Skin and soft tissue infections (SSTIs) have been defined as invasion of the epidermis, dermis, and subcutaneous tissue by bacteria. The term SSTI covers infections of all anatomical and surgical sites where the integrity of the skin has been breached [1]. If SSTIs are just presented with skin redness, they are called mild or superficial SSTIs (sSSTIs), and if present along with systemic signs such as tachycardia, fever, and hypotension, they are classified as deep-seated SSTIs (dSSTIs) [2]. The Infectious Diseases Society of America (IDSA) classifies SSTIs into 2 categories: purulent infections (e.g., furuncles, carbuncles, and abscesses) and non-purulent infections (e.g., erysipelas, cellulitis, and necrotizing fasciitis) [1]. SSTIs are usually associated with prolonged hospital stay, increased medical cost, and diverse etiology. The management of dSSTIs is challenging and often requires hospitalization, incision, drainage, or debridement [3]. Predisposing factors include old age, trauma, cardio-pulmonary or hepato-renal disease, diabetes mellitus, and immunosuppression [4].
Although SSTIs affect all age groups, they are more frequent among men aged <5 years and >65 years, involving the lower leg region [5]. Annual outpatient visits for SSTIs are estimated at >14 million/year in the United States [2]. Nearly 7%–10% of admitted patients are affected by SSTIs, and they represent the third most common diagnosis after chest pain and asthma in emergencies [6].
SSTIs can be mono-microbial or poly-microbial. Methicillin-resistant
Similarities in clinical presentation and low probability of isolating an organism make the diagnosis challenging [5]. Treatment decisions are often empirical and based on educational guess, host characteristics, likely pathogens, and local susceptibility patterns [5]. Treatments are frequently topical, oral, intravenous, or surgeries [11]. Oral formulations are preferred to avoid higher cost and adverse effects of intravenous administration. Intravenous treatment is reserved for inpatients, for life-threatening dSSTIs, or for those who are unable to absorb oral formulations or fail to achieve adequate concentration at the infection site [12].
The increase in antibiotic resistance and its rapid spread among pathogens has posed a threat to public health worldwide [10]. The growing prevalence of multidrug-resistant pathogens like MRSA and carbapenem-resistant enterobacteriaceae (CRE) is a global concern [9]. Although few studies from Pakistan report the incidence rate and antimicrobial susceptibility profile of
Ethical approval was obtained from the Ethical Review Committee of the Sindh Institute of Urology and Transplantation (approval No. SIUT-ERC-2020/A-244). Because this was a laboratory-based study, the ERC had exempted this research from obtaining informed consent from patients.
A prospective laboratory-based study in the Department of Microbiology, Sindh Institute of Urology and Transplantation (SIUT), Pakistan, conducted from November 2020 to May 2021.
A total of 447 patients of all ages and both sexes attending out-patient clinics or admitted in wards with SSTIs were included. A physician recorded demographic characteristics and underlying cause and stratified the SSTIs into sSSTIs and dSSTIs.
Mono-bacterial growth either gram-positive cocci (GPC) or GNRs. We used the STROBE cross-sectional checklist to report our results.
Transplant and burns patients, poly-microbial growth, yeasts/fungus, gram-positive rods, and gram-negative cocci.
Pus swabs, discharge/secretion, exudates, aspirate, or tissue samples from SSTIs were inoculated on the chocolate, blood, and MacConkey agar (Oxoid Ltd, Hampshire, UK).
Bacteria were identified using standard methods, such as Gram staining, catalase, coagulase, oxidase, mannitol salt agar (MSA), DNAse, bile esculin agar, and fermentation of different sugars. Antimicrobial susceptibility was determined for only top 4 most prevalent organisms using Kirby–Bauer disk diffusion method against the following antibiotics:
(ORAL) trimethoprim–sulfamethoxazole (SXT) (25 μg), ciprofloxacin (5 μg), amoxicillin + clavulanic acid (AMC) (30 μg), erythromycin (15 μg), clindamycin (2 μg), (injectable) ceftriaxone (30 μg), amikacin (30 μg), tazobactam + piperacillin (TZP) (110 μg), sulbactam + cefoperazone (SCF) (105 μg), and (carbapenem) imipenem (10 μg).
Susceptibility to polymyxin B and vancomycin was determined using the microbroth dilution method and E test, respectively. Polymyxin B MIC interpretation was done as intermediate = 2 μg/mL and resistant = 4 μg/mL. A cefoxitin 30 μg disk was used to determine MRSA. The SCF zone diameter of ≤15 mm was interpreted as resistant, 16–20 mm as intermediate, and ≥21 mm as sensitive [18]. The Clinical Laboratory Standard Institute (CLSI) M100 guidelines were used to interpret the results [19].
