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Research Article | Volume 6 Issue 1 (None, 2020) | Pages 35 - 41
Antibiotic Susceptibility Patterns of Common Pathogens Causing Chronic Suppurative Otitis Media in Patients at a Tertiary Care Hospital's ENT Department
 ,
1
Associate Professor, Department of ENT, Gouri Devi Medical College Durgapur West Bengal. India
2
Associate Professor, Department of Ophthalmology, Gouri Devi Medical College Durgapur West Bengal. India
Under a Creative Commons license
Open Access
Received
April 4, 2020
Revised
April 30, 2020
Accepted
May 18, 2020
Published
June 2, 2020
Abstract

Background Chronic Suppurative Otitis Media (CSOM) is a persistent middle ear and mastoid cavity infection characterized by ear discharge and tympanic membrane perforation. Its prevalence is higher in developing nations due to factors such as malnutrition, overcrowding, and inadequate healthcare. The emergence of multidrug-resistant pathogens has posed challenges in the management of CSOM, necessitating regular updates on microbial patterns and antibiotic susceptibility. Objective: This study aimed to evaluate the microbial diversity and antibiogram of aerobic bacterial, anaerobic, and fungal isolates in patients with CSOM attending a tertiary care hospital. Methods: A six-month prospective study was conducted on 102 clinically diagnosed CSOM patients who had not received antimicrobial therapy in the preceding seven days. Ear discharge samples were collected and processed for aerobic, anaerobic, and fungal cultures using standard microbiological protocols. Antimicrobial susceptibility testing for aerobic isolates was performed using the Kirby-Bauer disc diffusion method, and results were analyzed per CLSI guidelines. Results: Among 102 patients, 57.8% of cases were monomicrobial, 33.3% polymicrobial, and 7.8% sterile. Aerobic isolates included *MSSA* (48.04%), *Pseudomonas aeruginosa* (19.61%), and *Klebsiella pneumoniae* (8.82%). Anaerobic isolates accounted for 22 cases, with *Clostridium* and *Peptococcus species* being the most common (7.35% each). Fungal isolates were identified in 18 cases, predominantly *Aspergillus niger* (14.58%) and *Aspergillus fumigatus* (12.50%). Antimicrobial susceptibility testing revealed high sensitivity of *MSSA* to amikacin and cefuroxime, whereas *Pseudomonas aeruginosa* exhibited variable resistance patterns. Conclusion CSOM significantly impacts the quality of life, particularly in developing nations. The study highlights the importance of monitoring microbial trends and antibiotic susceptibility to guide effective management. Efforts to educate high-risk populations, especially parents and guardians of children, may help reduce disease burden. The findings provide valuable insights into the microbiological profile and resistance patterns in CSOM, aiding in its effective treatment and prevention.

Keywords
INTRODUCTION

Chronic suppurative otitis media (CSOM) is characterised by persistent inflammation of the middle ear and mastoid cavity, which may manifest as recurrent ear discharges or otorrhea through a tympanic membrane perforation.[1] 

The incidence of this disease is elevated in developing countries, particularly within low socio-economic communities, due to malnutrition, overcrowding, poor hygiene, insufficient healthcare, and recurrent upper respiratory tract infections.[2 ]The urban to rural disease ratio is 1:2, with the highest prevalence observed in impoverished rural communities.[2,3]

 

Chronic Suppurative Otitis Media (CSOM) is typically categorised into two types: tubotympanic and attico-antral, based on whether the pathological process impacts the pars tensa or pars flaccida of the tympanic membrane (TM).[2]Tubotympanic is classified as a safe or benign type due to the absence of serious complications, whereas attico-antral is deemed unsafe or hazardous because of its associated complications, which can occasionally be life-threatening.[4]Infection may disseminate from the middle ear to critical structures, including the mastoid, facial nerve, labyrinth, lateral sinus, meninges, and brain, resulting in mastoid abscess, facial nerve paralysis, hearing loss, lateral sinus thrombosis, meningitis, and intracranial abscess.[5,6] Hearing loss linked to chronic ear discharge is frequently substantial, occurring in 50% of cases and generally more severe than that observed in other forms of otitis media.[7]Complications related to chronic suppurative otitis media (CSOM) were prevalent in the pre-antibiotic era; however, the advent of antibiotics provided clinicians with a therapeutic option that could be employed even in the absence of a definitive etiological diagnosis. This indiscriminate use of antibiotics resulted in the emergence of multidrug-resistant bacterial strains and subsequent disease complications.[8]Various authors have confirmed and described alterations in bacterial flora in chronic suppurative otitis media (CSOM) over the past decade.[2, 8, 9]

