INTRODUCTION:

Health Care-Associated Infection (HCAI) is an infection occurring in a patient during the process of care in a hospital or other health-care facility which was not present or incubating at the time of admission. This includes infections which are acquired in the hospital but appearing only after discharge and also occupational infections among staff of the facility.^[1]

It has been reported that the incidence of nosocomial infections in the intensive care unit (ICU) is about 2 to 5 times higher than in the general inpatient hospital population.^[2] The hike in morbidity and mortality, associated with nosocomial infections in the ICU is a matter of serious concern today.

Transmission of healthcare - associated pathogens generally occur via the contaminated hands of Health Care Workers (HCWs), often transmitting virulent and multi-drug resistant strains of bacteria.^[2] Acquisition of infection, especially cross-infection from one patient to another, is in many cases preventable by adhering to simple practices. Hand hygiene is one of the primary measures necessary for reducing HCAI.^[3] Although adhering to practices in maintaining hand hygiene is simple, the lack of compliance among HCWs continue to be a problem worldwide. The newly developed Five Moments for Hand Hygiene has emerged from the WHO Guidelines on Hand Hygiene in Health Care to add value to any hand hygiene improvement strategy.^[1]

Multidrug Resistant (MDR) organisms thus transmitted through the hands of health care workers are a major cause of HCAIs. MDR organisms are microbes (predominately bacteria) resistant to more than one class of microbial agents. Some of the MDR bacteria are MRSA (Methicillin Resistant Staphylococcus aureus) and VRE (Vancomycin Resistant Enterococcus).^[4][5]MRSA is a major cause for Hospital Acquired Infections (HAI) all over the world. In India, the prevalence of MRSA ranges from 20-80%.^[6][7]

Surveillance of hand hygiene is required to determine the implementation of hand hygiene measures for infection control. Assessment of knowledge among health care workers regarding hand hygiene practices also need to be done from time to time. The most commonly used hand sampling methods to evaluate hand hygiene are the Palm and finger press method, Swab method and the Glove juice technique.^[8]

A diminishing HCAI rate and good compliance to infection control practices contribute to improving patient care. In view of the above factors, this study was undertaken to study the carriage of MDR bacteria in the hands of HCWs using glove juice technique and to assess the knowledge of HCW.

AIMS AND OBJECTIVES:

1. To study the carriage of Multi Drug Resistant bacteria using Glove Juice Technique in the hands of Health Care Workers (HCWs).

2. To determine the frequency and pattern of microorganisms in the hands of Health Care Workers (HCWs).

3. To determine the antimicrobial susceptibility pattern in isolates.

4. To determine the extent of knowledge about hand hygiene practices based on the WHO hand hygiene questionnaire for Health Care Workers

MATERIALS AND METHODS:

Study Design and Period:

This is a cross-sectional study which was conducted at the Department of Microbiology in association with the Department of General Surgery, Department of Obstetrics and Gynaecology, Department of Emergency Medicine, Department of General Medicine and Intensive Care Unit (ICU) for a period of two months, after the approval of Institutional Ethics Committee (IEC) at Saveetha Medical College and Hospital, Thandalam, Chennai. Informed consent was obtained.

Inclusion criteria:

· Medical faculty: Doctors comprising of Assistant Professors, Postgraduates (PG) and Senior residents and students (CRRIs)

· Paramedical faculty: Nurses comprising of Staff nurses, Nursing assistants and Junior staff nurses and students belonging to Allied Health Sciences course (AHS)

Exclusion criteria:

Health Care Workers with signs of skin infection or inflammation in the palmar and dorsal surfaces of the hand were excluded.

