Assessment of Antimicrobial Activity of Cerumen (Earwax) and Antibiotics

Microbiology Research 2020; volume 11:8565

Assessment of antimicrobial nation of fatty acid). Another gland i.e. apoc- activity of cerumen (earwax) rine sweat glands release secretion that com- Correspondence: Iffat Naz, Department of bines with the sebum to form cerumen. It Biology, Scientific Unit, Deanship of and antibiotics against picks up discarded cells, ear follicles and Educational Services, Qassim University, pathogenic bacteria isolated may contain dust or other debris, but the Buraidah, 51452, Qassim, Kingdom of Saudi from ear pus samples resulting compound forms earwax or ceru- Arabia (KSA). men.6 Tel.: +966 533897891 E-mail: [email protected] ; There are two different types of geneti- [email protected] Iffat Naz cally determined earwax such as wet type Department of Biology, Scientific Unit, and dry type. The dry type is most common Key words: Ear pus samples; Pathogenic bac- Deanship of Educational Services, in Asians and Native Americans and has a teria; Antibiotics; Cerumen; Antibacterial Qassim University, Buraidah, Qassim, grey brownish colour while the wet type can potency. Kingdom of Saudi Arabia be found in Caucasians and Africians and has a brown or dark colour.7 About 30-50% of Acknowledgements: The author would like to South Asians, Central Asians and Pacific thanks Mr. Jamil & Miss. Javeria (M. Phil islanders have the dry type of cerumen. Scholars), for assisting in collection of ear pus Abstract Cerumen type has been used by anthropolo- samples from different hospitals of Peshawar, gist to track human migratory patterns, such KP, Pakistan. She is also grateful to Dr. Abdul The present study is focused on the Rehman for providing laboratory facilities, at as those of Eskimas.8 Further, the study of assessment of the antimicrobial activity of Department of Microbiology, Abasyn cerumen and antibiotics against bacteria earwax has shown controversy, as some University Peshawar, KP, Pakistan. Moreover, isolated from ear pus samples. Thus, a total authors have suggested that earwax has high the author has deep appreciation for Dr. Saleh of 50 ear pus samples were collected from level of nutrients which help in microbial S Alhewairini (Dean) Deanship of Educational infected patients using sterile swabs and growth and other hold a view that earwax has services, Qassim University, KSA for giving were screened using pure culture tech- some compounds that inhibit the growth of her an opportunity to conduct her research niques. Total of 04 different bacterial iso- microorganisms and prevent ear infec- onlyactivities smoothly. 9,10 lates were identified while, the prevalence tions. Ear infection in any form has a var- Conflict of interest: The Author declares no data revealed that Pseudomonas spp., were ied microbial etiology, which influences the potential conflict of interests. dominant (58%, n = 29) among isolated selection of an efficacious of anti-microbial agents. According to WHO survey, 42 mil- bacteria followed by Staphylococcus spp., Received for publication: 2 April 2020. lion people worldwide have hearinguse loss (22%, n = 11), Escherichia coli (14%, n = 7) Accepted for publication: 19 April 2020. and Proteus spp., (6%, n = 3). Further, where major cause is otitis media. Infection bioassay revealed that Pseudomonas spp., of the ear can be classified depending upon This work is licensed under a Creative and Staphylococcus spp., were most sensi- the site: otitis externa (infection of external