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ORIGINAL ARTICLE
Year : 2021  |  Volume : 14  |  Issue : 4  |  Page : 403-408  

Surveillance of health-care workers hand to detect carriage of multidrug-resistant Staphylococcus spp. in a tertiary care center: An observational study


1 Department of Microbiology, Hind Institute of Medical Science, Lucknow, Uttar Pradesh, India
2 Department of Emergency Medicine, SGPGI, Lucknow, Uttar Pradesh, India
3 Department of Microbiology, KGMU, Lucknow, Uttar Pradesh, India
4 Department of Microbiology, Era's Medical College, Lucknow, Uttar Pradesh, India
5 Department of Microbiology, RMLIMS, Lucknow, Uttar Pradesh, India
6 Department of Biostatistics and Health Informatics, SGPGI, Lucknow, Uttar Pradesh, India

Date of Submission03-Jul-2020
Date of Decision22-Oct-2020
Date of Acceptance02-Dec-2020
Date of Web Publication04-May-2021

Correspondence Address:
Tanmoy Ghatak
Rammohan Pally, Arambagh, Hooghly - 712 601, West Bengal
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/mjdrdypu.mjdrdypu_372_20

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  Abstract 


Objective: Healthcare-associated infection (HCAI) has become a potential peril in intensive care unit (ICU), operation theater (OT) as well as postoperative wards. Those infections are often caused by multidrug-resistant (MDR) organisms. Health-care workers (HCWs), who are taking care of sick patients, often colonize and transmit microorganism from infected to noninfected patient causing HCAIs. The purpose of this study was for surveillance of potential pathogens as hand carriage among HCWs. Materials and Methods: Hand swabs were collected from palmar surface and interdigital space of predominant hands of HCWs working in ICU, OT, and postoperative wards. Antimicrobial susceptibility profile of the potential pathogen isolates including Staphylococcus spp. was also determined for several antibiotics. Methicillin resistance was detected using cefoxitin 30 μg disc. Results: In our study, among 199 HCWs, there was a high carriage rate of Staphylococcus spp. in hands 98 (49.2%) (male: female 1:1). Among Staphylococcus spp., Coagulase-negative staphylococci (CoNS) was around 69 (34.6%) and Staphylococcus aureus was around 29 (14.5%). (including methicillin-resistant S. aureus [MRSA] and methicillin-resistant coagulase-negative Staphylococci [MR-CoNS]). Nearly 65% in MRSA and 75% MR-CoNS were macrolide resistant also. The MRSA hand carriage was significantly high in HCWs having <10 years of service (P = 0.035). No Gram-negative bacteria were identified. Nearly 54 (27%) HCWs were found to be noncarriers (sterile). Conclusion: In our tertiary care center, hand carriage of potential pathogens such as MDR Staphylococcus spp. was very high among HCWs.

Keywords: Hand carriage, health-care workers, multidrug resistance, Staphylococcus spp


How to cite this article:
Kulshrestha N, Ghatak T, Gupta P, Singh M, Agarwal J, Mishra P. Surveillance of health-care workers hand to detect carriage of multidrug-resistant Staphylococcus spp. in a tertiary care center: An observational study. Med J DY Patil Vidyapeeth 2021;14:403-8

How to cite this URL:
Kulshrestha N, Ghatak T, Gupta P, Singh M, Agarwal J, Mishra P. Surveillance of health-care workers hand to detect carriage of multidrug-resistant Staphylococcus spp. in a tertiary care center: An observational study. Med J DY Patil Vidyapeeth [serial online] 2021 [cited 2021 Aug 4];14:403-8. Available from: https://www.mjdrdypv.org/text.asp?2021/14/4/403/315470




  Introduction Top


Healthcare-associated infections (HCAIs) are infections that patients developed in a hospital or other health-care facility that first appear 48 h or more after hospital admission, or within 30 days after having received health care, which was neither present nor in the incubation phase during hospitalization.[1] HCAIs with methicillin-resistant Staphylococcus aureus (MRSA), vancomycin-resistant enterococci, and multidrug-resistant (MDR) Pseudomonas were reported.[2],[3],[4]

Health-care workers (HCWs), such as doctors, nursing staffs, cleaners, ward boy, and operation theater (OT) assistant, are meticulously taking care of and closely interacting with patients in intensive care unit (ICU), OT, and postoperative wards. These workers may serve as reservoirs or vectors of MDR pathogens.[2],[3],[4],[5],[6] They thus can play a role in harboring and transmitting potential MDR pathogens from infected to noninfected susceptible patients causing HCAIs.[2],[3],[4],[5],[6] The colonized HCWs can also contaminate the commonly used medical devices (such as machine knobs and computers).[6],[7],[8]

