African Journal of Microbiology Research Vol. 4(22), pp. 2343-2349, 18 November, 2010 Available online http://www.academicjournals.org/ajmr ISSN 1996-0808 2010 Academic Journals Full Length Research Paper Microbial flora on the hands of healthcare workers Fahriye Eksi*, Aysen Bayram, Murat Mehli, Sadik Akgun and Iclal Balci
Gaziantep University, Faculty of Medicine, Department of Medical Microbiology, Universite Bulvari, Gaziantep, 27310,
The aims of this study were to study the process of microbial contamination of healthcare workers’ (HCWs) hands during routine patient care and simultaneously to evaluate the state of antibiotic susceptibility of microorganisms isolated from the hands of HCWs. Samples were collected from the hands of 154 HCWs working at Gaziantep University Hospital. A standard bag broth technique was employed. In addition to conventional methods, VITEK 2 automated system and API ID 32C kits were used for identification of the isolated microorganisms. Antimicrobial susceptibility of bacterial agents was performed by disc diffusion method. For antifungal susceptibility, ATB Fungus 2 kit was used. Of 154 specimens, 148 (96.1%) showed microbial growth and 160 microorganisms were isolated as single or multiple members of the resident flora. Transient flora including one or more microorganisms (n = 47) were recovered from the hands of 39 (25.3%) HCWs. All gram-positive bacteria were detected to be sensitive to vancomycin, teicoplanin and linezolid, however 30.1% of the coagulase-negative staphylococci and 40% of Staphylococcus aureus isolates were resistant to methicillin. Multiple drug resistance was determined in Acinetobacter and Pseudomonas isolates. It can be concluded that transient flora members isolated from hands of HCWs can be causative agents of serious nosocomial infections due to their high and multiple antimicrobial resistance patterns. Key words: Healthcare workers, resident flora, transient flora, antimicrobial susceptibility.
Hand hygiene remains the major preventive measure
and Bacillus spp. were considered to be elements of
against nosocomial infections. In 2002, Centers for
transient flora and, therefore, potentially pathogenic
Disease Control and Prevention (CDC) revised the
microorganisms (Kampf and Kramer, 2004).
recommendations for hand hygiene to include the use of
Investigators have documented that the number of
alcohol-based products for standard hand hygiene
transient and resident flora varies considerably from
(Larson et al., 2007; Boyce and Pittet, 2002).
person to person and is relatively constant (Hugonnet
Three principal types of skin flora have been described.
and Pittet, 2000; Boyce and Pittet, 2002). A higher pre-
valence of antibiotic-resistant organisms on the hands of
distinguished in 1938. In addition, the infectious flora was
patient-care staff versus non-patient-care staff and/or
described with species such as Staphylococcus aureus
outpatients has been reported (Aiello et al., 2003).
and beta-hemolytic streptococci which were frequently
The purposes of this study were to describe the types
isolated from abscesses, whitlows, paronychia, or
and antimicrobial susceptibility patterns of hand flora
infected eczema. Resident flora consists of strains, such
among healthcare workers (HCWs) working in various
as coagulase-negative staphylococci and diphtheroids.
clinics and to examine whether job title and ward location
of HCWs can affect the growth of hand flora
staphylococci, Corynebacterium spp., Micrococcus spp.
MATERIALS AND METHODS *Corresponding
email@example.com. Tel: 90 342 3606060 77523. Fax: 90
This prospective study was conducted at the microbiology
laboratory of a University Teaching Hospital in Gaziantep, Turkey. The Hospital’s Medical Ethics Committee approved the trial. The
study hospital is occupied with 800 beds. Samples were collected
glabrata n = 1 and Candida guillermondii n = 1), 9 (5.8%)
from the hands of 154 (79 female and 75 male) HCWs during a
Acinetobacter spp. (Acinetobacter lwoffii n = 7;
three-month period from January to March 2008. HCWs were
Acinetobacter baumannii n = 2), 9 (5.8%) Enterococcus
classified according to their job titles and ward location. There were 55 (35.7%) nurses, 33 (21.4%) permanent physicians, 11 (7.1%)
spp. (Enterococcus faecalis n = 5; Enterococcus faecium
medical students, 25 (16.2%) nursing assistants and 30 (19.5%)
n = 4), 5 (3.2%) S. aureus, 4 (2.6%) Pseudomonas spp.
