Bioscience Biotechnology Research Communications

An Open Access International Journal

P-ISSN: 0974-6455 E-ISSN: 2321-4007

Bioscience Biotechnology Research Communications

An Open Access International Journal

Mohammad Zobaidul Alam* and Syeda Miskat Mantasha

Department of Microbiology, Faculty of Biological Sciences,
University of Chittagong, Chattogram, Bangladesh

Corresponding author email: zobaid@cu.ac.bd

DOI:

Article Publishing History

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Accepted After Revision:

ABSTRACT:

Mobile phone is an essential part of everyday life in modern days. Mobile phones act as vehicles for transmitting pathogenic bacteria due to lack of awareness and widespread use. This study aimed to investigate the bacterial contamination of mobile phones of different categories people at Chattogram city, Bangladesh.  During the present study, 40 swab samples were collected from the mobile phones of students, businessmen, fishermen, and hospital patients for the isolation, identification of mobile phone associated bacteria, and their antibiogram. In our study, total viable count (TVC) was performed by the pour plate method and total coliform count (TCC) by the most probable number (MPN) method. Besides these, five selective media were used to isolate pathogenic bacteria from mobile phones and then identified. Antibiotic sensitivity assay was performed by disc diffusion method with 10 different antibiotics. Mobile phones of hospital patients (20165 cfu/ml) and students (1578 cfu/ml) showed the highest and lowest TVC respectively.

Coliform bacteria were detected from the mobile phones of 100% hospital patients, 90% from both businessmen, and fishermen but only 30% from students. Klebsiella pneumoniae and Pseudomonas aeruginosa were found the most prevalent bacteria but Staphylococcus aureus, Staphylococcus epidermidis, Micrococcus sp., Bacillus sp., E. coli, Salmonella sp., Citrobacter sp., Serratia sp., Proteus sp., and Enterobacter sp. were also detected. Almost all the isolates were highly resistant to ampicillin, amoxicillin, rifampin, erythromycin and sensitive to ciprofloxacin, gentamicin, azithromycin, and tetracycline. Our findings ensure that mobile phones act as an important source of pathogenic organisms for humans and can serve as a vehicle for cross-transmission of microbiota. So, washing hands before and after handling food and also personal hygiene is very important.

KEYWORDS:

Coliform, Klebsiella pneumoniae, Pseudomonas aeruginosa

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INTRODUCTION

A mobile phone is a device that may make and receive calls over a communication system whilst touring a good geographical area. It does so by connecting to a cellular network provided by a portable operator, allowing access to the general public telephone network (Suganya and Sumathy 2012). It’s used for communication by different groups of individuals in every place and situation. A mobile phone can support many additional services like SMS, email, internet, and MMS for sending and receiving photos and videos (Roy et al. 2013).

It may also be used for business purposes, within the medical field, and in online banking and finance. Mobile phone is a potential carrier of a variety of microorganisms (Dave and Shende 2015; Olsen et al. 2020). Research has been shown that mobile phones may well be a health hazard with ten thousand microbes living on each square of the phone (Kilic et al. 2009). People carried their mobile phones in hospitals, toilets, kitchens, etc. as a result they became loaded with thousands of microorganisms (Bhoonderowa et al. 2014; Bhardwaj et al. 2020).

Selected groups of individuals don’t wash their hands after handling fish, meat, and animals as a result contamination of mobile phones occurred. Moreover, mobile phones may be contaminated with E. coli and other enterobacteriaceae by the water used for washing hands (Rather 2009). Human body surface is consistently in contact with environmental microorganisms and becomes readily colonized by certain microbial species (Prescott et al. 2005). Staphylococcus aureus is generally present on the skin and causes illnesses from pimples and boils to pneumonia and meningitis (Roy et al. 2013; Jamalludeen 2020).

Irrational use of antibiotics is one of the most significant factors for the presence of emerging multi-drug resistant microorganisms everywhere. Poor drug quality and inadequate doses are also major reasons for the emergence of multi-drug resistant bacteria especially in developing countries like Bangladesh (Okeke et al. 1999). If this case continues, no dose or levels of antibiotics are going to be effective against bacterial diseases (Debnath et al. 2017). Antibiotic-resistant bacteria led to high morbidity and mortality, long hospital stays, and higher treatment expenses (Olu-Taiwo 2020).

In this research, an attempt was made to detect and characterize mobile phone associated bacterial pathogens among four categories of people living in Chattogram city, Bangladesh using microbiological techniques. Furthermore, the antibiotic susceptibility pattern of the isolated bacteria was also determined.

