Abstract
Hospital cockroaches are probable sources of pathogenic bacteria. The present investigation was performed to assess the antibiotic resistance properties and distribution of virulence factors in the Streptococcus spp. isolated from hospital cockroaches. Six hundred and sixty cockroach samples were collected. Cockroaches were washed with normal saline, and the achieved saline was used for bacterial culture. Isolated Streptococcus spp. were subjected to disk diffusion. The distribution of virulence factors and antibiotic resistance genes were assessed using a polymerase chain reaction. The prevalence of S. pyogenes, S. agalactiae, and S. pneumonia amongst examined samples was 4.82%, 1.66%, and 6.96%, respectively. Cfb (53.93%), cyl (52.8%), scaa (51.68%) and glna (50.56%) were the most commonly detected virulence factors. Pbp2b (71.91%), pbp2x (58.42%), mefA (46.06%), ermB (46.06%) and tetM (46.06%) were the most commonly detected antibiotic resistance genes. Streptococcal spp. harbored the highest prevalence of resistance against tetracycline (80.89%), trimethoprim (65.16%), and penicillin (56.17%). To the best of our knowledge, this is the first prevalence report of virulence factors and antibiotic resistance genes in the Streptococcal spp. isolated from American, German, and oriental hospital cockroaches in Iran. Our findings indicated a certain role for cockroaches in nosocomial pathogens transmission in the hospital environment.
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Data availability
The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.
Abbreviations
- S. pneumoniae :
-
Streptococcus pneumonia
- S. pyogenes :
-
Streptococcus pyogenes
- S. agalactiae :
-
Streptococcus agalactiae
- bac :
-
Encode for β-antigen
- cyl :
-
Encode for β-hemolysin
- glnA :
-
Encode for glutamine synthetase
- cfb :
-
Encode for the Christie–Atkins–Munch–Peterson (CAMP) factor
- hylB :
-
Encode for hyaluronidase
- scaA :
-
Encode for aggregation factor
- bca :
-
Encode for α-antigen
- scpB :
-
C5a peptidase
- lmb :
-
Laminin-binding protein
- CLSI:
-
Clinical Laboratory Standards Institute
- PCR:
-
Polymerase chain reaction
References
Abdolmaleki Z, Mashak Z, Dehkordi FS (2019a) Molecular and virulence characteristics of methicillin-resistant staphylococcus aureus bacteria recovered from hospital cockroaches. Jundishapur J Microbiol. https://doi.org/10.5812/jjm.98564
Abdolmaleki Z, Mashak Z, SafarpoorDehkordi F (2019b) Phenotypic and genotypic characterization of antibiotic resistance in the methicillin-resistant Staphylococcus aureus strains isolated from hospital cockroaches. Antimicrob Resist Infect Control. https://doi.org/10.1186/s13756-019-0505-7
Ahmad Vahhabi A, Shemshad K, Mohammadi P et al (2011) Microbiological study of domestic cockroaches in human dwelling localities. Afr J Microbiol Res 5:5790–5792. https://doi.org/10.5897/AJMR11.1075
Billal DS, Hotomi M, Suzumoto M et al (2008) Determination of pneumococcal serotypes/genotypes in nasopharyngeal secretions of otitis media children by multiplex PCR. Eur J Pediatr 167:401–407. https://doi.org/10.1007/s00431-007-0510-3
Blumental S, Granger-Farbos A, Moïsi JC et al (2015) Virulence factors of Streptococcus pneumoniae comparison between African and French invasive isolates and implication for future vaccines. PLoS ONE 10:1. https://doi.org/10.1371/journal.pone.0133885