Sample size, sampling technique and statistical analyses:

Glove juice samples from 94 HCWs were collected. Statistical analysis of data was done using SPSS software Version 17. Significance of the questionnaire data was calculated using Fischer’s Exact test and Pearson’s Chi square test. Value of p < 0.05 was taken as significant

Method:

The hands of the HCWs were introduced into sterile gloves. 50 ml of phosphate buffer solution were instilled into the gloves of both the hands of each HCW. The gloves were tied with a rubber band each at the wrist. The hands were massaged for 60 seconds and 1 ml of the fluid was pipetted out from each of the gloves into two separate sterile test tubes.^[6][8] Knowledge about hand hygiene was assessed using WHO Hand Hygiene Questionnaire for Health Care Workers (revised August 2009) which includes multiple choice and “yes” or “no” questions.^[9] Questions 14 to 21 (one point for each of the 25 subdivisions) have been considered for scoring. Questions 12 and 13 have been excluded from scoring. A score of more than or equal to 19, 13 to 18 and less than or equal to 12 have been considered as having good, average and poor levels of knowledge respectively.

The collected samples were transported to Clinical Microbiology section of Central Laboratory Services for further processing. The Glove juice samples were inoculated onto Blood agar and Mac-Conkey agar plates which were appropriately labelled with study subject details. The plates were incubated at 37^oCelsius aerobically. The plate readings were done at the end of 24 hours and 48 hours and the findings were recorded. The plates which did not show any growth even after 48 hours were reported as sterile. Those plates which showed growth were further processed to identify the organisms by performing gram staining and appropriate biochemical reactions.

The bacterial isolates were subjected to Antibiotic Susceptibility Testing by Kirby bauer disc diffusion method as per Clinical Laboratory Standards Institute (CLSI) guidelines 2017. Screening for MRSA was performed by Kirby Bauer disc diffusion method using Cefoxitin (30µg) as the surrogate marker. Screening for Extended Spectrum Beta Lactamase (ESBL) among members of family Enterobacteriaceae was performed by disc diffusion using Cefotaxime (30µg) and Ceftazidime (30µg) according to the CLSI guidelines 2017 and confirmed by phenotypic confirmatory test in combination with Cefotaxime clavulanate. Appropriate quality control strains (E.coli ATCC 25922, Staphylococcus aureus ATCC 25923) were used. Vancomycin susceptibility was determined by performing Micro broth dilution method to determine the Minimum Inhibitory Concentration (MIC).^[10]

OBSERVATIONS AND RESULTS:

The study population comprised of 19 males (20.2%) and 75 females (79.8%), with the majority of the participants in the age group of 18-27 years (95.7%). A total of 43 nurses [comprising of staff nurses, junior staff nurses (JSN), nursing assistants (45.7%)], 26 CRRIs (27.6%), 17 paramedical students of Allied Health Sciences (AHS) (18.1%) and 8 medical faculty including Postgraduates (PG), Senior residents (SR) and Assistant Professors (AP) (8.5%) were included in the study. The majority of the samples were collected from Staff Nurses (34.0%) followed by CRRIs (27.7%) and AHS students (18.1%).

The various HCWs included in the study population were posted in different care areas of the hospital with the majority of the samples collected from the General Medicine ward (31 samples; 33.0%) and followed by Emergency room (26 samples; 27.7%) and OG ward (25 samples; 26.6%). 10 samples (10.6%) and 2 samples (2.1%) were collected from General Surgery and Intensive Care Units respectively.

Among the HCWs studied, 31 samples (33.0%) showed growth by the Glove Juice Technique. Among the paramedical staff, samples from 52.9% of AHS students, 42.9% of Junior Staff Nurses, 28.1% of staff nurses and 25% of Nursing Assistants had culture positivity. Among the organisms isolated, the most common was Staphylococcus aureus [16 of 94 (17.02%)] followed by Coagulase Negative Staphylococcus (CONS) [7 of 94 (7.4%)], followed by Escherichia coli which was isolated in 3 of 94 samples (3.2%). [Table 1]

