M genes and acute urinary tract infections. J Acute Dis 2016; 5: 71-76.
Datta P, Chander J, Gupta V, Mohi GK, Attri AK. Evaluation of various risk factors associated with multidrug-resistant organisms isolated from diabetic foot ulcer patients. J Lab Physicians 2019; 11: 58.
Pal N, Hooja S, Sharma R, Maheshwari R. Phenotypic detection and antibiogram of β"‘lactamase"‘producing Proteus species in a Tertiary Care Hospital, India. Ann Med Health Sci Res 2016; 6: 267-279.
Datta P, Gupta V, Arora S, Garg S, Chander J. Epidemiology of extended-spectrum β-lactamase, AmpC, and carbapenemase production in Proteus mirabilis. Jpn J Infect Dis 2014; 67: 44-46.
Adeyemo AT, Kolawole B, Rotimi VO, Aboderin AO. Multicenter study of the burden of multidrug-resistant bacteria in the etiology of infected diabetic foot ulcers. BioRxiv 2019: 625012.
Anvarinejad M, Pouladfar G, Japoni A, Bolandparvaz S, Satiary Z, Abbasi P, Mardaneh J. Isolation and antibiotic susceptibility of the microorganisms isolated from diabetic foot infections in Nemazee Hospital, Southern Iran. J Pathog 2015; 2015.
Chaudhry WN, Badar R, Jamal M, Jeong J, Zafar J, Andleeb S. Clinico"‘microbiological study and antibiotic resistance profile of mecA and ESBL gene prevalence in patients with diabetic foot infections. Exp Ther Med 2016; 11: 1031-1038.
Chen CM, Lai CH, Wu HJ, Wu LT. Genetic characteristic of class 1 integrons in Proteus mirabilis isolates from urine samples. Bio Med 2017; 7(2).
Alabi OS, Mendonça N, Adeleke OE, da Silva GJ. Molecular screening of antibiotic-resistant determinants among multidrug-resistant clinical isolates of Proteus mirabilis from Southwest Nigeria. Afr Health Sci 2017; 17: 356-365.
Saffar H, Niaraki NA, Tali AG, Baseri Z, Abdollahi A, Yalfani R. Prevalence of AmpC β-lactamase in clinical isolates of Escherichia coli, Klebsiella spp., and Proteus mirabilis in a Tertiary Hospital in Tehran, Iran. Jundishapur J Microbiol 2016; 9:12.
Helmy MM, Wasfi R. Phenotypic and molecular characterization of plasmid mediated AmpC β-lactamases among Escherichia coli, Klebsiella spp., and Proteus mirabilis isolated from urinary tract infections in Egyptian hospitals. Biomed. Res Int 2014; 2014.
Lin MF, Liou M-L, Kuo CH, Lin YY, Chen JY, Kuo HY. Antimicrobial susceptibility and molecular epidemiology of Proteus mirabilis isolates from three hospitals in Northern Taiwan. Microb Drug Resist 2019.
Shabeeb BT, Alghanimi YK, Ahmed MM. Molecular and Bacteriologic study of β-lactam resistance Proteus mirabilis associated with urinary tract infection in Holy Karbala province, Iraq. JPSR 2018; 10: 549-555.
Song W, Kim J, Bae IK, Jeong SH, Seo YH, Shin JH, Jang SJ, Uh Y, Shin JH, Lee MK. Chromosome-encoded AmpC and CTX-M extended-spectrum β-lactamases in clinical isolates of Proteus mirabilis from Korea. Antimicrob Agents Chemother 2011; 55: 1414-1419.
Bidet P, Verdet C, Gautier V, Bingen E, Arlet G. First description of DHA-1 ampC β-lactamase in Proteus mirabilis. Clin Microbiol Infect 2005; 11: 591-592.
Yong D, Lim Y, Song W, Choi YS, Park DY, Lee H, Yum JH, Lee K, Kim JM, Chong Y. Plasmid-mediated, inducible AmpC β-lactamase (DHA-1)-producing Enterobacteriaceae at a Korean hospital: wide dissemination in Klebsiella pneumoniae and Klebsiella oxytoca and emergence in Proteus mirabilis. Diagn Microbiol Infect Dis 2005; 53: 65-70.
Fam N, Gamal D, El Said M, El Defrawy I, El Dadei E, El Attar S, Sorur A, Ahmed S, Klena J. Prevalence of plasmid-mediated ampC genes in clinical isolates of Enterobacteriaceae from Cairo, Egypt. Microbiol. Res J Int 2013: 525-537.
Park SD, Uh Y, Lee G, Lim K, Kim JB, Jeong SH. Prevalence and resistance patterns of extended"spectrum and AmpC β"lactamase in Escherichia coli, Klebsiella pneumoniae, Proteus mirabilis, and Salmonella serovar Stanley in a Korean tertiary hospital. Apmis 2010; 118: 801-808.
Ibrahimagić A, Uzunović S, Bedenić B. Prevalence of co-existence genes and clonal spread of ESBL-producing isolates causing hospital and community-acquired infections in Zenica-Doboj Canton, Bosnia and Herzegovina. J Health Sci 2017; 7: 80-90.
Pokhrel RH, Thapa B, Kafle R, Shah PK, Tribuddharat C. Co-existence of beta-lactamases in clinical isolates of Escherichia coli from Kathmandu, Nepal. BMC Res Notes 2014; 7: 694.