Bouamama L, Sorlozano A, Laglaoui A et al (2010) Antibiotic resistance patterns of bacterial strains isolated from Periplaneta americana and Musca domestica in Tangier, Morocco. J Infect Dev Ctries 4:194–201
Burgess NRH (1993) Cockroaches (Blattaria). Medical insects and arachnids. Springer, Netherlands, Dordrecht, pp 473–482
Cattoir V (2016) Mechanisms of antibiotic resistance. In: Ferretti JJ, Stevens DL, Fischetti VA (eds) Streptococcus pyogenes: Basic biology to clinical manifestations [Internet]. University of Oklahoma Health Sciences Center, Oklahoma City (OK), PMID: 26866217
Chaichanawongsaroj N, Vanichayatanarak K, Pipatkullachat T et al (2004) Isolation of gram-negative bacteria from cockroaches trapped from urban environment. Southeast Asian J Trop Med Public Health 35:681–684
Chakraborty A, Pal NK, Sarkar S, Gupta MS (2015) Antibiotic resistance pattern of Enterococci isolates from nosocomial infections in a tertiary care hospital in Eastern India. J Nat Sci Biol Med 6(2):394–397. https://doi.org/10.4103/0976-9668.160018
Chang SC, Hsieh WC, Liu CY (2000) High prevalence of antibiotic resistance of common pathogenic bacteria in Taiwan. The antibiotic resistance study group of the infectious disease society of the Republic of China. Diagn Microbiol Infect Dis 36:107–112
Clinical and Laboratory Standards Institute Performance Standards for Antimicrobial Susceptibility Testing (2015) Wayne, PA, USA: CLSI
Ding Y, Zhao J, He X et al (2016) Antimicrobial resistance and virulence-related genes of Streptococcus obtained from dairy cows with mastitis in Inner Mongolia, China. Pharm Biol 54:162–167. https://doi.org/10.3109/13880209.2015.1025290
Dmitriev A, Tkáciková L, Suvorov A et al (1999) Comparative genetic study of group B streptococcal strains of human and bovine origin. Folia Microbiol (praha) 44:449–453
Dmitriev A, Hu YY, Shen AD et al (2002) Chromosomal analysis of group B streptococcal clinical strains; bac gene-positive strains are genetically homogenous. FEMS Microbiol Lett 208:93–98. https://doi.org/10.1016/S0378-1097(02)00446-9
Doosti A, Pourabbas M, Arshi A et al (2015) TEM and SHV genes in klebsiella pneumoniae isolated from cockroaches and their antimicrobial resistance pattern. Osong Public Heal Res Perspect 6:3–8. https://doi.org/10.1016/j.phrp.2014.10.011
Duarte RS, Bellei BC, Miranda OP et al (2005) Distribution of antimicrobial resistance and virulence-related genes among Brazilian group B streptococci recovered from bovine and human sources. Antimicrob Agents Chemother 49:97–103. https://doi.org/10.1128/AAC.49.1.97-103.2005
Edwards MS, Baker CJ (2005) Group B streptococcal infections in elderly adults. Clin Infect Dis an off Publ Infect Dis Soc Am 41:839–847. https://doi.org/10.1086/432804
Elgderi RM, Ghenghesh KS, Berbash N (2006) Carriage by the German cockroach (Blattella germanica) of multiple-antibiotic-resistant bacteria that are potentially pathogenic to humans, in hospitals and households in Tripoli, Libya. Ann Trop Med Parasitol 100:55–62. https://doi.org/10.1179/136485906X78463
Eskandarian N, Ismail Z, Neela V et al (2015) Antimicrobial susceptibility profiles, serotype distribution and virulence determinants among invasive, non-invasive and colonizing Streptococcus agalactiae (group B streptococcus) from Malaysian patients. Eur J Clin Microbiol Infect Dis 34:579–584. https://doi.org/10.1007/s10096-014-2265-x
Fakoorziba MR, Eghbal F, Hassanzadeh J, Moemenbellah-Fard MD (2010) Cockroaches (Periplaneta americana and Blattella germanica) as potential vectors of the pathogenic bacteria found in nosocomial infections. Ann Trop Med Parasitol 104:521–528. https://doi.org/10.1179/136485910X12786389891326