TABLE 1: Organisms isolated from the hands of HCWs

Organisms	Staff Nurse (n=32)	Nursing Asst (n=4)	JSN (n=7)	Senior Resident (n=2)	Asst. Prof (n=1)	PG (n=5)	CRRI (n=26)	AHS (n=17)	Total (n=94)
MRSA	1(3.1%)	0	1(14.3%)	0	0	0	2(7.7%)	2(11.8%)	6(6.4%)
MSSA	2(6.2%)	1(25%)	1(14.3%)	0	0	1(20%)	2(7.7%)	3(17.6%)	10(10.6%)
CONS	4(12.5%)	0	0	0	0	0	2(7.7%)	1(5.9%)	7(7.4%)
Acinetobacter spp	0	0	1(14.3%)	0	0	0	0	0	1(1.1%)
Pseudomonas spp	0	0	0	0	0	0	0	1(5.9%)	1(1.1%)
E.coli	2(6.3%)	0	0	0	0	0	0	1(5.9%)	3(3.2%)
ASB (Bacillus subtilis)	0	0	0	0	0	2(40%)	0	1(5.9%)	3(3.2%)
*Total growth*	9(28.1%)	1(25%)	3(42.9%)	0	0	3(60%)	6(23.1%)	9(52.9%)	31(33.0%)
*Total No growth*	23(71.9%)	3(75%)	4(57.1%)	2(100%)	1(100%)	2(40%)	20(76.9%)	8(47.1%)	63(67.0%)

MSSA – Methicillin Sensitive Staphylococcus aureus, MRSA – Methicillin Resistant Staphylococcus aureus, CONS – Coagulase Negative Staphylococcus, ASB – Aerobic Spore Bearing bacilli

TABLE 2: Antibiotic susceptibility pattern of Gram Positive Cocci by Disc diffusion method

	P	Cx	Co	Cd	Cf	Of	E	G	Tet	Lz
MRSA (n=6)	0	0	2(33.3%)	0	1(16.7%)	1(16.7%)	0	2(33.3%)	0	6(100%)
MSSA (n=10)	7(70%)	10(100%)	3(30%)	6(60%)	8(80%)	6(60%)	6(60%)	10(100%)	3(30%)	7(70%)
CONS (n=7)	1(14.3%)	7(100%)	2(28.5%)	7(100%)	5(71.4%)	5(71.4%)	4(57.1%)	6(85.7%)	0	2(28.5%)

Co – Cotrimoxazole (1.25/23.75µg), P – Penicillin (10units), G – Gentamicin (10µg), E – Erythromycin (15µg), Cf – Ciprofloxacin (5µg), Of – Ofloxacin (5µg), Cx – Cefoxitin (30µg), Cd – Clindamycin (2µg), Tet – Tetracycline (30µg), Lz – Linezolid (30µg)^[11]

TABLE 3: Antibiotic susceptibility pattern of Gram Negative Bacilli

Organism

Amp

Cft

Cpm

Caz

Cac

PTZ

Imp

Mrp

Acinetobacter spp (n=1)

(100%)

Not done

(100%)

Not done

(100%)

Pseudomonas spp (n=1)

Not done

(100%)

Not done

(100%)

E.coli (n=3)

(66.7%)

(33.3%)

(66.7%)

(100%)

Co – Cotrimoxazole (1.25/23.75µg), A – Ampicillin (10µg), G – Gentamicin (10 µg), Ak – Amikacin (30µg), Cf – Ciprofloxacin (5µg), Cft – Cefotaxime (30µg), Cpm – Cefepime (30µg), Caz – Ceftazidime (30µg), Cac – Cefotaxime Clavulanic Acid (30/10µg), PTZ – Piperacillin Tazobactam (100/10µg), Imp – Imipenem (10µg), Mrp – Meropenem (10µg).^[11]

TABLE 4: Practices of Hand hygiene

	Questions	Yes	No
Q12	Did you receive formal training in hand hygiene in the last three years?	63(67%)	31(33%)
Q13	Do you routinely use alcohol- based handrub for hand hygiene?	71(75.5%)	23(24.5%)

