|Year : 2019 | Volume
| Issue : 3 | Page : 147-152
Bacterial etiology and antimicrobial sensitivity patterns of ear infections at King Abdulaziz University Hospital, Jeddah, Saudi Arabia
Firas Addas1, Mohammed Algethami1, Nabeel Mahmalji1, Shadi Zakai2, Talal Alkhatib1
1 Department of Otolaryngology, King Abdulaziz University Hospital, Jeddah, Saudi Arabia
2 Department of Medical Microbiology and Parasitology, Faculty of Medicine, King Abdulaziz University, Jeddah, Saudi Arabia
|Date of Web Publication||1-Jul-2019|
Faculty of Medicine, King Abdulaziz University, P. O. Box: 9746, Jeddah 21423
Source of Support: None, Conflict of Interest: None
Objective: This study aimed to provide recent data about the causative organisms of ear infection and their antibiotic sensitivity at King Abdulaziz University Hospital. Materials and Methods: This retrospective study involved 160 patients with ear infection collected between March 2010 and February 2016. Ear swabs were investigated by conventional microbiology methods including cultures and biochemical reactions for identification of microorganisms and antibiotic sensitivity tests. Results: Out of total number of cases, 120 (75%) cases were infected by bacteria and 25 (15.6%) were infected by yeast cells. The majority of patients (n = 61, 38.1%) were of the children and young age group (0–17 years). Most of the patients were diagnosed with chronic suppurative otitis media (OM) (n = 73, 45.6%), followed by OM (n = 48, 30.0%), and otitis externa (n = 39, 24.4%). We also found that the most common pathogens cause ear infection were Pseudomonas aeruginosa, Staphylococcus aureus, and yeast cells. Conclusion: Ear infections are known as a mild disease and are usually treated with empiric therapy, and as our study revealed the most common causative agents of ear infections and their patterns of sensitivity and resistance, this will help in the proper selection of empiric therapy and prevention of the emergence of resistant strains.
Keywords: Antibiotic resistance, chronic suppurative otitis media, otitis externa, otitis media, Saudi Arabia
|How to cite this article:|
Addas F, Algethami M, Mahmalji N, Zakai S, Alkhatib T. Bacterial etiology and antimicrobial sensitivity patterns of ear infections at King Abdulaziz University Hospital, Jeddah, Saudi Arabia. J Nat Sci Med 2019;2:147-52
|How to cite this URL:|
Addas F, Algethami M, Mahmalji N, Zakai S, Alkhatib T. Bacterial etiology and antimicrobial sensitivity patterns of ear infections at King Abdulaziz University Hospital, Jeddah, Saudi Arabia. J Nat Sci Med [serial online] 2019 [cited 2019 Jul 16];2:147-52. Available from: http://www.jnsmonline.org/text.asp?2019/2/3/147/250752
| Introduction|| |
Infection of the ear is a common health problem in both children and adults worldwide. It can be acute or chronic and includes otitis externa (OE) which is an infection of the external auditory canal and otitis media (OM) which is an infection of the middle ear. An ear infection affects about 65–330 million people worldwide, and about 60% of them suffer from significant hearing loss. This accounts for a major health and economic problems, especially in the developing countries where resources for diagnosis and treatments are limited.
Although ear infection can be a self-limiting, if left untreated, it can cause serious complications such as recurrent acute OM, persistence of middle ear effusion, hearing impairment, mastoiditis, meningitis, chronic OM, brain abscess, and sepsis.
Despite the natural protective mechanisms of the cerumen (wax) which has antibacterial properties, normal skin flora such as Pseudomonas aeruginosa, Staphylococcus aureus, Proteus mirabilis, Klebsiella pneumoniae, and Escherichia coli can gain entry through perforated ear.
Although the disease can affect all age groups, infants and young children are more commonly affected due to the short Eustachian tube that allows easier entry of microorganisms to the nasopharynx.
