Bacteriological profile of paediatric skin and soft tissue infections and their antibiogram at a tertiary care teaching hospital in north India

Abstract

The increasing complexity of wound care in pediatric patients along with delay in the initiation of treatment predisposes these patients to many complications such as pressure ulcers, non-healing surgical wounds and skin damage. A retrospective study was conducted over a period of five years to gain insight into the etiology of pediatric wound infection. A total of 2819 wound culture positive cases were included. Most samples were from the burn ward (30.15%) followed by the general surgery ward (20.46%). Overall, the most common isolate was Staphylococcus aureus (39.73%) followed by Pseudomonas spp (19.12%). The prevalence of MRSA (Methicillin resistant S. aureus), CRE (Carbapenem-resistant Enterobacteriaceae), CRP (Carbapenem resistant Pseudomonas), CRAB (Carbapenem resistant Acinetobacter baumannii) was 47.3%, 62.5%, 70.5%, 96.4%, respectively. The high degree of resistance in children highlights the importance of regular surveillance for identification of common pathogens and optimization of antimicrobial treatment for multidrug resistant organisms.

Keywords

disease prevention disease bacterial infection epidemiology indian ocean islands location public health

Introduction

Wound infections among children are major public health problems and significant cause of morbidity and mortality.¹ A high incidence of childhood injuries is due to unawareness, impulsiveness, natural curiosity, and overall lapses in child supervision. Particular injuries are due to burns, fall from a height and road traffic accidents; these injuries frequently result in bacterial infections.² There is a higher incidence of wound sepsis in children as compared to adults because of a weaker immune system resulting in poor resistance against infection as well as a weaker skin barrier more easily traumatized. Surgical site or postoperative wound infection is also an important cause.³

The common bacterial agents associated with paediatric wound infection are similar to those in adults, the most common being Staphylococcus aureus, Pseudomonas aeruginosa, Klebsiella spp., Escherichia coli and Acinetobacter spp.²

Increased antibiotic resistance is the result of a rampant misuse of antibiotics and the use of antibiotics without prescription.⁴ The presence of multidrug drug resistant organisms in children is relatively unrecognized;⁵ thus a precise selection of antibiotics is important for effective therapy. Our study was therefore planned to determine the bacteriological profile of skin and soft tissue infections and their antibiogram in children with the aim of guiding clinicians with empiric antibiotic therapy.

Material and methods

Our retrospective study was conducted at the Vardhman Mahavir Medical College and Safdarjung Hospital from January 2016 to March 2020. All wound samples received from paediatric population were included in our study. Clinical samples of pus, aspirates and wound swabs from children suspected of wound infection were received from the various wards, the outpatient department (OPD) and intensive care units (ICU) and processed in our microbiology laboratory. All samples were processed aerobically using the standard microbiological culture techniques, and Gram-stained smears were prepared from all clinical samples. These were inoculated on MacConkey's and Blood agar (Hi Media, India) plates, and incubated in aerobic conditions at 37° C for 18–24 h. Identification of growth was by conventional technique, identification made by colony morphology, Gram staining and biochemical tests. Antimicrobial susceptibility testing (AST) was performed by the Kirby-Bauer disc diffusion method on Muller Hinton or Blood agar according to CLSI (Clinical and laboratory standards institute) guidelines. For quality control of antimicrobial susceptibility, Staphylococcus aureus (ATCC 25923) and Escherichia coli (ATCC 25922) strain were used. Antibiotic discs used for Gram positive organisms were penicillin (10U), cotrimoxazole (1.25/23.75 µg), cefoxitin (30 µg), clindamycin (2 µg), erythromycin (15 µg), linezolid (30 µg), and vancomycin (30 µg). For Gram negative bacteria, antibiotics disc used were amikacin (30 µg), ciprofloxacin (5 µg), cefotaxime (30 µg), cefuroxime (30 µg), ertapenem (10 µg), meropenem (10 µg), imipenem (10 µg), netilmicin(30 µg) and piperacillin/tazobactam (100/10 µg). Screening of MRSA was done by the disc diffusion method using cefoxitin (30 µg) disc. The diameter was measured and a zone of inhibition ≥ 22 mm was considered methicillin susceptible (MSSA) and zone ≤ 21 mm resistant (MRSA).

