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 Table of Contents  
ORIGINAL ARTICLE
Year : 2021  |  Volume : 14  |  Issue : 2  |  Page : 260-264

Emerging crisis of multidrug-resistant enterococci from a rural tertiary care hospital of North India


1 Department of Microbiology, SHKM, GMC, Nalhar, Nuh (Mewat), Haryana, India
2 Department of Microbiology, NMCH Jamuhar, Sasaram, Bihar, India

Date of Submission08-Nov-2020
Date of Acceptance03-May-2021
Date of Web Publication31-May-2021

Correspondence Address:
Dr. Jyoti Sangwan
Associate Professor, Department of Microbiology, SHKM, GMC, Nalhar, Nuh (Mewat), Haryana
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/kleuhsj.kleuhsj_392_20

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  Abstract 


INTRODUCTION: Enterococci are emerging as a major pathogen causing a variety of hospital-acquired nosocomial infections and community-acquired infections contributing significantly to patient's morbidity and mortality. The emergence of multidrug-resistant enterococci worsens the problem as multidrug resistance leaves fewer therapeutic options for clinicians in treating life-threatening infections.
MATERIALS AND METHODS: This was an observational study carried out from March 2019 to February 2020. Antimicrobial susceptibility testing of enterococci was done by Kirby–Bauer disc diffusion method, and results were interpreted as per the Clinical and Laboratory Standards Institute guidelines 2019.
RESULTS: Multidrug-resistant enterococci were reported to be 62.7%. A variable antimicrobial susceptibility pattern was seen with different antibiotics. Majority of isolates were resistant to β-lactam (96.6%), and high-level aminoglycoside resistance was seen in 39% of isolates. Glycopeptide resistance was observed in teicoplanin (14.6%). No vancomycin and linezolid resistance was noted.
CONCLUSION: The prevalence of multidrug-resistant enterococci was reported to be 63%; the resistance was more common in Enterococcus faecium as compared to Enterococcus faecalis. This study highlights the emergence of multidrug-resistant enterococci, especially to high-level aminoglycoside and glycopeptide which poses a serious therapeutic challenge.

Keywords: Antimicrobial susceptibility testing, high-level aminoglycoside resistance, minimum inhibitory concentration and multidrug-resistant enterococci


How to cite this article:
Sangwan J, Lohan K, Mane P, Kumar M. Emerging crisis of multidrug-resistant enterococci from a rural tertiary care hospital of North India. Indian J Health Sci Biomed Res 2021;14:260-4

How to cite this URL:
Sangwan J, Lohan K, Mane P, Kumar M. Emerging crisis of multidrug-resistant enterococci from a rural tertiary care hospital of North India. Indian J Health Sci Biomed Res [serial online] 2021 [cited 2021 Jun 17];14:260-4. Available from: https://www.ijournalhs.org/text.asp?2021/14/2/260/317411




  Introduction Top


Enterococci are a part of indigenous flora of intestinal tract and genitourinary tract of humans and animals. They are also known as “fecal streptococci,” a potential human pathogen, capable of causing a variety of infections in community as well as in hospital. They were considered harmless bacteria, but during the past few decades, they have emerged as an important nosocomial pathogen exhibiting multidrug resistance, contributing significantly to patient morbidity and mortality.[1]

Enterococci demonstrate variable degree of intrinsic resistance to most of the commonly used antibiotics such as cephalosporins (except ceftazidime), macrolides, sulfonamides, and streptogramins leaving few options for treatment. They are able to survive and disseminate in hospital environment and have ability to acquire resistance to most of the currently available antibiotics by mutation or through transfer of mobile genetic elements carrying resistance genes or virulence factors.