Internationally, the prevalence of ear infection differs depending on the health and economic status. For instance, in the USA and Europe, the prevalence is decreasing due to increased hygiene and awareness, whereas it is increasing in the developing countries. Furthermore, the etiology and frequency patterns vary from region to other, due to differences in geographical and climate conditions.
In Saudi Arabia, there is a scarcity of national epidemiological data about ear infections. Most of our information is dependent on the Western statistics,, and a limited number of local studies. Among the few studies carried out in the region, the prevalence of OME was 13.8% in Riyadh, 2.3% in Abha, and 7.5% in Qassim region. The most common bacteria isolated in several local studies were as follows: P. aeruginosa, S. aureus, and P. mirabilis.,, One study done in Hail University showed that Streptococcus pneumoniae, Haemophilus influenzae, Moraxella catarrhalis, S. aureus, and Streptococcus pyogenes are the most common organisms associated with acute otitis media and could occur after an episode of viral upper respiratory tract infection. Although most of these organisms are sensitive to most common antimicrobial agents used, resistance of bacterial isolates to these agents becomes an alarming global health problem., Surely, local studies of the prevalence of the disease and recent information about bacterial resistance are required at national level in different provinces in Saudi Arabia, to help in allocating sufficient financial and human resources.
Therefore, in this study, we aim to provide recent local information about the etiological organisms and their sensitivity to antibiotics in ear infections at King Abdulaziz University Hospital, Jeddah, Saudi Arabia.
| Materials and Methods|| |
This retrospective study was conducted at King Abdulaziz University Hospital. Records of patients who underwent an ear swab test for the susceptibility of an ear infection associated with ear discharge were reviewed. The data period ranged between March 2010 and February 2016. One hundred and sixty ear swabs were obtained from patients with ear discharge who presented at the otorhinolaryngology outpatient clinic in our institution. These swabs were sent to the King Abdulaziz University Microbiology Laboratory for culture and sensitivity tests. Any patient who underwent an ear swab collection at the otorhinolaryngology outpatient clinic was included in the study. There were no exclusion criteria. Patients who underwent an ear swab were due failure of medical management or persistence of infection. Ear swabs that were obtained from patients with OM were through transpiration of the tympanic membrane.
Patient's data such as initials, gender, age, and diagnosis were obtained from the Medical Records Department at King Abdulaziz University. The bacteriology and sensitivity results were obtained from the Medical and Molecular Microbiology Laboratory at King Abdulaziz University Hospital.
Isolation and identification of bacteria
For the detection of bacteria, sterile culture swabs were used to take specimens from the patients' ears. Ear discharge and swab samples were inoculated aerobically on blood agar plates, chocolate agar plates and MacConkey agar plate at 37°C, and Sabouraud agar plates at 30°C. All these plates were incubated for 48–72 h. These plates were manufactured by Saudi Prepared Media Laboratory. Isolation and identification of bacteria were done by VITEK 2 which is an automated microbiology system utilizing growth-based technology. This system accommodates colorimetric reagent cards that are incubated and interpreted automatically.
Antimicrobial susceptibility testing
Susceptibility testing was done using minimum inhibitory concentration breaking points. The antimicrobial agents tested were as follows: trimethoprim, clindamycin, erythromycin, oxacillin, cefazolin, ampicillin, amoxicillin/clavulanic acid, gentamicin, ciprofloxacin, and piperacillin. The antibiotic susceptibility profiles were selected based on the Clinical and Laboratory Standards Institute (CLSI 2016 guidelines).
A standard bacteriological procedure was followed to maintain correct laboratory test results. American Type Culture Collection (ATCC) standard reference strains (S. aureus ATCC 25923 and E. coli ATCC 25922) were used to control quality of culture and susceptibility testing.
All statistical analyses were performed using the statistical package for the social sciences for windows version 16 (SPSS Inc., Chicago, IL, USA).