Farrell DJ, Douthwaite S, Morrissey I et al (2003) Macrolide resistance by ribosomal mutation in clinical isolates of Streptococcus pneumoniae from the PROTEKT 1999–2000 study. Antimicrob Agents Chemother 47:1777–1783. https://doi.org/10.1128/AAC.47.6.1777-1783.2003
Feizhaddad MH, Kassiri H, Sepand MR, Ghasemi F (2012) Bacteriological survey of American cockroaches in hospitals. Middle East J Sci Res 12:985–989. https://doi.org/10.5829/idosi.mejsr.2012.12.7.7153
Fotedar R, Shriniwas UB, Verma A (1991) Cockroaches (Blattella germanica) as carriers of microorganisms of medical importance in hospitals. Epidemiol Infect 107:181–187. https://doi.org/10.1017/S0950268800048809
Franken C, Haase G, Brandt C et al (2001) Horizontal gene transfer and host specificity of beta-haemolytic streptococci: the role of a putative composite transposon containing scpB and lmb. Mol Microbiol 41:925–935. https://doi.org/10.1046/j.1365-2958.2001.02563.x
Hammad KM, Mahdy HM (2012) Antibiotic resistant-bacteria associated with the cockroach, Periplaneta americana collected from different habitat in Egypt. NY Sci J NY Sci J 55:198–206
Islam A, Aurjun ND, Islam K et al (2016) Isolation, identification and antimicrobial resistance profile of Staphylococcus aureus in Cockroaches (Periplaneta a mericana). J Adv Vet Anim Res Islam Al J Adv Vet Anim Res 3:221–228. https://doi.org/10.5455/javar.2016.c153
Kargar M, Baghernejad M, Ghorbani-Dalini S (2012) Multi-drug resistance and molecular pattern of erythromycin and penicillin resistance genes in Streptococcus pneumoniae. Afr J Biotechnol 11:968–973. https://doi.org/10.5897/AJB11.2783
Kasahara K, Maeda K, Mikasa K et al (2005) Clonal dissemination of macrolide-resistant and penicillin-susceptible serotype 3 and penicillin-resistant Taiwan 19F–14 and 23F–15 Streptococcus pneumoniae isolates in Japan: a pilot surveillance study. J Clin Microbiol 43:1640–1645. https://doi.org/10.1128/JCM.43.4.1640-1645.2005
Kassiri H, Shahnaz K (2012) Cockroaches [periplaneta americana (L.), dictyoptera; blattidae] as carriers of bacterial pathogens, khorramshahr County Iran. Jundishapur J Microbiol 5:320–322
Kassiri H, Kassiri A, Kazemi S (2014) Investigation on American cockroaches medically important bacteria in Khorramshahr hospital, Iran. Asian Pac J Trop Dis 4:201–203. https://doi.org/10.1016/S2222-1808(14)60505-3
Kayansamruaj P, Pirarat N, Katagiri T et al (2014) Molecular characterization and virulence gene profiling of pathogenic Streptococcus agalactiae populations from tilapia (Oreochromis sp.) farms in Thailand. J Vet Diagn Investig 26:488–495. https://doi.org/10.1177/1040638714534237
Krzyaściak W, Pluskwa KK, Jurczak A, Koaścielniak D (2013) The pathogenicity of the Streptococcus genus. Eur J Clin Microbiol Infect Dis 32:1361–1376
Lemos AA, Lemos JA, Prado MA et al (2006) Cockroaches as carriers of fungi of medical importance. Mycoses 49:23–25. https://doi.org/10.1111/j.1439-0507.2005.01179.x
LeshanWannigama D, Dwivedi R, Zahraei-Ramazani A (2013) Prevalence and antibiotic resistance of gram-negative pathogenic bacteria species isolated from periplaneta americana and blattella germanica in Varanasi, India. J Arthropod Borne Dis 8:10–20
