Antimicrobials Resistance Profiling and Clonal Lineages of Staphylococcus aureus Isolated from Cockroaches in University-Affiliated Hospitals, 2023
-
Mohsen Karami
,
Mehdi Safari
,
Yasin Saberi
,
Seyedeh Zohre Mirbagheri
,
Mehrdad Halaji
,
Jalal Jafarzadeh
,
Abazar Pournajaf
Abstract
Background: Cockroaches, recognized as mechanical vectors, play a crucial role in transmitting microbial pathogens. Staphylococcus aureus (S. aureus), particularly antibiotic-resistant strains, poses a significant threat as a nosocomial pathogen. This study aimed to investigate the resistance profiles to gentamicin, vancomycin, and antiseptics in S. aureus strains isolated from cockroaches in hospitals affiliated with Babol University of Medical Sciences.
Methods: In this cross-sectional study, 60 S. aureus strains were isolated from 376 cockroaches in three university-affiliated hospitals. Antibiotic susceptibility to gentamicin and vancomycin was tested by disk diffusion and agar dilution. PCR was used to detect resistance and antiseptic genes, and MLVA typing determined the genetic relatedness of resistant isolates.
Results: Among the 60 bacterial isolates, 46.7% (28) displayed resistance to gentamicin. The frequencies of aminoglycoside resistance coding genes (AMEs) for the aac(6')-Ie+aph(2″), ant(4')-Ia, aph(3')-IIIa and ant(6)-Ia genes were 64.3%, 42.8%, 17.8%, and 46.4%, respectively. Only 3.3% (2 isolates) exhibited vancomycin resistance, with one isolate (1.7%) carrying the vanA gene. The frequencies of genes encoding the antiseptic resistance genes qacA/B, qacC, qacD, psmA, sasX, and smr were 5%, 20%, 18.3%, 26.4%, 1.2%, and 31.7%, respectively. Analysis of agr gene types showed that agr type I was the most prevalent. In addition, the multiple-locus variable number tandem-repeat analysis (MLVA) identified 29 unique type sequences among the identified antibiotic-resistant isolates.
Conclusion: The high genetic diversity among antibiotic-resistant S. aureus isolates, as revealed by MLVA, underscores the importance of controlling hospital cockroach populations to curb the spread of antibiotic resistance.
1. Del Giudice P (2020) Skin infections caused by Staphylococcus aureus. Acta Derm Ve¬nereol. 100(9): 5725.
2. Dayan GH, Mohamed N, Scully IL, Cooper D, Begier E, Eiden J, Jansen KU, Gurtman A, Anderson AS (2016) Staphylococcus aureus: the current state of disease, path¬ophysiology and strategies for pre¬ven¬tion. Expert Rev Vaccines. 15(11): 1373–1392.
3. Foster TJ (2017) Antibiotic resistance in Staph¬ylococcus aureus. Current status and future prospects. FEMS Microbiol Rev. 41(3): 430–449.
4. Mahdiyoun SM, Kazemian H, Ahanjan M, Houri H, Goudarzi M (2016) Frequency of aminoglycoside-resistance genes in methi¬cillin-resistant Staphylococcus aureus (MRSA) isolates from hospitalized pa¬tients. Jundishapur J Microbiol. 9(8). e35052.
5. Cong Y, Yang S, Rao X (2020) Van¬co¬my-cin resistant Staphylococcus aureus in-fec¬tions: A review of case updating and clin¬ical features. J Adv Res. 21(1):169–176.
6. Zaki MES, Bastawy S, Montasser K (2019) Molecular study of resistance of Staph-ylococcus aureus to antiseptic quaternary ammonium compounds. J Glob Anti¬mi¬crob Resist. 17: 94–97.
7. McClure JA, Zaal DeLongchamp J, Conly JM, Zhang K (2017) Novel multiplex PCR assay for detection of chlorhexidine-qua¬ternary ammonium, mupirocin, and methi¬cillin resistance genes, with simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol. 55(6): 1857–1864.
8. Geraldes C, Tavares L, Gil S, Oliveira M (2023) Biocides in the hospital environ-ment: Application and tolerance devel-op¬ment. Microb Drug Resist. 29(10): 456–476.