Commons Attribution NonCommercial 4.0 tive to Clindamycin (94.73%) while dis- ear) and otitis media (infection on middle License (CC BY-NC 4.0). ear).11 Otitis is a bacterial infection of the ear played resistant to Ciprofloxacin and ©Copyright: the Author(s), 2020 Ampicillin. Similarly, E. coli and Proteus canal caused by rupture in the normal skin or cerumen, which is a protective barrier in the Licensee PAGEPress, Italy spp., were most sensitive to Ciprofloxacin Microbiology Research 2020; 11:8565 presence of elevated humidity and tempera- (92.8-95.21%) as compared to the other 12 doi:10.4081/mr.2020.8565 antibiotics. Moreover, antibacterial activity ture. It is commonly known as swimmer’s of cerumen was also assessed against test ear, though anything that disrupts this protective lipid layer can lead to the introduction fied the Microbacterium species organisms and its maximum activity was 13 observed against Pseudomonas spp., (90% and proliferation of bacteria. Trauma from (Microbacterium otitidis and equivalent to Clindamycin potency) and cleaning the ears with fingernails or cotton Microbacterium alconae) as key pathogens buds has been identified as the most common 17 Staphylococcus spp., (60% equivalent to in acute otitis externa. The present research predisposing factor locally.14 Moreover, the Amoxicillin potency) while least effective study was designed to isolate and identify two most common bacterial species isolated against E. coli (36%) and ProteusNon-commercial spp., use pathogeniconly bacteria from the infected ear pus from the external auditory canal of normal (22%). Thus, it was concluded that the anti- clinical samples and then, to estimate the individuals are the Staphylococcus species bacterial activity of cerumen might be due antimicrobial activity of cerumen and antibi- (Staphylococcus auricularis, Staphylococcus to the presence of potential chemicals i.e. otics against the isolated pathogenic bacteria. epidermidis, Staphylococcus aureus and flavonoids and terpenoids. Staphylococcus capitis) and the Corynebacterium species (Turicella otitidis Materials and Methods and Corynebacterium auris). The third most Introduction frequently recovered bacteria are the Sample collection Earwax (cerumen) is a grey brown or Streptococci and Enterococci. Together, they A total of 50 ear pus samples were collect- yellowish waxy substance secreted in the account for more than 90% of the normal ed from infected patients admitted in tertiary outer one third of ear canal and, is a protec- flora in the external auditory canal.14,15 care hospital at district Peshawar, KPK, tive barrier between the external environment Pseudomonas aeruginosa, S. epidermidis Pakistan, using sterile swabs under proper and deep external auditory canal.1 Chemical and S. aureus are the most common patho- hygienic conditions. The samples were labeled composition of earwax includes 60% desqua- genic bacteria isolated in acute diffuse otitis bearing the person code, age, sex and date. mated, 12-20% saturated and unsaturated externa locally.16 Doree and Burton,17 stud- Collected samples were suitably diluted and fatty acid and 6-10% cholesterol.2-5 It is a ied 2039 subjects with acute otitis externa were streaked on nutrient media. After incuba- secretion of specialized sets of glands, like and isolated similar bacterial species. tion, these were subjected for isolation of path- sebaceous glands that secrete sebum (combi- Further, the same research group also identi- ogenic bacteria using standard technique.