They cause serious life-threatening infections such as endocarditis, bacteremia, meningitis, intra-abdominal and pelvic infections, burn, and surgical site wound infections in both immunocompetent and immunocompromised individuals. They pose a higher risk for causing infections of catheter and other implanted medical devices in critically ill patients and cause late-onset sepsis, pneumonia, and meningitis in neonates.[2] Enterococci are receiving increased attention because of multidrug resistance which explains its prominence as nosocomial infections. The most common nosocomial infections are urinary tract infections, followed by surgical site infections.[3]

Development of multidrug-resistant enterococci has posed an enormous challenge for clinicians. Prolonged stay in hospital, empirical use of antibiotics and lack of sufficient information and program to control spread of enterococci has led to increase morbidity and mortality caused by enterococcal infections. The Centers for Disease Control and Prevention reported that enterococci account for 12% of health-care-associated infections (HAIs) and rank the third most common multidrug-resistant pathogen causing HAI.[4]

The antimicrobial therapy options for enterococcal infection are already limited including ceftazidime, aminoglycosides, and glycopeptides. The organism is notorious for acquiring resistance to the available antimicrobials.[5] Routine antimicrobial susceptibility is recommended for the organism, and a review of susceptibility results periodically is important. Therefore, this study was conducted with an aim to determine the antimicrobial resistance pattern and prevalence of multidrug resistance among enterocci isolated in a tertiary care center.


  Materials and Methods Top


Study design and settings

This was an observational study which was carried out from March 2019 to February 2020 in the Department of Microbiology in Nuh in Haryana after obtaining institutional ethics permission. Ethical clearance was obtained by Institutional Ethics Committee ( SHKM/IEC/2018/35 dated 29/10/2018).

Isolation and identification of enterococci

A total of 142 nonrepetitive clinical isolates of enterococci isolated from various clinical specimens received were identified till the species level with the help of conventional phenotypic methods which included Gram's stain, colony morphology, catalase test, bile-esculin test, growth in 6.5% NaCl, mannitol fermentation, and pyruvate fermentation test.

Antimicrobial susceptibility testing

All enterococcal isolates were tested for their susceptibility to various antibiotics by Kirby–Bauer disc diffusion method. The antibiotics tested were penicillin (10 units), ampicillin (10 mcg), ciprofloxacin (5 mcg), clindamycin (2 mcg), erythromycin (15 mcg), linezolid (30 mcg), teicoplanin (30 mcg), and vancomycin (30 mcg). For high-level aminoglycoside resistance (HLAR) testing, high-level gentamicin disc of 120 mg and high-level streptomycin disc of 300 mg were used. The test was performed on Mueller-Hinton agar and interpreted after 24 h of incubation at 37°C.[6]

Multidrug-resistant enterococci were taken for study which was defined as resistance to two or more than two groups of antibiotics.


  Results Top


Samples such as pus swabs, urine, blood, catheter tip, sputum, cerebrospinal fluid, and body fluids were received in the Department of Microbiology from March 2019 to February 2020. From 421 Gram-positive cocci, a total of 142 (33.7%) isolates were identified as enterococci. Out of 142 isolates, 89 (62.7%) were multidrug-resistant enterococci (resistant to two or more than two groups of antibiotics). Out of 89 isolates, 59 were Enterococcus faecalis and 30 were Enterococcus faecium [Figure 1]. No other enterococcal species were isolated.
Figure 1: Species observed as multidrug-resistant enterococci

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The age of the patients from whom multidrug-resistant enterococci were obtained varied from <1 year to 76 years of age. Maximum number of isolates were from age group more than >60 being 36 isolates (40.4%), followed by age group 45–60 years (20.2%) and 31–45 years (13.5%). The lowest percentage of multi drug resistant Enterococcus was seen in patients with age <10 years (11.2%). It was noticed that among the 89 isolates, 50 samples were from female patients and 39 samples were from male patients. Age- and sex-wise distribution is listed in [Table 1]. Among 89 isolates, majority of isolates were from the inpatient department 83 (93.2%). Department-wise distribution demonstrated the highest number from intensive care unit (ICU) (42.3%), followed by surgery (40.4%) and gynecology (12.3%) followed by other wards (5%) [Figure 2]. As depicted in [Figure 3], the most common clinical sample from which enterococci isolated was urine (40.4%), followed by pus swabs (35.9%) followed by blood (23.5%).
Table 1: Age- and sex-wise distribution of enterococci isolated (n=89)

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Figure 2: Department-wise distribution of multidrug-resistant enterococci

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Figure 3: Sample-wise distribution of multidrug-resistant enterococci