9. Yulianti D, Hikam A, Ambarningrum T, Sat¬wika T (2023) Detection of pathogen foodborne disease bacteria Staphy¬lococ-cus aureus from German Cockroach (Blat¬tella germanica) in the hospital area. IOP Conference Series: Earth and Environ¬mental Science; IOP Publishing.
10. Wannigama DL, Dwivedi R, Zahraei-Ram¬azani A (2014) Prevalence and antibiotic resistance of gram-negative pathogenic bacteria species isolated from Peri¬planeta americana and Blattella germanica in Varanasi, India. J Arthropod Borne Dis. 8(1): 10–20.
11. Abdolmaleki Z, Mashak Z, Safarpoor Dehkor¬di F (2019) Phenotypic and gen-otypic characterization of antibiotic re-sistance in the methicillin-resistant Staph¬ylococ¬cus aureus strains isolated from hos¬pital cockroaches. Antimicrob Resist Infect Control. 8: 1–14.
12. Vazirianzadeh B, Dehghani R, Mehdinejad M, Sharififard M, Nasirabadi N (2014) The first report of drug resistant bacteria isolated from the brown-banded cock¬roach, Supella longipalpa, in Ahvaz, south-west¬ern Iran. J Arthropod Borne Dis. 8(1): 53–59.
13. Rimi SS, Ashraf MN, Sigma SH, Ahammed MT, Siddique MP, Zinnah MA, Rahman MT, Islam MS (2024) Biofilm formation, agr typing and antibiotic resistance pat¬tern in methicillin-resistant Staphy¬lococ¬cus aureus isolated from hospital envi-ronments. Plos One. 19(8): e0308282.
14. Roussel S, Felix B, Vingadassalon N, Grout J, Hennekinne J-A, Guillier L, Brisabois A, Auvray F (2015) Staphylococcus au¬reus strains associated with food poi¬son¬ing outbreaks in France: comparison of different molecular typing methods, in¬cluding MLVA. Front Microbiol. 6: 882.
15. Melles D, Schouls L, Francois P, Herzig S, Verbrugh H, van Belkum A, Schrenzel J (2009) High-throughput typing of Staph-ylococcus aureus by amplified fragment length polymorphism (AFLP) or multi-locus variable number of tandem repeat analysis (MLVA) reveals consistent strain relatedness. Eur J Clin Microbiol Infect Dis. 28(1): 39–45.
16. Mahon CR, Lehman DC (2022) Textbook of Diagnostic Microbiology-E-Book: Text¬book of Diagnostic Microbiology-E-Book: Elsevier Health Sciences.
17. Islam A, Nath AD, Islam K, Islam S, Chakma S, Hossain MB, Al-Faruq A, Hassan MM (2016) Isolation, identification and anti¬microbial resistance profile of Staphy¬lo¬coccus aureus in Cockroaches (Peri¬planeta americana). J Adv Vet Anim Res. 3(3): 221–228.
18. Orhan Z, Kayış A, Kaya E, Aral M (2018) Phenotypic and genotypic analysis of Gen¬tamicin, Penicillin, Methicillin, Vanco¬my¬cin, Linezolid and Tetracycline re¬sistance in clinical isolates of Staphylococcus au¬reus. KSÜ Tarim Doğa Derg. 21(6): 957–965.
19. Institute CaLS (2021) Performance Stand-ards for Antimicrobial Susceptibility Test¬ing: Twentysecond Informational Sup¬ple¬ment M100-S22. CLSI, Wayne, PA, USA.
20. Moses VK, Kandi V, Rao SKD (2020) Min¬imum inhibitory concentrations of vanco¬mycin and daptomycin against methi¬cillin-resistant Staphylococcus aureus isolated from various clinical specimens: A study from south india. Cureus. 12(1): e6749.
21. Tiwari HK, Sen MR (2006) Emergence of vancomycin resistant Staphylococcus au-reus (VRSA) from a tertiary care hospital from northern part of India. BMC Infect Dis. 6: 1–6.
22. Peyvasti VS, Mobarez AM, Shahcheraghi F, Khoramabadi N, Rahmati NR, Doust RH (2020) High-level aminoglycoside re¬sistance and distribution of ami¬nogly-co¬side resistance genes among Entero-coc¬cus spp. clinical isolates in Tehran, Iran. J Glob Antimicrob Resist. 20: 318–323.