cleaning personnel. Forty-eight HCWs were employed at various
(P. aeruginosa n = 2; Pseudomonas stutzeri n = 2), 4
surgical clinics, 32 at internal medicine ICU, 23 at internal medicine
(2.6%) Enterobacter aerogenes, 3 (1.9%) Serratia
and cardiology clinics, 21 at pediatrics and newborn clinics, 11 at
marcescens and 2 (1.3%) Streptococcus pneumoniae.
oncology division of internal medicine, 10 at surgical ICU, and 9 at
Distribution of the transient flora members according to
Both hands of all participants were washed in 50 ml of brain-
heart infusion broth in a sterile plastic bag and kneaded for 30 s by
No statistically significant difference was observed
the standard bag broth technique (Larson, 1985; Larson et al.,
according to job titles among number of transient-flora-
1980). After removal of the hands from the bag, the broth was
member microorganisms isolated from HCWs’ hands (p =
transferred to a sterile container. An inoculum of 0.1 ml from each
0.312); however, a statistically significant difference was
sample was plated within 1 h or after storage at 4°C for up to 5 h
recorded according to ward location (p = 0.038). No
onto Columbia sheep blood agar (5%), Eosin-methylene blue agar, Sabouraud’s agar with chloramphenicol and gentamicin and bile
statistical difference was determined between number of
aesculin agar. All culture media were incubated at 37°C and
transient-flora-member microorganisms isolated from
observed daily for growth over 48 h for bacteria and up to 7 days for
hands of HCWs working in intensive care unit and non
yeast. Microorganisms grown on cultures were identified with
intensive care unit areas (p = 0.391). Moreover, there
conventional methods, VITEK 2 (BioMerieux, USA) automated
was also no significant difference between oncology and
system and API ID 32C (BioMerieux, France) kits as needed.
intensive care clinics (p = 0.071). However, a statistically
staphylococci (CNS) and transient bacterial flora members were
significant difference (p = 0.000) was recorded among
performed by disc diffusion method according to Clinical and
HCWs who worked in other clinics except intensive care
Laboratory Standards Institute’s (CLSI) recommendations (Clinical
unit and oncology clinics. Distribution of HCWs according
and Laboratory Standards Institute, 2005). Quality control was
to ward location and growth of transient flora is shown in
performed with S. aureus ATCC 25923 and Pseudomonas aeruginosa ATCC 27853 strains; inhibition zone diameters were in the ranges stipulated by the CLSI (Clinical and Laboratory
Growth of coagulase-negative staphylococci (CNS)
Standards Institute, 2005). We determined the antibiotic sensitivity
occurred on hands of 143 out of 154 HCWs. Among 143
pattern for coagulase-negative staphylococci because these
CNS, 43 were (30.1%) methicillin resistant coagulase-
organisms were present in almost all subjects as part of the
negative staphylococci (MRCNS), 100 were (69.9%)
staphylococci (MSCNS). Antibiotic susceptibilities of
staphylococcal strains, cefoxitin (30 µg) and oxacillin discs (1 µg) were used. CNS isolates that were clindamycin-susceptible (CL-S)
isolated CNS strains are shown in Table 3. In our study,
and erythromycin-resistant (ER-R) were tested for inducible
all CNS were sensitive to vancomycin and linezolid and
clindamycin resistance (ICR) by the D-test as described by CLSI
96% of MSCNS strains were resistant to penicillin. It was
(Clinical and Laboratory Standards Institute, 2005).