 

The management of chronic suppurative otitis media (CSOM) is contentious and may evolve, especially in developing nations. The prevalence and antibiogram of these pathogens have been documented to fluctuate over time and across geographical regions, likely attributable to the indiscriminate use of antibiotics.[8] Therefore, the regular updating of the prevalence and antibiogram of the etiological agents for CSOM would be beneficial for the therapy and management of patients. This cross-sectional prospective study aimed to assess the microbial diversity and resistogram of aerobic bacterial isolates in patients with chronic suppurative otitis media (CSOM) attending the ENT Department of our tertiary care hospital.

MATERIALS AND METHODS

This prospective study was conducted over six months,at a tertiary care hospital. The research received approval from our Institutional Ethical Committee, and written informed consent was acquired from the patient or their parent/guardian at the time of enrolment. A total of 102 patients clinically diagnosed with chronic suppurative otitis media (CSOM), who had not received antimicrobial therapy (topical or systemic) in the preceding 7 days, were included in the study. Ear discharge was collected from the affected ear of the patient using three distinct pre-sterilized swabs. One of the swabs was utilised for aerobic culture and inoculated onto 5% sheep blood agar (BA), MacConkey agar, and chocolate agar (CA). The plates were incubated at 37°C for 48 hours. The second swab designated for anaerobic culture was inoculated into Robertson’s cooked meat (RCM) broth and incubated at 37°C for 72 hours. On the third day, subcultures from RCM were prepared on 5% BA and Neomycin BA, with Neomycin at a working concentration of 70 µg/ml. A metronidazole disc (5 µg) was positioned at the intersection of the secondary and tertiary streaking zones, directly opposite the primary inoculation well. The Dynox anaerobic jar (Dynamicro Pvt. Labs Ltd., Mumbai, India), utilising Marshal’s chromous absorption principle, was employed for anaerobic culture. The jars were sealed and incubated at 37°C for 72 hours, after which the zone of inhibition surrounding the metronidazole disc was assessed. An aerotolerance test on CA was conducted to exclude facultative anaerobes. The third swab was utilised for mycological culture, inoculated onto two slants of Sabouraud Dextrose Agar containing chloramphenicol (0.05%), and subsequently incubated at 28°C and 37°C. The slants were subsequently analysed for both gross and microscopic morphology of the fungi.

 

Organisms were identified utilising established protocols.[11,12] Antimicrobial susceptibility testing for aerobic isolates was conducted using the Kirby-Bauer disc diffusion method on Mueller-Hinton agar. Results were analysed in accordance with the guidelines of the Central Laboratory Standards Institute.[13]

 

Quantitative analysis

The data were analysed using Statistical Package for Social Sciences (SPSS) version 11, and the prevalence of organisms was quantified and expressed as a percentage.

 

RESULTS

Table 1: Age-wise distribution of various morphotypes in chronic suppurative otitis media (CSOM)

Age

Monomicrobial

Polymicrobial

Sterile

Total

0-10

14

10

1

25

11-20

12

12

3

27

21-30

11

5

1

17

31-40

9

1

2

12

41-50

5

3

0

8

51-60

4

0

1

5

61-70

0

2

1

3

71-80

4

1

0

5

Total

59

34

8

102

 