23. Weigel LM, Donlan RM, Shin DH, Jensen B, Clark NC, McDougal LK, Zhu W, Musser KA, Thompson J, Kohlerschmidt D, DumasN, Limberger RJ, Patel JB (2007) High-level vancomycin-resistant Staph¬y¬lo¬coc¬cus aureus isolates associated with a polymicrobial biofilm. Antimicrob Agents Chemother. 51(1): 231–238.
24. Shokravi Z, Mehrad L, Ramazani A (2015) Detecting the frequency of amino¬gly¬co¬side modifying enzyme encoding genes among clinical isolates of methicillin-re¬sistant Staphylococcus aureus. Bioim¬pacts: BI. 5(2): 87–91.
25. Türkyilmaz S, Erdem V, Bozdigan B (2010) Investigation of antimicrobial suscep¬ti¬bil¬ity for enterococci isolated from cats and dogs and the determination of resistance genes by polymerase chain reaction. Turk J Vet Anim Sci. 34(1): 61–68.
26. Antiabong JF, Kock MM, Mbelle NM, Ehlers MM (2017) Diversity of multidrug efflux genes and phenotypic evaluation of the in vitro resistance dynamics of clinical Staph¬ylococcus aureus isolates using methicil¬lin; a model β-lactam. Open Microbiol J. 11: 132–141.
27. Mayer S, Boos M, Beyer A, Fluit AC, Schmitz FJ (2001) Distribution of the an¬tiseptic resistance genes qacA, qacB and qacC in 497 methicillin-resistant and sus¬ceptible European isolates of Staphylo¬coccus aureus. J Antimicrob Chemother. 47(6): 896–897.
28. Ammar A, Attia A, Abd El-Hamid M, El-Shorbagy I, Abd El-Kader S (2016) Ge-netic basis of resistance waves among methi¬cillin resistant Staphylococcus au-reus isolates recovered from milk and meat products in Egypt. Cell Mol Biol. 62(10): 7–15.
29. Costa SS, Falcão C, Viveiros M, Machado D, Martins M, Melo-Cristino J, Amaral L, Couto I (2011) Exploring the con¬tri-bution of efflux on the resistance to fluo¬roquinolones in clinical isolates of Staph¬ylococcus aureus. BMC Microbiol. 11: 241.
30. Monecke S, Müller E, Dorneanu OS, Vremeră T, Ehricht R (2014) Molecular typing of MRSA and of clinical Staph-ylococcus aureus isolates from Iaşi, Ro-mania. PloS One. 9(5): e97833.
31. Berube BJ, Sampedro GR, Otto M, Bubeck Wardenburg J (2014) The psm α locus regulates production of Staphylococcus aureus alpha-toxin during infection. In¬fect Immun. 82(8): 3350–3358.
32. Gilot P, Lina G, Cochard T, Poutrel B (2002) Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a popu¬la¬tion of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol. 40(11): 4060–4067.
33. Schouls LM, Spalburg EC, van Luit M, Huijsdens XW, Pluister GN, van Santen-Verheuvel MG, Han G J van der Heide, Grundmann H, Heck ME, de Neeling AJ (2009) Multiple-locus variable number tandem repeat analysis of Staphy¬lococ¬cus aureus: comparison with pulsed-field gel electrophoresis and spa-typing. PloS One. 4(4): e5082.
34. Zarchi AAK, Vatani H (2009) A survey on species and prevalence rate of bacterial agents isolated from cockroaches in three hospitals. Vector-Borne Zoonotic Dis. 9 (2): 197–200.
35. Nasirian H (2019) Contamination of cock-roaches (Insecta: Blattaria) by medically important bacteriae: a systematic review and meta-analysis. J Med Entomol. 56 (6): 1534–1554.
36. Soureshjani EH, Doosti A (2013) Exami-nation methicillin-resistant Staphy¬lococ-cus aureus (MRSA) prevalence in cock-roaches from hospital in Chaharmahal-va-Bakhtiari province, Iran by polymerase chain reaction (PCR). Int J Med Sci. 5(7): 324–329.
37. Isaac C, Orue PO, Iyamu MI, Ehiaghe JI, Isaac O (2014) Comparative analysis of pathogenic organisms in cockroaches from different community settings in Edo State, Nigeria. Korean J Parasitol. 52(2): 177–181.
