Microbial Contamination of Cell phones of Nursing Department Students in Technical Institute of Baqubah-Iraq Suhail Jawdat Fadhil Lecturer

Microbial Contamination of Cell phones of Nursing Department Students in Technical Institute of Baqubah-Iraq
Suhail Jawdat Fadhil
Lecturer, Technical Institute of Baqubah , Middle Technical University (MTU), Iraq
Abstract
This study aimed to investigate microbiological colonization of mobile phones used by students of Baqubah Technical Institute during June to August 2018. Out of 150 randomly collected cell phones, there were 133 bacterial isolates and 74 fungal species. Classical techniques were used to identify microbes, bacterial isolation were as follow: Staphylococcus aureus, Staphylococcus epidermidis, Pseudomonas aeruginosa, Bacillus subtilis, Escherichia coli, Streptococcus viridians and Proteus spp. at rate of 48, 25.2, 14.1, 7, 2.3, 2, 1.2 % respectively. Fungal growth was performed by mostly Cladosporium spp. and Alternaria spp. 36.1, 32% other species included Penicillium, Aspergillus fumigates and Aspergillus niger at rate of, 17, 9 and 6.3 %. Bacterial isolates were tested by antibiotic disks, generally they showed no resistance in high percentage for erythromycin, cefoxitin, ciprofloxacin and clindamycin, otherwise, a number of S.aureus and S.epidermides isolates were resistant to erythromycin and cefoxitin, on the other hand Proteus spp. and E.coli isolates were highly sensetive to Ampicilin, amikacin, cefepime, cefroxain and imipenem while P.aeroginose appear in two patterns for the same antibiotics. The outcome of this study indicates that mobile phones act as an important source of pathogenic organisms for human and can serve as vehicle for cross-transmission of these microorganisms.
Keywords : Cell phones; Microbial contamination; Nursing students; fungal species; Staphylococcus aureus
Introduction :
A mobile phones is an essential electronic device for personal telecommunication in daily life, and they are commonly used almost everywhere and usually kept in close contact with the human body. In many countries, mobile phones outnumber landline telephones since most adults and many teenagers now own mobile phones. At present, middle east countries have the fastest growth rate of cellular phone subscribers in the world (Ibrahim et al.,2014). This constant handling of the phone by different users exposes it to an array of microorganisms, and makes it a good carrier for microbes, especially those associated with the skin leading to the spread of different microorganisms from user to user (Al-Abdalall and Amira.,2014).

The problem are aggravated from the fact that many mobile users do not have regard for their personal hygiene (Roy et al.,2013). A constant handling of the phone by users in all places and occasions makes it open for arrays of microorganisms, It can harbour various potential pathogens of zoonotic importance and become a source of infection and a potential health hazard for self and family members (Gurang et al., 2008) .

The use of mobile phones by teachers and lectures may serve as a potential vehicle for the spread of pathogenic microorganisms (Ibrahim et al.,2014 ; Brady et al., 2006). Numerous genera and species of bacteria, including Staphylococcus aureus, Escherichia coli, Klebsiella spp, Enterococcus spp and Proteus spp are noted as etiologic pathogenic agents. In addition the normal Microbiota is harmless and may be beneficial in their normal location in the host but it can also produce disease if introduced into foreign locations or a compromise host (Roy et al.,2013; Amadi et al., 2013).Fungal species like Trichophyton mentagrophytes, Aspergillus niger, Pencillium sp. have the ability to grow on cell phones when exposed to mobile waves for 20 minutes (Fawole and Ose,2001).
Hand washing may not usually be performed often enough thus, many people may use personal mobiles phone in the course of a working day. Hence the potential act of mobile phones as a source of microbial transmission is considerable (Ibrahim et al.,2014; Suganya and Sumathy,2012).
Over the last decade the use of mobile has increased rapidly from being rare and expensive pieces of equipment used primarily by the business elite, to a common low-cost personal item. Microbiologists say that the combination of constant handling with the heat generated by the phones creates a prime breeding ground for many microorganisms that are normally found on the skin and also may be resistant to some antibiotics(Dave and Shende,2015; Zakai et al.,2016).

