Antimicrobial Susceptibility Profile of Pseudomonas aeruginosa and Staphylococcus aureus Implicated in Wound Sepsis Among Paediatric Patients in Abakaliki, Nigeria

Received 25 Feb, 2021

Accepted 19 May, 2021

Published 10 Jun, 2021

Background and Objectives: Wound infections contribute significantly to morbidity and mortality among paediatric patients globally. The objectives of this study are to determine the antimicrobial susceptibility profile of Pseudomonas aeruginosa and Staphylococcus aureus implicated in wound sepsis among paediatric patients. Materials and Methods: A total of 162 samples were collected from patients wound using sterile cotton swabs and presences of bacteria isolates were screened and their antimicrobial susceptibility profiles were determined using standard microbiological procedures. Statistical analysis were done using SPSS version 16. Results: The prevalence of wound infection was 67.9% among the paediatric patients. The P. aeruginosa and S. aureus isolates had percentage of 24.1 and 56.8. There was a statistically significant difference in the prevalence of both isolates at (p<0.05). P. aeruginosa and S. aureus had 67 (58.3%) prevalence from burns. Wound infection due to P. aeruginosa was 18 (15.7%) and S. aureus 49 (42.6%). In Orthopaedic unit, 43 (91.5%) had their wound infected by both organisms. Thus, P. aeruginosa had percentage of 38.2 and Staphylococcus aureus had 67.1. Ciprofloxacin (81.6% to 94.4%) was the most active antibiotic against the both isolates. Gentamicin and sulphamethoxazole/trimethoprim also presented high susceptibility pattern among the isolates. Conclusion: Antibiotics misusage contributed heavily to the high prevalence of multi-drug resistant organisms obtained in this study. Therefore, treatment guidelines for use of antibiotics should be implemented to avoid indiscriminate use and there should be reviewed occasionally to ensure rational use of antibiotics by clinicians in treatment of patients.

INTRODUCTION

Wound infection is one of the major important causes of disease and death rate worldwide; children intend to have developing or low immunity and bacteria resisting antibiotics increases the complications upon treatment of the disease¹. A wound results following disruption of the skin which can be intentional or accidental, these leads to pain, discomfort, inconvenience, disability, financial drain, and even death due to complications such as septicemia². Wound management as a result of infection or contamination by microorganisms is still a serious problem facing the globe especially among paediatric patients. The infection can be caused by either single or multiple organisms. The existence of multi-drug-resistant strains of bacteria have increased the frequency of burn wound infections, sepsis, accident wound infection and associated death³.

Pseudomonas aeruginosa and Staphylococcus aureus are considered by Infectious Disease Society of America, as the most commonly obtained organisms from patients with burn and wound infection in intensive care unit⁴. P. aeruginosa is known for about 10 - 20% of infections as a result of nosocomial in the form of septicaemia in intensive-care units (ICUs), burn, accidental, bite wound infections and cystic fibrosis⁵. It causes financial strain on the health services due to the required high cost of hospitalization and management of the patients. A number of factors contribute to wound infection; however microorganisms are the major cause with bacteria being the most prevalent⁶. The skin is included as the major impediments to the settlement of infections by bacteria organisms in inside tissues (first line of defense) meanwhile wounds results in physical disruption of the skin, creating a medium through which these pathogens can access the internal tissues⁷.

Early recognition of wound infection and appropriate management is important. Antibiotic therapy and surgical management are the cornerstone measures whereby antibiotics offer adjuvant treatment. Wound infection can be caused by single bacteria or multiple microorganisms⁸. In surgical procedures, Staphylococcus aureus is the most common gram positive pathogen while Pseudomonas aeruginosa is the most common Gram negative bacilli. Life-threatening infection caused by P. aeruginosa continues to cause complications in hospital-acquired infections. P. aeruginosa demonstrates resistance to multiple antibiotics, thereby jeopardizing the selection of appropriate treatment⁹. Resistant bacteria causes severe infections that are expensive to diagnose and difficult to treat¹⁰. The mechanism by which resistance develops is complex and can result in multi-drug resistant bacterial strains due to simultaneous development of resistance to several antibiotics. There are factors that increase the risk of wound infection which include patient characteristics such as; age, obesity, malnutrition, endocrine and metabolic disorders, smoking, hypoxia, anemia, malignancies and immunosuppressant’s¹¹. Bacterial wound infections are commonly found in open injuries. Severe and poorly managed infections can lead to gas gangrene and tetanus which may cause long-term disabilities. Chronic infection can cause septicemia or bone infection which can lead to death. Sepsis associated encephalopathy increases morbidity and mortality especially in the ICU patients¹². Thus, there is need to study antimicrobial susceptibility profile of Pseudomonas aeruginosa and Staphylococcus aureus implicated in wound sepsis among paediatric patients.

