Medically, cockroaches are much more important than generally realized as they have been demonstrated to harbor some pathogenic and non-pathogenic microorganisms. Since various workers have reported the isolation of various human pathogens from these insects, cockroaches are known vectors of human enteropathogens. Their filthy and nocturnal habits cause them to be ideal carriers for transmitting numerous pathogenic microorganisms. Klebsiella spp., E. coli, P. aeruginosa, Streptococcus spp. and some other potential pathogens have been isolated from cockroaches gathered from hospitals [3–6].
The present investigation was conducted to assess the prevalence rate, antibiotic resistance pattern and genotyping evaluation of antibiotic resistance and virulence factor of the Streptococcus spp. isolated from American, German, Oriental and other species of hospital cockroaches. We found that S. pneumoniae had the highest prevalence among the studied cockroaches (6.96%). Oriental cockroaches had the highest prevalence of S. pyogenes (5.71%) and S. agalactiae (2.85%), while German cockroaches had the highest prevalence of S. pneumoniae (6.83%). Presence of hospital cockroaches in different parts of hospitals, and sewage system caused high prevalence of Streptococcus spp. Although American cockroaches harbored considerable prevalence of bacteria, this species was more often gathered in kitchens, restaurants and supply rooms. In the hospital environment, this distribution, as a vector for nosocomial infections, may reduce its potential. German cockroaches can be a more significant potential vector for nosocomial infections, as they were more commonly found in nursing stations, outpatient rooms, registration rooms, wards, medical record storage rooms as well as drug storage rooms. Various studies have been carried out in this field. For example, Fotedar et al. (1991) [18] indicated that one hundred and fifty-eight out of 159 (99 − 4%) cockroaches gathered from hospital (test) and 113 out of 120 (94 − 2%) cockroaches gathered from residential areas (control) carried medically significant microorganisms. They indicated that 10–20% of cockroaches harbored Streptococcus spp.. Kassiri et al. (2014) [19] disclosed that culturing outer surface wash of cockroaches resulted in the isolation of Klebsiella, Pseudomonas, E. coli, Staphylococcus, Proteus and Streptococcus. The main common bacteria were Klebsiella (35%) and Pseudomonas (30%). Elgderi et al. (2006) [20] indicated that 27 and 25 species of potential pathogen were isolated from the hospital and household cockroaches, respectively, with Klebsiella, Enterobacter, Serratia and Streptococcus being predominant. Salehzadeh et al. (2007) [21] demonstrated that 130 out of 133 (98%) German cockroaches had contamination with high bacterial load (more than 1 × 103). Enterobacter (22.60%), Klebsiela (21%), Enterococcus (17.30%), Staphylococcus (16.50%), E. coli and Streptococcus (8.3%), Pseudomonas (3%), as well as Shigella, Haemophilus and group A ß-hemolytic Streptococcus (less than 1%) were the most commonly detected bacteria. Pai et al. (2004) [5] revealed that the prevalence of Streptococcus spp. in the intestinal content and surface of American and German cockroaches were 38.10% and 38.80% and 32.80% and 17.20%, respectively. Similar findings were achieved in the studies conducted in Iran [22, 23], Thailand [24] and Brazil [25].