TABLE 5: Comparison of Knowledge about Hand hygiene among HCWs

	Questions	Medical faculty	Paramedical faulty	P value
Q14	Main route of cross transmission? (a)	16 (47.1%)	33 (55%)	0.459
Q15	Frequent source of germs for HCAIs? (c)	7(20.6%)	33 (55%)	0.001*
Which of the following prevents transmission of germs to patients?
Q16a	Before touching a patient (Yes)	30(88.2%)	50 (83.3%)	0.521
Q16b	Immediately after risk of body fluid exposure (Yes)	28 (82.4%)	56 (93.3%)	0.161
Q16c	After exposure to the immediate surroundings of patient (No)	7 (20.6%)	8 (13.3%)	0.356
Q16d	Immediately before a clean /aseptic procedure (Yes)	32 (94.1%)	50 (83.3%)	0.2
Which of the following prevents transmission of germs to HCW?
Q17a	After touching a patient (Yes)	29 (85.3%)	51 (85%)	0.969
Q17b	Immediately after risk of body fluid exposure (Yes)	30(88.2%)	54(90%)	0.79
Q17c	Immediately before a clean /aseptic procedure (No)	6 (17.6%)	19 (31.7%)	0.139
Q17d	After exposure to the immediate surroundings of patient (Yes)	27 (79.4%)	51 (85%)	0.488
Which of the following statements of hand washing and hand rubbing are true?
Q18a	Hand rubbing is more rapid for hand cleansing than handwashing? (True)	30(88.2%)	48 (80%)	0.307
Q18b	Hand rubbing causes skin dryness more than handwashing? (False)	15 (44.1%)	26 (43.3%)	0.941
Q18c	Hand rubbing is more effective against germs than handwashing? (False)	15 (44.1%)	9 (15%)	0.002*
Q18d	Handwashing and hand rubbing are to be performed in sequence? (False)	6 (17.6%)	9 (15%)	0.736
Q19	Minimal time required for alcohol - based hand rub to kill germs? [20seconds]	17(50%)	31(51.7%)	0.877
Which type of hand hygiene method is required in the following situations?
Q20a	Before palpation of the abdomen (Rubbing)	20(58.8 %)	26(43.3%)	0.149
Q20b	Before giving an injection (Rubbing)	20(58.8 %)	20 (33.3%)	0.016*
Q20c	After emptying a bedpan (Washing)	31(91.2%)	47(78.3%)	0.111
Q20d	After removing examination gloves (Washing)	22(64.7%)	37(61.7%)	0.77
Q20e	After making a patient’s bed (Rubbing)	11(32.4%)	20(33.3%)	0.923
Q20f	After visible exposure to blood (Washing)	30(88.2%)	47(78.3%)	0.231
Which of the following should be avoided, as associated with increased likelihood of hand colonization with harmful germs?
Q21a	Wearing jewellery (Yes)	28(82.4%)	49(81.7%)	0.934
Q21b	Damaged skin (Yes)	32(94.1%)	47(78.3%)	0.045*
Q21c	Artificial fingernails (Yes)	33(97.1%)	54(90%)	0.416
Q21d	Regular use of hand cream (No)	16(47.1%)	24(40%)	0.506

TABLE 6: Knowledge score among HCWs

HCWs	Good	Average	Poor	Total	Chi square	P-value
Medical	7	25	2	34 (36.17%)	8.4728	0.014*
Paramedical	2	49	9	60 (63.82%)
Total	9 (9.57%)	74 (78.72%)	11 (11.7%)	94

DISCUSSION:

The hands of Health care workers are common vehicles for transmission of health care associated pathogens from patient to patient and within the health care setting. The importance of hand hygiene is not adequately recognised by the HCWs and non-compliance is a major problem. Multimodal Strategies such as staff education and motivation, the use of performance indicators, and support from hospital management are needed to improve hand hygiene compliance.^[11]