Staphylococcus spp. colonizes in mucous membrane of HCWs, especially anterior nares.[6],[7] From the anterior nares, Staphylococcus spp. can be lodged in other extranasal sites such as hands, pharynx, and axillae due to self-inoculation by fingers touching the nose.[6] Because of this, assessment of hand carriage of MDR organisms among HCWs, working in ICU, OT, and postoperative words, has become a significant issue demanding investigation. The apparently subtle looking contaminant, coagulase-negative Staphylococcus (CoNS) are also potential pathogens and have been isolated in several HCAIs including bloodstream infections.[9] CoNS similarly colonize different parts of the skin and mucous membranes of humans, and methicillin resistance becomes common in them.[7],[10]

Much have been talked on the bacterial carriage in anterior nares of HCWs and its prevention, but hand carriage of MDR bacteria by HCWs is important to know.[7] Extensive search on surveillance of hand transmission of MDR organisms by HCWs yields a few researches combining hand and objects, hand, and anterior nares.[2],[11] There is only one “hands only” study from neonatal ICU, New York.[12] We found one study from south India which focuses on hand and object surveillance of HCWs in ICU.[3] Our institutional protocol is performing hand hygiene by HCWs before and after every ICU/OT patient contact mostly by carefully rubbing their hands with an alcoholic compound. This study is therefore undertaken as part of a hospital infection control surveillance program of our tertiary care center in nonoutbreak period.


  Materials and Methods Top


Institutional ethical committee clearance was taken for this surveillance study. The study period is May 2015–October 2015. Specimen collection process is explained to HCWs. Sociodemographic characteristics of HCWs and their last handwashing/alcohol-based hand rubbing status were documented. A written and informed consent was obtained from each HCW participating in the study. The sample size of this study was estimated, using the prevalence of hand carriage of S. aureus among HCWs was 8%.[12],[13] With 4% margin of error in the given prevalence, at two sided 95% confidence interval, estimated sample size was 177. The sample size was estimated using software Power analysis and sample size version-16 ((PASS-16, NCSS, LLC, Utah, USA). In this study, we included 199 HCWs.

Specimens were taken from palmar surface and interdigital space of predominant hand of HCWs, i.e., doctors, nursing staffs (includes nursing staffs, physiotherapist, and OT assistants) and cleaners (includes cleaners and ward boys). All the samples are collected in working hours.

Exclusion criteria

Staffs who are not actively working in ICU, OT, and postoperative words and staff having dermatitis and skin lesion in hands were excluded from the study.

Specimen collection

With gloved hands, sterile cotton wool swab stick was removed from screw-capped polypropylene tube (Hi-Media Laboratories, Mumbai, India). A single swab was premoistened with nonbacteriostatic normal saline and rubbed over the palmar surface and interdigital space of predominant hand of HCWs (10 s). Screw-capped polypropylene tube was labeled with appropriate information.

These swabs were inoculated on 5% sheep blood agar (Hi-Media Laboratories, Mumbai, India) and MacConkey agar (Hi-Media Laboratories, Mumbai, India) without delay. These plates were incubated aerobically at 35°C for 48 h. The plates were read at the end of 48 h and the plates which did not show any growth even after 24 h were considered sterile. Colony characteristics on the culture plates and Gram-staining were used to further confirm the bacteria. Gram staining helped to ascertain that there were no other contaminants by confirming the characteristic morphology. Isolates that were Gram-positive, cocci-shaped, arranged in pairs, and clusters were identified as Staphylococcus spp. Catalase, dimethyl sulfoxide oxidase, DNAse, and coagulase tests helped to identify species of Staphylococcus.[14],[15] S. aureus result in the typical golden yellow colonies on sheep blood agar.[14] Growth of Gram-negative bacteria was also noted.

Antimicrobial susceptibility testing

Antibiogram was made by the Kirby–Bauer Disc Diffusion method as per the CLSI standards.[16] The zone diameters were interpreted against the following antibiotics – penicillin G (10 Units), ampicillin (10 μg), erythromycin (15 μg), tetracycline (30 μg), gentamicin (10 μg), vancomycin (30 μg), co-trimoxazole (1.25/23.75 μg), ciprofloxacin (10 μg), linezolid (30 μg), and imipenem (10 μg). Methicillin resistance was detected using cefoxitin 30 μg disc (Hi-Media Labs, India). Zone of inhibition of size <21 mm for S. aureus and < 24 mm for CONS was considered as resistant.[16]

S. aureus isolates with constitutive resistance display resistance to erythromycin and clindamycin on in vitro testing. S. aureus isolates with inducible resistance show resistance to erythromycin but appears sensitive to clindamycin on disc diffusion testing. Inducible clindamycin resistance in staphylococci was tested by “D test” as per the CLSI guidelines.[17] Erythromycin (15 μg) disc was placed at a distance of 15 mm (edge to edge) from clindamycin (2 μg) disc on a Mueller-Hinton agar plate, previously inoculated with 0.5 McFarland standard bacterial suspensions.