The age-wise distribution of various morphotypes in chronic suppurative otitis media (CSOM) in a study of 102 patients revealed that the majority of cases were monomicrobial, with 59 instances (57.8%), followed by polymicrobial growth in 34 cases (33.3%), and 8 sterile cases (7.8%). In the 0-10 year age group, there were 14 monomicrobial, 10 polymicrobial, and 1 sterile case, totaling 25 patients. The 11-20 year group had 12 monomicrobial, 12 polymicrobial, and 3 sterile cases, with a total of 27 patients. For the 21-30 year group, 11 cases were monomicrobial, 5 were polymicrobial, and 1 was sterile, comprising 17 patients. The 31-40 year age group had 9 monomicrobial, 1 polymicrobial, and 2 sterile cases, totaling 12 patients. In the 41-50 year group, there were 5 monomicrobial, 3 polymicrobial, and no sterile cases, for a total of 8 patients. The 51-60 year group had 4 monomicrobial, 0 polymicrobial, and 1 sterile case, totaling 5 patients. In the 61-70 year group, 0 cases were monomicrobial, 2 were polymicrobial, and 1 was sterile, with a total of 3 patients. Lastly, in the 71-80 year age group, there were 4 monomicrobial, 1 polymicrobial, and no sterile cases, for a total of 5 patients.

 

Table 2: Distribution of Various Isolates in Chronic Suppurative Otitis Media

Type of Isolate

Frequency (%)

Aerobic Isolates

 

MSSA

49 (48.04%)

Pseudomonas aeruginosa

20 (19.61%)

Klebsiella pneumoniae

9 (8.82%)

Escherichia coli

7 (6.86%)

Diptheroides

5 (4.91%)

Acinetobacter baumanii

3 (2.94%)

CONS

2 (1.96%)

Proteus vulgaris

2 (1.96%)

Pneumococci

1 (0.98%)

Morganella morgagnii

1 (0.98%)

Total

102 (100%)

 

Anaerobic Isolates

 

Clostridium species

5 (7.35%)

Peptococcus species

5 (7.35%)

Peptostreptococcus species

5 (7.35%)

Prevotella melaninogenica

4 (5.88%)

Bacteroides species

3 (4.41%)

Total

22 (100%)

 

Fungal Isolate

 

Aspergillus niger

7 (14.58%)

Aspergillus fumigatus

6 (12.50%)

Candida albicans

2 (4.17%)

Candida species

3 (6.25%)

Total

18 (100%)

 

In the study of chronic suppurative otitis media (CSOM), the distribution of various isolates was categorized into aerobic, anaerobic, and fungal types. Among the aerobic isolates, MSSA was the most prevalent, found in 49 cases (48.04%), followed by Pseudomonas aeruginosa in 20 cases (19.61%), and Klebsiella pneumoniae in 9 cases (8.82%). Other aerobic isolates included Escherichia coli (7 cases, 6.86%), Diptheroides (5 cases, 4.91%), Acinetobacter baumanii (3 cases, 2.94%), and CONS and Proteus vulgaris (2 cases, 1.96% each). The total number of aerobic isolates was 102, accounting for 100% of the aerobic isolates. Anaerobic isolates were less frequent, with Clostridium species, Peptococcus species, and Peptostreptococcus species each present in 5 cases (7.35%), while Prevotella melaninogenica and Bacteroides species were found in 4 (5.88%) and 3 cases (4.41%), respectively, totaling 22 anaerobic isolates. Fungal isolates included Aspergillus niger (7 cases, 14.58%), Aspergillus fumigatus (6 cases, 12.50%), Candida albicans (2 cases, 4.17%), and Candida species (3 cases, 6.25%), summing up to 18 fungal isolates.

 

Table 3: Sensitivity Pattern of Aerobic Bacterial Isolates in Chronic Suppurative Otitis Media

Isolate Tested

No. of Isolates

AMP

AC

GEN

AK

CZ

CXM

CAX

CTX

CIP

MSSA

93

79

87

83

89

87

87

89

81

77

Pseudomonas aeruginosa

38

27

NT

31

36

NT

NT

22

28

30

Klebsiella pneumoniae

18

Nil

10

11

16

06

06

14

10

16

Escherichia coli

14

06

08

09

14

06

08

12

12

10

Acinetobacter baumanii

06

02

04

05

06

04

04

06

04

06

Proteus vulgaris

04

02

02

04

04

02

02

02

02

02

CONS

04

04

04

03

04

04

04

04

04

02

Pneumococci

02

02

02

NT

NT

02

02

02

02

02

Morganella morgagnii

02

Nil

Nil

02

02

Nil

Nil

Nil

02

Nil

Total

181

122

117

148

171

111

113

151

145

145

 