MATERIAL AND METHODS

The study was carried out in Chattogram city which is a major coastal seaport city and financial center in southeastern Bangladesh. A total of 40 mobile phone samples were collected from 4 categories of people living in Chattogram city such as 10 from students, 10 from fishermen, 10 from hospital patients, and 10 from businessmen. Sterile cotton swab was first moistened with normal saline and scratched over both surfaces of the tested mobile phones. The cotton ends of these swabs were cut off and soaked in 50 ml of sterile peptone water. The sample bottles were preserved in a basket fitted with ice to limit bacterial growth at 4-8oC and were carried to the laboratory for analysis within 4-5 hours of collection and preserved at 4oC until analysis.

Live microbial load on mobile phones can able to estimate by this method and the count represents the number of colony-forming units (cfu/ml) of the sample. TVC was conducted by means of the serial dilution agar plating method (Marzan et al. 2017). In this method, 1 ml of peptone water containing sample was inoculated into 9 ml of distilled water to get 10-1 dilution and then serially made up to 10-6 dilutions. One ml sample from each dilution was dispensed in the sterilized Petri plate and then melted nutrient agar (about 45oC) was poured in each Petri plate, mixed uniformly by rotated clockwise and anti-clockwise, and then allowed to solidify. Then the plates were incubated at 37oC for 24 hours and 30-300 colonies containing plates were only allowed for counting. The TVC was calculated according to the following formula:

cfu/ml= (Number of colonies) / (volume plated × dilution factor)

Total coliform bacteria were analyzed through the MPN technique according to the standard method (Clesceri et al. 1996). This test indicating only the presence of coliforms and not their numerical presentation. It is carried out in three continuous stages: presumptive test, confirmed test, and completed test. For the presumptive test procedure, 3 sets of test tubes containing MacConkey broth are required for each sample under analysis. All the test tubes were incorporated with Durham’s tube for detection of gas formation by Gram-negative coliform bacteria. Test tubes were incubated with half-circled screw caps at 37°C for 48 hours. This procedure was followed for all of the 40 samples individually. For confirm test, brilliant green lactose bile broth was inoculated with samples from the tubes showing a positive result in the presumptive test and incubated for 48 hours at 37oC. During incubation, formation of gas in the tube indicates a positive confirmed test.

A complete test was performed on all samples showing a positive result in the confirmed test. One or more plates of Eosin methylene blue were streaked with the positive sample and incubated for 24 hours at 37°C. After incubation, one or more typical colonies (nucleated, with or without metallic sheen) were transferred to a Lauryl tryptose broth fermentation tube and a nutrient agar slant and incubated at 37°C for 24-48 hours. During incubation, formation of gas in the Durham’s tube and the presence of Gram-negative, non-spore-forming, rod-shaped bacteria in the agar culture were considered a satisfactorily completed test, which ensure the presence of coliform bacteria.

Five selective media were used to check microbial contamination of mobile phones. These were: Eosin Methylene Blue (EMB) agar (E. coli) and other coliform groups of bacteria, Xylose Lysine Deoxycholate (XLD) agar (Salmonella sp.), Salmonella-Shigella (SS) agar (Shigella sp.), Cetrimide agar (Pseudomonas sp.), and Mannitol salt agar (Staphylococcus sp.). The presence of pathogens was examined by streaking of inoculums on selective media from a gas positive sample of MPN. After incubation, the grown colonies on the selective agar media were then transferred to nutrient agar slants and preserved for further microscopic, biochemical characterization, and antimicrobial susceptibility tests.

Susceptibility and resistance of different antibiotics were measured in-vitro by employing the Kirby-Bauer method (Bauer et al. 1996). This method can rapidly determine the efficacy of a drug by measuring the diameter of the zone of inhibition. A suspension of pure bacterial culture was prepared in peptone broth and incubated at 37oC for 24 hours. The broth was spread by sterile cotton swab homogenously on the solidified Mueller-Hinton agar plate. Antibiotic discs were placed aseptically to the surface of the inoculated plates.

The plates were then kept at freeze for 30 minutes and then incubated at 37oC for 24 hours. The used antibiotic discs were: gentamicin (10 µg), azithromycin (15 µg), ciprofloxacin (5 µg), ampicillin (10 µg), tetracycline (30 µg), erythromycin (15 µg), amoxicillin (15 µg), rifampicin (5 µg), chloramphenicol (30 µg), ceftriaxone (30 µg). After incubation, the plates were examined and the diameters of the zone of inhibition were observed.