Ethical approval was obtained from the Unit of Biomedical Ethics at King Abdulaziz University. All data obtained from patients' records were treated with complete confidentiality and privacy.
| Results|| |
In this study, a total of 160 swabs were collected from KAU Hospital from March 2010 to February 2016 from patients presenting with symptoms and signs suggesting ear infection such as fever, otalgia, hearing impairment, tympanic membrane redness, bulging or perforation, and most importantly persistent ear discharge despite empiric therapy.
Out of these swabs, 120 (75%) cases were infected by bacteria, 25 (15.6%) cases were infected by yeast cells, and 15 (9.4%) cases showed no organism isolation. Moreover, out of the 120 swabs that were infected with bacteria, 8 swabs (6.67%) showed mixed bacterial growth.
Of the participants, 61 (38.1%) were in the age group between 0 and 17 years, 38 (23.8%) participants were between 18 and 39 years, 43 (26.9%) participants were between 40 and 64 years, and 18 (11.3%) participants were above 65 years. The majority of the participants were females (n = 86, 53.7%) in comparison to males (n = 74, 46.3%). Most of the patients were diagnosed with chronic suppurative OM (CSOM) (n = 73, 45.6%), followed by OM (n = 48, 30.0%), and OE (n = 39, 24.4%) [Table 1].
The most commonly isolated organism was P. aeruginosa (n = 30, 20.7%), followed by yeast cells (n = 25, 17.2%), followed by S. aureus (n = 23, 15.8%), including 3 (2.1%) methicillin-resistant S. aureus (MRSA), followed by coagulase-negative staphylococci (CoNS) (n = 18, 12.4%), followed by P. mirabilis (n = 12, 8.2%) [Table 2].
In CSOM, the majority of the patients were females (n = 48, 65.8%) in comparison to males (n = 25, 34.2%). The majority (42.5%) fell in the young age group 0–17 years, whereas the elderly (>65 years) represent the least percentage (6.8%). The most isolated organisms were P. aeruginosa (25%), followed by S. aureus (16.2%) including two MRSA, followed by yeast cells and P. mirabilis (14.7%).
In contrast, in OE, the majority of patients were males (33, 84.6%) in comparison to females (6, 15.4%). The majority fell in the age group between 40 and 64 years (38.5%) and above 65 years (28.2%), whereas only (7.7%) were of young age group (0–17). The most isolated organism was yeast cells (42.3%) and CoNS (23.1%), followed by S. aureus and P. aeruginosa (15.4%).
In OM, the majority of patients were males (n = 28, 54.9%) in comparison to females (n = 23, 45.1%). Young age group represents the majority of patients diagnosed with OM, whereas 3.9% were above 65 years of age. The most isolated organisms were S. aureus (25.6%), followed by P. aeruginosa (20.9%) and CoNS (18.6%) [Table 3] and [Table 4].
S. aureus was found to be highly sensitive to cefazolin (100%), clindamycin (95.2%), trimethoprim (86.9%), oxacillin (86.9%), and erythromycin (84.2%). In addition, three MRSA were isolated showed 100% sensitivity to trimethoprim and clindamycin, 66.6% sensitivity to erythromycin, and 100% resistance to oxacillin and cefazolin [Table 5].
|Table 5: Antibiotic susceptibility tests for Gram-positive and Gram-negative isolates|
Click here to view
P. aeruginosa was found to be highly sensitive to piperacillin (100%), gentamycin (96.4%), and ciprofloxacin (92.8%).
P. mirabilis was found to be highly sensitive to ciprofloxacin (81.8%), gentamycin (75%), and piperacillin (70%).
E. coli was found to be highly sensitive to ciprofloxacin (100%) and gentamycin (66.7%), while it was resistant to piperacillin (100%) and trimethoprim (66.7%) [Table 5].
| Discussion|| |
Ear infection is a common disease among all age groups; therefore, correct identifying of the microbial etiology and antibiotic susceptibility will aid in the treatment and prevent antibiotic resistance.
