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ORIGINAL ARTICLE Table of Contents   
Year : 2010  |  Volume : 53  |  Issue : 4  |  Page : 738-741
Staphylococcus aureus phage types and their correlation to antibiotic resistance

1 Department of Microbiology, National Staphylococcal Phage Typing Center, Maulana Azad Medical College, New Delhi-110 002, India
2 Department of Microbiology, L N Hospital, New Delhi-110 002, India

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Date of Web Publication27-Oct-2010


Context: Staphylococcus aureus is one of the most devastating human pathogen. The organism has a differential ability to spread and cause outbreak of infections. Characterization of these strains is important to control the spread of infection in the hospitals as well as in the community. Aim: To identify the currently existing phage groups of Staphylococcus aureus, their prevalence and resistance to antibiotics. Materials and Methods: Study was undertaken on 252 Staphylococcus aureus strains isolated from clinical samples. Strains were phage typed and their resistance to antibiotics was determined following standard microbiological procedures. Statistical Analysis: Chi square test was used to compare the antibiotic susceptibility between methicillin resistant Staph. aureus (MRSA) and methicillin sensitive S. aureus (MSSA) strains. Results: Prevalence of MRSA and MSSA strains was found to be 29.36% and 70.65% respectively. Of these 17.56% of MRSA and 40.44% of MSSA strains were community acquired. All the MSSA strains belonging to phage type 81 from the community were sensitive to all the antibiotics tested including clindamycin and were resistant to penicillin. Forty five percent strains of phage group III and 39% of non-typable MRSA strains from the hospital were resistant to multiple antibiotics. Conclusion: The study revealed that predominant phage group amongst MRSA strains was phage group III and amongst MSSA from the community was phage group NA (phage type 81). MSSA strains isolated from the community differed significantly from hospital strains in their phage type and antibiotic susceptibility. A good correlation was observed between community acquired strains of phage type 81 and sensitivity to gentamycin and clindamycin.

Keywords: Community acquired Staphylococcus aureus, phage typing, sensitivity to clindamycin

How to cite this article:
Mehndiratta P L, Gur R, Saini S, Bhalla P. Staphylococcus aureus phage types and their correlation to antibiotic resistance. Indian J Pathol Microbiol 2010;53:738-41

How to cite this URL:
Mehndiratta P L, Gur R, Saini S, Bhalla P. Staphylococcus aureus phage types and their correlation to antibiotic resistance. Indian J Pathol Microbiol [serial online] 2010 [cited 2021 Aug 5];53:738-41. Available from: https://www.ijpmonline.org/text.asp?2010/53/4/738/72065

   Introduction Top

Staphylococcus aureus has emerged as a prime pathogen of nosocomial and community acquired infections around the world. [1] The increasing prevalence of multiple drug resistant strains is an additional problem for the patients responding poorly to treatment and to the hospitals performing infection control and prevention program. [2] Available data on epidemiology of Staphylococcus aureus shows that epidemical methicillin resistant Staphylococcus aureus (MRSA) strains of certain phage types are more virulent and spread rapidly in hospitals. These phage types responsible for infections may vary from time to time and hospital to hospital in their antibiotic resistant patterns. [3] Typing of these strains is important in epidemiology to differentiate and evaluate the importance of these strains in spreading the infection.

The present study was undertaken to study the epidemiology of Staphylococcus aureus strains with reference to currently existing phage types, their prevalence and resistance of different phage groups to antibiotics.

   Materials and Methods Top

Two hundred and fifty two strains of S. aureus isolated from clinical samples collected during the period from January 2008 to October 2008 were studied. Of the total 252 strains 208 strains were isolated from pus, 18 strains from blood, 22 from body fluids and four from the catheter tip.

Strains were confirmed as S. aureus by standard techniques based on colony morphology, gram staining, catalase, slide and tube coagulase tests. [4]

Antibiotic sensitivity testing was performed using modified stokes same plate comparative disc diffusion test. [5] Antibiotic discs used were:-methicillin (5μg), penicillin (10 I.U), cephalexin (30μg), gentamycin (10μg), erythromycin (15μg), ciprofloxacin (5μg), clindamycin (2μg), rifampicin (2μg), fusidic acid (10μg) and vancomycin (30μg). Separate plates were used for methicillin testing on Mueller Hinton agar and these plates were incubated at 30 0 C for 24 hours. All methicillin resistant strains were confirmed by oxacillin screening using 6μg/ ml oxacillin in Mueller Hinton agar with 4% Na Cl. [6] Staph. aureus ATCC 25293 was used as control.

Phage typing was performed at Staphylococcal phage typing center, MAM College New Delhi. Typing was done by standard methods at 100x RTD (routine test dilution) using an international set of 23 phages. [7] The strains were classified as Group I- 29, 52, 52A, 79, 80, Group II- 3A, 3C, 55, 71, Group III- 6, 42E, 47, 53, 54, 75, 77, 83A, 84, 85, Group IV- 94, 96 and non allocated 81,95, The results were interpreted using the criteria of differentiating the strains if they showed the difference of two strong reactions.