38. Moges F, Eshetie S, Endris M, Huruy K, Muluye D, Feleke T, Silassie FG, Ayalew G, Nagappan R (2016) Cockroaches as a source of high bacterial pathogens with multidrug resistant strains in Gondar town, Ethiopia. Biomed Res Int. 2016: 2825056.
39. Menasria T, Samir T, Mahcene D, Benam-mar L, Megri R, Boukoucha M, Manel Debabza M (2015) External bacterial flora and antimicrobial susceptibility patterns of Staphylococcus spp. and Pseudo¬mo¬nas spp. isolated from two household cock¬roaches, Blattella germanica and Blatta orientalis. Biomed Environ Sci. 28(4): 316–320.
40. Oliveira PS, Souza SG, Campos GB, Silva DCd, Sousa DS, Araújo SP, Ferreira LP, Santos VM, Amorim AT, Santos AM, Timenetsky J, Cruz MP, Yatsuda R, Marques LM (2014) Isolation, patho-genic¬ity and disinfection of Staphylococ¬cus aureus carried by insects in two public hospitals of Vitória da Conquista, Bahia, Brazil. Braz J Infect Dis. 18(2): 129–136.
41. Pai HH, Chen WC, Peng CF (2004) Cock-roaches as potential vectors of noso¬com-ial infections. Infect Control Hosp Epi-demiol. 25(11): 979–984.
42. Miyazaki NHT, Abreu AO, Marin VA, Rezende CA, Moraes MT, Villas Bôas MHS (2007) The presence of qacA/B gene in Brazilian methicillin-resistant Staphy¬lo¬coccus aureus. Ann Clin Microbiol An¬timicrob. 102: 539–540.
43. Jaglic Z, Cervinkova D (2012) Genetic basis of resistance to quaternary ammonium compounds--the qac genes and their role: a review. Vet Med. 57(6): 275–281.
44. Sobral D, Schwarz S, Bergonier D, Brisabois A, Feßler AT, Gilbert FB, Kadlec K, Lebeau B, Loisy-Hamon F, Treilles M, Pourcel Ch, Vergnaud G (2012) High throughput multiple locus variable num¬ber of tandem repeat analysis (MLVA) of Staphylococcus aureus from human, an¬imal and food sources. PLoS One. 7(5): e33967.
45. Ikawaty R, Willems RJ, Box AT, Verhoef J, Fluit AC (2008) Novel multiple-locus variable-number tandem-repeat analysis method for rapid molecular typing of hu¬man Staphylococcus aureus. J Clin Mi¬crobiol. 46(9): 3147–3151.
46. Brandt KM, Mellmann A, Ballhausen B, Jenke C, van der Wolf PJ, Broens EM, Becker K, Köck R (2013) Evaluation of multiple-locus variable number of tan-dem repeats analysis for typing live-stock-as¬sociated methicillin-resistant Staphylo¬coc¬cus aureus. PLoS One. 8(1): e54425.
2. Dayan GH, Mohamed N, Scully IL, Cooper D, Begier E, Eiden J, Jansen KU, Gurtman A, Anderson AS (2016) Staphylococcus aureus: the current state of disease, path¬ophysiology and strategies for pre¬ven¬tion. Expert Rev Vaccines. 15(11): 1373–1392.
3. Foster TJ (2017) Antibiotic resistance in Staph¬ylococcus aureus. Current status and future prospects. FEMS Microbiol Rev. 41(3): 430–449.
4. Mahdiyoun SM, Kazemian H, Ahanjan M, Houri H, Goudarzi M (2016) Frequency of aminoglycoside-resistance genes in methi¬cillin-resistant Staphylococcus aureus (MRSA) isolates from hospitalized pa¬tients. Jundishapur J Microbiol. 9(8). e35052.
5. Cong Y, Yang S, Rao X (2020) Van¬co¬my-cin resistant Staphylococcus aureus in-fec¬tions: A review of case updating and clin¬ical features. J Adv Res. 21(1):169–176.
6. Zaki MES, Bastawy S, Montasser K (2019) Molecular study of resistance of Staph-ylococcus aureus to antiseptic quaternary ammonium compounds. J Glob Anti¬mi¬crob Resist. 17: 94–97.