Microbiological methods to assess hand hygiene have been increasingly utilised to assess hand hygiene compliance. Various techniques include the glove juice, rinse, swab and impression method. The glove juice technique is a widely accepted technique used by the American Society for Testing Materials (ASTM) in the development and testing of antimicrobial hand wash products, such as surgical scrubs and health care personnel hand wash products.^[12][13][14] The glove juice requires expertise and it is time consuming. It is quantifiable and sampling of the webspaces between fingers is possible. It also includes germs on the back of hand even though they are less related to transmission risk.^[15]

The present study was done on Health Care Workers in various departments of our tertiary care hospital. Ninety four (94) HCWs were randomly chosen and the study population consisted of 20.2% males and 79.8% females in the mean age group of 18-27 years. The HCWs included in our study were Nurses comprising of staff nurses, junior staff nurses and nursing assistants [n=43, (45.7%)], medical students (CRRIs) [n=26, (27.6%)], Paramedical students such as students of Allied Health Sciences (AHS) [n= 17, (18.1%)] and Medical doctors [n=8, (8.5%)] comprising of Assistant Professors, Postgraduates and Senior Residents, working in various health care areas of the hospital. Other studies have been done using swab technique for finding the prevalence of carriage of Multidrug resistant bacteria on frequently contacted surfaces and hands of Health Care Workers on similar study population. In a study by Malini J et al., the proportion of HCWs with hand carriage of MRSA was 2%.^[16]

The hands of HCWs become progressively colonized with commensal flora as well as with potential pathogens during patient care.^[1] In the present study, sampling of hands of health care workers revealed the presence of growth of bacteria in 31 of 94 health care workers (33.0%). The most common bacterial isolate was Methicillin Sensitive Staphylococcus aureus [n=10, (10.6%)] followed by Coagulase negative Staphylococcus [n=7, (7.4%)], Methicillin Resistant Staphylococcus aureus [n=6, (6.4%)], Escherichia coli [n=3, (3.2%)], Acinetobacter spp [n=1, (1.1%)], Pseudomonas spp [n=1, (1.1%)] and Aerobic Spore Bearing bacilli [n=3, (3.2%)].

Morgen et al., assessed the role of environmental contamination in the transmission of multidrug resistant bacteria to the clothing of healthcare workers and reported an isolation of 32.9% of Acinetobacter baumannii followed by multidrug-resistant Pseudomonas aeruginosa (17.4%) and methicillin-resistant Staphylococcus aureus (13.8%).^[17] Sanderson et al., have reported recovery of coliform type organisms from the hands of nurses and patients in an Orthopaedic Hospital. These organisms were recovered from hands of nurses after touching patients' clothing, after bed making, handling clean or dirty linen, etc. ^[18]

The main reservoir of MRSA are the anterior nares, but other body sites are also frequently colonised such as the hands, skin, axillae, and intestinal tract.^[1] Increased risk of infection has been associated with nasal carriage of Staphylococcus aureus and a similar increased risk is expected for intestinal carriage.^[19] Healthcare workers transmit MRSA via their contaminated hands by acting as vectors apart from being the main source of MRSA transmission. The MRSA isolation rate in our study was 6.4% (n=6). No vancomycin resistance was detected. The six HCWs from whom MRSA was isolated from the hands, were reported to the Infection Control Team for further screening and also to screen for nasal carriage of MRSA.