MATERIALS AND METHODS

Study area: This study was carried out for a period of five months from March 2019 to July 2019 atthe laboratory unit of the Department of Applied Microbiology, Faculty of Science, Ebonyi State University, Abakaliki, Nigeria. Samples were collected from paediatric unit of the tertiary hospital in Abakaliki.

Bio-data and Samples collection: Bio-data were collected using a well structured questionnaire. The patients and parent or guardians of the child were interviewed to get information on the bio-data. A total of 162 wound samples were collected from the paediatric patients, (Orthopaedic unit - 47 samples) and (Buns unit - 115 samples) using sterile cotton swab sticks. The samples were collected before wound cleaning and precautions were taken to avoid cross contamination at all stages. The swab sticks were carefully removed and returned to their respective containers and labeled accordingly. The samples were transported to the microbiology laboratory of Ebonyi State University, Abakaliki within one hour of collection for bacteriological examination⁷.

Isolation, characterization and antimicrobial susceptibility: The culture media was prepared and poured in petri dishes up to a depth of4mm then allowed to cool. The inoculums were applied to a small area then spread using asterile loop of wire to provide for single colonies. Mannitol salt agar, Mueller Hinton agar and Centrimide agar, Nutrient agar, Nutrient broth, Peptone water media were used. All inoculated plates were labeled and incubated at 37°C for 24 hours for the organisms to grow. Identification of the bacteria was done using the recommended standard microbiological procedures. Kirby and Bauer disc diffusion susceptibility test was used to determine susceptibility patterns. The antibiotic discs used are ceftazidime (CAZ; 30 μg), cefotaxime (CTX; 30 μg), ceftriaxone (CRO; 30 μg), amoxicillin/clavulanic acid (AMC; 20/10 μg), cloxacillin (OB; 5 μg), cefoxitin (FOX; 5 μg), meropenem (MEM; 10 μg), ciprofloxacin (CIP; 5 μg), gentamicin (CN; 10 μg) and sulphamethoxazole/trimethoprim (SXT; 25 μg). Appropriate sensitivity discs were placed on the surface of Mueller Hinton agar 30 mm away from each and the drug activity was shown by zones of inhibition of growth around the discs after 18 to 24 hours of incubation. The diameter of the zones was compared to a standard and categorized as resistant or sensitive^13,14.

Statistical Analysis: The data obtained was analyzed using the statistical software package SPSS version 16.0 (T-test and Chi-square). The results were considered statistically significant at p value is less than 0.05 (p<0.05).

RESULTS

Pseudomonas aeruginosa and Staphylococcus aureus were isolated as the major bacterial organisms associated with wound infection among children in paediatric ward. A total of 162 patients selected from paediatric ward (115 burns patients) and (47 orthopaedic patients) were recruited in the study. The mean age of the participants was 7.5 years. However, almost one-half 47.5% of the participants were between 11 to 15 years of age, 43.2% were within 6 to 10 year and 9.3% were below 5 years of age. There were 88 (54.3%) males and 74 (46.7%) females; the ratio of male-to-female patients was 1.2 : 1. Thus, 75.9 percent of the participants were school children, the rest were not attending school. Burns and accidents were the most common causes of wound with percentage frequency of 38.8 and 51.2 respectively. Notably, most cases of patient with wound infection were found from burns unit with percentage prevalence of 71 (Table 1). The average durations of wound healing among the patients were between 31 to 60 days with frequency of 21 (13%). The duration of wound healing for 67 (41%) patients was between 11 to 30 days. The least frequency of wound healing was recorded for 18 (11%) patients to be between 61 to 90 days (Table 2). There was a statistically significant difference in the frequencies of wound durationat p<0.05. The overall percentage prevalence of wound infection among the patients were 67.9; P. aeruginosa isolates had 24.1 and S. aureus isolates had total prevalence of 56.8 (Table 3). There was a statistically significant difference in the prevalence of S. aureus and P. aeruginosa between the paediatric patients at p<0.05.