found out that 41 (95.3%) of MRCNS strains were
antifungal susceptibility, ATB Fungus 2 (BioMerieux- France) kit
erythromycin-resistant, and 16 (37.2%) of them showed
was used. Candida parapsilosis ATCC 22019 was used as the quality control strain.
constitutive clindamycin resistance. In 8 (18.6%) MRCNS
Results were analyzed using Chi-square test. Statistical analysis
strain ICR was detected. It was found out that 68% of
were performed with Epi Info (version 3.4.3), and values of p < 0.05
MSCNS strains were erythromycin-resistant. Constitutive
were considered to indicate statistical significance.
clindamycin resistance was seen in 13% of MSCNS
strains and ICR was detected in 11% cases (Table 3).
Antibiotic resistance among isolated gram positive and
gram negative bacteria are shown in Tables 4 and 5,
respectively. All gram positive bacteria were sensitive to
Specimens were collected from 154 HCWs and 148
vancomycin, teicoplanin and linezolid. Two of five (40%)
(96.1%) of them showed microbial growth. One hundred
isolated S. aureus strains were detected to be MRSA. Two
and sixty microorganisms from 148 HCWs were isolated
strains of five (40%) isolated E. faecalis were resistant to
as single or multiple members of the resident flora. Of
quinupristin/dalfopristine; besides, all strains of E.
160 isolates, 143 (89.4%) were CNS and 10 (6.3%) were
faecalis and 3 E. faecium strains out of 4 (75%) were
Corynebacterium spp. and 7 (4.4%) were Bacillus spp.
detected to be resistant to co-trimoxazole. All S. aureus
No growth was observed in samples of 6 (3.9%) HCWs.
strains were resistant to penicillin and all S. pneumoniae
Transient flora including one or more microorganisms
strains were resistant to erythromycin, clindamycin,
was recovered from the hands of 39 (25.3%) (21 male,
ampicillin and gentamicin. All strains of Serratia
18 female) HCWs. Members of the transient flora (n = 47;
marcescens were detected to be resistant to ampicillin,
30.5%) isolated from the hands of 154 HCWs were as
follows; 11 (7.1%) Candida spp. (C. parapsilosis n = 4,
Besides, Acinetobacter spp. and Pseudomonas spp.
Candida tropicalis n = 3, Candida albicans n = 2, Candida Table 1. Transient bacterial flora of HCWs according to job title. Permanent physicians Cleaning students assistant Microorganism personnel n = 30 (100%)
Table 2. Distribution of HCWs according to ward location and growth of transient flora. Pediatrics Internal Coronary Surgical Pediatric medicine + ICU+ Internal Surgical ICU oncology oncology Microorganism Cardiology medicine ICU
Eleven species of Candida were isolated from 154
and Kramer, 2004). In the present study, 143 CNS, 10
HCWs’ hands. Antifungal susceptibilities of Candida spp.
Corynebacterium spp. and 7 Bacillus spp. were isolated
from 154 HCWs’ specimens. Thirty-three (30.1%) of 143
CNS were MRCNS while 100 (69.9%) were MSCNS. The
incidence of oxacillin resistance among isolates of S. DISCUSSION epidermidis was up to 64.3% (Lee et al., 1994) and was
higher in health care workers who have direct contact
The resident flora consists of permanent inhabitants of
with patients than in those who do not (Slight et al.,
the skin. They are found mainly on the surface of the skin
1987). One study reported that methicillin-resistant CNS
and under the superficial cells of the stratum corneum.
was significantly higher among nurses with closest and
These bacteria are not regarded as pathogens on intact
most frequent patient contact (Klingenberg et al., 2001).
skin but may cause infections in sterile body cavities, in
In previous studies, rates of oxacillin resistance among
the eyes, or on non-intact skin. The dominant species is
CNS from nurses’ hands ranged from 26 - 79% (Horn et
Staphylococcus epidermidis, which is normally found on
al., 1988; Cook et al., 2007). CNS, such as S.