Li XX, Xiao SZ, Gu FF et al (2019) Serotype distribution, antimicrobial susceptibility, and multilocus sequencing type (MLST) of Streptococcus pneumoniae from adults of three hospitals in Shanghai. China Front Cell Infect Microbiol. https://doi.org/10.3389/fcimb.2019.00407
Lin K, Tierno PM Jr, Komisar A (2004) Increasing antibiotic resistance of streptococcus species in New York City. Laryngoscope 114:1147–1150. https://doi.org/10.1097/00005537-200407000-00003
Lopardo HA, Vidal P, Jeric P et al (2003) Six-month multicenter study on invasive infections due to group B streptococci in Argentina. J Clin Microbiol 41:4688–4694
Malhotra-Kumar S, Lammens C, Piessens J, Goossens H (2005) Multiplex PCR for simultaneous detection of macrolide and tetracycline resistance determinants in streptococci. Antimicrob Agents Chemother 49:4798–4800. https://doi.org/10.1128/AAC.49.11.4798-4800.2005
Manning SD, Ki M, Marrs CF et al (2006) The frequency of genes encoding three putative group B streptococcal virulence factors among invasive and colonizing isolates. BMC Infect Dis. https://doi.org/10.1186/1471-2334-6-116
Musher DM (1992) Infections caused by streptococcus pneumoniae: clinical spectrum, pathogenesis, immunity, and treatment. Clin Infect Dis 14:801–809. https://doi.org/10.1093/clinids/14.4.801
Naccache SN, Lustestica M, Fahit M et al (2018) One year in the life of a rapid syndromic panel for meningitis/encephalitis: a pediatric tertiary care facility’s experience. J Clin Microbiol. https://doi.org/10.1128/JCM.01940-17
NajafiMosleh M, Gharibi M, Alikhani MY et al (2014) Antimicrobial susceptibility and analysis of macrolide resistance genes in Streptococcus pneumoniae isolated in Hamadan. Iran J Basic Med Sci 17:595–599. https://doi.org/10.22038/ijbms.2014.3193
Pai H-H, Chen W-C, Peng C-F (2004) Cockroaches as potential vectors of nosocomial infections. Infect Control Hosp Epidemiol 25:979–984. https://doi.org/10.1086/502330
Paul S, Khan AM, Baqui MA, Muhibullah M (1992) Evaluation of the common cockroach Periplaneta americana (L.) as carrier of medically important bacteria. J Commun Dis 24:206–210
Persson E, Berg S, Bevanger L et al (2008) Characterization of invasive group B streptococci based on investigation of surface proteins and genes encoding surface proteins. Clin Microbiol Infect 14:66–73. https://doi.org/10.1111/j.1469-0691.2007.01877.x
Pomés A, Arruda LK (2014) Investigating cockroach allergens: aiming to improve diagnosis and treatment of cockroach allergic patients. Methods 66:75–85. https://doi.org/10.1016/j.ymeth.2013.07.036
Prado MA, Gir E, Pereira MS et al (2006) Profile of antimicrobial resistance of bacteria isolated from cockroaches (Periplaneta americana) in a Brazilian Health Care Institution. Braz J Infect Dis 10:26–32
Ranjbar R, Chehelgerdi M (2018) Genotyping and antibiotic resistance properties of helicobacter pylori strains isolated from human and animal gastric biopsies. Infect Drug Resist. https://doi.org/10.2147/IDR.S187885
Ranjbar R, Farsani FY, Dehkordi FS (2018) Phenotypic analysis of antibiotic resistance and genotypic study of the vacA, cagA, iceA, oipA and babA genotypes of the Helicobacter pylori strains isolated from raw milk. Antimicrob Res Infect Control 7:1–4
Ruppen C, Notter J, Strahm C et al (2018) Osteoarticular and skin and soft-tissue infections caused by Streptococcus agalactiae in elderly patients are frequently associated with bacteremia. Diagn Microbiol Infect Dis 90:55–57. https://doi.org/10.1016/j.diagmicrobio.2017.09.008