Statistical Analysis

Chi square test was used to compare the antibiotic susceptibility between MSSA (methicillin sensitive Staph. aureus) and MRSA strains and between phage groups.

   Results Top

Of the total 252 strains, 74 (29.36%) were found to be resistant and 178 (70.63%) were sensitive to methicillin. Susceptibility of MSSA and MRSA strains to various antibiotics is shown in [Figure 1].
Figure 1 :Susceptibility of methicillin resistant Staphylococcus aureus and methicillin sensitive Staphylococcus aureus strains to antibiotics

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Of the 74 MRSA strains 13 (17.56 %) and out of 178 MSSA, 72 (40..44 %) were community acquired i.e. the clinical samples were obtained from outpatient or within 48 hours of admission and were unrelated to any interventional procedure however the previous history of hospitalization and other risk factors is not known.

Conventional phages of the basic set could type 178 (70.63 %) of the 252 strains. Percentage typeability among the MSSA and MRSA strains was found to be 87.71% and 40.54% respectively. Phage group distribution amongst MSSA and MRSA strain is found as Group I (32.02% MSSA and 9.45 % MRSA), Group II (10.11 % MSSA and 2.70 % MRSA), Group III (8.99 % MSSA and 14.86 % MRSA), Group IV (2.24 % MSSA and 0.00% MRSA), Mixed group (10.11% MSSA and 10.81 % MRSA) and NA group (20.22% MSSA and 2.70 % MRSA). Correlation of different phage groups of MRSA and MSSA to antibiotic susceptibility is shown in [Table 1] and [Table 2] respectively. A remarkable difference in the phage group distribution amongst MRSA and MSSA strains from the community was observed as shown in [Figure 2].
Table 1 :Prevalence of various phage groups and their susceptibility to antimicrobial agents among methicillin resistant Staphylococcus aureus strains

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Table 2 :Prevalence of various phage groups and their susceptibility to antimicrobial agents among methicillin sensitive Staphylococcus aureus strains

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Figure 2 :Distribution of phage groups amongst methicillin resistant Staphylococcus aureus and methicillin sensitive Staphylococcus aureus strains from community

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   Discussion Top

The epidemiology of Staphylococcus aureus has continued to change during the past few decades. Methicillin resistant strains which were initially isolated in health care settings are now emerging in the community. [8] To control the spread of these strains it is important to understand the epidemiological relatedness between the organisms. Bacteriophage typing is an established method for epidemiological typing of S. aureus strains. On analysis of the results of phage typing we found that phage group III is predominant amongst MRSA strains isolated from the hospital acquired infections and phage group NA is predominant amongst MSSA strains from the community. Predominance of phage Group I and III strains was reported in hospitals by many workers with cyclic fluctuations every 10 - 12 years. [3] In a study during the year 1999, the most common phage group was found to be mixed group followed by Phage 85. [9] In the year 2001 a slight deviation was observed in the circulating phages however phage Group III was reported as predominant phage group which is prevailing in the MRSA strains of the present study. [10],[11] Predominance of phage group II in MSSA and phage Group III in MRSA strains has been reported by several studies. [12],[13] Zierdt and coworkers [14] found in their study that 54% of their strains belonged to mixed group of phages. Kareiviene et al. [3] found that 12.9% of their strains belonged to ungroupable phages.

On comparing the antibiotic susceptibility between MRSA and MSSA strains [Figure 1] it was clear that MSSA strains were significantly more sensitive to majority of antibiotics as compared to MRSA strains (P<0.0001 for cephalexin, gentamycin, erythromycin, fusidic acid, clindamycin and rifampicin). The reason for low prevalence of resistance to multiple antibiotics amongst MSSA strains can be explained by the fact that a large number (40.44%) of our MSSA strains were isolated from the community. The antibiotic selective pressure is much lower within the community than in the hospitals so the survival of multiple drug resistance is lower. It is also documented by various studies that community acquired isolates are generally more susceptible to multiple antimicrobial agents other than ί lactams. [2]

Further, it is known that certain resistant patterns are characteristic of certain phage groups. [15] Phage group II strains had been more frequently isolated amongst the MSSA strains from the community. [3] In our study, the predominant phage group amongst MSSA strains from the community was NA (phage type 81) 20.22%, followed by Group II (10.11 %) and Group IV (2.24 %). A significant finding about these strains was that all phage type 81 strains were sensitive to all the antibiotics tested including clindamycin but were resistant to penicillin. Our results are comparable to the findings of Kareieve et al. [3] They reported that their ungroupable MSSA strains (phage type 81 and 95) were susceptible to all investigated antibiotics. Clindamycin susceptibility has also shown a significant correlation with community acquired strains. [2] Strains belonging to phage type 52,52A, 80, 81 complexes were reported significantly more resistant to erythromycin and doxycyclin than Group IV and Group II to tetracycline. [3] Strains of phage type 83 A were reported as related to resistance to methicillin. [15]