Resistance to either imipenem or meropenem was taken as carbapenem resistance for Gram negative organisms.

The data were entered in MS EXCEL spreadsheet and analysis was done using Statistical Package for Social Sciences (SPSS) version 21.0.

Results

A total of 2819 culture positive samples were included in our study, among which, 1769 (62.7%) were from males. The highest prevalence of bacterial infection was noted in the age group of 1–5 years (40.97%), followed by 5–10 years (32.74%). Most samples were from the burn ward, 850 (30.15%) followed by the general surgery ward, 577 (20.46%) and ICU, 338 (11.9%), respectively (Table 1).

Table 1.

Demographic details of the study group (Total 2819 patients).

Age	Numbers (Percentage)
< 1 year	305 (10.8%)
1–5 years	1155 (41.0%)
5–10 years	1003 (35.6%)
10–14 years	356 (12.6%)
Department
OPD*	611 (21.6%)
ICU^†	338 (12%)
Wards:
Burn ward	850 (30.15%)
Surgery ward	577 (20.46%)
Pediatric ward	273 (9.68%)
Orthopedics ward	63 (2.23%)
Otorhinolaryngology ward	41 (1.45%)
Others	66 (2.34%)

*OPD- Outpatient department, ^†ICU- Intensive Care Unit.

Overall, the most common isolate was Staphylococcus aureus, 1121 (39.73%), followed by Pseudomonas, 541 (19.12%), and Acinetobacter, 399 (14.10%). The bacteriological profile is shown in Table 2.

Table 2.

Bacteriological profile of wound infections in pediatric patients in 5 years (Total 2819).

Organisms	Number of isolates (percentage)
Staphylococcus aureus	1121 (39.73%)
Pseudomonas spp	541 (19.19%)
Acinetobacter spp	399 (14.15%)
Klebsiella spp	358 (13%)
Escherichia coli	211 (7.40%)
Proteus spp	52 (1.84%)
Enterococcus spp	44 (1.56%)
Enterobacter spp	37 (1.31%)
Streptococcus spp	34 (1.21%)
Citrobacter spp	4 (0.14%)
Morganella spp	2 (0.07%)
Stenotrophomonas	1 (0.03%)
Others	15 (0.53%)

Resistance to penicillin among S. aureus was very high, ranging from 98 to 100% throughout the study period, whilst resistance to erythromycin increased from 64.6 to 80.5% in 2016–2018 and decreased to 25.17% in 2019 before increasing again to 65.2% in 2020 (R² = 0.23; p = 0.5); however the trend was not significant. The prevalence of MRSA was 47.3%. Resistance to cotrimoxazole increased in 2016–2017 from 67.4 to 73.3% and decreased (21.9%) in 2018 and then again increased from 28.5% to 58.6% in 2019–2020 (R² = 0.039, p = 0.80), (Figure 1).

Figure 1.

Trends of antimicrobial resistance in Staphylococcus aureus to common antibiotics from 2016 to 2020.

Resistance to third generation cephalosporins in Acinetobacter spp increased from 96.3% in 2016 to 100% in 2020 (R² = 0.89; p = 0.016), E. coli from 80% in 2016 to 100% in 2020 (R² = 0.50; p = 1.17) and Klebsiella from 59.77% in 2016 to 100% in 2020 (R² = 0.14; p = 0.05), (Table 3).

Table 3.

Percentage resistance of gram negative rods (GNR) to different antibiotics (over five year period from 2016–2020).

