EPIDEMIOLOGY ROUND

Year : 2014 | Volume : 59 | Issue : 2 | Page : 143--150

The clinical spectrum and antibiotic sensitivity patterns of
staphylococcal pyodermas in the community and hospital

Shireen Furtado
1
, Ramesh M Bhat
1
, B Rekha
2
, D Sukumar
1
, Ganesh H Kamath
1
, Jacintha
Martis
1
, B Nandakishore
1
,
1
Department of Dermatology, Venereology and Leprology, Fr. Muller Medical College, Mangalore,
Karnataka, India
2
Department of Microbiology, Fr. Muller Medical College, Mangalore, Karnataka, India
Correspondence Address:
Shireen Furtado
Department of Dermatology, Venereology and Leprology, Fr. Muller Medical College, Mangalore - 575
002, Karnataka
India

Abstract

Context: The uncontrolled use of antibiotics has resulted in a relentless spread of
multiresistant strains of Staphylococcus aureus. There are studies conducted in medical
colleges in Chandigarh, Chennai, Mumbai and Vellore comparing pyodermas in the
community and hospital setting based on clinical and bacteriological
parameters. Aims: This study, conducted over 1 years from March 2009 to August
2010, aimed at analyzing the clinical spectrum and antibiotic sensitivity pattern of
community and hospital-associated (HA) staphylococcal pyoderma. It also assessed the
prevalence of methicillin-resistant S. aureus (MRSA) in the community and hospital
cohort settings. Subjects and Methods: The study comprised of 200 cases of
staphylococcal pyodermas, derived from the community (150 cases) and hospital (50
cases). Patients were evaluated based on their clinical presentation; antibiotic
susceptibility was tested using the Kirby-Bauer disk diffusion method. Statistical
Analysis Used: Statistical significance between individual attributes between the
community and HA staphylococcal pyoderma groups was analyzed using Chi-square test
and mean differences using studentSQs t-test. Results: Factors associated with
community-associated (CA) pyodermas were young age (P = 0.0021), primary
pyodermas, and involvement of extremities, while those with HA pyodermas were middle
age, secondary pyodermas, and significantly increased body surface involvement (P =
0.041). Incidence of CA-MRSA was 11.3%, while that of HA-MRSA was
18%. Conclusions: A high level of resistance to first-line drugs such as penicillin,
ciprofloxacin and cotrimoxazole was observed, more so in the hospital strain than in the
community strain. S. aureus demonstrated good susceptibility to cephalosporins. Though
the two strains of MRSA differed clinically, they showed 100% sensitivity to vancomycin
and linezolid.

How to cite this article:
Furtado S, Bhat RM, Rekha B, Sukumar D, Kamath GH, Martis J, Nandakishore B. The clinical
spectrum and antibiotic sensitivity patterns of staphylococcal pyodermas in the community and
hospital.Indian J Dermatol 2014;59:143-150

How to cite this URL:
Furtado S, Bhat RM, Rekha B, Sukumar D, Kamath GH, Martis J, Nandakishore B. The clinical
spectrum and antibiotic sensitivity patterns of staphylococcal pyodermas in the community and
hospital. Indian J Dermatol [serial online] 2014 [cited 2014 May 22 ];59:143-150
Available from: http://www.e-ijd.org/text.asp?2014/59/2/143/127674

Full Text
Introduction


There are numerous interacting causes of infection in any body tissue, many of which
also aid in the persistence of the infection. Various organisms have been isolated and
incriminated in pyoderma. Staphylococcus aureus and -hemolytic streptococcus are the
most common etiological agents. [1],[2] Pyoderma, commonly caused by S. aureus,
accounts for up to 17% of clinical visits in dermatological practice. [3] S. aureus often
colonizes hospitalized as well as healthy people without any sign of infection. The
preferential sites of colonization are anterior nares, perineum, axilla, and web spaces
and these sites may act as reservoirs. [4]

Most strains of S. aureus are encountered in patients and carriers outside hospitals, and
around 90% of those found in hospitals are now resistant to penicillin. This resistance is
due to the ability of the microorganism to produce penicillinase, a -lactamase. These
organisms also show cross-resistance to other penicillins such as ampicillin, amoxicillin,
carbenicillin, azlocillin, and piperacillin. [5]