RESULTS AND DISCUSSION

All the 40 samples were examined randomly and found 100% of mobile phones were contaminated with microbiota. The average cfu/ml was calculated and the highest average cfu/ml was observed in the mobile phones of hospital patients (20,165 cfu/ml) followed by fishermen (18,600 cfu/ml), businessmen (15,870 cfu/ml) and the lowest in students (1578 cfu/ml) mobile phones (Figure 1).This result indicated that students are handled their mobile phones carefully and kept them clean as a result carry comparatively less microorganisms, on the other hand,  hospital patients should aware of the cleanliness of their mobile phones because of the highest TVC found on their mobile phones.

Otherwise, nosocomial infections will be spread by mobile phones. The results are in accordance with other findings who observed that 99% of the phones of healthcare workers were contaminated with pathogenic microorganisms and multi-drug resistant bacteria (Bhat et al. 2011). A study was conducted in Kashmir on which the highest TVC was found in animal handlers and lowest in veterinary surgeon’s mobile phones (Roy et al. 2013; Huffman et al. 2020; Olsen et al. 2020; Simmonds et al. 2020).

Figure 1: Average cfu/ml of mobile phones of different user groups. The presented
values are the mean and standard error of mean. N=40 (10 mobiles for each group).

The total coliform count includes a wide range of aerobic and facultative anaerobic, Gram-negative, non-spore forming bacilli capable of growing in the presence of relatively high concentrations of bile salts with the fermentation of lactose and production of acid within 24 hours at 35-37oC. The presence of coliforms in collected samples indicates that mobile phones were contaminated with pathogenic organisms. These happen because people carry their phones in the toilet, kitchen, etc., and are not aware of the hygienic conditions of mobile phones. Thus, mobile phones become loaded with coliforms and other types of bacteria.

The values for total coliforms ranged from minimum 0 to a maximum of 2400 MPN per 100 ml. In total, 77.5% of mobile phones of four different categories of people were found contaminated with coliform bacteria which indicated the poor hygienic condition of the mobile phones of the study area. These mobile phones can act as a vehicle for the transmission of coliform. Some of these mobile phones can also be a cause of nosocomial infections. 22.5% of mobile phones were not contaminated with coliform which indicates a relatively good hygienic condition of these mobile phones.

Table 1. Results of MPN test for estimation of total coliform count according to WHO guidelines

Mobile phones of different groups Sample No. MPN index /     100 ml Average   (%)        in each groups Mobile    phones of different groups Sample No. MPN index /     100 ml Average (%)     in each groups
MM1 150 MM21 28
MM2 23 MM22 28
MM3 0 MM23 21
MM4 0 MM24 1100
Students MM5 0 30% Businessmen MM25 210 90%
MM6 1100 MM26 460
MM7 0 MM27 23
MM8 0 MM28 93
MM9 0 MM29 20
MM10 0 MM30 0
MM11 >2400 MM31 15
MM12 210 MM32 75
MM13 0 MM33 7
MM14 1100 MM34 7
Fishermen MM15 7 90% Hospital patients MM35 150 100%
MM16 >2400 MM36 460
MM17 120 MM37 210
MM18 64 MM38 150
MM19 460 MM39 15
MM20 150 MM40 460

In our result, the mobile phones collected from students were found less contaminated with coliforms (30%). On the contrary, the highest percentage of coliform contamination (100%) was found among mobile phones of hospital patients and 90% from businessmen and fishermen (Table 1). The presence of Gram-negative rod, Enterobacter aerogens, a number of coliforms, indicates the possibility of the presence of fecal contamination on mobile phones (Dave and Shende 2015). Our data revealed that students are relatively more aware of the maintenance of hygienic conditions of mobile phones and hospital patients should handle their mobile phones carefully (Olsen et al. 2020).

To check the microbial contamination of the mobile samples, contaminating bacteria were identified and confirmed using microscopic, cultural, and biochemical tests (Table 2). After 24 hours of incubation at 37oC, dark colonies with a green metallic sheen and dark colonies without green metallic sheen on EMB agar, colonies that appeared as red or entirely black were on XLD agar, colorless colonies and pink-colored colonies on SS agar, yellow and pink colored colonies on mannitol salt agar plates were picked and purified. The purified isolates were then subjected to Gram staining along with different morphological and biochemical tests to identify the bacterial strain. Comparing with the standard description given in ‘Bergey’s Manual of Determinative Bacteriology’ the bacterial isolates were identified up to species level (Buchanan and Gibbons 1974; Huffman et al. 2020).