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Cerumen collection Flavonoid determination sion method. Nutrient agar plates were pre- Earwax or cerumen samples were col- About 2-3 ml of aqueous extract of ceru- pared and approximately, 50 µl inoculum of lected from both male and female healthy men was taken in labelled test tubes and then every selected pathogenic bacterial specimen persons of approximately same age groups, 2% NaOH was added to it drop by drop. were homogeneously spreaded on specified using sterile ear buds and the amount of ceru- After this, concentrated HCl was added to the plates with the help of glass spreader. After men was measured in milligram (mg). Then solution. If color of the solution was disap- the period of five minutes, three wells of the samples were pooled and dissolved in pearing after addition of HCl, then it indicat- about 8 mm diameter were bored in the 18 sodium bicarbonate-glycerol buffer (pH 8.2) ed the presence of flavonoids. media plates, one well was used for positive at 1-5% concentration. control (antibiotic), one well was used for Phenolic compounds determination negative control (distilled water) while the Isolation and identification Aqueous extract of cerumen was used for remaining one was used for earwax extract. determination of phenolic compounds The equal volume (50 µL) of controls as well of pathogenic bacteria through Ferric chloride test. Almost 1 ml of as extract were poured into these wells. The Isolation and identification of pathogenic aqueous extract was mixed with 2 ml dis- plates were incubated for 24 h at 37°C. After bacteria from the collected samples were car- tilled water and only a few drops of 10% incubation, zones of inhibition were meas- ried out using standard bacteriological proce- Ferric chloride was added to it. If blue and ured in millimeter (mm) to evaluate the dures i.e. cultural characteristics, microscopy green color appeared after addition of Ferric potency of earwax extract against test patho- and different biochemical tests (catalase, oxi- chloride, then it is indication of the presence genic bacterial specimens. dase, urease, indole, coagulase and triple of phenolic compounds and if there was no sugar iron tests) according to the Berges th coloration then the test was considered as Manual of Determinative Bacteriology 9 negative for phenolic compounds.18 Results Edition. Terpenoids determination Bacteriological analysis of ear pus Antibiotic susceptibility assay Aqueous extract of cerumen was used for samples and prevalence of isolated Antibiotic susceptibility assay was per- the existence of terpenoids through bacteria formed according to Kirby-Bauer disc diffu- Salkowski test. About 2 ml of chloroform Inonly the present study, 50 ear pus samples sion assay in order to determine the efficacy of was mixed thoroughly with the sample were screened for the presence of various narrow and broad-spectrum antibiotics. extract solution and then 3 ml of concentrated bacterial pathogens and 4 different pathogen- Antibiotic selection was based on standard sulfuric acid was in safety mixed to form a ic bacterial isolates i.e. Pseudomonas spp., guidelines and 5 different commercially avail- layer. The presence of terpenoids was shownuseStaphylococcus spp., E. coli and Proteus able antibiotics disc i.e. Amoxicillin, by the appearance of reddish brown col- spp., were identified and characterized by Ampicillin, Ciprofloxacin, Clindamycin and oration of the border.18 pure culturing technique as shown in Table 1. Gentamycin were used in the present study While, the data regarding the prevalence of against test organisms. In antibiotic sensitivity Determination of antibacterial activi- various bacterial species is shown in Figure assay, Mueller-Hinton agar plates were pre- ty of cerumen (earwax) 1. Among the isolates, n = 29 (58%) were pared by spreading 0.1 ml of diluted inoculum The antibacterial activity of cerumen Pseudomonas spp., which was the most of each test bacterial isolate over media sur- extracts against pathogenic bacterial isolates prevalent bacterial species while, n = 11 face. After spreading, was allowed to dry for 5 were evaluated by utilizing agar well diffu- (22%) samples were Staphylococcus spp., min and then with the help of sterilized for- ceps, antibiotic discs were placed gently on the surface of bacterial lawn at equal distance. The plates were then incubated at 37ºC for 24 h, after incubation the antibiotics sensitive bacteria have made clear rings or zone of inhibition around the discs, which was then measured in millimeter (mm) to evaluate the in vitroNon-commercialpoten- use only cy of antibiotics against test organisms.