7. McClure JA, Zaal DeLongchamp J, Conly JM, Zhang K (2017) Novel multiplex PCR assay for detection of chlorhexidine-qua¬ternary ammonium, mupirocin, and methi¬cillin resistance genes, with simultaneous discrimination of Staphylococcus aureus from coagulase-negative staphylococci. J Clin Microbiol. 55(6): 1857–1864.
8. Geraldes C, Tavares L, Gil S, Oliveira M (2023) Biocides in the hospital environ-ment: Application and tolerance devel-op¬ment. Microb Drug Resist. 29(10): 456–476.
9. Yulianti D, Hikam A, Ambarningrum T, Sat¬wika T (2023) Detection of pathogen foodborne disease bacteria Staphy¬lococ-cus aureus from German Cockroach (Blat¬tella germanica) in the hospital area. IOP Conference Series: Earth and Environ¬mental Science; IOP Publishing.
10. Wannigama DL, Dwivedi R, Zahraei-Ram¬azani A (2014) Prevalence and antibiotic resistance of gram-negative pathogenic bacteria species isolated from Peri¬planeta americana and Blattella germanica in Varanasi, India. J Arthropod Borne Dis. 8(1): 10–20.
11. Abdolmaleki Z, Mashak Z, Safarpoor Dehkor¬di F (2019) Phenotypic and gen-otypic characterization of antibiotic re-sistance in the methicillin-resistant Staph¬ylococ¬cus aureus strains isolated from hos¬pital cockroaches. Antimicrob Resist Infect Control. 8: 1–14.
12. Vazirianzadeh B, Dehghani R, Mehdinejad M, Sharififard M, Nasirabadi N (2014) The first report of drug resistant bacteria isolated from the brown-banded cock¬roach, Supella longipalpa, in Ahvaz, south-west¬ern Iran. J Arthropod Borne Dis. 8(1): 53–59.
13. Rimi SS, Ashraf MN, Sigma SH, Ahammed MT, Siddique MP, Zinnah MA, Rahman MT, Islam MS (2024) Biofilm formation, agr typing and antibiotic resistance pat¬tern in methicillin-resistant Staphy¬lococ¬cus aureus isolated from hospital envi-ronments. Plos One. 19(8): e0308282.
14. Roussel S, Felix B, Vingadassalon N, Grout J, Hennekinne J-A, Guillier L, Brisabois A, Auvray F (2015) Staphylococcus au¬reus strains associated with food poi¬son¬ing outbreaks in France: comparison of different molecular typing methods, in¬cluding MLVA. Front Microbiol. 6: 882.
15. Melles D, Schouls L, Francois P, Herzig S, Verbrugh H, van Belkum A, Schrenzel J (2009) High-throughput typing of Staph-ylococcus aureus by amplified fragment length polymorphism (AFLP) or multi-locus variable number of tandem repeat analysis (MLVA) reveals consistent strain relatedness. Eur J Clin Microbiol Infect Dis. 28(1): 39–45.
16. Mahon CR, Lehman DC (2022) Textbook of Diagnostic Microbiology-E-Book: Text¬book of Diagnostic Microbiology-E-Book: Elsevier Health Sciences.
17. Islam A, Nath AD, Islam K, Islam S, Chakma S, Hossain MB, Al-Faruq A, Hassan MM (2016) Isolation, identification and anti¬microbial resistance profile of Staphy¬lo¬coccus aureus in Cockroaches (Peri¬planeta americana). J Adv Vet Anim Res. 3(3): 221–228.
18. Orhan Z, Kayış A, Kaya E, Aral M (2018) Phenotypic and genotypic analysis of Gen¬tamicin, Penicillin, Methicillin, Vanco¬my¬cin, Linezolid and Tetracycline re¬sistance in clinical isolates of Staphylococcus au¬reus. KSÜ Tarim Doğa Derg. 21(6): 957–965.
19. Institute CaLS (2021) Performance Stand-ards for Antimicrobial Susceptibility Test¬ing: Twentysecond Informational Sup¬ple¬ment M100-S22. CLSI, Wayne, PA, USA.
20. Moses VK, Kandi V, Rao SKD (2020) Min¬imum inhibitory concentrations of vanco¬mycin and daptomycin against methi¬cillin-resistant Staphylococcus aureus isolated from various clinical specimens: A study from south india. Cureus. 12(1): e6749.