From our study, a total of 12 different types of bacteria were isolated from 40 samples collected from students, fishermen, businessmen, hospital patients. We found average percentage of Klebsiella pneumoniae (75%) and Pseudomonas aeruginosa (58%) were the most prominent bacteria from all types of mobiles followed by Micrococcus sp. (35%), Staphylococcus aureus (25%), Salmonella sp. (25%), Bacillus sp. (10%), Proteus sp. (8%), Staphylococcus epidermidis (5%), Serratia sp. (5%), Citrobacter (3%), E. coli (3%), and Enterobacter sp. (3%) (Table 3). The study is in accordance with the findings of others in which S. aureus, P. aeruginosa, E. coli, S. typhi, and S. epidermidis were isolated on mobile phones of healthcare workers in Bangladesh (Debnath et al. 2017).

From the mobile phones of dentists 52.52% Pseudomonas sp. were detected and a higher percentage of Klebsiella sp. was identified from mobile phones of healthcare university students which supports our results. Klebsiella pneumoniae was isolated from all mobile phone handlers with the highest prevalence in fishermen, businessmen, and hospital patients (80%) and lowest in students (60%) (Table 3). Pseudomonas aeruginosa was also isolated from mobile phones of all groups with the highest prevalence in fishermen, businessmen, and hospital patients (60%) and lowest in students (50%) (Lee and Lee 2019; Olu-Taiwo et al. 2021).

Many pathogens particularly P. aeruginosa have been proven to remain viable for months on inanimate surfaces (Kramer et al. 2006). The presence of Pseudomonas sp., K. pneumoniae, and E. coli on mobile phones need serious attention from the public as this organism is associated with hospital infections and may serve as a vehicle for the spread of nosocomial infections. The highest contamination of S. aureus was isolated from hospital patients (50%) and lowest from fishermen (10%) mobile phones.

S. aureus is a normal flora of humans, carried on hands, nose, mouth, skin, clothes, bed linen, and other human environments. In our study, S. epidermidis was only isolated from the mobile phones of fishermen (20%) whereas Serratia sp., Enterobacter sp., Salmonella sp., Proteus sp., Citrobacter sp. and E. coli was completely absent in the mobile phones of students (Melnick and Edward 2004; Karabay et al. 2007; Olu-Taiwo et al. 2021).

Table 2. Microscopic and biochemical properties of the bacteria isolated from drinking
water sample of different schools in Chattogram city, Bangladesh

 

 

Bacterial Isolates

 

 

Shape Gram stain Indole Citrate Catalase  

TSI

 Oxidase    MR    VP  Nitrate R. Urease
Butt Slant H2S Gas
E. coli Rods + + + A A + + + + +
K. pneumoniae Rods + + A A + + + +
P. aeruginosa Rods + + K K + +
S. aureus Cocci + + + A A + + + +
S. epidermidis Cocci +   – + A A + + +
Bacillus sp. Rods + + + NC A + +
Salmonella sp. Rods + + A K + + + +
Proteus sp. Rods + + A K + + + + +
Citrobacter sp. Rods + + A A + + + +
Enterobacter sp. Rods + + A A + + +
Micrococcus sp. Cocci + + NC K + + + +
Serratia sp. Rods + + A K + + +

TSI= Triple sugar iron test, A=Acidic (Yellow), K= Alkaline (Red), NC= No change, MR= Methyl red, VP= Voges-Proskauer,  + = Positive/Present, =Negative/Absent, R= Reductase, KKlebsiella,  SStaphylococcus, P- Pseudomonas, E- Escherichia

Table 3. Comparison of percentages of isolated bacteria among samples collected from
mobile phones of students, fishermen, businessmen, hospital patients

Isolated Bacteria Students (%) Fishermen (%) Businessmen (%) Hospital patients (%) Average (%)
K. pneumoniae 60 80 80 80 75
P. aeruginosa 50 60 60 60 58
S. aureus 20 10 20 50 25
S. epidermidis 0 20 0 0 5
Micrococcus sp. 60 30 40 10 35
Bacillus sp. 10 20 10 0 10
Serratia sp. 0 0 10 10 5
Enterobacter sp. 0 0 10 0 3
Salmonella sp. 0 30 10 60 25
Proteus sp. 0 10 0 20 8
Citrobacter sp 0 10 0 0 3
E. coli 0 0 10 0 3

The presence of E. coli is a direct indicator that other enterobacteriaceae could be carried on mobile phones (Karabay et al. 2007; Tambekar et al. 2008). The highest percentage of Micrococcus sp. (60%) and Salmonella sp. (60%) was isolated from student’s and hospital patient’s mobile phones respectively (Table 3). The observations of the present study coincide with the findings of others (Roy et al. 2013).