almost every person's hand (Kampf and Kramer, 2004;
epidermidis, mainly causes catheter-associated primary
Lee et al., 1994). Other regular residents are
bloodstream infections. In ICUs, approximately one-third
Staphylococcus hominis and other CNS, followed by
of all blood culture isolates from patients with nosocomial
bloodstream infections were found to be CNS (Kampf
corynebacteria, dermabacteria, and micrococci (Kampf
Table 3. Antibiotic susceptibilities of MRCNS and MSCNS strains. MRCNS (n = 43) MSCNS (n = 100) Antibiotics Resistant n (%) Sensitive n (%) Resistant n (%) Sensitive n (%)
MRCNS: Methicillin resistant coagulase-negative staphylococci; MSCNS: Methicillin susceptibility coagulase-negative staphylococci.
Table 4. Antibiotic resistance of gram positive transient flora members. S. aureus (n = 5) E. faecalis (n = 5) E. faecium (n = 4) S. pneumonia (n = 2) Antibiotics Resistance n (%) Resistance n (%) Resistance n (%) Resistance n (%)
In the current study, all CNS were sensitive to
streptogramin B (MLSB) family of antibiotics is commonly
vancomycin and linezolid and 96% of MSCNS strains
used in the treatment of staphylococcal infections
were resistant to penicillin. The macrolide-lincosamide-
(Fiebelkorn et al., 2003). However, this widespread use
Table 5. Antibiotic resistance of gram negative transient flora members. Acinetobacter spp. Pseudomonas spp. Serratia marcescens Enterobacter Antibiotics aerogenes (n = 4) Resistance n (%) Resistance n (%) Resistance n (%) Resistance n (%) Table 6. Antifungal susceptibilities of Candida spp.
Flucytosine Amphotericin B Fluconazole Itraconazole Candida spp.
S: susceptible; I: intermediate; R: resistant.
has led to an increase in the number of staphylococci
isolated from hands of nurses and 3 strains of
strains being resistant to MLSB antibiotics (Lim et al.,
Pseudomonas out of 4 were isolated from hands of per-
2002). Consequently, ICR was investigated beside
manent physicians respectively. No statistical difference
constitutive resistance for clindamycin in our study. It was
found out that 41 (95.3%) of MRCNS strains were
organisms isolated from HCWs’ hands was observed in
erythromycin-resistant, and 16 (37.2%) of them showed
job title (p = 0.312) but statistically significant difference
constitutive clindamycin resistance. In 8 (18.6%) of
was noticed in ward location (p = 0.038). Some clinical
MRCNS strains ICR was detected. It was found out that
situations are associated with a higher bacterial load on
68% of MSCNS strains were erythromycin-resistant.
the hands of health care workers: direct contact with
Constitutive clindamycin resistance was seen in 13% of
patients, respiratory tract care, contact with body fluids,
MSCNS strains and ICR was detected in 11% cases. The
and after being interrupted while caring for a patient
transient skin flora consists of bacteria, fungi, and viruses
(Pittet et al., 1999). Due to immunosuppressive patient
that may be found on the skin only at times. They usually
population in oncology clinic, it was considered that
do not multiply on the skin, but they survive and
various microorganisms could be more frequently
occasionally multiply and cause disease (Kampf and
colonized in skin flora of these patients and HCWs
Kramer, 2004). In our study, transient flora was
working in this clinic can be easily contaminated with
recovered from hands of 39 (25.3%) HCWs. When
these microorganisms. Since 2006, HCWs at this hospital
evaluated in terms of job titles, maximum yeast growth
have been advised to use non-medicated soap and dry
occurred in nurses, additionally 3 S. marcescens strains
paper towels for hand washing and to use an alcohol-
based disinfectant as hand hygiene procedure during
Most reports of cross-transmission of specific gram-
routine patient care. We think that health care staff
negative bacteria come from critical-care areas, such as
should be controlled periodically for the proper and
neonatal ICUs and burn units (Kampf and Kramer, 2004).