Gebreyesus et al., reported the hand carriage of MRSA among health care workers as 6.2% while a nasal carriage was detected among 14.1% of the HCWs. No vancomycin resistance was reported in the MRSA isolated from hands.^[20] Visalachy et al., reported MRSA hand carriage in 2 of 157 samples (1.3%) taken from HCWs.^[6]

Coagulase negative Staphylococci (CONS) are a major cause of infections in immunocompromised and neonate patients (neonatal sepsis). Virulent CONS are acquired in the hospital environment. HCWs are likely to be an important cause for cross-contamination. Hence, good hand hygiene is important to reduce the transfer of CONS.^[21] Seng et al studied the prevalence of MR-CONS in the hospital environments and found that 70.1% (251/358 environmental samples) of hospital environmental regions were colonized by MR-CONS, of which the laboratory clothes were the most contaminated. All the isolates were vancomycin sensitive. The isolation rate of CONS from the hands of HCWs in our study is 7.4% (n=7). No MR-CONS was isolated in our study.^[22]

The WHO Hand Hygiene Knowledge Questionnaire for Health - Care Workers (revised August 2009) was given to the HCWs to assess their knowledge regarding hand hygiene practices. In our study, 63 of 94 (67%) received formal training in hand hygiene in the last 3 years and 71 of 94 (75.5%) routinely used alcohol – based handrub [Table 4]. In a study conducted by Harpreet Kaur et al., 7.5% of the staff nurses had washed their hands both before and after administration of medications, while 11.5% of the staff nurses had not performed hand hygiene practices.^[23]

About 49 HCWs (52.1%) in our study, were aware that the main route of cross transmission in a health-care facility is through unclean hands of health care workers. Less than half the study population [n=40 (42.6%)] was aware that the source of germs responsible for the spread of nosocomial infections was present within/on the patient. About 48 HCWs (51.1%) had good knowledge about the minimal time required by alcohol – based handrubs to destroy germs in the hands. [Table 5].

In a study conducted by Thakker et al., to assess the knowledge about hand hygiene, less than 50% undergraduate students (medical 46.4%, dental 48.6%, and nursing 37.5%) were aware that unhygienic hands of healthcare workers were the main route of transmission of potential harmful germs and less than 35% students (medical 23.1%, dental 36.4%, and nursing 25%) were aware that the main source of germs in nosocomial infections was from patients. Only a small number of undergraduate students knew that 20 seconds is the minimum time required for effective alcohol-based hand rub as per the WHO guideline.^[24]

Veena Maheshwari et al., reported that 45% of residents and 27% of nurses knew that the most frequent source of germs responsible for HCAI’s were the germs already present on or within the patient, with residents having significantly better knowledge in this aspect. Significant knowledge difference of 37 (46%) and 28 (35%) regarding effectiveness of alcoholic hand-rubs being more effective against germs than hand washing was observed. With regards to what needs to be avoided for increased colonization, a significant difference of knowledge was observed regarding use of jewellery i.e., 62 (77.5%) against 77 (96.3%) and artificial nails, 64 (80%) against 72 (90%) amongst residents and nurses respectively.^[9]

In our study, 63 out of 94 (67%) of the HCWs received formal training in hand hygiene. 75.5% of HCWs (71 HCWs) routinely used alcohol-based hand-rub in maintaining hand hygiene. Significant knowledge difference of 7 (20.6%) among medical staff and 33 (55%) among paramedical staff regarding the most frequent source of germs responsible for health care-associated infections was observed. With regards to hand rubbing being more effective than hand washing, significant knowledge difference of 15 (44.1%) and 9 (15%) were observed among medical and paramedical staff respectively. In situations where hand rubbing is considered essential before administering an injection to a patient, significant knowledge difference of 20 (58.8%) and 20 (33.3%) were found among medical and paramedical staff. 32 (94.1%) and 47 (78.3%) of medical and paramedical staff respectively, agreed that damaged skin in the hands of HCWs is associated with increased likelihood of hand colonization with germs for which a significant difference in knowledge was also observed. [Table 5]

In a study conducted by Cherian et al., to assess the knowledge among nurses regarding infection control practices, among the 60 nurses surveyed, 23.3% exhibited adequate knowledge and the rest 78% did not have adequate knowledge. ^[25] Our study assessed the overall knowledge regarding hand hygiene practices and it was found that good level of knowledge was found among 9 HCWs, out of which 7 were medical staff (77.77%). 74 HCWs had an average score of which 49 were paramedical staff and out of 11 HCWs with a poor score, 9 HCWs were paramedical staff. There is significant difference in the knowledge between medical and paramedical staff. The p-value was 0.014. [Table 6].