Results of our investigation indicated that the Streptococcus spp. strains isolated from cockroaches harbored the high prevalence of resistance against commonly used antibiotic, particularly tetracycline, trimethoprim, enrofloxacin, erythromycin, lincomycin and penicillin. The findings demonstrate the antibiotic resistance seriousness of the common pathogenic bacteria in Iran. A boost prevalence of antibiotic resistance was also reported in the pathogenic bacteria in the hospitals of Taiwan [26]. More than 30% of S. pneumoniae, S. aureus, Enterobacteriaceae, P. aeruginosa, Acinetobacter baumannii, Haemophilus influenzae, coagulase-negative staphylococci, beta-hemolytic streptococci, viridans streptococci, and enterococcal isolates of Taiwanese hospitals were resistant to different antibiotics [26]. Pai et al. (2004) [5] reported that all of the species of common pathogenic bacteria (Streptococcus spp. S. aureus and P. aeruginosa) isolated from cockroaches harbored resistance against ampicillin, chloramphenicol, tetracycline, trimethoprim and sulfamethoxazole. Bouamama et al. (2010) [27] reported that pathogenic bacterial strains isolated from American cockroaches in Spain harbored the high prevalence of resistance against ampicillin, amoxicillin-clavulanate, cefoxitin; gentamicin, cotrimoxazole and ciprofloxacin antibiotics. Hammad and Mahdy (2012) [28] reported the high prevalence of antibiotic resistance of Streptococcus spp. isolated from cockroaches against ampicillin, cephalothin, chloramphenicol, ciprofloxacin, gentamycin, nalidixic acid, tetracycline, trimethoprim and sulfamethoxazole. Different patterns of antibiotic resistance of pathogenic bacterial strains isolated from cockroaches have been reported from Bangladesh [29], Nigeria [30], and India [31]. Such differences in the prevalence of antibiotic resistance reported in different study may be due to the differences in the idea of medical practitioners in antibiotic prescription, availability and expense of antibiotics and finally laws of various countries for antibiotic prescription. Furthermore, high prevalence of antibiotic resistance reported in the present study may be due to the irregular and unauthorized prescription of antibiotics. Phenotypic pattern of antibiotic resistance was supported by the genotypic profile of antibiotic resistance genes. We found that the genes encoding resistance against penicllins (pbp), tetracyclines (tetK, tetM, tetO and tetL), macrolides (erm and mef), streptogramins A and B (rplV), and the lytA gene had considerable prevalence in the Streptococcus spp. strains isolated from hospital cockroaches. To the best of our knowledge, there existed no previously published data in this filed all around the world. High prevalence of pbp, tetK, tetM, tetO, tetL, erm, mef, rplV and lytA antibiotic resistance genes was reported in the Streptococcus spp. strains isolated from different hospital infections [32–34]. Kargar et al. (2012) [35] reported the high prevalence of ermB, mefA, pbp1a, pbp2b and pbp2x genes in the S. pneumonia strains isolated from different types of the hospital infections of hospitalized patients in Intensive Care Unit (ICU) centers. Presence of these genes in the Streptococcus spp. caused their severe resistance against some specific antibiotics. Our findings were also disclosed higher incidence of phenotypic profile of resistance to some antibiotic agents than genotypic profile. This finding is maybe owing to the fact that presence of antibiotic resistance genes is one of the known procedures for occurrence of antibiotic resistance in bacteria. In the other hand, higher incidence of phenotypic resistance toward antibiotics may support by procedures other than presence of antibiotic resistance genes.
The final part of the present research was focused on detecting putative virulence genes in the Streptococcus spp. strains isolated from different types of hospital cockroaches. We found that bac, cyl, glnA, cfb, hylB, scaA, bca, scpB and lmb had considerable prevalence in the Streptococcus. Spp. strains isolated from hospital cockroaches. To the best of our knowledge, there existed no previously published data in this filed all around the world. The α-protein of protein C was encoded by bac and bca genes. This gene group helps bacteria to enter the host cells. Genes bac and bca were detected in 1.12% and 6.74% of bacteria, respectively. Eskandarian et al. (2015) [36] reported the bca and bac genes were found in 14.6% and 9.7% of Streptococcus isolates of hospital infections. Lower prevalence of the bac gene was reported from the United States, New Zealand and Europe [37–39]. We found that the prevalence of cyl, lmb, and scpB genes was 52.80%, 22.47% and 7.86%, respectively. Duarte et al. (2005) [40] reported that the prevalence of lmb and scpB genes in the Streptococcus spp. strains isolated from clinical samples was 97.30% and 96.70%, respectively, which was higher than our findings. Franken et al. (2001) [41] and Dmitriev et al. (1999) [42] also reported higher prevalence of these genes. Cfb gene is encoded by complement factor B facilitating production of the essential component of the alternative course of complement activation. Factor B circulates in the blood as one chain polypeptide. This gene was also predominant in the Streptococcus spp. strains isolated from different hospital infections [43, 44].
Totally, the current survey revealed that hospital cockroaches, particularly oriental and American types, may be sources and reservoirs of pathogenic and antibiotic resistant Streptococcus spp. Thus, monitoring the presence of hospital cockroaches may be useful to decrease the dissemination of virulent and resistant bacteria in hospital environment.