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Out of these 89 isolates, 86 isolates (96.6%) were resistant to penicillin, ampicillin, and cotrimoxazole. Fifty-four (60.7%) isolates were resistant to ciprofloxacin and 45 (50.6%) isolates were resistant to levofloxacin [Table 2]. Fifty isolates (56.2%) were resistant to clindamycin. Among these, 24 isolates demonstrated inducible clindamycin resistance [Figure 4]. A total of 58 (65.2%) isolates were resistant to high-level gentamicin [Figure 5] and 44 (49.4%) were resistant to high-level streptomycin by disc diffusion method. These 44 isolates were resistant to both high-level streptomycin and high-level gentamycin. All isolates were sensitive to vancomycin and linezolid.
Table 2: Antimicrobial susceptibility percentage resistance of enterococcal isolates (Kirby-Bauer disc diffusion method)

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Figure 4: Inducible clindamycin resistance in enterococcal isolate

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Figure 5: Kirby–Bauer disc diffusion method depicting high-level gentamicin-resistant enterococcal isolate

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  Discussion Top


Enterococci are emerging as one of the most common agents of nosocomial infections in the hospital and also cause opportunistic infections in immunocompromised individuals. It is a well-known fact that they can cause a variety of serious life-threatening infections such as endocarditis and bloodstream infections and also cause wound infections and urinary tract infections.[2] Their survival ability under adverse environmental conditions along with the property of intrinsic and acquired resistance to a variety of antibiotics makes them the difficult pathogen to treat. Hence, it is essential to detect them early and institute rationale therapy based on the antimicrobial susceptibility pattern. With the emergence of multidrug-resistant enterococci, the situation has worsened leaving very few options of selecting antibiotics for the treatment of this multidrug-resistant organism. With this context, the present study was attempted to assess the incidence of multidrug resistance among the clinical isolates of enterococci recovered from the patients of a tertiary care institute located in southern rural Haryana.

A total of 89 enterococcal isolates were identified from samples including urine, blood, and pus from March 2019 to February 2020.

Majority of enterococcus isolates were recovered from inpatients (93.2%) than from outpatients (6.8%), which is higher than the findings of Acharya et al. who reported 72% of specimens from hospitalized patients and 28% of specimens from outpatients.[7] This happens because hospitalized patients get colonized with Enterococci more as compared to community settings.

From 89 isolates, majority of isolates were from the inpatient department (93.2%) including ICU (42.3%), followed by surgery (40.4%) and gynecology (12.3%) followed by other wards (4.5%). Paule et al. reported 13.9% of enterococcal isolates from ICU and 12% from non-ICU patients.[8] The risk factors observed in ICU patients were the presence of intravenous catheters, patient on endotracheal intubation, patient on urinary catheterization, the presence of comorbid conditions such as diabetes and heart disease, prolonged hospitalization, and broad-spectrum antibiotic usage such as third-generation cephalosporins. The pus samples from surgical patients were chronic ulcers and discharge from abdominal wound (no drain). In medicine patients, comorbid conditions, broad-spectrum antibiotic usage, and recurrent infections were the associated risk factors. In pediatric patients, malnutrition and prolonged hospitalization were observed. The present study showed similar isolation rates with other studies such as Salem-Bekhit et al., who reported an enterococcal isolation rate of about 85% from ICU, about 27.9% from surgical patients, and 11.3% from internal medicine ward.[9],[10]

In our study, the most common clinical sample from which enterococci isolated was urine (40.4%), followed by pus swabs (35.9%) followed by blood (23.5%). Similarly, Chakraborty et al. reported majority of enterococcal isolates urine (66%) from their study.[11] The explanation is that enterococci inhabit large intestine and can easily responsible for ascending urinary tract infection.