Qualitative analysis of chemical constituents of cerumen (earwax) Cerumen was analyzed for different chemical constituents such as flavonoids, terpenoids and phenolic compounds using stan- Figure 1. Percentage distribution of isolated bacteria in ear pus samples (n = 50). dard procedure as described below.

Table 1. Bacteriological analysis of ear pus samples. Isolates Gram’s Reaction Catalase Oxidase Coagulase Urease Indole TSI test Identified Organisms 1 - + + - - - NC Pseudomonas spp. 2 + + - + + - K/A, AG Staphylococcus spp. 3 - + - - - + K/A, AG E. coli 4 - + - - + - NC Proteus spp. AG = Acid and gas; + = Positive; = Negative; A = Acid production; K = alkaline reaction; NC = No change; reduction; K/A = Red/yellow; K/NC = Red/no color change.

[page 6] [Microbiology Research 2020; 11:8565] Article and n = 7 (14%) for E. coli. The least prevalent bacterial species detected was Proteus which was found to be 6% (n = 3).

Antibiotics susceptibility profile of isolated bacteria The antibiotics susceptibility profile of isolated bacterial species was drawn by using agar disc diffusion method while percent value was calculated using CLSI zone of inhibition as standard values.19 The results regarding the antibiotic susceptibility profile of Pseudomonas spp., against the antibiotics used is shown in Figure 2. Antibiotics susceptibility profile against Pseudomonas spp. Figure 2. The data suggested that Pseudomonas spp. was most sensitive to Clindamycin (94.73%) followed by Amoxicillin (82.2%), Gentamycin (76.47%) while has shown resistance to Ciprofloxacin and Ampicillin, where the potency was 33.28 and 40% respectively. The results regarding the antibiotic susceptibility profile of Staphylococcus spp., against the antibiotics used is shown in Figure 3. According to results, only Staphylococcus spp., was most sensitive to Clindamycin (94.73%) followed by Gentamycin (94.44%), Amoxicillin (55.55%) while resistant to Ciprofloxacin and Ampicillin, and have shown potency use Figure 3. Antibiotics susceptibility profile against Staphylococcus spp. of 31.4 and 43.3% respectively. The results regarding the antibiotic susceptibility profile of the tested antibiotics against E. coli is shown in Figure 4. It was observed that E. coli was most sensitive to Ciprofloxacin (95.21%) followed by Clindamycin (94.11%) and Amoxicillin (92.85%) while displayed resistant to Gentamycin and Ampicillin, where the potency was 33.3 and 46.6% respectively. The results regarding the antibiotic susceptibility profile of the tested antibiotics against Proteus spp., is shown in Figure 5. According to results, Proteus spp., was most sensitive to Ciprofloxacin (92.85%) followed by ClindamycinNon-commercial use only (92.11%) and Gentamycin (83.28%) while Figure 4. Antibiotics susceptibility profile against E. coli. displayed resistant to Amoxicillin and Ampicillin, and demonstrated efficacy of 54.7 and 66.6% respectively.

Qualitative analysis of chemical constituents of cerumen (earwax) Aqueous extract of cerumen was tested for qualitative analysis of chemical constituents including flavonoids, phenolic compounds and terpenoids using standard procedure and results are shown in Table 2. It was observed that aqueous extract of cerumen have contained different chemicals i.e. flavonoids and terpenoids while, phenolic compounds were absent in the extract. Figure 5. Antibiotics susceptibility profile against Proteus spp.