Methicillin-resistant S. aureus (MRSA) is notorious in causing serious infection among
hospitalized patients, with outbreaks of such infections posing a major problem in
therapy and infection control. [6],[7],[8] Outbreak reports of MRSA are available from
the Veteran Affairs Medical Center of Long Beach, CA, USA; and hospitals in Australia,
France, Saudi Arabia, South Africa, and the UK. [6],[7],[8],[9],[10] Hospitals in these
countries report MRSA infections between 20% and 65% in domiciliary and intensive
care settings. [6],[7],[8] A gradual reduction in MRSA infection acquisition rate was
noted over a 12-month period following daily clinical laboratory surveillance, monthly
prospective microbiology surveys of high-risk inpatients, and the recognition of
previously infected patients. [7] Unlike nosocomial or hospital-associated MRSA (HA-
MRSA) isolates, community-associated MRSA (CA-MRSA) isolates from patients without
known MRSA risk factors, patients with open wounds, visitors or relatives of infected
patients, healthcare personnel, IV drug abusers, immunodeficient patients, are generally
multidrug susceptible. Multidrug resistance may develop rapidly with indiscriminate and
inappropriate antibiotic use. [9]

Data from national nosocomial infection surveillance study from centre of disease control
and prevention show that S. aureus infection had increased to 54.5% in 2000. [10] In
India, MRSA prevalence overall increased from 12% in 1992 to 80.83% in 1997. [11]
Owing to the epidemiological and genomic differences including antibiotic resistance
between HA-MRSA and CA-MRSA infecting organisms, strategies to prevent and treat
these infections understandably differ. [12]

This study compares the clinical and antibiotic spectra of staphylococcal pyodermas in
HA-MRSA and CA-MRSA, derives the prevalence of the infection in study cohorts
presenting to an out-patient and in-patient facility in a medical college. It presents the
differences inpatient demographics, clinical features, and antibiotic susceptibility in both
the study groups. As a corollary, a possible guide to empirical treatment of MRSA
infections is provided based on the obtained antibiotic susceptibility.
Subjects and Methods


Clinical and bacteriological studies were conducted on patients with pyodermas and
positive S. aureus isolates on culture. Two hundred cases of staphylococcal pyodermas
were analyzed, of whom 150 were outpatients comprising the community-associated S.
aureus pyoderma (CA-SAP) group. Fifty inpatients comprised the hospital-associated S.
aureus pyoderma (HA-SAP) group. The sample size of both study groups was selected
based on the frequency of encountering a patient with staphylococcal pyodermas, which
were higher in the out-patient setting. Since a selection criterion was used for both study
groups as outlined below, randomization was not required. The clinical investigator
involved with interpretation of antibiotic susceptibility data was blinded to both study
groups. The cross-sectional study was conducted over a period of 1 years from March
2009 to August 2010 at the author's medical college based in Mangalore, Karnataka
after obtaining clearance from the institutional ethical review board.

Inclusion criteria

For HA-SAP, the criteria were: (a) A history of hospitalization or surgery or dialysis such
that infection was not present or incubating on admission in a patient hospitalized >48
h, or residence in long-term care facility within 1 year of study; (b) a permanent
indwelling catheter or percutaneous medical device at the time of study; and (c) a
positive culture for S. aureus, 48 h after admission.

For CA-SAP, a positive culture for S. aureus in patients without hospitalization in the past
year and no antibiotic treatment in the previous month were the criteria. Patients
attending the outpatient dermatology clinic would effectively represent the CA-MRSA
group of the area served by the teaching hospital. Pyoderma caused by other
bacteriological agents was effectively excluded.

Evaluation

A detailed history that elicited information on occupation, nutritional status, hygiene,
duration of disease, and the co-existence of any other cutaneous or systemic disease
was taken. General and system-specific examinations were conducted in all the patients.
Lesions were classified into primary (pyoderma occurring without a predisposing cause
or skin lesion) and secondary pyodermas (pyoderma in which an existing skin lesion
becomes secondarily infected).

Microbiological examination

Specimen collection

Intact pustules were first cleaned with 70% alcohol. They were then ruptured with a
sterile needle and the expressed pus was collected on two sterile cotton swabs. In case
of ulcers and crusted lesions, normal saline was used to clean the wound, while the
surrounding normal skin was cleaned with 70% alcohol. Two sterile swabs were rubbed
over the expressed pus or the advancing edge of the ulcer.

Bacteriological methods

Gram's stain

Smears were prepared using pus from the first swab and were stained by Gram's
method. They were examined for the type and number of bacteria.

Culture

The pus from the second swab was inoculated on blood agar and MacConkey's agar. The
culture plates were aerobically inoculated at 37C for 24-48 h. Colonies grown on the
plate were identified by Gram's staining, colony morphology, and biochemical
characteristics.