Distribution of the isolates according to age of the patients at burns unit showed the percentage frequency of total infected to be 49 (42.6) for S. aureus and 18 (15.7) for P. aeruginosa isolates. Children within the age bracket of 11 to 15 year old haboured more of the organisms in their wound with the percentage frequency of 22.6 for S. aureus and 8.7 for P. aeruginosa isolate (Table 4). There was no statistically significant difference in the prevalence of S. aureus and P. aeruginosa between infected males and infected females at p>0.05. Thus, patients at Orthopaedic unit had percentage frequency of the infected patients for S. aureus to be 43 (91.5) and P. aeruginosa to be 21 (44.7). Patients within the same age bracket above had 51.1% of S. aureus and 27.7% of P. aeruginosa isolates in their wound (Table 5).

Furthermore, out of forty-nine S. aureus isolated from patients obtaining wound treatment from burns unit, highest sensitivity was seen with ciprofloxacin (81.6%), followed by gentamicin (77.6%) and sulphamethoxazole/trimethoprim (73.5%) and meropenem (51.0%). High level of resistance to cloxacillin (79.6%) was seen followed by ceftazidime (69.4%) and cefoxitin (61.2%). Out of eighteen P. aeruginosa isolates, highest sensitivity was seen with ciprofloxacin (94.4%), followed by gentamicin (88.9%), sulphamethoxazole/trimethoprim (77.8%) and meropenem (50.0%). Ceftriaxone, ceftazidime, cefoxitin showed resistance of 55.6% and cefotaxime 61.1% (Table 6). There was a statistically significant difference in the resistance frequency of S. aureus and P. aeruginosa at p<0.05. Among patients at orthopaedic unit, (43) S. aureus were isolated, they showed highest sensitivity to ciprofloxacin (86.1%), followed by gentamicin (74.4%) and sulphamethoxazole/trimethoprim (65.1%) and amoxycillin/clavulanic acid (55.8%). High degree of resistance to cefotaxime (81.4%) was seen followed by cefoxitin, ceftazidime (74.4%), cloxacillin (69.8%) and cefoxitin (61.2%). Out of twenty one P. aeruginosa isolates, highest sensitivity was seen with ciprofloxacin (90.5%), followed by gentamicin (85.7%) and sulphamethoxazole/trimethoprim (71.4%). The isolates were highly resistant to ceftriaxone (76.2%) and cefotaxime (71.4%) (Table 7). There was a statistically significant difference in the resistance frequency of S. aureus and P. aeruginosa at p<0.05.

Table 1: Demographic characteristics of the paediatric patients
Demographic group	Frequency (N)	Percentage (%)
Age (years)
0 - 5	15	9.3
6 - 10	70	43.2
11 - 15	77	47.5
Sex
Male	88	54.3
Female	74	46.7
Attending School
Yes	123	75.9
No	39	24.1
Cause of wound
Burns	58	35.8
Accident	83	51.2
Bites	21	13.0
Ward/unit admitted to
Orthopaedic unit	47	29.0
Burnsunit	115	71.0

Table 2: Durations of wound healing and co-morbidity
Duration and Morbidity	Frequency (N)	Percentage (%)
Wound duration
1 - 10 days	31	19.1
11 - 30 days	67	41.4
31 - 60 days	21	13.0
61 - 90 days	18	11.1
91 days and above	25	15.4
Co-morbidity
Yes	0	0.0
No	162	100
P-value = 0.02

Table 3: The prevalence of wound infection among the paediatric patients
Source/Patients	Sample Size	Total Number Infected (%)	P. aeruginosa (%)	S. aureus(%)	P-value
Burns	115	67 (58.3)	18 (15.7)	49 (42.6)	0.02
Orthopaedic	47	43 (91.5)	21 (44.7)	43 (91.5)
Total	162	110 (67.9)	39 (24.1)	92 (56.8)