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Determination of antibacterial activ- also conducted similar studies and identi- all these complications could be minimized ity of cerumen (earwax) fied different pathogenic bacteria from the up to some extent by maintaining hygienic Table 3 depicted that cerumen displayed ear pus using conventional culturing tech- condition in daily life. maximum zone of inhibition against nique and concluded that P. aeruginosa was Efficacy of antimicrobial properties of 11,20 Pseudomonas and Staphylococcus spp., the most widely recognized bacteria. human earwax has been a subject of debate 24 while it was less effective against E. coli The antibiotics susceptibility profile for for different researchers since many years. and Proteus spp. In addition to this, Table 3 isolated bacterial species were drawn by Researchers believed that absence of ear- also illustrates the bactericidal effect of using agar disc diffusion method while per- wax mediates an alkaline environment cerumen against test organisms. Where as cent value was calculated using CLSI stan- which promotes growth of different 19 90% bactericidal activity was observed dard values. In the present study, 5 differ- microbes within ear and hence resulted into 21,25 against Pseudomonas spp., followed by ent commercially available antibiotics were different infections. In fact, earwax has 60% against Staphylococcus spp., 36% evaluated for antimicrobial activity against been shown to have significant antibacterial 26 against E. coli and 22% against Proteus spp. the prevailing bacterial isolates with the aim and anti-fungal properties. Earwax is a to be used for the prevention of different grey brown or yellowish waxy substance clinical complications. The results of the secreted in the outer one third of ear canal. experiments revealed that Pseudomonas It is a protective barrier between the exter- Discussion and Staphylococcus spp., were most sensi- nal environment and deep external auditory tive to Clindamycin, Amoxicillin and canal.1 Table 3 depicted that cerumen dis- The pathogens present in ear pus sam- Gentamycin while these displayed resistant played maximum zone of inhibition against ples pose a serious threat of infections to Ciprofloxacin and Ampicillin. Devi et Pseudomonas and Staphylococcus spp., which may leads to some acute and chronic al.21 also conducted similar study and found while it was less effective against E. coli infectious diseases if proper care is not that Clindamycin, Amoxicillin and and Proteus spp. 3 taken. The use of antibiotics to stop and Gentamycin were more effective antibiotic The current research investigation cure the infections in ear is the major mean against both Gram-positive and Gram-nega- demonstrated that cerumen has antibacterial 10 in modern medicinal practices. The pres- tive bacteria isolated from the infected ear properties, which played significant role in ent research study was focused on isolation pus samples. However, in the present study, the protectiononly of the external auditory canal. and identification of pathogenic bacteria E. coli and Protues spp., were most sensi- Interestingly, Schwaab et al.27 proved that from infected ear pus samples and then to tive to Clindamycin, Amoxicillin and cerumen of some mammals possess anti- determine the activity of commercially Ciprofloxacin while these bacteria dis- Staphylococcal and anti-Micrococcal activ- available antibiotics and earwax against iso- played resistant to Amoxicillin use and ities. In the current study, it was observed lated bacteria. Herein, 50 ear pus samples Gentamycin. Similar results were also that for Pseudomonas spp., cerumen were collected from infected patients at dis- reported by Vaghela et al..22 A possible rea- showed 90% of activity, which was equiva- trict Peshawar, Pakistan using sterile swabs son for antibiotic resistance might be irra- lent to Clindamycin (94% effect), for under proper hygienic conditions. Samples tional use of antibiotics therefore, it was Staphylococcus spp., cerumen showed 60% were then processed and different bacterial suggested that antibiotics must be used after of activity, which was approximately equiv- isolates were identified through pure cultur- performing susceptibility test and by doing alent to Amoxicillin (56% effect), for E. coli ing technique. Isolated bacteria were identi- this, the phenomenon of antibiotic resist- cerumen showed 36% of activity, which fied according to Bergey’s Manual of ance might be reduced to greater extent. was equivalent to Gentamycin (33%) while th Determinative Bacteriology (9 Edition). Furthermore, Magnet et al.23 also described Proteus spp., displayed resistant pattern On the basis of microscopic and biochemi- that genetic variation among bacterial iso- against cerumen (22% of activity). Our cal analyses, 04 different bacterial isolates lates was the most significant reason for findings on the bactericidal effect of ceru- were identified, out of which one was Gram antibiotic resistance and also suggested that men on Pseudomonas were in alignment positive (Staphylococcus spp.,) while three were Gram negative (Pseudomonas spp., E. coli and Proteus spp.,). Further, the data regarding the prevalence of various bacteri- Table 2. Qualitative analysis of chemical constituents of cerumen (earwax) al species depicted that PseudomonasNon-commercial spp., use only were 58% (n = 29) among isolated bacteria Components Aqueous Extract Cerumen (Earwax) followed by Staphylococcus spp., (22%, n = Flavonoids +++ 11)), E. coli (14%, n = 7) and Proteus spp., Phenolic compounds - (6%, n = 3). Microbial infection in ear might be due to maintaining sub-standard Terpenoids ++ hygienic conditions. Different researchers - = absent; + = little bit color; ++ = Intermediate; +++ =Strong

Table 3. Bactericidal activity of cerumen (earwax) against test organisms. Bacterial Isolate Conc. of cerumen Diameter of disc (D) Diameter of zone (d) Zone of inhibition Potency % (%) (mm) (mm) (ZI = D-d) Pseudomonas spp. 3 8 32 24 90 Staphylococcus spp. 3 8 24 16 60 E. coli 3 8 14 6 36 Proteus spp. 3 8 12 4 22

[page 8] [Microbiology Research 2020; 11:8565] Article with the findings of Swain et al..28 wax is leading to earache or conductive al. Seasonal variation of Pseudomonas However, some researchers found insignifi- hearing loss. Furthermore, proper care and aeruginosa in culture positive otitis cant bactericidal effect and stated that preventive measures should be taken for externa in South East Pseudomonas was not a normal commensal patients with ear infections in order to min- England. Epidemiol Infect 2018;146: of the ear canal, and thus might not be rec- imize the chances of infections. 1811-2. ognized by the immune system of the ear 14. Nagaraj G, Girdhar A, Chinnappa J, et canal.29,30 Yang et al.31 reported inconsis- al. Bacterial Profile of Middle Ear Fluid tent bactericidal activity of cerumen against References with Recurrent Acute Otitis Media S. aureus. Different researchers reported Infection Using Culture Independent 1. Gabriel OT. 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