Skip to main content
Download PDF
  • Research note
  • Open access
  • Published:

Identification of hemolysin encoding genes and their association with antimicrobial resistance pattern among clinical isolates of coagulase-negative Staphylococci

BMC Research Notes volume 13, Article number: 68 (2020) Cite this article

Abstract

Objective

Coagulase-negative staphylococci (CoNS) are as considered opportunistic pathogens which capable of producing several toxins, enzymes and resistance genes. The current study aimed to determine the occurrence of different hemolysins genes and patterns of antibiotic resistance among CoNS species.

Results

The highest frequency of antibiotic resistance was observed against cefoxitin in 49 isolates (53.8%), and the lowest resistance was against novobiocin in 5 isolates (5.5%). None of the isolates was resistant to vancomycin. The prevalence of hla, hla_yidD, hld, and hlb genes was: 87.9%, 62.6%, 56%, and 47.3%, respectively. The hla/yidD and hld genes were detected in 69.4% of S. epidermidis and the hla gene in 94.6% of S. haemolyticus isolates; the hlb gene was detected in 53.1% of the S. epidermidis isolates. The mecA gene was identified in 50 (55%) of the CoNS isolates. In conclusion, the results of statistical analysis showed that the hld gene had a significant association with resistance to levofloxacin and erythromycin antibiotics, the hlb with clindamycin resistance and the hla/yidD with rifampicin and novobiocin resistance. The results of this study showed that there is a significant relationship between hemolysin encoding genes and antibiotic resistance patterns; therefore, detection of virulence factors associated with antibiotic resistance has become a significant issue of concern.

Introduction

Coagulase-negative staphylococci (CoNS) are considered as opportunistic pathogens that cause a variety of infections, particularly among immunocompromised, long-term hospitalized patients, preterm infants and in patients with indwelling or different implant polymer bodies [1,2,3]. Among various CoNS species, Staphylococcus epidermidis, Staphylococcus haemolyticus, and Staphylococcus saprophyticus have been confirmed to be responsible agents for the vast majority of nosocomial infections [4]. Treatment of CoNS infections has become more complicated, as many isolates in hospitals show high rates of resistance to multiple antimicrobial agents of clinical relevance [5]. CoNS is also a reservoir for resistance genes that can be transmitted to other pathogens [6]. About 80–90% of CoNS isolates associated with nosocomial infections are methicillin-resistant coagulase-negative Staphylococci [7]. Most antibiotic resistance genes are carried on a plasmid and more often found in methicillin-resistant [8]. CoNS are capable of producing several toxins and enzymes characteristically associated with Staphylococcus aureus such as hemolysins, which are responsible for the invasion of host cells [9, 10]. Hemolysins of staphylococci are categorized into four different types, including alpha (α), beta (β), gamma (γ), and delta (δ). The α-toxin is encoded by the hla and acts as a pore-forming cytotoxin (PFT) which actives against a wide array of human cells. Pathogenicity of this toxin is due to hemolytic, dermonecrotic, and neurotoxic effects [11,12,13,14]. β-toxin which encoded by the hlb gene is known as Mg2+ -dependent sphingomyelinase. Incubation at temperatures below 10 °C intensifies the cytolytic activity of β-toxin; thus, it is often referred to as the ‘hot–cold’ hemolysin [15, 16]. The hld gene encodes a 26 amino acid peptide, which is referred to as delta (δ) hemolysin. This toxin with its detergent function degrades erythrocytes. The delta toxin may cause intestinal diseases that can vary from acute diarrhea to severe enteritis [15, 17, 18]. Because the association between antimicrobial resistance and virulence factors of CoNS isolates had never been done before as well as in a similar work in staphylococcus aureus strains observed a significant relationship between antibiotic resistance and hemolysin genes thus we made attempt to determine this association in this study.

Main text

Methods

Identification of CoNS isolates

A total of the 91 CoNS isolates were collected from various clinical specimens submitted to three teaching hospitals (including Beheshti, Besat, and Farshchian) located in Hamedan, Iran, from September 2017 to November 2018. All isolates were investigated by conventional methods. The origins of the isolates were as follows: blood, urine, catheters, and wounds. This study was approved by the Ethics Committee of Hamadan University of Medical Sciences (Code No: IR.UMSHA.REC.1396.827).