Multidrug resistance (MDR) is defined as bacterial resistance to at least 1 agent in 3 or more antimicrobial classes [7].
Data analysis was performed using MS excel, SPSS version 20, and GraphPad prism 9.3.1.
A total of 447 specimens from 447 SSTI patients ranging in age from 1 to 78 years, with mean age of 33.76 ± 21.27 years, were included in this study. Of these, mono-microbial growth was isolated from 347 (78%) patients, of which 61% were inpatients and 39% were outpatients.
Of 347 patients, 67% were male and 33% were female. Most of the patients (157 (45%)) were in the 21–50 years age group, 26% were older than 51 years, and 18% were in the 1–20 years age group. The age data were missing for 38 (11%) patients
Demographic characteristics and distribution of cases among inpatients and outpatients suffering from sSSTIs and dSSTIs
Inpatient | 63 | 30 | 148 | 70 | 211 | 61 |
Outpatient | 61 | 45 | 75 | 55 | 136 | 39 |
Male | 88 | 38 | 144 | 62 | 232 | 67 |
Female | 36 | 31 | 79 | 69 | 115 | 33 |
≤20 | 23 | 38 | 38 | 62 | 61 | 18 |
21–50 | 56 | 36 | 101 | 64 | 157 | 45 |
≥51 | 35 | 38 | 56 | 62 | 91 | 26 |
Chronic kidney disease | 47 | 37 | 80 | 63 | 127 | 37 |
Diabetes mellitus | 36 | 39 | 56 | 61 | 92 | 27 |
Malignancy | 13 | 28 | 33 | 72 | 46 | 13 |
Immunosuppression | 16 | 42 | 22 | 58 | 38 | 11 |
Chronic liver disease | 9 | 28 | 23 | 72 | 32 | 9 |
Heart failure | 3 | 25 | 9 | 75 | 12 | 3 |
Wound infection | 82 | 66 | - | - | - | - |
Diabetic foot ulcer | 15 | 12 | - | - | - | - |
Impetigo | 15 | 12 | - | - | - | - |
Cellulitis | 12 | 10 | - | - | - | - |
Abscess | - | - | 138 | 62 | - | - |
Surgical site infection | - | - | 72 | 32 | - | - |
Necrotizing fasciitis | - | - | 13 | 6 | - | - |
|
57 | 45 | 69 | 55 | 126 | 36 |
|
27 | 35 | 49 | 65 | 76 | 22 |
|
14 | 24 | 43 | 76 | 57 | 16 |
|
9 | 24 | 29 | 76 | 38 | 11 |
|
7 | 58 | 5 | 42 | 12 | 3 |
|
5 | 45 | 6 | 55 | 11 | 3 |
|
3 | 30 | 7 | 70 | 10 | 3 |
CoNS | - | - | 6 | 100 | 6 | 2 |
|
2 | 40 | 3 | 60 | 5 | 1.4 |
|
- | - | 4 | 100 | 4 | 01 |
|
- | - | 1 | 100 | 1 | 0.2 |
|
- | - | 1 | 100 | 1 | 0.2 |
CoNS, coagulase-negative
The prevalence of
Most of the samples in our study were dSTTIs (64%). The common sites among dSTTIs were abscess (62%) and surgical sites (32%), and the least common was necrotizing fasciitis (6%). Wound (66%) was the most common representative site for sSSTIs, followed by diabetic foot ulcer and impetigo (12% each), and cellulitis (10%). The most common underlying condition was chronic kidney disease (37%), followed by diabetes mellitus (27%), malignancy (13%), immunosuppression (11%), chronic liver disease (9%), and heart failure (3%)
A number of other GNRs including
For oral antibiotics, all 3 GNRs revealed a high level of resistance (>65%) against ciprofloxacin and SXT.
For injectable antibiotics, the least level of resistance among each GNR was determined against amikacin, and the highest was determined against ceftriaxone.