This research investigates microbial contamination of mobile phones used by Nursing department students in Baqubah Technical institute and identifies the microbes regularly associated with mobile phones and also studies the sensitivity of bacterial isolates to some antibiotics.
Material and methods :
Study design:
This study was performed during summer training at health centers from the period June to August 2018, at the laboratory of Medical Microbiology, Baqubah institute, Middle Technical University (MTU), Diyala, Iraq. A total of 150 randomly collected cell phones of 2nd-year Nursing department students were examined by taking swabs for isolation of bacteria and fungi.

The samples were collected from the mobile phones with sterile cotton swab sticks. these sticks were dipped in sterile saline and subsequently rubbed on both surfaces of mobile phones. Two swabs from each mobile were separately inoculated into tubes containing 3 ml Luria – Bertani broth (LB broth) and tube containing Sabouraud dextrose broth.

Bacterial Isolation:
After an overnight incubation of swabs in LB broth, streaking on to blood agar, MacConkey’s agar were carried out. Plates were incubated aerobically at 37°C for 24 hrs. Isolated organisms were processed according to colony morphology and gram stain. Organisms were identified according to standard protocol and observed for growth and colonial description of the isolates (Roy et al.,2013; Arora et al.,2009). Mobility tests, biochemical tests and Microorganisms plates were identified grown on with conventional techniques. A slide coagulase test ( Microgen Staph, Microgen Bioproducts, Camberley, UK ) was used to differentiate Staphylococcus aureus from other coagulase-negative Staphylococci (Zakai et al.,2016; Brooks et al.,2013).

Biochemical Analysis :
Following purification, single colonies were subjected to gram staining and biochemical tests, namely, carbohydrate fermentation test, IMViC tests (Indole test, Methyl Red test, Voges Proskauer test and Citrate test), mannitol motility test, growth in triple sugar iron agar (TSI), nitrate reduction test and urease test according to standard procedures. (Brooks et al.,2013; Kuma and Aswathy,2014).

Antibiotic susceptibility test :
The bacterial inoculum was prepared and the turbidity adjusted to that of 0.5 McFarland by the technique of Kirby-Bauer disk diffusion method according to the NCCLs recommendation M100 – S25 (2015). Briefly, the adjusting suspension wasstreaked by the swab over the Muller – Hinton agar surface (Shahlol et al.,2015). Commercially available antibiotic disks were used for antibiotics susceptibility testing. In these tests antibiotics dispensed onto the surface of the inoculated agar. All the plates were incubated at 35C° for 18 hours. The zones of inhibitions were measured and interpreted according to the Clinical and Laboratory Standards Institute (Wayne,2011).The following antibiotic discs with concentration of the drug: Tetracycline, erythromycin, cefoxitin, cipro?oxacin and clindamycin for Gram positive bacteria, ampicillin, amikacin, cefepime, ceftriaxone and imipenem for Gram negative bacteria were used (Zakai et al.,2016; Julian et al.,2012).

Fungal Isolation :
After incubation for 24 hrs at room temperature, swabs were streaked on the Sabouraud dextrose agar and potato dextrose agar, The samples were cultured for the growth of isolated colonies on potato dextrose agar. Then the plates were incubated at 37 °C for 24 hrs, the colonies grown on two media were examined for their morphology and staining. The isolated fungal species further identified and characterized by using standard microbiology method (Kampf and Kramer,2004).