In our study, the majority of participants were in the age group between 0 and 17 years. This might be because children are exposed to more crowded areas such as daycares and exposed to other infected children which is also associated with poor hygiene and aerosol spread of respiratory infections that ascend to the middle ear. In addition, physiologically children have a shorter and more horizontal Eustachian tube, compared to older individuals, which is associated with easier reflux of nasopharyngeal secretions.
The results also showed that the prevalence of ear infection among females (53.7%) was slightly higher than males (46.3%), Alenezi et al. and Klein also found similar results, but there is no clear explanation whether there is a gender predilection in ear infections.
Regardless of the diagnosis, the most isolated bacterium in our study was P. aeruginosa. It is a highly virulent pathogen; although it is considered an opportunistic pathogen, it can affect immunocompetent individuals infecting any type of tissue. The reasons for its virulence are attributed to many factors, including the presence of flagella and pili which are essential for the pathogen's motility and adherence. Another factor is the presence of enzymes such as proteases and elastases that break down tissue proteins.,
This study also showed that out of the 145 swabs that yielded organisms, 25 swabs (17.2%) showed the presence of yeast cells. Many reasons might have caused this significant number of fungal ear infection in Jeddah, which include warm temperatures throughout the year, increased humidity, and a dusty environment which are all considered favorable for fungal growth.,,
In CSOM, the most isolated organism was P. aeruginosa. Our finding is consistent with studies done in Riyadh, UAE, and Pakistan. In contrary, two studies done Saudi Arabia found methicillin-sensitive S. aureus (MSSA) as the most common isolate.,
Regarding OM, the most common isolated organism was S. aureus; this finding agrees with Al- Al-Mazrou et al., Al-Shara, and Mekelle, while S. pneumoniae was found to be the most common organism in Saudi Arabia and found that populations which are using pneumococcal vaccines have lowered the rate of OM caused by S. pneumoniae.
With regard to OE, yeast cells are the most common isolate followed by CoNS. Similar results were found in the UK and Italy, while in Jordan and Sudan, the most common bacteria was P. aeruginosa.,
Our study reveals variable patterns of susceptibility of the causative bacteria to antibiotics. P. aeruginosa was found to be highly sensitive to piperacillin (100%), gentamycin (95.83%), and ciprofloxacin (92.8%). Similar results were found in different studies including India, UAE, Saudi Arabia, India, and Gaza.,,
MSSA isolates were sensitive to cefazolin (100%), clindamycin (95.2%), and trimethoprim-sulfamethoxazole (86.9%). Our findings were similar to those found in India and to lesser extent in Ethiopia.
MRSA showed 100% sensitivity to trimethoprim and clindamycin, 66.6% sensitivity to erythromycin, and 100% resistance to oxacillin and cefazolin.
| Conclusion|| |
Ear infections are known as a mild disease and are usually treated with empiric therapy, and as our study revealed the most common causative agents of ear infections and their patterns of sensitivity and resistance, this will help in the proper selection of empiric therapy and prevention of the emergence of resistant strains.
In this study, there was difficulty in identifying whether the swab origin was an OM with effusion or a CSOM, we depended on retrospective data and labeling to determine the origin. Another limitation was that some organisms were not tested for sensitivity and resistance patterns with certain agents. Furthermore, this study gives data about this hospital only and does not provide regional data.
The research team would like to acknowledge the following otolaryngology consultants that some of the samples were taken from their clinics: Dr. Kinan Sendi, Dr. K. Alghamdi, Dr. M. Mandura, Dr. K. Alnoury, Dr. H. Alem, Dr. S. Almuhayawi, Dr. H. Almarzouki, Dr. T. Jamal, Dr. A. Aljiffry, and Dr. A. Fida. The authors would also like to acknowledge the Department of Laboratory at King Abdulaziz University Hospital, for their help in processing and analyzing the ear swabs.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Bluestone CD, Klein JO. Otitis Media in Infants and Children. 4th
ed. Hamilton, Ontario, Canada: BC Decker, Inc.; 2007.