The maximum number of enterococci were isolated from patients aging more than >60 years comprising 29 isolates (32.5%) total cases, followed by 31–45 years (21.3%) and age group 45–60 years (20.2%). Acharya et al. isolated about 30.5% enterococci from pediatric patients which is more than our study finding.[7]

From 89 isolates, 50 samples were from female patients and 39 samples were from male patients. This is in contrary to the findings of Salem-Bekhit et al. who reported a male preponderance of about 91% in their study.[9]

In our study, we observed that E. faecalis is the predominant species, followed by E. faecium which correlates with the findings of our study. In other studies, Perlada et al. reported 69% E. faecalis, 29% E. faecium, and 1% each of Enterococcus avium and Enterococcus durans. Prakash et al. reported 2.5% Enterococcus raffinosus, 2.5% Enterococcus hirae, and 1.7% Enterococcus mundtii, and Salem-Bekhit et al. reported 2.1% E. avium and 0.8% E. hirae. We did not report these species.[9],[12],[13]

On studying the antibiotic susceptibility pattern, we found that most of the enterococcal isolates were resistant to β-lactam (96.6%). This is expected as intrinsic resistance exists against these antibiotics.[14]

Multidrug resistance, i.e. resistance to penicillin, doxycycline, and aminoglycoside, was a common finding in our study among the E. faecium isolates as observed by the studies of Ghoshal et al. and Agarwal et al. (2009) from Lucknow, Central India.[15],[16]

HLAR was also observed. The HLAR was observed in E. faecalis isolates 68% and about 80% in E. faecium. Our findings were similar to the report by Mohanty et al. from North India with a HLAR rate of about 73.3% and 77% by Ghoshal et al. from Lucknow. Furthermore, resistance to streptomycin was observed only in a total of 44 isolates (49.4%) and resistance to gentamicin was observed in 58 isolates (65.2%) in our study which was a little higher than the reports from Salem-Bekhit et al. from Saudi Arabia 20.9% to gentamicin and 19.4% for streptomycin.[9],[16],[17],[18],[19]

This emphasizes the need for conducting frequent surveillance programs for prompt identification of multidrug-resistant enterococci in hospitals and community. This also emphasizes the need for implementation of stringent infection control measures such as rational use of antibiotics, environmental cleanliness, and hand hygiene.[20] These measures are to be strictly followed to bring down the mortality and morbidity associated with these nosocomial infections.


  Conclusion Top


Enterococcal infections are emerging as a pathogen causing a variety of nosocomial and community-acquired infections contributing to morbidity and mortality. The emergence of multidrug resistance leaves hardly any options for clinicians. In this study, 89 multidrug-resistant enterococci were identified using standard laboratory test. The prevalence of multidrug-resistant enterococci was reported to be 63%; resistance was more common in E. faecium as compared to E. faecalis. This study highlights the emergence of multidrug-resistant enterococci, especially in high-level aminoglycoside and glycopeptide which poses a serious therapeutic challenge among clinicians.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

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Higuita NI, Huycke MM. Enterococcal disease, epidemiology, and implications for treatment. In: Enterococci: From Commensals to Leading Causes of Drug Resistant Infection. Boston: Massachusetts Eye and Ear Infirmary; 2014.  Back to cited text no. 2
    
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Kristich CJ, Rice LB, Arias CA. Enterococcal infection – Treatment and antibiotic resistance. In: Enterococci: From Commensals to Leading Causes of Drug Resistant Infection. Boston: Massachusetts Eye and Ear Infirmary; 2014.  Back to cited text no. 5
    
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Acharya A, Khanal A, Kanungo R, Mohapatra T. Characterization and susceptibility patterns of clinically important Enterococcus species in eastern Nepal. Nepal Med Coll J 2007;9:250-4.  Back to cited text no. 7
    
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Trick WE, Paule SM, Cunningham S, Cordell RL, Lankford M, Stosor V, et al. Detection of Vancomycin-Resistant Enterococci Before and After Antimicrobial Therapy:Use of Conventional Culture and Polymerase Chain Reaction. CID 2004;38:780-86.  Back to cited text no. 8
    
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Chakraborty A, Pal NK, Sarkar S, Gupta MS. Antibiotic resistance pattern of Enterococci isolates from nosocomial infections in a tertiary care hospital in Eastern India. J Nat Sci Biol Med 2015;6:394-7.  Back to cited text no. 11
    
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Agarwal J, Kalyan R, Singh M. High-level aminoglycoside resistance and beta-lactamase production in enterococci at a tertiary care hospital in India. Jpn J Infect Dis 2009;62:158-9.  Back to cited text no. 15
    
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