21. Tiwari HK, Sen MR (2006) Emergence of vancomycin resistant Staphylococcus au-reus (VRSA) from a tertiary care hospital from northern part of India. BMC Infect Dis. 6: 1–6.
22. Peyvasti VS, Mobarez AM, Shahcheraghi F, Khoramabadi N, Rahmati NR, Doust RH (2020) High-level aminoglycoside re¬sistance and distribution of ami¬nogly-co¬side resistance genes among Entero-coc¬cus spp. clinical isolates in Tehran, Iran. J Glob Antimicrob Resist. 20: 318–323.
23. Weigel LM, Donlan RM, Shin DH, Jensen B, Clark NC, McDougal LK, Zhu W, Musser KA, Thompson J, Kohlerschmidt D, DumasN, Limberger RJ, Patel JB (2007) High-level vancomycin-resistant Staph¬y¬lo¬coc¬cus aureus isolates associated with a polymicrobial biofilm. Antimicrob Agents Chemother. 51(1): 231–238.
24. Shokravi Z, Mehrad L, Ramazani A (2015) Detecting the frequency of amino¬gly¬co¬side modifying enzyme encoding genes among clinical isolates of methicillin-re¬sistant Staphylococcus aureus. Bioim¬pacts: BI. 5(2): 87–91.
25. Türkyilmaz S, Erdem V, Bozdigan B (2010) Investigation of antimicrobial suscep¬ti¬bil¬ity for enterococci isolated from cats and dogs and the determination of resistance genes by polymerase chain reaction. Turk J Vet Anim Sci. 34(1): 61–68.
26. Antiabong JF, Kock MM, Mbelle NM, Ehlers MM (2017) Diversity of multidrug efflux genes and phenotypic evaluation of the in vitro resistance dynamics of clinical Staph¬ylococcus aureus isolates using methicil¬lin; a model β-lactam. Open Microbiol J. 11: 132–141.
27. Mayer S, Boos M, Beyer A, Fluit AC, Schmitz FJ (2001) Distribution of the an¬tiseptic resistance genes qacA, qacB and qacC in 497 methicillin-resistant and sus¬ceptible European isolates of Staphylo¬coccus aureus. J Antimicrob Chemother. 47(6): 896–897.
28. Ammar A, Attia A, Abd El-Hamid M, El-Shorbagy I, Abd El-Kader S (2016) Ge-netic basis of resistance waves among methi¬cillin resistant Staphylococcus au-reus isolates recovered from milk and meat products in Egypt. Cell Mol Biol. 62(10): 7–15.
29. Costa SS, Falcão C, Viveiros M, Machado D, Martins M, Melo-Cristino J, Amaral L, Couto I (2011) Exploring the con¬tri-bution of efflux on the resistance to fluo¬roquinolones in clinical isolates of Staph¬ylococcus aureus. BMC Microbiol. 11: 241.
30. Monecke S, Müller E, Dorneanu OS, Vremeră T, Ehricht R (2014) Molecular typing of MRSA and of clinical Staph-ylococcus aureus isolates from Iaşi, Ro-mania. PloS One. 9(5): e97833.
31. Berube BJ, Sampedro GR, Otto M, Bubeck Wardenburg J (2014) The psm α locus regulates production of Staphylococcus aureus alpha-toxin during infection. In¬fect Immun. 82(8): 3350–3358.
32. Gilot P, Lina G, Cochard T, Poutrel B (2002) Analysis of the genetic variability of genes encoding the RNA III-activating components Agr and TRAP in a popu¬la¬tion of Staphylococcus aureus strains isolated from cows with mastitis. J Clin Microbiol. 40(11): 4060–4067.
33. Schouls LM, Spalburg EC, van Luit M, Huijsdens XW, Pluister GN, van Santen-Verheuvel MG, Han G J van der Heide, Grundmann H, Heck ME, de Neeling AJ (2009) Multiple-locus variable number tandem repeat analysis of Staphy¬lococ¬cus aureus: comparison with pulsed-field gel electrophoresis and spa-typing. PloS One. 4(4): e5082.
34. Zarchi AAK, Vatani H (2009) A survey on species and prevalence rate of bacterial agents isolated from cockroaches in three hospitals. Vector-Borne Zoonotic Dis. 9 (2): 197–200.