All the strains of MRSA and MSSA were found to be sensitive to vancomycin. Analysis of the data on MRSA strains showing resistance to multiple antibiotics i.e. more than five antibiotics tested, it was noticed that 45% strains of Group III and 39 % non-typable strains were multiresistant. These findings are in consistence of other studies. [16]

The study demonstrated that the isolates considered as representing community acquired strains differ from the nosocomial isolates in both phage types and antimicrobial susceptibility. The data indicated that phage Group III was predominant amongst MRSA strains and NA group (phage type 81) was most predominant amongst MSSA strains. A good correlation was observed between phage type 81 and sensitivity to clindamycin in MSSA strains isolated from the community.

   References Top

1.Sheagren JN. Staphylococcus aureus, the persistent pathogen. New Eng J Med 1984;310:1368-73.   Back to cited text no. 1
2.Suntharam N, Hacek D, Peterson LR. Low Prevalence of Community-Acquired Methicillin-Resistant Staphylococcus aureus in Adults at a University Hospital in the Central United States. J Clin Microbiol 2001;39:1669-71.   Back to cited text no. 2
3.Kareiviene V, Pavilonis A, Sinkute G, Liegiute S, Gailiene G. Staphylococcus aureus resistance to antibiotics and spread of phage types. Medicina (Kaunas) 2006;42:332-9.  Back to cited text no. 3
4.Baird D. Staphylococcus. Cluster forming gram positive cocci. In: Mackie and McCartney Practical Medical Microbiology.14 th ed. New York: Churchill Livingestone; 1996. p. 245-58.  Back to cited text no. 4
5.Stokes EJ, Ridgeway GL, Wren MW. In: Antimicrobial drugs in Clinical Microbiology. 7 th ed. London: Edward Arnold; 1993. p. 234-80.  Back to cited text no. 5
6.Thornsberry C, Mcdougal LK. Successful. Use of Broth Microdilution in Susceptibility Tests for Methicillin-Resistant (heteroresistant) Staphylococci. J Clin Microbiol 1983;18:1084-91.  Back to cited text no. 6
7.Blair JE, Williams RE. Phage typing of Staphylococci. Bull WHO 1961;4:771-84.   Back to cited text no. 7
8.Chambers HF. The changing Epidemiology of Staphylococcus aureus? Emerg Infect Dis 2001;7:178-85.  Back to cited text no. 8
9.Gupta N, Krishna Prakash S, Malik VK, Mehndiratta PL, Mathur MD. Community Acquired Methicillin Resistant Staphylococcus aureus: a new threat for hospital outbreaks? Indian J Pathol Microbiol 1999;42:421-6.  Back to cited text no. 9
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10.Vidhani S, Mehndiratta PL, Mathur MD. Study of methicillin resistant s. aureus (MRSA) isolates from high risk patients. Indian J Med Microbiol 2001;19:87-90.  Back to cited text no. 10
11.Mehndiratta PL, Vidhani S, Mathur MD. A study on Staphylococcus aureus strains submitted to a reference laboratory. Indian J Med Res 2001;114:90-4.   Back to cited text no. 11
12.Usman CW, Okubo T, Okamoto R. Antimicrobial Susceptibilities and Phage typing of Staphylococcus aureus Clinical Isolates in Indonesia. J Infect Chemother 1996;2:29-33.  Back to cited text no. 12
13.Samba Z, Gadba R. Antibiotic susceptibility and Phage typing of methicillin resistant Staphylococcus aureus Clinical Isolates blood cultures of 692 patients in 15 Israeli hospitals. Eur J Epidemiol 1993;9:559-62.  Back to cited text no. 13
14.Zierdt CH, Robertson EA, William RL, Mac Lowry DJ. Computer analysis of Staphylococcus aureus phage typing data from 1957 to 1975, citing epidemiological trends and natural evolution within the phage typing system. Appl Environ Microbiol 1980;39:623-9.   Back to cited text no. 14
15.Rosendal K, Biilow P. Staphylococcus aureus strains isolated in Danish hospitals. Acta Pathol Microbial Scand 1967;71:422-38.  Back to cited text no. 15
16.Udo EE, AL-Sweih N, Dhar R, Mokaddas EM, Johny M, AL-Obaid IA, et al. Surveillance of Antimicrobial Resistance in Staphylococcus aureus Isolated in Kuwaiti hospitals. Med Princ Pract 2008;17:71-5.  Back to cited text no. 16

Correspondence Address:
P L Mehndiratta
Department of Microbiology, National Staphylococcal Phage Typing Center, Maulana Azad Medical College, New Delhi-110 002
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0377-4929.72065

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  [Figure 1], [Figure 2]

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