CONCLUSION:

Staphylococcus aureus was the most commonly isolated organism from the hands of Health Care Workers. The predominant multidrug resistant organism to be isolated was Methicillin Resistant Staphylococcus aureus (MRSA) which was noted in 6.4% of the HCWs. Gram Negative bacilli were also isolated from the hands of HCWs namely Escherichia coli, Pseudomonas spp and Acinetobacter spp. No multidrug resistance was observed among the gram negative bacilli. The WHO Hand Hygiene Knowledge Questionnaire for Health - Care Workers (revised August 2009) revealed significant knowledge difference among the various categories of HCWs with respect to hand hygiene practices. The results of this study could help us to strengthen Infection Control surveillance activities.

ACKNOWLEDGEMENTS:

This research was approved by ICMR (STS 2017-02616).

REFERENCES:

1. WHO Guidelines on Hand Hygiene in Health Care: First Global Patient Safety Challenge Clean Care Is Safer Care. Geneva: World Health Organization; 2009. 21, The WHO Multimodal Hand Hygiene Improvement Strategy.

2. Ewans TM, Ortiz CR, LaForce FM. Prevention and control of nosocomial infection in the intensive careunit. In: Irwin RS, Cerra FB, Rippe JM, editors. Intensive Care Medicine. 4th ed. New York: LippincotRavan;1999.p. 1074–80.

3. Lolita S.M. D’Souza., Malarvizhi M., Joicy John. Prevention of Nosocomial infection in NICU. Asian J. Nur. Edu. and Research 4(2): April- June 2014; Page 255-257.

4. Siegel JD, Rhinehart E, Jackson M, Chiarello L, and the Healthcare Infection Control Practices Advisory Committee, 2007 Guideline for Isolation Precautions: Preventing Transmission of Infectious Agents in Healthcare Settings.

5. Sreeja. M.K, Gowrishankar N.L, Adisha. S, Divya. K.C. Antibiotic Resistance-Reasons and the Most Common Resistant Pathogens – A Review. Research J. Pharm. and Tech. 2017; 10(6): 1886-1890.

6. Visalachy S, Palraj KK, Kopula SS, Sekar U. Carriage of Multidrug Resistant Bacteria on Frequently Contacted Surfaces and Hands of Health Care Workers. Journal of Clinical and Diagnostic Research : JCDR. 2016;10(5):DC18-DC20. doi:10.7860/JCDR/2016/19692.7772.

7. Shanthi M, Uma S. Antimicrobial susceptibility pattern of methicillin resistant Staphylococcus aureus at Sriramachandra Medical Centre. Sri Ramachandra Journal of medicine. 2009;2(2):1–4.

8. Adherence M.H.H., 2009. Overcoming the challenges. Ohio : The Joint Commission.

9. Maheshwari V, Kaore NCM, Ramnani VK, Gupta SK, Borle A, Kaushal R. A Study to Assess Knowledge and Attitude Regarding Hand Hygiene amongst Residents and Nursing Staff in a Tertiary Health Care Setting of Bhopal City. Journal of Clinical and Diagnostic Research : JCDR. 2014;8(8):DC04-DC07. doi:10.7860/JCDR/2014/8510.4696.

10. Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. 27^thed.CLSI supplement M100 (ISBN 1-56238-804-5 [Print];ISBN 1-56238-805-3 [Electronic]). Clinical and Laboratory Standards Institute, 950 West Valley Road, Suite 2500,Wayne, Pennsylvania 19087 USA,2017.