Antibiotic susceptibility testing

The Antibiotic susceptibility testing of 91 CoNS species carried out using the standard disk agar diffusion (DAD) method according to the Clinical and Laboratory Standards Institute (CLSI) guidelines [19]. Mueller–Hinton agar culture medium (Merck, Germany) was inoculated with a saline suspension of isolated CoNS equivalent to McFarland 0.5 standard. After that, antibiotic discs were placed on the surface of the agar. After 16-18 h incubation at 37 °C, CoNS isolates were categorized to be resistant, intermediately resistant, or sensitive based on the size of growth inhibition zone. The antimicrobial agents used in current study were as follows: for the following antimicrobial agents: chloramphenicol (30 µg), cefoxitin (30 µg), clindamycin (2 µg), doxycycline (30 µg), erythromycin (15 µg), gentamicin (10 µg), levofloxacin (5 µg), novobiocin (5 µg), rifampicin (5 µg), trimethoprim-sulfamethoxazole (25 µg) and vancomycin (30 µg) (MAST, Merseyside, UK). S. aureus ATCC33591 was used as a quality control.

DNA extraction from isolates

CoNS Chromosomal DNA was extracted by boiling method. Quality of extracted DNA was assessed by the Nanodrop ND–1000 (Nanodrop Technologies, Inc., Wilmington, DE, USA).

Detection of hemolysin genes

Identify of hemolysin encoding genes was performed by Multiplex PCR (hla haem, hla/yidD epid and hlb_epid) and single PCR (hld_epi) using specific primers (Additional file 1: Table S1), The PCR conditions included an initial denaturation at 94 °C for 4 min, followed by amplification; 30 cycles at 94 °C for 1 min, 58 °C for 1 min (45 °C-1 min for hld_epi), 72 °C for 1 min and 72 °C for 5 min. hla_haem: S. haemolyticus ATCC 29970, hlb_epid: S. epidermidis ATCC 12228 and hla/yidD_epid: S. epidermidis ATCC 12228, were used as control.

Detection of mecA gene

PCR assay was designed to amplify the mecA gene, using specific primers which are presented in Table 1. Amplification involved an initial denaturation at 95 °C for 10 min, followed by 35 cycles of denaturation (95 °C for 30 s), annealing (55 °C for 30 s), and extension (72 °C for 60 s), with a final extension step (72 °C for 7 min). S. aureus ATCC29247 was used as control.

Table 1 Prevalence of antibiotic-resistant strains among MR-CoNS and MS-CoNS
Full size table

Statistical analysis

Cramer’s V, Phi and Chi Square test were per-formed to assess of variables correlation. Phi and Cramer’s V have ranges from 0 to 1, where 1 indicates a significant association and 0 indicates no relationship. Interpretation of the Phi and Cramer’s V results; > 0; No or very weak, > 0.05 weak; > 0.10 moderate; > 0.15 strong; > 0.25 very strong. The Chi Square test was done by SPSS software version 20. P value < 0.05 was considered as statistically significant.

Results

Isolation and prevalence of CoNS isolates

Of the 91 clinical isolates of CoNS, 49 (53.8), 37 (40.7%) and 5 (5.5%) isolates were recognized as S. epidermidis, S. haemolyticus, and S. saprophyticus, respectively. Isolates were recovered from blood 39 (42.9%), urine 33 (36.3%), catheter 13 (14.3%) and wound 6 (6.6%).

Antimicrobial susceptibility testing

The results of the antibiotic susceptibility testing of the 91 CoNS isolates, including 50 isolates (55%) of the Methicillin-resistant CoNS (MR-CoNS) and 41 isolates (45%) of the Methicillin-susceptible CoNS (MS-CoNS) are presented in Table 1. Multi-drug resistance was identified among 96% (48 isolates) of the MR-CoNS isolates and 63.4% (26 isolates) of the MS-CoNS isolates. Among MR-CoNS strains, the most frequent resistant, was to cefoxitin (98%). Among CoNS species, the highest resistance was observed for cefoxitin (53.8%,). None of the CoNS species was identified as being resistant to vancomycin.