Results and Dissection :
Mobile phones as inanimate objects have been shown to posses the potential for the survival of microorganisms. Some bacteria can survive for months, viruses such as corona, coxackie, influenza can persist for few days; and herpes virus can persist for a week (Kampf and Kramer,2004). Many studies conducted around the world show that there is a high prevalence of microbial contamination in cell phones (Karabay et al.,2007).
Table -1- Grouping of microbial contamination of cell phones.
No. of isolated Microorganisms Bacteria Fungal
No. % No. %
No contamination 17 11.3 76 28
1 type 33 22 24 17.3
2type 47 31.3 33 30
3 or more 53 35.3 17 24.7
The results in table (1) referred to the highest rate which belongs to cell phone contaminated with 3 or more types of bacteria (35,5%), while the non contaminated cell phone recorded as lowest rate (11,3%). These results approximate Chawla et al with his findings which included a number of cell phones that showed no growth of bacteria, the contaminated phones with 2 types of bacteria reported as the highest rate (Chawla et al.,2009). Cell phones which show no fungal growth recorded the highest rate 76%, while those that appear in the lowest rate 17% show growing of 3 or more fungal types. Many studies conducted around the world refers to high prevalence of microbial contamination in cell phones (Karabay et al.,2007).
The rate and number of isolated bacterial types (spp.) were summarized in table (2)
Staphylococcus aureus and Staphylococcus epidermidis were the predominant bacteria in rate of 48% and 25.5%. These results were parallel with Akinyemi et al(Akinyemi et al.,2009) and with Datta et al(Datta et al.,2009) in their study reporting that coagulase-negative staphylococci were the most prevalent bacterial agents isolated from mobile phones, followed by Staphylococcus aureus (Chawla et al.,2009) in which S.aures were the predominant bacterial spp. In rate of (48%), among other species including 7 types of bacteria were isolated from totally 150 cell phones which are in accordance with frequency as follows: Staphylococcus epidermidis 25,2%, Pseudomonas aeruginosa 14.1%, Bacillus subtilis 7%, Escherichia. coli 2.3%, Streptococcus viridians 2% and Proteus spp 1.2% sequently .

Staphylococcus aureus is carried by healthy people on the skin and nose. It can cause mild to serious infections if it enters the body through cuts, wounds, etc(Angadi et al.,2014). The main reservoir of S. aureus is the hand from where it is introduced into food during preparation (Suganya and Sumathy,2012 ; Morubagal et al.,2017).

Cell phones can transfer pathogens like Staphylococcus epidermidis by contacting with other plastic surfaces such as catheters or prostheses, and by this way they let them into the body. Staphylococcus epidermidis is the most prevalent cause of sepsis and of common causes of urinary tract infections(Al-Abdalall and Amira ;Akinyemi et al.,2009 ; Jalalmanesh et al.,2017). Pseudomonas aeruginosa. was observed in rate of (14.1%).This is close to Famurewa and David who observed that 22.6% of the investigated cell phones owned by volunteers in the university premises were contaminated with Pseudomonas aeruginosa (Famurewa and David,2009).
There is always a major concern about the contamination of foodstuff and hospital devices with species of these bacteria (Gurang et al.,2008 ; Julian et al.,2012) since the cell phones can play a role as a vector .The prevalence of other bacterial spp. isolated from student’s cell phones were Bacillus subtilis(7%), Escherichia coli (2.3%), Streptococcus viridance (2%) and the lower percentage (1.2%) was Proteus spp.. Based on previous studies conducted in Iran, the prevalence of bacillus species were 60% and 26.3%, respectively(Karabay et al.,2007;Jalalmanesh et al.,2017). Our results do not agree with another study performed by Sedihgi et al. isolates Bacillus spp. By about (0.8%) from the cell phone of Health Care Providers in a Teaching Hospital in Hamadan Province, Iran (Sedighi et al.,2015).

Escherichia .coli, streptococcus viridians and Proteus spp were isolated by a small percentage compared with other isolates mentioned. Presence of E. coli signifies fecal contamination of hands through bed pans or poor personal hygiene (Amadi et al.,2013) . TA et al observed that 9.77% of examined cell phones were contaminated with E.coli and Proteus spp. in a rate of (7.47%) with many other bacterial species in different rates (Ibrahim et al.,2014). The results were also close the findings of Zakai et al. in regards to total isolation of bacteria which was about (20%) (Zakai et al.,2016).

Table -2- Bacterial species isolates from cell phones :
Bacterial isolates No. %
Staphylococcus aureus 264 48
Staphylococcus epidermidis 137 25.2
Pseudomonas aeruginosa 77 14.1
Bacillus subtilis 36 7
Escherichia .coli
13 2.3
streptococcus viridians 9 2
Proteus spp 7 1.2

Table -3- Fungal species isolates from phones :
Fungal isolates No. %
Cladosporium spp 17 36.1
Alternaria sps 15 32
Penicillium 8 17
Aspergillus fumigatus 4 9
Aspergillus niger 3 6.3
Cell phones are likely to be a soruce of microbial transmission, inculding human pathogens and that increase the incidence for bacterial and fungal infections. Recently many rersearches conducted the bacteriological and fungal contamination of mobile phone surfaces (D?bek et al.,2013) .