Table 4: Distribution of Staphylococcus aureus and Pseudomonas aeruginosa isolates according to age of the patients admitted at burns unit
Age	No. Examined		No. Infected (%)		Total No. Infected	No. Infected (%)		Total No. Infected
	Male	Female	Male	Female		Male	Female
			Staphylococcus aureus			Pseudomonas aeruginosa
0 - 5	8	7	3 (6.1)	1 (2.0)	4 (3.5)	0 (0.0)	0 (0.0)	0 (0.0)
6 - 10	25	25	12 (24.5)	7 (14.3)	19 (16.5)	6 (33.3)	2 (11.1)	8 (7.0)
11 - 15	25	25	16 (32.7)	10 (20.4)	26 (22.6)	4 (22.2)	6 (33.3)	10 (8.7)
Total	58	57	31 (63.3)	18 (36.7)	49 (42.6)	10 (55.6)	8 (44.4)	18 (15.7)
P-value =0.406

Table 5: Distribution of Staphylococcus aureus and Pseudomonas aeruginosa isolates according to age of the patients admitted at Orthopaedic unit
Age	No. Examined		No. Infected (%)		Total No. Infected	No. Infected (%)		Total No. Infected
	Male	Female	Male	Female		Male	Female
			Staphylococcus aureus			Pseudomonas aeruginosa
0 - 5	0	0	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)
6 - 10	14	6	13 (30.2)	6 (14.0)	19 (40.4)	6 (28.6)	2 (9.5)	8 (17.0)
11 - 15	16	11	14 (32.6)	10 (23.2)	24 (51.1)	8 (38.1)	5 (23.8)	13 (27.7)
Total	30	17	27 (57.5)	16 (42.5)	43 (91.5)	11 (52.4)	10 (47.6)	21 (44.7)
P-value = 0.802

Table 6: Antibiotics susceptibility pattern of bacterial isolates from wound of paediatric patients admitted at burns unit
Antibiotics	Staphylococcus aureus		Pseudomonas aeruginosa
	Susceptible (%)	Resistant (%)	Susceptible (%)	Resistant (%)
Amoxycillin/clavulanic acid	17 (34.7)	32 (65.3)	9 (50.0)	9 (50.0)
Gentamicin	38 (77.6)	11 (22.4)	16 (88.9)	2 (11.1)
Ceftriaxone	20 (40.8)	29 (59.2)	8 (44.4)	10 (55.6)
Cloxacillin	10 (20.4)	39 (79.6)	9 (50.0)	9 (50.0)
Cefoxitin	19 (38.8)	30 (61.2)	8 (44.4)	10 (55.6)
Ceftazidime	15 (30.6)	34 (69.4)	8 (44.4)	10 (55.6)
Meropenem	25 (51.0)	24 (49.0)	9 (50.0)	9 (50.0)
Ciprofloxacin	40 (81.6)	9 (18.4)	17 (94.4)	1 (5.6)
Cefotaxime	18 (36.7)	31 (63.3)	7 (38.9)	11 (61.1)
Sulphamethoxazole/trimethoprim	36 (73.5)	13 (26.5)	14 (77.8)	4 (22.2)
P-value = 0.00

Table 7: Antibiotics susceptibility pattern of bacterial isolates from wound of paediatric patients admitted at Orthopaedic unit
Antibiotics	Staphylococcus aureus		Pseudomonas aeruginosa
	Susceptible (%)	Resistant (%)	Susceptible (%)	Resistant (%)
Amoxycillin/clavulanic acid	24 (55.8)	19 (44.2)	11 (52.4)	10 (47.6)
Gentamicin	32 (74.4)	11 (25.6)	18 (85.7)	3 (14.3)
Ceftriaxone	20 (46.5)	23 (53.5)	6 (28.6)	15 (71.4)
Cloxacillin	13 (32.2)	30 (69.8)	10 (14.3)	12 (57.1)
Cefoxitin	11 (25.6)	32 (74.4)	11 (52.4)	10 (47.6)
Ceftazidime	11 (25.6)	32 (74.4)	9 (42.9)	12 (57.1)
Meropenem	18 (41.9)	25 (58.1)	11 (52.4)	10 (47.6)
Ciprofloxacin	37 (86.1)	6 (13.9)	19 (90.5)	2 (9.5)
Cefotaxime	8 (18.6)	35 (81.4)	5 (23.8)	16 (76.2)
Sulphamethoxazole/trimethoprim	28 (65.1)	15 (34.9)	15 (71.4)	7 (28.6)
P-value = 0.02