35. Nasirian H (2019) Contamination of cock-roaches (Insecta: Blattaria) by medically important bacteriae: a systematic review and meta-analysis. J Med Entomol. 56 (6): 1534–1554.
36. Soureshjani EH, Doosti A (2013) Exami-nation methicillin-resistant Staphy¬lococ-cus aureus (MRSA) prevalence in cock-roaches from hospital in Chaharmahal-va-Bakhtiari province, Iran by polymerase chain reaction (PCR). Int J Med Sci. 5(7): 324–329.
37. Isaac C, Orue PO, Iyamu MI, Ehiaghe JI, Isaac O (2014) Comparative analysis of pathogenic organisms in cockroaches from different community settings in Edo State, Nigeria. Korean J Parasitol. 52(2): 177–181.
38. Moges F, Eshetie S, Endris M, Huruy K, Muluye D, Feleke T, Silassie FG, Ayalew G, Nagappan R (2016) Cockroaches as a source of high bacterial pathogens with multidrug resistant strains in Gondar town, Ethiopia. Biomed Res Int. 2016: 2825056.
39. Menasria T, Samir T, Mahcene D, Benam-mar L, Megri R, Boukoucha M, Manel Debabza M (2015) External bacterial flora and antimicrobial susceptibility patterns of Staphylococcus spp. and Pseudo¬mo¬nas spp. isolated from two household cock¬roaches, Blattella germanica and Blatta orientalis. Biomed Environ Sci. 28(4): 316–320.
40. Oliveira PS, Souza SG, Campos GB, Silva DCd, Sousa DS, Araújo SP, Ferreira LP, Santos VM, Amorim AT, Santos AM, Timenetsky J, Cruz MP, Yatsuda R, Marques LM (2014) Isolation, patho-genic¬ity and disinfection of Staphylococ¬cus aureus carried by insects in two public hospitals of Vitória da Conquista, Bahia, Brazil. Braz J Infect Dis. 18(2): 129–136.
41. Pai HH, Chen WC, Peng CF (2004) Cock-roaches as potential vectors of noso¬com-ial infections. Infect Control Hosp Epi-demiol. 25(11): 979–984.
42. Miyazaki NHT, Abreu AO, Marin VA, Rezende CA, Moraes MT, Villas Bôas MHS (2007) The presence of qacA/B gene in Brazilian methicillin-resistant Staphy¬lo¬coccus aureus. Ann Clin Microbiol An¬timicrob. 102: 539–540.
43. Jaglic Z, Cervinkova D (2012) Genetic basis of resistance to quaternary ammonium compounds--the qac genes and their role: a review. Vet Med. 57(6): 275–281.
44. Sobral D, Schwarz S, Bergonier D, Brisabois A, Feßler AT, Gilbert FB, Kadlec K, Lebeau B, Loisy-Hamon F, Treilles M, Pourcel Ch, Vergnaud G (2012) High throughput multiple locus variable num¬ber of tandem repeat analysis (MLVA) of Staphylococcus aureus from human, an¬imal and food sources. PLoS One. 7(5): e33967.
45. Ikawaty R, Willems RJ, Box AT, Verhoef J, Fluit AC (2008) Novel multiple-locus variable-number tandem-repeat analysis method for rapid molecular typing of hu¬man Staphylococcus aureus. J Clin Mi¬crobiol. 46(9): 3147–3151.
46. Brandt KM, Mellmann A, Ballhausen B, Jenke C, van der Wolf PJ, Broens EM, Becker K, Köck R (2013) Evaluation of multiple-locus variable number of tan-dem repeats analysis for typing live-stock-as¬sociated methicillin-resistant Staphylo¬coc¬cus aureus. PLoS One. 8(1): e54425.
| Files | ||
| Issue | Vol 19 No 1 (2025) | |
| Section | Original Article | |
| DOI | https://doi.org/10.18502/jad.v19i1.19997 | |
| Keywords | ||
| Gentamicin; Vancomycin; Molecular typing; Cross resistant MLVA | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Karami M, Safari M, Saberi Y, Mirbagheri SZ, Halaji M, Jafarzadeh J, Pournajaf A. Antimicrobials Resistance Profiling and Clonal Lineages of Staphylococcus aureus Isolated from Cockroaches in University-Affiliated Hospitals, 2023. J Arthropod Borne Dis. 2025;19(1):71–85.