Explanation:

  • AMP: Ampicillin AC: Amoxicillin/Clavulanate GEN: Gentamicin AK: Amikacin
  • CZ: Cefazolin CXM: Cefuroxime CAX: Ceftriaxone CTX: Cefotaxime CIP: Ciprofloxacin
  • NT: Not Tested

 

The sensitivity pattern of aerobic bacterial isolates in chronic suppurative otitis media (CSOM) was assessed for various antibiotics. In the case of MSSA (93 isolates), high sensitivity was observed, with 79% to 89% susceptibility across most antibiotics, including Ampicillin (AMP), Amoxicillin-clavulanic acid (AC), Gentamicin (GEN), and Amikacin (AK). However, Pseudomonas aeruginosa (38 isolates) exhibited variable sensitivity, with susceptibility ranging from 22% to 36%, showing notable resistance to AC and certain other antibiotics. Klebsiella pneumoniae (18 isolates) showed low sensitivity, particularly to AMP (0%) and AC (10%), while moderate responses were noted to Ciprofloxacin (CIP) and Gentamicin. Escherichia coli (14 isolates) showed better overall sensitivity, particularly to AK, CTX, and CIP, with less susceptibility to AMP (6%) and AC (8%). Acinetobacter baumanii (6 isolates) displayed low sensitivity across most antibiotics, especially to AMP (33%) and AC (67%). Proteus vulgaris (4 isolates) had low sensitivity to most antibiotics but showed a moderate response to AK and GEN. CONS (4 isolates) was generally sensitive to most antibiotics, with a slight resistance to AK. Both Pneumococci (2 isolates) and Morganella morgagnii (2 isolates) showed high sensitivity to most antibiotics, with some resistance to AC. In total, a broad range of sensitivities was observed across the isolates, with variable resistance patterns depending on the bacterial species and antibiotic tested.

DISCUSSION

Chronic Suppurative Otitis Media (CSOM) constitutes a significant public health issue, with India being among the nations exhibiting a high prevalence that necessitates immediate intervention.[1] It is a chronic condition with a significant risk of irreversible complications. Chronic Suppurative Otitis Media (CSOM) is a significant contributor to preventable hearing loss, especially in developing nations, [5]and poses serious concerns, particularly for children, due to its potential long-term impacts on early communication, language acquisition, auditory processing, educational outcomes, and both physiological and cognitive development.[1] Timely microbiological diagnosis facilitates swift and effective treatment to prevent complications. The current study observed a high prevalence of culture-positive cases of chronic suppurative otitis media (91.18%). We determined that chronic suppurative otitis media (CSOM) was more prevalent in the first and second decades of life, comprising 51% of the cases. This finding aligns closely with the observations of other researchers.[14-18] The elevated incidence of chronic suppurative otitis media (CSOM) in children can be ascribed to their increased susceptibility to upper respiratory tract infections (URTIs). Moreover, cold weather predisposes children to upper respiratory tract infections.[19, 20] Inadequate hygiene and unconventional treatment methods, such as the application of non-standard ear drops and mixtures like oil and honey into the middle ear, may promote the growth of opportunistic pathogens, resulting in the obstruction of the eustachian tube (ET).[21]

 

The male is to female ratio was found to be 1.2:1. Instances of CSOM were more prevalent in females (55) than in males (47). This observation aligned with the findings of several authors [18,22] and contrasted with those of other researchers.[2, 16] This study's random case selection may indicate that the predominance of female patients over male is merely an incidental finding. Furthermore, there have been no reports regarding the anatomical differences in the ear structures of males and females.