DISCUSSION

There is increasing prevalence of wound infections/sepsis that affects the children globally as a result of microbial contamination, these leads to morbidity and mortality among them. Inappropriate antimicrobial use is associated with increased resistance of microorganism implicated¹⁵. This present study observed that wound infections are common across all the age groups included in this study. The total prevalence of wound infection was 67.9% among the paediatric patients. Pseudomonas aeruginosa isolates had percentage frequency of 24.1 and Staphylococcus aureus isolates had total prevalence rate of 56.8. The prevalence of wound infection as observed in this study is in agreement with the work of Orrett and Land¹⁶ on Methicillin-resistant Staphylococcus aureus prevalence in wound at Trinidad. Also akin with the research work of Ahmed¹⁷ on prevalence of nosocomial wound infection among patients in Sudan. Thus, S. aureus had higher percentage frequency of (56.8) than P. aeruginosa isolates that had 24.1 among the paediatric patients^18,20. Studies have also shown that S. aureus and P. aeruginosa was the major Gram positive and Gram negative bacteria implicated in wound infection worldwide. A study carryout on children in Ibadan, South West Nigeria reported S. aureus to have the highest frequency rate of (51.7%), followed by P. aeruginosa (11.0%), Proteus spp. (6.9%) and Escherichia coli (3.4%) to be the major bacteria isolates implicated in wound infection²¹. This is in line with the recent findings of this research, where S. aureus isolates had total prevalence of 56.8 and P. aeruginosa isolates had percentage frequency of 24.1. The frequency of P. aeruginosa in the current research is similar to other studies carried out on wounds infection in Iraq (27.0%)²², Tunisia (27.0%)²³, and South Africa (14.5%)²⁴, as well as a previous research in the same governorate, in which (19.5%) P. aeruginosa prevalence rate was reported²⁵. However, higher frequency rates were recorded in other similar studies on wounds of burns patients in Pakistan and Egypt²⁶. The high prevalence of S. aureus (56.8) as reported in this research, agrees with the findings of other researchers who recorded that 70.0% of the bacteria isolated from wound in FMC Owerri were Staphylococcus species; likewise the isolates from Christiana Hospital had 58% of Staphylococcus species. The high frequency of S. aureus could be associated with the fact that they are microbial flora of the human skin²⁷.

Study on infected wounds of paediatric patients in Niger State, Nigeria, observed that P. aeruginosa 20.0% and S. aureus 46.67% was the most common bacteria isolated from burns and orthopaedic wound samples⁷ and is in accordance with the findings of this study. A retrospective study by Motayo et al.²⁸ in south western part of Nigeria, observed that P. aeruginosa (25.4%) and S. aureus (14.7%) was implicated in wound sepsis. The low percentage frequency S. aureus observed in their study is not in line with the present findings of this research.

A study on the children of Nepal identified those of age less than 1 year was at higher risk of wound infections by bacteria. S. aureus followed by P. aeruginosa were the most common bacteria causing wound infections in children²⁹. Our research observed that children within the age bracket of 11 to 15 year harboured more of the isolates in their wound and 1 to 5 years had the least prevalent rate among the paediatric patient obtaining treatment within burns and orthopaedic unit. Male children haboured more of the S. aureus and P. aeruginosa isolates in their wound compare to the female children in this study. The observation of this study disagreed with the work of Rai et al.²⁹. Cultures from burn wound of patients at Thiruvananthapuram, Kerala, India revealed P. aeruginosa as the most common organism followed by S. aureus, E. coli, Acinetobacter baumannii and Klebsiella pneumoniae³⁰. This is not in agreement with the result obtained in our study.Shrestha and Basnet³¹ also reported S. aureus to be the most prevalent bacteria isolate causing wound infections which akin with this study. The high occurrence of S. aureus and P. aeruginosa isolates as observed among the paediatric patients in our study is an indication of poor personal hygiene on the part of the patients. These may give room for the spread of clinically important organisms since plasmids carrying resistance genes can easily be transferred and acquired amongst bacterial population and these can replicate alongside the bacterial chromosome²⁷. Furthermore, due to presence of the S. aureus as normal flora of human body, the endogenous infections are also possible¹.