Prevalence of hemolysin genes among CoNS isolates

The distribution of hemolysin genes among CoNS isolates is presented in Table 2. Our results showed a high frequency of hemolytic activity among CoNS strains isolated from blood, followed by urine, catheter, and wound, respectively. 80 isolates (87.9%) with hla gene, 57 isolates (62.6%) with hla/yidD_epid, 51 isolates (56%) with hld and 43 isolates (47.3%) with hlb. Only 15 isolates (16%) had one type of the hemolysin, included; 12, 1 and two hla, hlb and hla/yidD positive CoNS isolates, respectively. Two types of the hemolysins were identified in 32 (35%) of the strains, the greatest coexistence of genes was observed for the hla + hla/yidD gene combination (14%), predominating followed by; hla + hld = 12 (13%), hla + hlb = 4 (0.04%), hld + hla/yidD = 2 (0.02%) and hlb + hla/yidD = 1 (0.01%). 14 (15%) of the strains were carrying three types of the hemolysins; hla + hlb + hla/yidD,hlb + hld + hla/yidD = 4 (0.04%) and hla + hld + hla/yidD = 3 (0.03%). All hemolysin genes were detected in 23 (25%) of the identified isolates.

Table 2 Prevalence of hemolysin encoding genes among various CoNS species and various clinical samples
Full size table

Prevalence of mecA gene among CoNS isolates

The distribution of mec A gene among CoNS isolates and the prevalence of hemolysin genes among MR-CoNS species are presented in Additional file 1: Table S2. S. epidermidis strains had the highest frequency of mecA gene. Among the MR-CoNS isolates, the hla gene was the most common with frequency of 90%, followed by the hla_yiD (60%), hld (58%) and hlb genes (48%).

Statistical analysis

Statistical analysis results are presented in Table 3. Statistically, a significant association between CoNS species and the occurrence of hld and hla/yiD genes was observed in this study. It was found a meaningful relationship between antibiotic resistance and the presence of the genes for alpha, delta and beta hemolysins.

Table 3 Statistical analysis results for determining possible relationship between the following variables and the presence of types of hemolysins genes
Full size table

Discussion

In the present study, S. epidermidis (53.8%) was the most clinically significant of the CoNS species and S. haemolyticus (40.7%) was identified as the second, which is in agreement with other reports [20,21,22]. The rate of the CoNS isolation was highest in blood (43%) followed by urine (36.3%), catheter (14.3%) and wound samples (6.6%). Aher et al, and Parashar et al, were also reported that the vast majority of CoNS species isolated from blood compared to urine [23, 24]. In our study, the highest resistance rate of the CoNS isolates was against methicillin (55%), followed by cefoxitin (53.8%). According to previous studies, which have found significant discrepancies in resistance ratio against cefoxitin with frequencies of 58% to 84.7% and high resistance to erythromycin (76.9%) and Trimethoprim-sulfamethoxazole (74.9%) [7, 25,26,27]. In current study, the resistance ratio to methicillin was determined in 50 (55%) of CoNS isolates; the findings were comparable to other studies [28,29,30,31], those reported resistance to methicillin with frequencies of 43.8%, 59.64%, 62.8%, and 73.3%, respectively. In this study, the prevalence rate of multiple antibiotic resistance was significantly higher among MR-CoNS isolates compared to MS-CoNS isolates which is similar to the results of Koksal et al, [31]. The results of our studies indicated that the mecA gene was identified in all CoNS isolates revealing phenotypical resistance to cefoxitin, and only one strain of mecA-positive S. epidermidis was phenotypically cefoxitin-susceptible, which is in agreement with the others [27, 32]. Like other studies [25, 33], this study show that all CoNS isolates were also completely sensitive to vancomycin. However, there are reports of the occurrence of decreased susceptibility to vancomycin in CoNS isolates [34, 35]. Out of the 91 CoNS isolates, the percentage of strains with hemolytic activity were the highest among S. epidermidis (53.8%), followed by S. haemolyticus (39.5%) which is in agreement with the findings of Cunha et al, and Pinheiro et al., [36, 37], but, in contrary with the findings of Akinkunmi et al., [20]. Among CoNS species, 94.6% and 81.6% of the S. haemolyticus and S. epidermidis strains were determined to be positive to the hla gene, respectively. The hlb gene was detected in 53% and 46% of the S. epidermidis and S. haemolyticus strains, respectively. On the other hand, according to Okee MS et al., the occurrence of hlb gene not observed in any of the CoNS species isolated and the hla gene found in only 20% of S. epidermidis, which is also in contrary to a similar survey carried out by Pinheiro et al, who demonstrated the emergence of the hla and hlb genes in 92.9% of the S. epidermidis strains and hla with the same frequency (91.7%) in S. hemolyticus strains [37, 38]. In this study, the largest number of the strains carrying the hld gene belonged to S. epidermidis with frequency of 69.4%, then S. hemolyticus (37.8%), according to Pinheiro et al, 95.3% of the S. epidermidis and none of the S. haemolyticus were carrying hld gene, [37]. In the comparative statistical analysis among the MR-CoNS and MS-CoNS isolates found no significant association between the emergence of the hemolysins and methicillin resistance (p value from 0.472 to 0.962). All the isolated MR-CoNS demonstrated hemolytic activity either alone or in combined forms, while only one of the MS-CoNS strains was nonhemolytic which belonged to a S. haemolyticus recovered from urine sample. Among MR-CoNS, the highest number of strains carrying hemolysin genes are isolated from the blood rather than urine. But in a similar study done by Motamedi et al, S. aureus hemolytic isolates were identified more in blood and ulcers compared to urine and catheter samples [39]. Regarding with the pattern of antimicrobial resistance in CoNS isolates found a significant association between the occurrence of hld gene and resistance to levofloxacin and erythromycin (P = 0.04, φ = 0.21 and P = 0.04, V = 0.26, respectively), the hla/yidD and resistance to rifampicin and novobiocin (P = 0.02, φ = 0.19 and P = 0.003, φ = 0.31, respectively), as well as between hlb and clindamycin resistance (P = 0.009, φ = 0.28). Our results showed that the frequency of hemolytic agent genes of hla, hlb, hld were higher in cefoxitin resistant isolates compared to susceptible ones. The analysis of our results demonstrated that there is no significant association between different clinical samples and hemolysins which is similar to the results of studies conducted by Corredor Arias et al., in S. aureus strains [40]. Arabestani et al., Lee et al., and Osman et al. have been proved significant associations between pathogenicity factors and antibiotic resistance [41,42,43].