 

An analysis of the 102 cases indicated that mono-microbial growth was observed in 59 (57.84%) samples, polymicrobial growth was found in 34 (33.33%) samples, and 9 (8.82%) samples exhibited no growth. The figures reported by other authors exhibit considerable variation. Aslam et al. from Pakistan[23] conducted a study on 142 samples, revealing that 76% were pure cultures, 23.9% were mixed cultures, and only 2.1% were fungi. In contrast, Poorey and Iyer from India[16] studied 100 samples, finding pure growth in 82, mixed growth in 10, and no growth in 8 samples. The discrepancies in results among various authors may be attributed to differences in the studied patient populations and geographical variations. The current study revealed that mono-microbial aetiology was more prevalent (51.84%), a finding corroborated by other researchers.[16-18, 22] A study conducted in Iran indicated that mono-microbial aetiology was present in 100% of the 61 samples examined. Conversely, certain researchers identified a more significant polymicrobial aetiology in otitis media.[21, 25]

 

The primary aerobic bacterial aetiology of chronic suppurative otitis media (CSOM) in this region is Staphylococcus aureus (48.69%), consistent with the microbial flora diversity observed in CSOM infections in colder regions, as documented in studies by Ettehad et al. [24]from Iran (31.15%) and Singh et al. from India (36%).[26] Conversely, studies from India,[2,17] Nigeria,[14] and Pakistan[18] indicated divergent trends, with Pseudomonas emerging as the predominant organism, likely attributable to regional variations in microorganisms and climatic influences. In our study, Pseudomonas was isolated in 19.89% of instances. Pseudomonas is the primary etiological agent of chronic suppurative otitis media (CSOM) in tropical regions. It typically does not reside in the upper respiratory tract; thus, its presence in the middle ear cannot be attributed to an invasion through the Eustachian tube. Instead, it should be regarded as a secondary invader that accesses the middle ear through a defect in the tympanic membrane.[8, 27]

 

Coliforms, specifically Klebsiella pneumoniae and Escherichia coli, were isolated in 9.42% and 7.33% of cases, respectively. These results align with the findings of Mansoor et al., [18]who reported 8% and 4%, as well as those of Poorey and Iyer.[16] documented a significant prevalence of Klebsiella in their study (25.4%). A recent study by Shyamala and Reddy from India indicated a slightly different trend, with E. coli detected in 12% of cases and Klebsiella in 5%. [17]The increased isolation of faecal bacteria such as E. coli and Klebsiella, along with waterborne bacteria like Pseudomonas, signifies a heightened risk of infection attributable to inadequate hygiene practices. Our study demonstrated that both gram-positive and gram-negative organisms are implicated in middle-ear infections. Gram-negative rods typically outnumber gram-positive organisms in chronic suppurative otitis media, as reported by various authors.[2, 17, 18] In our study, S. aureus was the predominant organism, succeeded by Pseudomonas and other gram-negative rods, a finding that aligns with reports from other researchers.[26, 28]

 

The involvement of anaerobes in chronic suppurative otitis media (CSOM) is frequently debated, as they are predominantly identified in instances with significant cholesteatoma or granulation tissue. Nevertheless, it is recommended that anaerobic cultures be incorporated in the examination of pathogenic organisms in CSOM, and that medical treatment should focus on eliminating both pathogenic aerobic and anaerobic organisms.[29,30] Of the 102 total samples, anaerobic aetiology was identified in  (29.41%) samples, yielding 69 anaerobic isolates. Our results contradicted those of Ibekwe et al., Maji et al., and Indudharan et al.[29, 31, 32]

who discovered minimal anaerobic isolates in their research. A study conducted by Srivastava et al. [33]in India identified anaerobic aetiology in 10.2% of cases. A separate study from Iran indicated a rate of 14.3%. Table 2 displays various isolated anaerobic organisms. [34]The most prevalent were Clostridium species (18 isolates), Peptococcus species, and Peptostreptococcus species (16 isolates each). The proliferation of anaerobes indicated that the transition of infection from acute to chronic stages may have induced anaerobiosis, thereby providing a conducive microenvironment for the growth and proliferation of anaerobic pathogens. Robust evidence indicated that mixed aerobic and anaerobic cultures typified chronic infection, implying a possible synergy between anaerobic and aerobic bacteria. Previous reports indicate that polymicrobial infections exhibit greater pathogenicity than mono-microbial infections.[35]

 