Gram-negative bacteria were only identified and biochemically tested but not processed for culture sensitivity.

Statistical analysis

Descriptive statistics of the continuous data were presented as mean ± standard deviation (SD) and median (range) while categorical data in frequency (%). Chi-square test/Fisher's exact test was used to compare the proportions between the groups as appropriate. A P < 0.05 was considered statistically significant. Statistical Package for the Social Sciences software version-23 (SPSS-23, IBM, Chicago, IL, USA) was used for data analysis.


  Results Top


Samples obtained

A total of 220 HCWs were targeted. Sixteen HCWs were excluded (11 HCWs were inactively involved in patient care and five negatively consented). Five samples were discarded due to plate contamination. A total of 199 samples were analyzed from ICU, OT, and wards. Mean (SD) and median (range) of age of the HCWs were 37.6 (18.5) and 34 (20–61). Almost equal proportions of male and female HCWs (47.2% vs. 52.8%, P = 0.436) were assessed. Out of total samples, highest were belonged to doctors (78, 39.3%) followed by nursing staff (67, 33.6%) and cleaners and ward boys (54, 27.1%).

Microorganisms detected

In our study among 199 HCWs, there was a carriage rate of Staphylococcus spp. in hands 98 (49.2%) (male: female [M:F] 1:1). Among them, coagulase-negative Staphylococcus (CoNS) was 69 (34.6%) and S. aureus was 29 (14.5%). Importantly, 20 (10.05%) was MRSA (M:F = 3:2), and MR-CoNS was 33 (16.6%) (M:F = 1:1). The MRSA carriage was significantly high in HCWs having <10 years of service (P = 0.035) [Table 1].
Table 1: Sociodemographic characteristics of health-care workers

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In further subgroup analysis of the organisms as well as HCWs was done to know percentage of MRSA and MR CoNS carriage. Doctors (n = 78) were carrying 8 (10.2%) MRSA (M:F = 5:3) and 17 (22.3%) MR-CoNS (M:F = 1:1) in their hands. Similarly, hand swabs of nursing staffs (n = 67) growing 2 (3%) MRSA (M:F = 1:1) and 5 (7.5%) MR-CoNS (M:F = 2:3) in their hands. While hands of cleaners and ward boys (n = 54) have 10 (18.5%) MRSA (M:F = 3:2) and 11 (20.3%) MR-CoNS (M:F = 7:4). No Gram-negative bacteria were identified. Fifty-four (27%) hand samples were sterile [Table 2].
Table 2: Percentage of organisms found in doctors, nursing staffs, and cleaner's hands

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For the MR-CoNS group, male was 70.6%, 40.1%, and 36.3% in doctors, nursing, and cleaner groups (P = 0.171), while in MRSA group, it was 62.5%, 50%, and 60% (P = 0.998), respectively.

Antibiogram of multidrug-resistant organisms

Of all MRSA found in hands of HCWs, 65% having macrolide resistance. Of doctors, 62.5% were macrolide resistant (M:F = 4:1). All were constitutive resistance. Of all MRSA found in hand of nursing staffs, 100% of were macrolide resistant (M:F = 1:1). Of them, 50% were inducible resistance. Of all MRSA found in hand of cleaners, 60% were also macrolide resistant (M:F = 5:1). All were constitutive resistance [Table 3].
Table 3: Antibiogram of methicillin-resistant Staphylococcus aureus found in health-care worker's hand

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Of MR-CoNS found in HCWs, 75% having macrolide resistance. Doctor's having (M: F= 8:5) 78.4% of macrolide resistance among MR-CoNS, 7% of them were inducible resistance. Nursing staffs having 60% macrolide resistance MR-CoNS (M: F = 1:2). Of 60% of macrolide resistance, all were constitutive resistances. Of all MR-CoNS found in hand of cleaners, 81.8% were also macrolide resistant (M:F = 2:1). Of that, 12% were inducible resistance [Table 4].
Table 4: Antibiogram of methicillin-resistant coagulase-negative staphylococci found in hand of health-care workers

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All isolates of Staphylococcus (MRSA and MR-CoNS) were sensitive to linezolid, aminoglycoside, TMP-SMZ, and tetracycline.