The relatively higher resistance of the bacteria isolated from the children to the commonly used antibiotics is a matter of great concern.Resistance profiles of S. aureus and P. aeruginosa isolated from paediatric patients receiving treatment of their wound at burns and orthopaedic unitagainst antimicrobial agents tested in this study reviewed that the isolates were mostly β-lactam resistant strains compare to fluoroquinolones antibiotics. It has been noted that inappropriate use of antibiotics can lead to development of resistance to antibiotics. Inappropriate use such as; no indication, incorrect choice, incorrect application of drugs and divergence from institutional guidelines could lead to resistance¹⁵.The high susceptibility of S. aureus and P. aeruginosato ciprofloxacin and gentamicin antibiotic as observed in this study is in consistent to the findings of other studies, where they observed that ciprofloxacin, gentamicin, and ofloxacin were active against S. aureus and P. aeruginosa^2,21. Abubakar et al.⁷ observed that S. aureus and P. aeruginosa were resistant to ciprofloxacin and gentamycin and is not in agreement with the present findings, but the high level of resistant observed against amoxycillin/clavulanic acid is in line with the findings of this study. Tsige et al.³² in their study on bacterial isolates from wound infection showed that gentamycin had great activities against the isolates. The ceftazidime resistance in this study was relatively high ranging from 55.6 to 57.1% and 69.4 to 74.4% for S. aureus and P. aeruginosa respectively, which is in agreement with work done in Egypt, where they discovered P. aeruginosa isolates to have resistant frequency of 86.0 and another study had 60% to ceftazidime antibiotic. Moreover, many other studies showed high resistance rates of ceftazidime as well as other third generation cephalosporins as in Benin (67.5%)⁵. S. aureus isolates were found to be resistant to cloxacillin (79.6%) and cefoxitin (61.2%). The resistance of S. aureus to β- lactam antibiotics is due to the production of penicillinase that hydrolyzed the β-lactam ring. Thus, the high level of resistance observed among the S. aureus isolates to cloxacillin and cefoxitin could be as a result of acquisition of community acquired methicillin resistance gene such as macA encoded in their chromosomal cassette. Moderate level of resistance was observed among the Staphylococcus aureus and Pseudomonas aeruginosa isolates to a powerful class of antibiotics such as meropenem.

CONCLUSION

In conclusion, the results of this research work have shown that Staphylococcus aureus and Pseudomonas aeruginosa are highly prevalence among paediatric patients hospitalized in tertiary hospital in Abakaliki, Nigeria. Children within the age bracket of 11 to 15 year were at higher risk of wound infections by bacteria, and there was a decreasing trend in rates of wound infections with decrease in age. Relatively high resistance to β-lactam antibiotics among P. aeruginosa and S. aureus isolates was observed and these isolates tend to be multi-drug resistant, since they resisted more than one classes of antibiotics. Thus, most of the isolates were highly susceptible to fluoroquinolones (ciprofloxacin) antibiotics. Resistance to high class of antibiotics like meropenem was also observed. The high prevalence of multi-drug resistant S. aureus and P. aeruginosa obtained in this study is due to extensive and inappropriate use of this antibiotic class in the communities for empirical treatment of wound infections and sepsis caused by P. aeruginosa and S. aureus and the treatment of different type of bacteria associated illness. Therefore, treatment guidelines for use of antibiotics should be implemented to avoid indiscriminate use in these centers; and there should be reviewed occasionally to ensure rational use of antibiotics within communities.

SIGNIFICANCE STATEMENT

The findings of this research were to help in identifying appropriate antibiotics to be recommended for the treatment of wound sepsis among paediatric patients. This was done by taken into consideration the susceptibility profiles or patterns of some selected microorganisms such as Pseudomonas aeruginosa and Staphylococcus aureus that was known to be the major organisms causing wound sepsis or infections among children. The data from this research have provided significant information on how to tackle antibiotic resistance, misuse and overuse as a result of self medication and hospital misuse. This study observed that the use of right antibiotics, appropriate care and management of the infected wounds is very crucial in mitigating long hospitalization and duration of wound healing among children. These results are significant for the empirical use of antibiotics and effective treatment of wound sepsis/infections caused by microorganisms in children and also reduced financial burden of hospitalization among the paediatric patients. It also helps in mitigating the negative impact on the life of children at their tender age.

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