S. aureus colonies were identified using catalase test, coagulase test, oxidation
fermentation (OF) test by Hugh Leifson's method, mannitol fermentation test, and
urease test. Gram-positive cocci arranged in clusters with catalase positivity were further
tested by coagulase test (slide and tube method), OF test, urease test, and mannitol
fermentation. Those found positive for the above tests were identified as S. aureus. [5]

Antibiotic susceptibility testing for S. aureus

All S. aureus isolates were tested for their antibiotic susceptibility by Kirby-Bauer disk
diffusion method using commercially available antibiotic disks (Himedia, Bombay, India;
Beckton and Dickinson, Franklin Lakes, NJ, USA) according to Clinical and Laboratory
Standard Institute guidelines. [13]

The antibiotics for which sensitivity was tested along with the disk content are illustrated
in [Table 1]. The zone of inhibition was noted and interpreted using the Kirby-Bauer
chart. [13]{Table 1}

Detection of methicillin-resistant S. aureus

Methicillin resistance was detected using oxacillin and cefoxitin. Those having a zone of
inhibition 10 mm for oxacillin and 19 mm for cefoxitin were further subjected to a
minimum inhibitory concentration (MIC) test. The strains having MIC of 4 mcg/ml for
oxacillin and 4 mcg/ml for cefoxitin were considered resistant to methicillin (MRSA)
[Figure 1]. [13] The susceptibility of these strains to second-line antibiotics, vancomycin
and linezolid, was tested.{Figure 1}

Statistical analysis

Statistical analyses were performed with SPSS for Windows (SPSS; SPSS Inc., Chicago,
IL, USA). A test for significance of individual attributes in the clinical spectrum and
antibiotic sensitivity pattern of CA and HA staphylococcal pyoderma was conducted using
Chi-square test. Student's t-test was used to calculate mean differences of each
individual attributes such as age, body surface area between the CA and HA
staphylococcal pyoderma groups. Significance was indicated by a two-tailed P < 0.05.
Results


The mean age of the patients was 33.19 19 years (range: 19-90 years) with a median
age of 32 years. The mean age of the CA-SAP group was 30.8 years with a median age
of 28 years. The mean age of the HA-SAP group was 40.57 with a median age of 47
years. There was a statistical difference in the mean value of patient's age between the
two groups (P = 0.0021). The male to female ratio was 1:0.67 for the CA cases and
1:0.61 for the HA cases, indicating that both groups were well matched in sex
distribution. Pre-schoolers, students, and skilled workers formed the majority of cases in
the community group, whereas the number of housewives, businessmen, and infants
was significantly more in the hospital group [Table 2].{Table 2}

Poor personal hygiene was seen in 15 (10%) of the community cases, whereas there
was only one such case in the hospital group. Primary pyodermas constituted majority of
the CA-SAP group with 79 (52.66%) cases, whereas secondary pyodermas were
common in the HA-SAP group with 28 (56%) cases [Table 3]. In the CA-SAP group, the
primary pyodermas were constituted by folliculitis and furunculosis, whereas the
secondary pyodermas included infected scabies and eczema. The HA-SAP group had a
larger proportion of secondary pyodermas such as infected eczema, ulcers, toxic
epidermal necrolysis, and infected burns [Figure 2]. Though most of the lesions were on
the legs in both the groups, a significantly more body surface area involvement (P =
0.041) was seen in the HA-SAP group than in the CA-SAP group [9.67 0.36 cm vs.
4.82 0.17 cm] [Figure 3]. As shown in [Figure 4] and [Table 4], the CA pyodermas
were more sensitive to most of the tested antibiotics than the HA staphylococcal
pyodermas and conversely, the HA pyodermas were resistant to many of the tested
drugs. Least sensitivity was observed to penicillin in both the groups [Figure 4] and
[Table 4], whereas maximum sensitivity was seen to oxacillin and cephalosporins.
Cephalosporins demonstrated least resistance in both the groups. However, statistically
significant resistance or sensitivity patterns were not noted when comparing both
groups.{Figure 2}{Figure 3}{Figure 4}{Table 3}

Antibiotic sensitivity

The hospital group demonstrated higher resistance to antibiotics such as penicillin,
cotrimoxazole, and ciprofloxacin on comparison with the {Table 4}community group
[Table 4]. Though no statistically significant differences were present in the resistance
patterns, ciprofloxacin resistance was higher in the hospital (60%) group than in the
community (40%) group [Table 4] and [Figure 4]. [Table 4] also compares the results of
this study against those of other studies and also reveals an increased resistance to
antimicrobials such as cotrimoxazole and gentamicin.