  Discussions Top


To our knowledge, this is the recent largest Indian study to screen hand carriage by HCWs in the ICU, OT, and postoperative ward. We got a high carriage rate of Staphylococcus spp. in hands 98 (49.2%) among 199 HCWs.

The multicenter study in neonatal ICU from New York assessed 1000 hand samples of HCWs.[12] They showed 12% hand carriage of potentially pathogenic organisms such as S. aureus (8%), enterococci (3%), and Gram-negative bacilli (2%). They found CoNS and diphtheroid in around 97% of the hand samples, but MRSA carriage was very low (0.6%). They accepted that organism's carriage in their study was relatively low because of HCWs frequent hand hygiene practice and glove use. In our study, we got high carriage may be because of low compliance with the hand hygiene practices that needs to be studied separately.

In our study, we got significantly high MRSA hand carriage in HCWs having <10 years of service. In the previous study, there is a relation between S. aureus nasal carriage with HCWs services year duration.[18] The highest rate of 59% nasal carriage was observed among those who worked for 4–6 years services. We got similar result in hand carriage. This is due to poor knowledge among youngsters regarding the importance of hand hygiene practices.

We found one study from south India, which focuses on hand and object surveillance of HCWs in ICU.[3] Out of the 157 hand sampling done by glove juice method, 67 (42.7%) of them showed growth. The potential pathogens grown were 13 (8.3%), consisting of methicillin-sensitive S. aureus (MSSA) 6 (3.8%), MRSA 2 (1.3%), Pseudomonas spp. 4 (2.6%), and Acenitobacter spp. 1 (0.6%). In our study, MRSA rates were 10.05%.

Previous studies have shown male HCWs were more likely to have hand carriage of potential pathogens as they have reduced hand hygiene compliance when compared to female HCWs.[11],[12],[19] We found that hand carriage of MRSA and MR-CoNS in HCWs was nearly 1:1 in male: female ratio. One important observation we got a male predominance in both MDR S. aureus and MDR CoNS isolate in doctor and cleaner's population.

We did not find Gram-negative bacilli in our hand samples. Some studies of HCP hand carriage of Gram-negative bacilli were found during outbreaks.[19],[20] Most of the potential Gram-negative bacilli was associated with artificial nails. In Indian setup, artificial nails are uncommon, and so we did not get Gram-negative bacterial carriage.

In our study, hand carriage of MRSA and MR-CoNS reveals nursing staff carrying less pathogen than doctor and cleaners. Previous studies have shown hand carriage of Staphylococcus spp. among physicians was high compared to nurses.[11],[21] In some study, potential pathogens from hand samples from nurses versus nonnurses were similar[12] that may be due to our nursing staffs are more conscious regarding handwashing than doctors and cleaners just seen in other studies.[21]

One important observation we got in our study is MDR status of MRSA and MR-CoNS isolated from hands of HCWs. Other studies targeting hand surveillance claims hand carriage of MDR MRSA also.[11],[22] In one of them, where MRSA carriage was 6.2% among 177 HCWs, the highest resistance was observed for ampicillin (88.9%) and tetracycline (86.1%).[11] The highest resistance was observed for ampicillin (88.9%) and tetracycline (86.1%).[11] Contrary to this, our study showed a higher percentage of hand carriage of MDR S. aureus and CoNS (macrolide resistance). The most probable cause of difference could be strict following of infection control and hand hygiene practices and better doctor population ratio.

Importantly, hand hygiene practices compliance, staffing pattern, staff awareness toward hand hygiene, adoption of antibiotic stewardship programs play role in hand carriage of MDR bacteria in HCWs, and cross-transmission of infections as well.

This study had some limitations such as:

  1. Sample size can be improved by multi-institutional collaboration. We are planning for multi-institutional ICU study
  2. Nondominant hand of HCWs not considered in sampling, though infection can be spread from nondominant hand also
  3. Most samples were collected during day shifts
  4. Glove juice technique of sample collection from hands was not considered. Although it is more sensitive than imprint/contact method, it is costly.



  Conclusion Top


The study showed that the HCWs were a carrier for MDR organisms specially MDR Staphylococcus spp. Second, there is a relation between S. aureus hand carriage with HCWs services year duration. Third, our study gives an impression of MRSA and MR-CoNS isolates from hand flora and their MDR pattern in our institute. Last but not the least, regular hand screening of HCWs is essential for inhibition of transmission of nosocomial infections.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 1], [Table 2], [Table 3], [Table 4]



 

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