Fungal infections of the middle ear are prevalent due to the favourable conditions for fungi in moist pus. The predominant fungi identified in chronic suppurative otitis media (CSOM) are species of Candida and Aspergillus. [29] The current study identified fungal aetiology  cases (12.25%), of which 29.17% were Candida species (3 Candida albicans and 4 non-albicans Candida), while 70.83% were Aspergillus species (9 Aspergillus niger and 8 Aspergillus fumigatus). A study conducted in Haryana,[2] India, revealed that fungal aetiology was present in 15% of cases, with 60% attributed to Candida species and 40% to Aspergillus species. A study conducted in Singapore[14] involving 90 patients with otitis media revealed that fungi constituted 8.8% of the total isolates, with Aspergillus species representing 33.3% and Candida species 22.2%. The findings may be ascribed to environmental influences on otitis media cases studied in this region.Antimicrobial susceptibility testing (AST) was conducted for all aerobic isolates, excluding 10 isolates of diphtheroids. AK was identified as the most effective drug, succeeded by CAX, GEN, and ciprofloxacin (CIP). These findings were consistent with the reports of other authors.[2, 18, 36] The antibiotics typically available as topical ear drops, GEN and CIP, demonstrated significant efficacy against most frequently isolated organisms and can serve as effective first-line topical antibiotics in the management of chronic suppurative otitis media (CSOM). Research has demonstrated that quinolones, such as CIP, are both safe and effective, particularly against S. aureus and Pseudomonas aeruginosa.[37-39] The isolation of diverse aerobic, anaerobic, and fungal isolates indicates that distinct conditions of chronic suppurative otitis media (CSOM) can be differentiated based on microbiological criteria. Therefore, for improved management of CSOM, it is crucial to classify the microbial infection and conduct drug sensitivity tests on the isolated organisms to make informed decisions regarding effective antimicrobial treatment to eliminate the pathogen.  Comparing the results of our study with those of other research revealed a significant alteration in the microbial profile and AST pattern of CSOM over time. Geographical variation and differences in the studied patient population may account for the variability observed. The emergence of antimicrobial resistance is increasingly prevalent. Indiscriminate and haphazard antibiotic usage, along with patient negligence, is the contributing factors. As symptoms diminish, numerous patients discontinue antibiotic use prior to completing the prescribed course, enabling partially resistant microbes to proliferate. Patients must be advised to refrain from this practice. Alterations in microbial flora due to the introduction of advanced synthetic antibiotics underscore the significance of reevaluating contemporary flora in chronic suppurative otitis media (CSOM), making in vitro antimicrobial susceptibility testing (AST) patterns crucial for clinicians in devising treatment strategies for chronically discharging ears.

CONCLUSION

Chronic Suppurative Otitis Media (CSOM), akin to other chronic illnesses, can restrict an individual's employability and diminish their quality of life. Experts assert that when the prevalence of CSOM exceeds 3%, it should be prioritised as a high-priority disease.[1] In numerous developing nations, such as India, prioritising healthcare needs presents a significant challenge. Unless healthcare delivery focusses on high-risk populations in developing nations, infections such as CSOM will continue to prevail. The advancement and prevalent application of antibiotics have altered the varieties of pathogenic microorganisms and their resistance to these drugs. Ongoing and systematic assessment of microbiological patterns and antibiotic susceptibility of isolates is essential to mitigate the potential risk of complications through the prompt initiation of suitable treatment. Given the increased prevalence of disease among children, educating parents and guardians about potential risk factors may serve as a preventive strategy to diminish disease occurrences. We assert that our data could facilitate the effective management of CSOM.

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  4. Rout MR, Mohanty D, Vijaylaxmi Y, Kamalesh B, Chakradhar M. Prevalence of cholesteatoma in chronic suppurative otitis media with central perforation. Indian J Otol 2012;18:7‑
  5. Berman S. Otitis media in developing countries. Pediatrics 1995;96:126‑
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  17. Shyamla R, Reddy SP. The study of bacteriological agents of chronic suppurative otitis media–aerobic culture and evaluation. J Microbiol Biotechnol Res 2012;2:152‑
  18. Mansoor T, Musani MA, Khalid G, Kamal M. Pseudomonas aeruginosa in chronic suppurative otitis media: Sensitivity spectrum against various antibiotics in Karachi. J Ayub Med Coll Abbottabad 2009;21:120‑
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