For carbapenem,
Antimicrobial resistance pattern of common bacteria isolated from sSSTIs and dSSTIs against oral, injectable, and carbapenem antibiotics
sSSTI (n = 57) | 43 (75.4) | 42 (73.6) | 22 (38.5) | - | - | 2 (3.5) | 14 (24.5) | 13 (22.8) | 38 (66.7) | 9 (15.7) | |
dSSTI (n = 69) | 48 (70) | 56 (81) | 40 (58) | - | - | 9 (13) | 23 (33) | 25 (36) | 61 (88) | 14 (20) | |
sSSTI (n = 27) | 16 (59) | 21 (77.8) | 17 (63) | - | - | 9 (33.3) | 9 (33.3) | 10 (37) | 22 (81.4) | 7 (25.9) | |
dSSTI (n= 49) | 38 (78) | 40 (82) | 30 (61) | - | - | 20 (41) | 24 (49) | 27 (55) | 43 (88) | 17 (35) | |
sSSTI (n = 9) | 9 (100) | 6 (66.6) | - | - | - | 4 (44.4) | 4 (44.4) | 5 (55.5) | - | 6 (66.6) | |
dSSTI (n = 29) | 26 (90) | 20 (69) | - | - | - | 11 (38) | 9 (31) | 11 (38) | - | 14 (48) | |
sSSTI (n = 14) | 8 (57.1) | 13 (92.8) | 11 (78.5) | 10 (71.4) | 3 (21.4) | - | - | - | - | - | |
dSSTI (n= 43) | 16 (37) | 39 (91) | 35 (81) | 29 (67) | 5 (12) | - | - | - | - | - |
−, not done; AK, amikacin; AMC, amoxicillin + clavulanic acid; CIP, ciprofloxacin; CRO, ceftriaxone; DA, clindamycin; dSSTIs, deep-seated skin and soft tissue infections; E, erythromycin; IPM, imipenem; n, number of isolates; P.O., Per os; SCF, sulbactam + cefoperazone; sSSTIs, superficial skin and soft tissue infections; SXT, trimethoprim–sulfamethoxazole; TZP, tazobactam + piperacillin.
The MDR prevalence of
MDR pattern of bacteria isolated from sSSTIs and dSSTIs
sSSTI (n = 57) | 8 (14) | 8 (14) | 14 (25) | 6 (11) | 14 (25) | 34 (60) | |
dSSTI (n = 69) | 4 (6) | 8 (12) | 21 (30) | 10 (14) | 23 (33) | 54 (78) | |
sSSTI (n = 27) | 2 (7) | 4 (15) | 5 (19) | 4 (15) | 9 (33) | 18 (67) | |
dSSTI (n = 49) | 2 (4) | 4 (8) | 9 (18) | 5 (10) | 25 (51) | 39 (80) | |
sSSTI (n = 9) | 3 (33) | 0 (0) | 1 (11) | 0 (0) | 5 (56) | 6 (66.6) | |
dSSTI (n= 29) | 4 (14) | 5 (17) | 5 (17) | 2 (7) | 9 (31) | 16 (55) | |
sSSTI (n = 14) | 0 (0) | 1 (7) | 7 (50) | 3 (21) | 2 (14) | 12 (86) | |
dSSTI (n = 43) | 2 (5) | 9 (21) | 21 (49) | 4 (9) | 5 (12) | 30 (70) |
dSSTIs, deep-seated skin and soft tissue infections; MDR, multidrug resistance; sSSTIs, superficial skin and soft tissue infections.
In this study, mono-bacteria were isolated from 78% of patients, of which 67% were males. Similar results have been reported from Pakistan and Ethiopia with the single pathogen isolation (77% and 82%, respectively) with male dominance [11, 7]. In the present study, the incidence of SSTIs was higher (45%) among patients in the 21–50 years age group; this is in agreement with previous studies that report higher prevalence in the 15–44 years age group [11, 7]. Moreover, the rate of SSTIs was higher among inpatients (61%) in our study, which is analogous to a previous study (72.8%) [7]. In this study, dSSTIs were more common (64%), among which abscess and surgical sites were the major sites (94%), whereas wound was the most common site (66%) for sSSTIs. This was in agreement with a similar study from Pakistan, where abscess was the most common site [11]. Chronic kidney disease and diabetes mellitus were major underlying conditions (64%) in our patients. A previous study has reported diabetes mellitus, chronic kidney disease, and heart failure as the most common underlying medical conditions [8].
In the current study, the GNR/GPC ratio was 4:1. Furthermore, the prevalence rate of GNR was higher (79%) than reported in the studies conducted in India, Ethiopia, and Greece (57%, 57%, and 55%, respectively) [7,8,9]. The most frequent GNRs in this study were
In our study, >65% of all 3 GNRs revealed resistance against each oral antibiotic tested. This was in agreement with a similar study from Nepal that reported the majority of
For injectable antibiotics, only a least number of GNRs were resistant against amikacin and a highest number were resistant against ceftriaxone in our study. We report >79% of
In contrast to a previous study from Pakistan where resistance against TZP among
In this study, a very high level of resistance against carbapenem was found among
We noticed differences in the resistance pattern of isolates from dSSTIs and sSSTIs. A comparatively high number of
The cumulative resistance rate of bacteria from hospitalized patients was higher in our study, indicating the circulation of highly resistant bacteria, particularly MDR
The predominant GPC in our study was
The high prevalence of SSTIs was found among males in the 21–50 years age group. The predominant isolates were