The mobile phones of students of Cape Coast University showed high levels of bacterial contamination like Bacillus sp. and Pseudomonas sp. (Tagoe et al. 2011). From the mobile phone of health workers, marketers, food vendors, lecturers, students’ different pathogens like S. aureus, Enterococcus feacalis, P. aeruginosa, E. coli, Klebsiella sp., Serratia sp., Proteus vulgaris, and Bacillus sp. were frequently isolated (Akinyemi et al. 2009; Kilic et al. 2009; Famurewa and David 2009; Al-Abdalall 2010; Singh et al. 2010; Gashaw et al. 2014; Olu-Taiwo et al. 2021).

Antibiotic sensitivity assay of 12 different isolates was performed by disc diffusion method, using 10 different types of antibiotics and the results are presented (Table 4). From the results of the antibiotic sensitivity test, it is observed that most of the organisms were found highly resistant to ampicillin, amoxicillin, erythromycin, and rifampin. On the contrary, most of the organisms were found highly sensitive to ciprofloxacin, gentamicin, azithromycin, and tetracycline (Olu-Taiwo et al. 2021).

Table 4. Antibiotic sensitivity profile of different bacteria from drinking water samples

Bacterial isolates AMP (10µ) AMX (10µ) ERY (15µg) RMP     (5 µg) TET (30µg) CRO (30µg) CAP (30µ) AZM (15µg) CIP  (5µg) GEN   (10µg)
K. pneumoniae R R R R S S S S S S
S. aureus R R I R S I S S S S
P. aeruginosa R R R R R I R S S S
S. epidermidis R R R R I I I I S S
E. coli R R R R S R S S S S
Enterobacter sp. R R R R S I R S S S
Serratia sp. R R R R S R S S S S
Citrobacter sp. S S R R S I I S S S
Micrococcus sp. R R R R I I R I S S
Bacillus sp. R R R R S I I S S S
Salmonella sp R I R R S S S S S S
Proteus sp. S S S S S S S S S S

S-sensitive; R-resistant; I-intermediate; AMX-amoxicillin, AMP –ampicillin, ERY-erythromycin, RMP-rifampin, TET-tetracycline, CRO- ceftriaxon, CAP- chloramphenicol, AZM-azithromycin, CIP -ciprofloxacin, GEN-gentamicin, KKlebsiella, SStaphylococcus, P- Pseudomonas, E- Escherichia

In Bangladesh, for many years antibiotics are randomly used for treatment purposes which are available in any pharmacy. The antibiotic resistance of the isolated bacteria was due to indiscriminate use (misuse, overuse, self-medications) of the antibiotics by people and also due to not completing the dose of antibiotics prescribed by physicians. Thus, resistant strains might be emerged by genetic recombination against one or more antimicrobial agents (Buxton and Fraser 1977). In Kashmir, the majority of the pathogens like E. coli, K. pneumoniae, P. aeruginosa, E. faecalis, and S. aureus had already developed resistance to the most commonly used antibiotics including ampicillin. Multi-drug resistant community-acquired pneumonia and typhoid are common in the valley (Ahmad 2008).

S. aureus, E. coli, and K. pneumoniae was found highly resistant to ampicillin by others which supports our results. Antibiotic drug resistance bacteria may cause high treatment failures, increased healthcare costs, and also increase morbidity and mortality (Brady et al. 2009; Neidell et al. 2012; Olu-Taiwo et al. 2021). So, our results revealed that pathogenic bacteria can harbor on mobile phones and some of the isolated bacteria become multi-drug resistant which will help us to select the most suitable antibiotics to fight against these organisms.

CONCLUSION

The findings of the present study suggests that mobile phones act as a vehicle for transmitting infectious agents. In the collected sample, coliform and other bacteria were highly present in the mobile phones of hospital patients which are alarming for the hospital patients and their visitors. On the contrary, students’ mobile phones were found less contaminated. In all the mobile phones, K. pneumoniae and P. aeruginosa were present with a huge percentage. Most of the organisms were found highly resistant to ampicillin, amoxicillin, erythromycin and rifampin and highly sensitive to ciprofloxacin, gentamicin, azithromycin, and tetracycline. There are no restrictions for using mobile phones, as a result, pathogens carried by mobile phones cause diarrhea, skin infections, pneumonia, and meningitides. So, we should be aware of limiting mobile phone usage as it has a high risk for spreading infectious agents. Mobile phone users should follow and adopt cost-effective and simple hygienic measures for a safe and healthy life.

ACKNOWLEDGEMENTS

This research was financially supported by the Department of Microbiology, University of Chittagong, Bangladesh.

Conflict of interests: Authors declare no conflict of interests to disclose.

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