11. Infection control as a major World Health Organization priority for developing countries Pittet, D. et al. Journal of Hospital Infection , Volume 68 , Issue 4 , 285 – 292.

12. Mahl MC. New method for determination of efficacy of health care personnel hand wash products. Journal of Clinical Microbiology. 1989;27(10):2295-2299.

13. American Society for Testing and Materials International. “ASTM E 1174-06: Standard test method for evaluation of the effectiveness of healthcare personnel handwash formulations”. West Conshohocken, PA: American Society for Testing and Materials; 2006

14. Kampf G, Ostermeyer C, Heeg P, Paulson D. Evaluation of Two Methods of Determining the Efficacies of Two Alcohol-Based Hand Rubs for Surgical Hand Antisepsis. Applied and Environmental Microbiology. 2006;72(6):3856-3861. doi:10.1128/ AEM.02746-05.

15. Kaltenthaler EC, Pinfold JV. Microbiological methods for assessing handwashing practice in hygiene behaviour studies. J Trop Med Hyg. 1995;98:101–106.

16. Malini J, Shruti AH, Padmavathy M, Umapathy BL, Navaneeth BV, Keerthi Mannan J, Girish MS. Methicillin-resistant Staphylococcus aureus carriage among the health care workers in a tertiary care hospital. JCDR. 2012;6(5):791–3.

17. Morgan DJ, Rogawski E, Thom KA, et al. Transfer of multidrug-resistant bacteria to healthcare workers’ gloves and gowns after patient contact increases with environmental contamination. Critical Care Medicine. 2012;40(4):1045-1051. 19.

18. Sanderson P.J., Weissler S. Recovery of coliforms from the hands of nurses and patients: activities leading to contamination. Journal of Hospital Infection, 21 (2) 1992., pp. 85-93.

19. Dulon M, Peters C, Schablon A, Nienhaus A. MRSA carriage among healthcare workers in non-outbreak settings in Europe and the United States: a systematic review. BMC Infectious Diseases. 2014;14:363. doi:10.1186/1471-2334-14-363.

20. Gebreyesus A, Gebre-Selassie S, Mihert A. Nasal and hand carriage rate of methicillin resistant Staphylococcus aureus (MRSA) among health care workers in mekelle hospital, north ethiopia” Ethiop Med J. 2103;51(1):41–7.

21. Hira V, Sluijter M, Goessens WHF, et al. Coagulase-Negative Staphylococcal Skin Carriage among Neonatal Intensive Care Unit Personnel: from Population to Infection. Journal of Clinical Microbiology. 2010;48(11):3876-3881. doi:10.1128/JCM.00967-10.

22. Seng R, Kitti T, Thummeepak R, et al. Biofilm formation of methicillin-resistant coagulase negative staphylococci (MR-CoNS) isolated from community and hospital environments. De Lencastre H, ed. PLoS ONE. 2017;12(8):e0184172. doi:10.1371/ journal.pone.0184172.

23. Harpreet Kaur, Jasbir Kaur. Hand Hygiene Practices among Staff Nurses during Drug Administration at Selected Tertiary Health Care Centre of Ludhiana, Punjab. Asian J. Nur. Edu. and Research 5(2): April-June 2015; Page199-201.

24. Thakker VS, Jadhav PR. Knowledge of hand hygiene in undergraduate medical, dental, and nursing students: A cross-sectional survey. Journal of Family Medicine and Primary Care. 2015;4(4):582-586. doi:10.4103/2249-4863.174298

25. Vigy Elizebth Cherian, Rose Rajesh. A Study to Assess The Knowledge and Practice among Nurse on Infection Control Measures in Pediatric Unit at Pondicherry Institute of Medical Science, Puducherry. Int. J. of Advances in Nur. Management. 2018; 6(3): 215-219.

Received on 13.03.2020 Modified on 08.05.2020

Research J. Pharm. and Tech. 2021; 14(2):650-656.

DOI: 10.5958/0974-360X.2021.00116.5