Sadeghifard N, Ranjbar R, Zaeimi J et al (2010) Antimicrobial susceptibility, plasmid profiles, and RAPD-PCR typing of Acinetobacter bacteria. Asian Biomed 4(6):901–911
Sadowy E, Matynia B, Hryniewicz W (2010) Population structure, virulence factors and resistance determinants of invasive, non-invasive and colonizing Streptococcus agalactiae in Poland. J Antimicrob Chemother 65:1907–1914. https://doi.org/10.1093/jac/dkq230
Salehzadeh A, Tavacol P, Mahjub H (2007) Bacterial, fungal and parasitic contamination of cockroaches in public hospitals of Hamadan. Iran J Vector Borne Dis 44:105–110
Sapkota AR, Ojo KK, Roberts MC, Schwab KJ (2006) Antibiotic resistance genes in multidrug-resistant Enterococcus spp. and Streptococcus spp. recovered from the indoor air of a large-scale swine-feeding operation. Lett Appl Microbiol 43:534–540. https://doi.org/10.1111/j.1472-765X.2006.01996.x
Stevens DL, Bryant AE (2016) Severe group a streptococcal infections. In: Ferretti JJ, Stevens DL, Fischetti VA (eds) Streptococcus pyogenes: Basic biology to clinical manifestations [Internet]. University of Oklahoma Health Sciences Center, Oklahoma City (OK), PMID: 26866227
Tetteh-Quarcoo PB, Donkor ES, Attah SK et al (2013) Microbial carriage of cockroaches at a tertiary care hospital in ghana. Environ Health Insights 7:59–66
Tunkel AR, Sepkowitz KA (2002) Infections caused by Viridans Streptococci in patients with neutropenia. Clin Infect Dis 34:1524–1529. https://doi.org/10.1086/340402
Udo EE, Boswihi SS, Al-Sweih N (2013) Genotypes and virulence genes in group B streptococcus isolated in the maternity hospital, Kuwait. Med Princ Pract 22:453–457. https://doi.org/10.1159/000349932
Xu X, Cai L, Xiao M et al (2010) Distribution of serotypes, genotypes, and resistance determinants among macrolide-resistant Streptococcus pneumoniae isolates. Antimicrob Agents Chemother 54:1152–1159. https://doi.org/10.1128/AAC.01268-09
Zeng X, Kong F, Wang H et al (2006) Simultaneous detection of nine antibiotic resistance-related genes in Streptococcus agalactiae using multiplex PCR and reverse line blot hybridization assay. Antimicrob Agents Chemother 50:204–209. https://doi.org/10.1128/AAC.50.1.204-209.2006
Acknowledgements
The authors would like to thank the Clinical Research Development Unit of Baqiyatallah Hospital, Tehran, Iran, for guidance and advice. The authors also gratefully acknowledge the Biotechnology Research Center, Shahrekord Branch, Islamic Azad University, Shahrekord in southwest Iran for their sincere support.
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RR and MC conceived and designed the study; MC conducted the research; MC performed the experiments. RR and MC analyzed the data. MC carried out the writing and drafting of the manuscript. All authors read and approved the final manuscript.
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This Research was approved in the Baqiyatallah University of Medical Sciences, Tehran, Iran (Project Ref Number 96-91002480). Verification of this research project and the licenses related to the sampling process were approved by Prof. Reza Ranjbar (Approval Ref Number Med-96-91002480).
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Chehelgerdi, M., Ranjbar, R. Virulence factors and antibiotic resistance properties of Streptococcus species isolated from hospital cockroaches. 3 Biotech 11, 321 (2021). https://doi.org/10.1007/s13205-021-02874-w
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DOI: https://doi.org/10.1007/s13205-021-02874-w