Conclusion

The results of this study demonstrated the significant role of antibiotic resistance in different infections due to increasing resistance to methicillin and the other antimicrobial agents among CoNS isolates. This study showed that the hla and hla_yidD genes and resistance to methicillin, cefoxitin, and trimethoprim-sulfamethoxazole antibiotics are widely distributed among the majority of CoNS isolated from human.

Limitations

The number of bacteria isolates was rather low. If the number of bacteria was more, the results would be better and also we have to design another study which focus on gene expression of the resistance and virulence factors.

Availability of supporting data

The Additional files included Additional file 1: Tables S1 and S2.

Abbreviations

CoNS:

Coagulase-negative staphylococci

PFT:

Pore-forming cytotoxin

BHI:

Brain Heart Infusion

DAD:

Disk agar diffusion

CLSI:

Clinical and Laboratory Standards Institute

MS-CoNS:

Methicillin-susceptible CoNS

References

  1. Soumya K, Philip S, Sugathan S, Mathew J, Radhakrishnan E. Virulence factors associated with coagulase negative Staphylococci isolated from human infections. 3 Biotech. 2017;7(2):140.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Azih A, Enabulele I. Species distribution and virulence factors of coagulase negative Staphylococci isolated from clinical samples from the University of Benin Teaching hospital, Edo State, Nigeria. J Nat Sci Res. 2013;3(9):38–43.

    Google Scholar 

  3. Nanoukon C, Argemi X, Sogbo F, Orekan J, Keller D, Affolabi D, et al. Pathogenic features of clinically significant coagulase-negative staphylococci in hospital and community infections in Benin. Int J Med Microbiol. 2017;307(1):75–82.

    Article  PubMed  Google Scholar 

  4. Mehri H, Jahanbakhsh R, Shakeri F, Ardebili A, Behnampour N, Khodabakhshi B, et al. Investigation of glycopeptide susceptibility of coagulase-negative staphylococci (CoNS) from a tertiary care hospital in Gorgan, northern Iran. Arch Pediatr Infect Dis. 2017;5(1):e37264.

    Google Scholar 

  5. Xu Z, Mkrtchyan HV, Cutler RR. Antibiotic resistance and mecA characterization of coagulase-negative staphylococci isolated from three hotels in London, UK. Front Microbiol. 2015;6:947.