Doherty G, Way L. Current Diagnosis and Treatment Surgery. 14th
ed. New York: Lange Medical Books/McGraw-Hill Companies, Inc.; 2015. p. 244-5.
Woodfield G, Dugdale A. Evidence behind the WHO guidelines: Hospital care for children: What is the most effective antibiotic regime for chronic suppurative otitis media in children? J Trop Pediatr 2008;54:151-6.
Wasihun AG, Zemene Y. Bacterial profile and antimicrobial susceptibility patterns of otitis media in ayder teaching and referral hospital, Mekelle University, Northern Ethiopia. Springerplus 2015;4:701.
Winn W, Allen S, Janda W. Koneman's Color Atlas and Textbook of Diagnostic Microbiology, 6th
ed. Lippincott's Williams and Wilkins, Philadelphia, 2006. p. 439-40.
Abera B, Kibret M. Bacteriology and antimicrobial susceptibility of otitis media at dessie regional health research laboratory, Ethiopia. Ethiop J Health Dev 2011;25:161-7.
Adoga AS, Ma'an EN, Malu D, Badung BP, Obiesie IV, Nwaorgu OG, et al.
Swab and aspiration specimen collection methods and antibiogram in chronic suppurative otitis media at Jos University teaching hospital: Which is superior? Ann Afr Med 2010;9:230-4.
] [Full text]
Muluye D, Wondimeneh Y, Ferede G, Moges F, Nega T. Bacterial isolates and drug susceptibility patterns of ear discharge from patients with ear infection at Gondar University hospital, Northwest Ethiopia. BMC Ear Nose Throat Disord 2013;13:10.
Fiellau-Nikolajsen M. Epidemiology of secretory otitis media. A descriptive cohort study. Ann Otol Rhinol Laryngol 1983;92:172-7.
Hallett CP. The screening and epidemiology of middle-ear disease in a population of primary school entrants. J Laryngol Otol 1982;96:899-914.
Sillanpää S, Sipilä M, Hyöty H, Rautiainen M, Laranne J. Antibiotic resistance in pathogens causing acute otitis media in Finnish children. Int J Pediatr Otorhinolaryngol 2016;85:91-4.
el-Sayed Y, Zakzouk S. Point prevalence of type B tympanogram in Riyadh. Int J Pediatr Otorhinolaryngol 1995;31:53-61.
Abolfotouh MA, Ghieth MM, Badawi IA. Hearing loss and other ear problems among schoolboys in Abha, Saudi Arabia. Ann Saudi Med 1995;15:323-6.
Humaid AH, Ashraf AH, Masood KA, Nuha AH, Saleh AD, Awadh AM, et al.
Prevalence and risk factors of otitis media with effusion in school children in Qassim region of Saudi Arabia. Int J Health Sci (Qassim) 2014;8:325-34.
Al-Mazrou KA, Shibl AM, Kandeil W, Pirçon JY, Marano C. A prospective, observational, epidemiological evaluation of the aetiology and antimicrobial susceptibility of acute otitis media in Saudi children younger than 5 years of age. J Epidemiol Glob Health 2014;4:231-8.
Attallah MS. Microbiology of chronic suppurative otitis media with cholesteatoma. Saudi Med J 2000;21:924-7.
Ahmad S. Chronic suppurative otitis media due to Staphylococcus aureus
in Saudi Arabia. Phys Acad 2017;11:53-7.
Fouda SI, Kadry AA, Shibl AM. Beta-lactam and macrolide resistance and serotype distribution among Streptococcus pneumoniae
isolates from Saudi Arabia. J Chemother 2004;16:517-23.
Vishwanath S, Mukhopadhyay C, Prakash R, Pillai S, Pujary K, Pujary P, et al.
Chronic suppurative otitis media: Optimizing initial antibiotic therapy in a tertiary care setup. Indian J Otolaryngol Head Neck Surg 2012;64:285-9.
Wiertsema SP, Leach AJ. Theories of otitis media pathogenesis, with a focus on indigenous children. Med J Aust 2009;191:S50-4.