Organism (Total number = N)	Amikacin N (%)	Cephalosporin N (%)	Carbapenem N (%)	Netilmicin N (%)	Piperacillin- tazobactam N (%)
Escherichia coli (211)	108 (51.18%)	194 (91.94%)	100 (47.39%)	98 (46.4%)	136 (64.4%)
Klebsiella spp (358)	219 (61.1%)	310 (86.59%)	256 (71.5%)	242 (67.59%)	125 (65%)
Pseudomonas spp (590)	404 (74.67%)	445 (82.2%)	382 (70.6%)	375 (69.32%)	396 (73.19%)
Acinetobacterspp (399)	368 (92.4%)	393 (98.7%)	384 (96.4%)	225 (56.5%)	382 (95.9%)

Carbapenem resistance emerged from 2016 and by 2020, its inefficacity towards Enterobacteriaceae, Pseudomonas, and Acinetobacter baumannii was 62.5%, 70.5%, 96.4%, respectively. In 2016, carbapenem resistance was 88% in both Acinetobacter and Pseudomonas but by 2020 it had increased to 93.2% in Acinetobacter (R² = 0.89; p = 0.016) though decreasing to 70.21% in Pseudomonas (R² = 0.089, p = 0.6). Carbapenem resistant Enterobacteriaceae (CRE) increased from 55.9% in 2016 to 78.94% in 2020 (R² = 0.74; p = 0.05), (Figure 2).

Figure 2.

Trends of Carbapenem resistance in various gram negative organisms from 2016–2020.

Discussion

Child wound infections account for a large number of hospital visits, general morbidity and increased health care costs.¹ They are a potential source of life-threatening bacteremia and metastatic abscess. Antimicrobials are lifesaving and need to be administered to eliminate responsible microbial pathogens; thus, knowledge regarding the aetiology of wound infection is vitally important.

Male children (1769; 62.7%) predominate, as found elsewhere,^6,7 possibly explained by hyperactivity of boys over girls outdoors. The incidence of wound infections can vary in different geographical areas among different age-group of children. In the present study the highest incidence of infection was observed in the 1–5-year age group. This could be because of the higher chances of childhood injuries in that age group as a result of ignorance of the child, impulsiveness and natural curiosity. A high prevalence of childhood injury ranging from 6–58% has been observed across the globe.^2,6,7

Burn wound infections accounted for nearly one third of the wound infection in the present study. This is of concern as the immune mechanisms are not robust so there are higher chances of invasion by colonizing flora leading to sepsis and multisystem involvement.^3,8

As found elsewhere, Staphylococcus aureus was our most common isolate,^9,10 and Pseudomonas (19.12%) the second common.^5,10,11 Contamination from care givers is an important suspected source.^10,12,13 The importance of hand hygiene, and the implementation of infection control practices are key preventive strategies.

A high prevalence of MRSA is no surprise,^12–15 and is a serious global concern as none of the ß-lactam drugs are effective in these cases. The reserve drug, vancomycin, is associated with many serious side effects.

High resistance to other commonly prescribed antibiotics was observed in S. aureus isolates is well known, as is resistance to cephalosporins. Alarmingly this showed an increasing trend of resistance during our study period, probably related to an increased empiric usage of these drugs. Indeed, some studies have shown that restricting the use of antibiotic in particular settings does indeed lower resistance rates.¹⁶ Antibiotic recycling and active surveillance of resistance patterns should be part of local policy.

Carbapenem resistance to non-fermenters such s Acinetobacter and Pseudomonas was very high, and probably owing to an increased use. Since multidrug resistance abounds, the resort to use of broad-spectrum antimicrobials inevitably ensues; therefore, the distinction between multidrug resistant health care and community infection use becomes blurred because of mobile genetic elements (MGE) encoding the resistance genes in these organisms.^17,18 A close relationship between environmental (including healthcare worker) and clinical strains is suggestive of cross transmission within the hospital and community.

The main factor behind the emergence of multidrug resistant strains is over-prescription of broad-spectrum antibiotics, a widespread practice in children. The selective pressure of antibiotic use as well as innate immune alterations of an already immature immune system in children quickly leads to overexpression of resistance genes.^19,20 Studies have found that children exposed to antibiotics in early life carry these resistance genes for a long period of time.^20,21

Further accentuation by poor hygiene practice in children,^20,21 self-medication by parents, underdosing and inappropriate prescription of antibiotics adds to the high level of antimicrobial resistance.

A continuous surveillance of multidrug resistant pathogens is mandatory. Many patients may require combination therapy and a longer duration of treatment for complete cure in cases of multidrug resistant organisms.

Footnotes

Acknowledgements

The authors would like to acknowledge Mrs Lata Kalra for her technical assistance

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Manisha Jain

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