    PubMed  PubMed Central  Google Scholar 

  6. May L, Klein EY, Rothman RE, Laxminarayan R. Trends in antibiotic resistance in coagulase-negative staphylococci in the United States, 1999 to 2012. Antimicrob Agents Chemother. 2014;58(3):1404–9.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Shrestha LB, Bhattarai NR, Khanal B. Antibiotic resistance and biofilm formation among coagulase-negative staphylococci isolated from clinical samples at a tertiary care hospital of eastern Nepal. Antimicrob Resist Infect Control. 2017;6(1):89.

    Article  PubMed  PubMed Central  Google Scholar 

  8. Chovanová R, Mikulášová M, Vaverková Š. In vitro antibacterial and antibiotic resistance modifying effect of bioactive plant extracts on methicillin-resistant Staphylococcus epidermidis. Int J Microbiol. 2013. https://doi.org/10.1155/2013/760969.

    Article  PubMed  PubMed Central  Google Scholar 

  9. Moraveji Z, Tabatabaei M, Aski HS, Khoshbakht R. Characterization of hemolysins of Staphylococcus strains isolated from human and bovine, southern Iran. Iran J Vet Res. 2014;15(4):326.

    CAS  PubMed  PubMed Central  Google Scholar 

  10. Gemmell C, Roberts E. Toxins and enzymes of coagulase-negative staphylococci isolated from human infections. J Hyg Epidemiol Microbiol Immunol. 1974;18(3):276–8.

    CAS  PubMed  Google Scholar 

  11. Qiu J, Niu X, Dong J, Wang D, Wang J, Li H, et al. Baicalin protects mice from Staphylococcus aureus pneumonia via inhibition of the cytolytic activity of α-hemolysin. J Infect Dis. 2012;206(2):292–301.

    Article  CAS  PubMed  Google Scholar 

  12. Berube B, Wardenburg J. Staphylococcus aureus α-toxin: nearly a century of intrigue. Toxins. 2013;5(6):1140–66.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Ebrahimi A, Akhavan Taheri M. Characteristics of staphylococci isolated from clinical and subclinical mastitis cows in Shahrekord, Iran. Iran J Vet Res. 2009;10(3):273–7.

    Google Scholar 

  14. Oliveira D, Borges A, Simões M. Staphylococcus aureus toxins and their molecular activity in infectious diseases. Toxins. 2018;10(6):252.

    Article  PubMed Central  Google Scholar 

  15. Burnside K, Lembo A, de los Reyes M, Iliuk A, BinhTran N-T, Connelly JE, et al. Regulation of hemolysin expression and virulence of Staphylococcus aureus by a serine/threonine kinase and phosphatase. PLoS ONE. 2010;5(6):e11071.

    Article  PubMed  PubMed Central  Google Scholar 

  16. Zhang YQ, Ren SX, Li HL, Wang YX, Fu G, Yang J, et al. Genome-based analysis of virulence genes in a non-biofilm-forming Staphylococcus epidermidis strain (ATCC 12228). Mol Microbiol. 2003;49(6):1577–93.

    Article  CAS  PubMed  Google Scholar 

  17. Marconi C, Cunha M, Araújo J Jr, Rugolo L. Standardization of the PCR technique for the detection of delta toxin in Staphylococcus spp. J Venom Anim Toxins Incl Trop Dis. 2005;11(2):117–28.

    Article  CAS  Google Scholar 

  18. Cunha CR. Toxigenicity in Staphylococcus aureus and coagulase-negative staphylococci: epidemiological and molecular aspects. Microbiol Insights. 2008;1:MBI. S796.

    Article  Google Scholar 

  19. Wayne PA. CLSI In; Performance standards for antimicrobial susceptibility testing. 29th ed. CLSI supplement M100, Clinical and Laboratory Standards Institute; 2019.

  20. Akinkunmi E, Lamikanra A. Species distribution and antibiotic resistance in coagulase-negative staphylococci colonizing the gastrointestinal tract of children in Ile-Ife, Nigeria. Trop J Pharm Res. 2010;9(1):35–43.

    Article  Google Scholar 

  21. Begum ES, Anbumani N, Kalyani J, Mallika M. Prevalence and antimicrobial susceptibility pattern of coagulase-negative Staphylococcus. Int J Med Public Health. 2011;1(4):59–62.

    Article  Google Scholar 

  22. Al Tayyar IA, Al-Zoubi MS, Hussein E, Khudairat S, Sarosiekf K. Prevalence and antimicrobial susceptibility pattern of coagulase-negative staphylococci (CoNS) isolated from clinical specimens in Northern of Jordan. Iran J Microbiol. 2015;7(6):294.