This study additionally tested the susceptibility of S. aureus to amoxicillin-clavulanic acid
and cephalosporins such as cefuroxime, cefotaxime, and cefixime. The antibiotic
sensitivity patterns for all cephalosporins were consistent above 85%. However,
amoxicillin-clavulanic acid had almost similar susceptibility patterns when compared with
cotrimoxazole and ciprofloxacin, and lower susceptibility in comparison to cephalosporins
[Table 4].

MRSA

Among the 150 community patients with S. aureus pyodermas, 133 (88.66%) were
methicillin-sensitive S. aureus (MSSA) and 17 (11.33%) were MRSA. Among the 50
hospital patients, 41 (82%) were MSSA, whereas the rest 9 (18%) were MRSA [Table 5].
The total prevalence of MRSA from both the groups was 26 (13%). MRSA strains were
isolated in a younger age group (27-29 years) in both study groups. CA-MRSA lesions
were mostly those of infected scabies and folliculitis. HA-MRSA was isolated more
frequently from lesions such as ulcers, burns, and eczema [Table 6]. Five patients with
CA-MRSA had a history of similar lesions in other members of the community (scabies).
There was no statistical difference in the mean of patient's age between the CA-MRSA
and HA-MRSA groups.{Table 5}{Table 6}

The distribution of the lesions was predominant on the legs in the CA-MRSA group and
widespread in the HA-MRSA group. Though 100% resistant to all first-line antibiotics,
both the strains were 100% sensitive to vancomycin and linezolid. Two patients with HA-
MRSA succumbed to the infection despite treatment with vancomycin.
Discussion


The skin infections caused by S. aureus range from primary infections such as impetigo,
ecthyma, folliculitis, furunculosis, carbuncle, and sycosis barbae to secondary infections
such as eczema, infestations, and ulcers. Mucin appears to be the critical surface that is
colonized in a process involving interactions between staphylococcal protein and mucin
carbohydrate. [14] Resistance to penicillin was noted within 4 years of introduction of
penicillin and was due to the production of enzymes called -lactamase (penicillinase) by
previously susceptible bacteria. [1] Methicillin, the first -lactamase stable semi-
synthetic penicillin was introduced in 1960. [8] Resistance was detected within a year of
its introduction. [1],[15] MRSA strains are resistant to allb-lactam antibiotics. [1],[9] In
the last decade, the prevalence of resistance to penicillin G among isolates of S. aureus
and Staph. epidermidis has consistently exceeded 90%. [16] Resistance to penicillin G is
due to the production of -lactamases under the control of transmissible plasmids and
can be overcome with -lactamase-resistant (second generation) penicillins such as
nafcillin or methicillin. [17] For most other antibiotics, resistance develops in a multistep
process during the course of multiple exchanges of the organism between patients and
carriers. The staphylococci with multiple drug resistance, typically seen in a hospital
setting, are known as "hospital-associated Staphylococcus." [18]

There has been a gradual trend of increasing antibiotic resistance over the years. In the
community group of staphylococcal infections, Ohana demonstrated a higher
susceptibility to erythromycin and gentamicin as compared to that observed in this
study. [19] Penicillin demonstrated highest resistance in this study, similar to the
findings reported by Patil and Nagaraju [Table 4]. [2],[20],[21],[22]

The hospital group generally showed a higher resistance to first-line antibiotics when
compared to the community group. Though no statistically significant differences were
present in the resistance patterns, ciprofloxacin resistance was observed more in the
hospital (60%) group than in the community (40%).

The multidrug resistance characterizing the nosocomial strains may be a result of the
exposure of S. aureus to multiple antibiotics. [23] Antibiotics like erythromycin which
constitute the first-line drugs against many infections are becoming increasingly
ineffective. [24] [Table 4], which compares results of various studies in relation to this
study, reveals an increased resistance to cotrimoxazole and gentamicin.