Enterobacter agglomerans (n = 5) was the frequently
In the present study, transient-flora-member gram
detected gram negative bacteria species in the study of
positive bacteria isolated from hands of 154 HCWs were
Aiello et al. (2003). In this study, multi-drug resistance
Enterococcus spp. in 9 (5.8%), S. aureus in 5 (3.2%),
was observed in strains of Acinetobacter spp. and
Streptococcus pneumoniae in 2 (1.3%). Aiello et al.
Pseudomonas spp. but all strainsof S. marcescens were
(2003) reported in their study that there were 12 different
resistant to ampicillin, ampicillin/sulbactam, cefazolin and
species of gram negative bacteria and 11 different
species of CNS on the nurse hand samples (n = 119);
Yeasts (n = 11) isolated from HCWs' hands were
and there were four nurses with S. aureus on their hands.
identified as follows: 4 C. parapsilosis, 3 C. tropicalis, 2
Enterococcus species were the most frequently isolated
C. albicans and a single strain of C. glabrata as well as
gram positive bacteria species in our study. Strains of
C. guillermondii strains. In another study, Candida
enterococci causing nosocomial infections have occa-
carriage was found in 34.1% of 214 HCWs (Yıldırım et
sionally been found on the hands of medical personnel
al., 2007) and the most frequently yielded isolates were
and have frequently been isolated from environmental
C. parapsilosis (38.4%), C. tropicalis (26.0%) and C.
sources in hospitals and nursing homes. The importance
albicans (23.3%). C. parapsilosis is an important
of these findings is difficult to assess, because the
pathogen as it implies the possibility of nosocomial trans-
mission of fungaemia by the hands of HCWs (Levin et al.,
contaminated by stool or urine from infected patients
1998). In a long-term-care facility, 41% of 42 health care
(Moellering, 2000). According to literature, vancomycin-
workers were found to have Candida spp. on their hands
resistant enterococcus can be found on the hands of up
(Mody et al., 2003). Lupetti et al. (2002) concluded that
to 41% of health care workers (Hayden, 2000).
horizontal transmission of C. parapsilosis occurred
In our study, out of 9 isolated Enterococcus species, 5
through direct interaction between nurses and the
were E. faecalis and 4 were E. faecium. Being a
patients. With respect to antifungal susceptibility, it was
satisfactory result, no vancomycin resistance was
found out that C. parapsilosis and C. albicans are highly
susceptible to the studied antifungals. In the present
In our study, two of 5 S. aureus strains (40%) were
study the susceptibility of C. tropicalis to antifungals
determined to be MRSA. Colonization of HCWs’ hands
except itraconazole was a satisfactory result for the
with S. aureus ranged between 10.5 and 78.3%. MRSA
was isolated from the hands of up to 16.9% of HCWs.
In conclusion, transient flora members were isolated
Hand carriage of pathogens such as S. aureus, MRSA, or
mostly from HCWs working in oncology clinic. Bacterial
S. epidermidis has repeatedly been associated with
contamination of HCWs’ hands was likely to occur due to
different types of nosocomial infections (Kampf and
immunosuppressive patient population in oncology clinic.
Kramer, 2004). A study by Cespedes et al. (2002)
Acinetobacter spp. and Pseudomonas spp. strains were
reported that significantly more medical personnel
multi-drug resistant. The role of the hand flora of HCWs
compared with non-medical hospital personnel were
in the development of nosocomial infections is significant.
colonized with antibiotic-resistant S. aureus. All gram
These results, suggest that transient flora members
positive bacteria were found to be sensitive to
isolated from hands of HCWs can be causative agents of
vancomycin, teicoplanin and linezolid and most were
serious nosocomial infections due to their high and
detected to be sensitive to quinupristin/dalfopristine.
multiple antimicrobial resistance patterns.
Moreover, all strains of E. faecalis and three of four E. faecium strains were found to be resistant to
cotrimoxazole. All strains of S. aureus were found to be
resistant to penicillin; however, all strains of S.
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