    PubMed  PubMed Central  Google Scholar 

  23. Aher CS. The isolation pattern, species distribution and antibiotic susceptibility profile of coagulase negative Staphylococci: emerging opportunistic pathogens. Int J Biomed Adv Res. 2014;5(01):23–5.

    Article  Google Scholar 

  24. Parashar S. Significance of coagulase negative Staphylococci with special reference to species differentiation and antibiogram. Indian Med Gaz. 2014:255–8.

  25. Goudarzi M, Seyedjavadi SS, Goudarzi H, Boromandi S, Ghazi M, Azad M, et al. Characterization of coagulase-negative staphylococci isolated from hospitalized patients in Tehran, Iran. J Paramed Sci. 2014;5(2):2008–14.

    Google Scholar 

  26. Fowoyo P, Ogunbanwo S. Antimicrobial resistance in coagulase-negative staphylococci from Nigerian traditional fermented foods. Ann Clin Microbiol Antimicrob. 2017;16(1):4.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Chajęcka-Wierzchowska W, Zadernowska A, Nalepa B, Sierpińska M, Łaniewska-Trokenheim Ł. Coagulase-negative staphylococci (CoNS) isolated from ready-to-eat food of animal origin–phenotypic and genotypic antibiotic resistance. Food Microbiol. 2015;46:222–6.

    Article  PubMed  Google Scholar 

  28. Perveen I, Majid A, Knawal S, Naz I, Sehar S, Ahmed S, et al. Prevalence and antimicrobial susceptibility pattern of methicillin-resistant Staphylococcus aureus and coagulase-negative Staphylococci in Rawalpindi, Pakistan. J Adv Med Med Res. 2013;3:198–209.

    Article  Google Scholar 

  29. Gilani M, Usman J, Latif M, Munir T, Gill MM, Anjum R, et al. Methicillin resistant coagulase negative staphylococcus: from colonizer to a pathogen. Pak J Pharm Sci. 2016;29(4):1117–21.

    CAS  PubMed  Google Scholar 

  30. Mehdinejad M, Sheikh AF, Jolodar A. Study of methicillin resistance in Staphylococcus aureus and species of coagulase negative staphylococci isolated from various clinical specimens. Pak J Med Sci. 2008;24(5):719–24.

    Google Scholar 

  31. Koksal F, Yasar H, Samasti M. Antibiotic resistance patterns of coagulase-negative staphylococcus strains isolated from blood cultures of septicemic patients in Turkey. Microbiol Res. 2009;164(4):404–10.

    Article  CAS  PubMed  Google Scholar 

  32. Vyletelova M, VlkoVá H, Manga I. Occurrence and characteristics of methicillin resistant Staphylococcus aureus and methicillin resistant coagulase-negative staphylococci in raw milk manufacturing. Czech J Food Sci. 2011;29:11–6.

    Article  Google Scholar 

  33. Keim LS, Torres-Filho SR, Silva PV, Teixeira LA. Prevalence, aetiology and antibiotic resistance profiles of coagulase negative staphylococci isolated in a teaching hospital. Braz J Microbiol. 2011;42(1):248–55.

    Article  PubMed  PubMed Central  Google Scholar 

  34. Pinheiro L, Brito CI, Pereira VC, Oliveira Ad, Camargo CH, Cunha MdLRd. Reduced susceptibility to vancomycin and biofilm formation in methicillin-resistant Staphylococcus epidermidis isolated from blood cultures. Memorias do Instituto Oswaldo Cruz. 2014;109(7):871–8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Mashaly GES, El-Mahdy RH. Vancomycin heteroresistance in coagulase negative Staphylococcus blood stream infections from patients of intensive care units in Mansoura University Hospitals, Egypt. Ann Clin Microbiol Antimicrob. 2017;16(1):63.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Cunha MdLRd, Rugolo LMSdS, Lopes CAdM. Study of virulence factors in coagulase-negative staphylococci isolated from newborns. Memórias do Instituto Oswaldo Cruz. 2006;101(6):661–8.