Community-associated MRSA

Recent reports conclude that strains of MRSA have become established in the community
across the world. Unlikely to have been derived from hospitals, these strains represent a
widespread community MRSA infiltrating the hospital-setups [25] Unlike nosocomial
MRSA isolates, community acquired strains from patients without known MRSA risk
factors are generally multidrug susceptible (except to b-lactams) and have distinctive
molecular characteristics. Their resistance is usually limited to methicillin. Saracolatz
found MRSA to be endemic in Detroit, USA, accounting for 38% of all community
acquired S. aureus infections. [26] Ohana reported the incidence of MRSA in community
acquired S. aureus skin infections to be as low as 1% in Afula, Israel. [19] In a study in
New Zealand, Riley reported 10% of all community acquired S. aureus infections to be
caused by MRSA. [27] Of concern is the recent identification of strains of S. aureus with
intermediate level resistance to vancomycin, the drug of choice for MRSA. [28] CA-MRSA
is pauci-resistant and more polyclonal. It produces skin diseases and severe pneumonia
in otherwise healthy people. [29]

Differences between CA-MRSA and HA-MRSA

HA-MRSA infections are well known. In 1982, an American hospital outbreak reported an
incidence of 30% MRSA. [30] Studies conducted in Japan reported an incidence of about
41.5%. [31] There are many reports of increasing resistance of S. aureus from India.
[32],[33] Methicillin resistance was seen in 40.47% among hospital-acquired skin
infection in a South Indian study. [24] This study demonstrated its prevalence to be
11.33% in the community and 18% in the hospital group, comparable to rates published
by Nagaraju and Thankiwale. [21],[22],[34] Both the CA-MRSA and HA-MRSA were
associated more with secondary pyoderma (64.9% and 87%, respectively) in our study.
Also, 60% of the CA-MRSA isolates were from lesions of scabies and folliculitis, whereas
HA-MRSA was isolated predominantly from ulcers, eczemas, and erosions (89%).

The risk factors for acquiring CA-MRSA include infancy, history of similar lesions in the
community, chronic illnesses, prison-hood, athletes, and people with homosexual
orientations. [22] In this study, 29% of the CA-MRSA patients were identified to have
the first two risk factors.

Therapy for treating infections due to MRSA is often limited to glycopeptide antibiotics
like vancomycin or the newly approved drugs such as linezolid and
quinupristin/dalfopristin. [1] Reports of reduced susceptibility to vancomycin are posing
a great threat to the viability of the available treatment options. [1] There have been
reports of hetero-vancomycin intermediate S. aureus, subpopulations with reduced
susceptibility within the strains with an MIC within the susceptible range of 4 g/ml.
[35]

Clinically, the CA pyodermas were commonly primary infections, occurring more
frequently in young adults and over the extremities. HA pyodermas were more often
secondary pyodermas in middle-aged patients and were characterized by a larger
surface area of involvement.

An alarming resistance pattern was noted to commonly used antibiotics in this study.
Amoxiclav has a mid-range susceptibility pattern similar to cotrimoxazole and
ciprofloxacin. A strong sensitivity pattern to cephalosporins was seen. Prevalence of
MRSA isolated from community was 11.3% (CA-MRSA) and nosocomial was 18% (HA-
MRSA), with an overall prevalence of MRSA was 13%. Phakade found no MRSA in 619
cases of CA-SAP in a study conducted at KEM Hospital, Mumbai, India, whereas 45% of
HA-SAP was methicillinresistant. [41] The prevalence of HA-MRSA in our study was
found to be lower than other reports, but that of CA-MRSA was found concordant with
reported series [Table 7]. Tiwari reported a prevalence of HA-MRSA isolated from tissue
fluids in a tertiary hospital in Bhubaneshwar, India, the maximum 45% was from pus.
MRSA strains were having 100% sensitivity to vancomycin and linezolid as noted by us
in our study and 92.9% sensitivity to teicoplanin. [42] Fatality due to MRSA among 200
cases of pyoderma in our study was 1%. These patients belonged to the HA-MRSA group
and succumbed to MRSA infection despite treatment with vancomycin. Septicemia and
multiorgan failure had set in before the institution of susceptible antibiotic in
them.{Table 7}

In order to reduce the problem of antibiotic resistance, it is mandatory to survey and
screen clinical isolates for resistance. This is necessary in situations of staphylococcal
outbreaks inclosed surroundings (MRSA or MSSA infections in a critical care environment
or high dependency domiciliary centers as in old-age homes). Isolates can be obtained
from the axilla, nasal cavity, groin, perineum, and throat. [6],[7],[8] However, it may
not be practical in an out-patient setting. Efforts must then be channeled toward prudent
antibiotic use based on maximal field susceptibility in a given locality, as documented in
this study, and by minimizing confounding factors for the development and persistence
of infection.
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