Alenezi NG, Alenazi AA, Elboraei YA, Alenazi AA, Alanazi TH, Alruwaili AK, et al.
Ear diseases and factors associated with ear infections among the elderly attending hospital in Arar city, Northern Saudi Arabia. Electron Physician 2017;9:5304-9.
Klein JO. Otitis media. Clin Infect Dis 1994;19:823-33.
Lyczak JB, Cannon CL, Pier GB. Establishment of Pseudomonas aeruginosa
infection: Lessons from a versatile opportunist. Microbes Infect 2000;2:1051-60.
Breidenstein EB, de la Fuente-Núñez C, Hancock RE. Pseudomonas aeruginosa
: All roads lead to resistance. Trends Microbiol 2011;19:419-26.
Kerr KG, Snelling AM. Pseudomonas aeruginosa
: A formidable and ever-present adversary. J Hosp Infect 2009;73:338-44.
Bieth JG. The elastases. J Soc Biol 2001;195:173-9.
García-Agudo L, Aznar-Marín P, Galán-Sánchez F, García-Martos P, Marín-Casanova P, Rodríguez-Iglesias M, et al.
Otomycosis due to filamentous fungi. Mycopathologia 2011;172:307-10.
Aneja KR, Sharma C, Joshi R. Fungal infection of the ear: A common problem in the North Eastern part of Haryana. Int J Pediatr Otorhinolaryngol 2010;74:604-7.
Yassin A, Maher A, Moawad MK. Otomycosis: A survey in the Eastern Province of Saudi Arabia. J Laryngol Otol 1978;92:869-76.
Yeli S, Fattah HA. Bacterial isolates and their antibiotic susceptibility in chronic discharging ears in population. Int J Curr Microbiol Appl Sci 2014;3:271-6.
Sattar A, Alamgir A, Hussain Z, Sarfraz S, Nasir J, Badar-e-Alam, et al.
Bacterial spectrum and their sensitivity pattern in patients of chronic suppurative otitis media. J Coll Physicians Surg Pak 2012;22:128-9.
Ahmad S. Antibiotics in chronic suppurative otitis media: A bacteriologic study. Egypt J Ear Nose Throat Allied Sci 2013;14:191-4.
Al-Shara M. A five-year review on the etiology and antimicrobial susceptibility pattern of otitis media pathogens in Jordanian children. Oman Med J 2012;27:358-63.
Alshammari MS, Alshaya HK, Alkhalaf AA, Al Marshadi JA, Alshdokhi AM, Ahmed HG. The common microbial causes of otitis media with especial focus in Saudi Arabia. Res Otolaryngol 2017;6:67-72.
Ninkovic G, Dullo V, Saunders NC. Microbiology of otitis externa in the secondary care in United Kingdom and antimicrobial sensitivity. Auris Nasus Larynx 2008;35:480-4.
Pane G, Cacciola G, Giacco E, Mariottini GL, Coppo E. Assessment of the antimicrobial activity of algae extracts on bacteria responsible of external otitis. Mar Drugs 2015;13:6440-52.
Battikhi MN, Ammar SI. Otitis externa infection in Jordan. Clinical and microbiological features. Saudi Med J 2004;25:1199-203.
Suliman FE. Etiology of Ear Infection Among Sudanese Patients Attending Khartoum Ear, Nose and Throat Hospital-2015 [Master Dissertation]: Sudan University of Science and Technology; 2015.
Elmanama AA, Tayyem NE, Allah SA. The bacterial etiology of otitis media and their antibiogram among children in Gaza Strip, Palestine. Egypt J Ear Nose Throat Allied Sci 2014;15:87-91.
Argaw-Denboba A, Abejew AA, Mekonnen AG. Antibiotic-resistant bacteria are major threats of otitis media in Wollo area, Northeastern Ethiopia: A Ten-year retrospective analysis. Int J Microbiol 2016;2016:8724671.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]