    Article  Google Scholar 

  37. Pinheiro L, Brito C, de Oliveira A, Martins P, Pereira V, da Cunha M. Staphylococcus epidermidis and Staphylococcus haemolyticus: molecular detection of cytotoxin and enterotoxin genes. Toxins. 2015;7(9):3688–99.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Okee MS, Joloba ML, Okello M, Najjuka FC, Katabazi FA, Bwanga F, et al. Prevalence of virulence determinants in Staphylococcus epidermidis from ICU patients in Kampala, Uganda. J Infect Dev Ctries. 2012;6(3):242–5050.

    Article  PubMed  Google Scholar 

  39. Motamedi H, Asghari B, Tahmasebi H, Arabestani MR. Identification of hemolysine genes and their association with antimicrobial resistance pattern among clinical isolates of Staphylococcus aureus in West of Iran. Adv Biomed Res. 2018;7:153. https://doi.org/10.4103/abr.abr_143_18.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Corredor Arias LF, Espinal L, Samara J, Moncayo Ortiz JI, Santacruz Ibarra JJ, Álvarez Aldana A. Relationship between super antigenicity, antimicrobial resistance and origin of Staphylococcus aureus isolated. Colombia Médica. 2016;47(1):15–20.

    PubMed  Google Scholar 

  41. Arabestani MR, Rastiyani S, Alikhani MY, Mousavi SF. The relationship between prevalence of antibiotics resistance and virulence factors genes of MRSA and MSSA strains isolated from clinical samples, West Iran. Oman Med J. 2018;33(2):134–40.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Lee GY, Lee H-H, Hwang SY, Hong J, Lyoo K-S, Yang S-J. Carriage of Staphylococcus schleiferi from canine otitis externa: antimicrobial resistance profiles and virulence factors associated with skin infection. J Vet Sci. 2019;20(2):e74. https://doi.org/10.4142/jvs.2019.20.e6.

    Article  Google Scholar 

  43. Osman K, Alvarez-Ordóñez A, Ruiz L, Badr J, ElHofy F, Al-Maary KS, et al. Antimicrobial resistance and virulence characterization of Staphylococcus aureus and coagulase-negative staphylococci from imported beef meat. Ann Clin Microbiol Antimicrob. 2017;16(1):35.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors of this article are grateful to Hamadan University of Medical Sciences for their financial support in conducting research. This work was supported by the vice chancellor and Research technology of Hamadan University of Medical Sciences on the Grant Number, 9612087936.

Funding

The Research and technology of Vice Chancellor of Hamadan University of Medical Sciences (Project Number: 9612087936). This funding’s devoted just for purchasing materials which used in our study.

Author information

Authors and Affiliations

  1. Department of Microbiology, Faculty of Medicine, Hamadan University of Medical Sciences, Shahid Fahmideh Street, Park Mardome, Hamadan, IR, Iran

    Mona Nasaj, Zahra Saeidi, Babak Asghari & Mohammad Reza Arabestani

  2. Department of Biostatistics, School of Health, Hamadan University of Medical Sciences, Shahid Fahmideh Street, Park Mardome, Hamadan, IR, Iran

    Ghodratollah Roshanaei

  3. Nutrition Research Center, Hamadan University of Medical Sciences, Shahid Fahmideh Street, Park Mardome, Hamadan, IR, Iran

    Mohammad Reza Arabestani

Authors
  1. Mona Nasaj
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zahra Saeidi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Babak Asghari
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ghodratollah Roshanaei
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohammad Reza Arabestani
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

MN and ZS performed the tests, collected and analyzed the data, BA was advisor and contributor in writing and editing the manuscript, GR, performed the analysis of the data. MA designed the project and contributes in the whole steps of the projects. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Mohammad Reza Arabestani.

Ethics declarations

Ethical approval and consent to participate

This study was approved by the ethics committee of the Hamadan University of Medical Sciences ((Code No: IR.UMSHA.REC.1396.827)) and about the consent to participate is not applicable.

Consent for publication

Its not applicable

Competing interests

The authors declare that they have no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Additional file 1: Table S1.

Primers used in this study. Table S2. The prevalence of mecA gene and types of hemolysins among MR-CoNS species.

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nasaj, M., Saeidi, Z., Asghari, B. et al. Identification of hemolysin encoding genes and their association with antimicrobial resistance pattern among clinical isolates of coagulase-negative Staphylococci. BMC Res Notes 13, 68 (2020). https://doi.org/10.1186/s13104-020-4938-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1186/s13104-020-4938-0

Keywords

BMC Research Notes

ISSN: 1756-0500

Contact us