Table -3- showed the pathogenic fungi isolated based on mycelia, colour and spores from swabs taken from the cell mobile device with different values started from Cladosporium sps at a higher rate (36.1%) to Aspergillus niger which was in the lowsr prsentage (6.3%). Many of recent studies about microbial contamination of cell phones have confirmed a high mycotic contamination degree with species of Aspergillus and Penicillium (D?bek et al.,2013) .

Present research also is in parallel with Coutino et al. who analyzed the incidence of fungal contamination of mobiles in high level when he isolate 34 species of fungal from public telephones in Brazil (Coutinho et al.,2007).

These isolates can significantly in?uence food spoilage and food infection through theproduction of toxins. Filamentous fungi, have strong allergenic properties, and can induce dermal mycoses which is considered as opportunistic human pathogens (D?bek et al.,2013) . The results are consistent with isolation of cladosporium spp. In a rate of 20.9% and Aspergillus fumigates at a rate 2.3% among fungal isolates including Aspergillus .niger 20.7%, and other pathogenic species from mobile phones in eastern Saudi Arabia (Al-Abdalall and Amira,2010) .

Sweta Dave and Dr. Kishor Shende pointed out to the isolation of a group of pathogenic fungi in similar proportion to the same rates obtained by us but differ with the isolation rate of Aspergillus. niger (32.0%) which was reported as a high percentage (Dave and Shende,2015) .

Table – 4- Antibiotic sensitivity pattern of Gram-positive bacteria isolated :
Antibiotics Bacteria
S.aureus S.epidermidis Bacillus subtilis s.viridians
S R S R S R S R
TE 232 32 95 42 26 10 7 2
E 193 71 83 54 21 15 5 4
CX 213 51 76 61 17 19 9 –
CIP 231 33 104 33 27 9 6 3
CD 217 47 97 40 29 7 8 1
TE: tetracycline ; E: erythromycin; CX: cefoxitin ; CIP: cipro?oxacin; CD: clindamycin
Table – 5- Antibiotic sensitivity pattern of Gram-negative bacteria isolated :
Antibiotics Bacteria
P. aeruginosa E. coli Proteus spp
S R S R S R
A 49 28 10 3 6 1
AK 46 31 12 1 7 –
CPM 32 45 13 – 5 2
CTR 55 22 9 4 6 1
IPM 37 40 13 – 7 –
A: ampicillin ; AK: amikacin; CPM: cefepime; CTR: ceftriaxone; IPM: imipenem
The sensitivity tests for bacterial isolates were presented according to Gram positive and Gram negative in table 4 and 5 respectively. Generally antibiotic sensitivity test results revealed that all bacterial strains were sensitive to the studies antibiotics but at different rates.

Most of S.aureus, S.epidermidis, Bacillus subtilis and s.viridians isolates were sensitive to tetracycline, erythromycin, cefoxitin, cipro?oxacin and clindamycin. P. aeruginosa, E. coli and Proteus spp were moderately sensitive to the following antibiotics ampicillin, amikacin, cefepime, ceftriaxone and imipenem. Proteus spp didn’t show any resistance to amikacin and imipenem same as E. coli to cefepime and was to imipenem .This agree with Saha Roy et al. findings according to E. coli and Proteus spp isolates that showed highly sensitivity to Ciprofloxacin, Erythromycin, Amikacin.
There is an increase in the use of mobile devices without awareness of the risks that it may cause, especially the contamination of these devices with microbes may lead to serious health problems especially when it used without caring heygin precautions (Martínez et al.,2017).
Recent research included contamination of 133 out of 150 mobile devices with bacterial and among of 150 total examined cell phones only 74 devices were contaminated with fungal spp. The ability of pathogens to survive on the surface of cell phones, survival time, and the risk of transmitting of these pathogens to from patients should be taken into account the minimum risk. This study aimed to isolate and identify microorganisms and create awareness that mobile could also serve as a vector for transfer pathogenic agents from one individual to another, and causes of infections Therefore it’s important to take care of personal hygiene and mobile decontaminations be eradicated or reduced by regular cleaning of the phones with alcohol or methylated spirit.

Conclusion :
This study revealed that there is colonization of pathogenic bacteria and fungal agents on the mobile phones, in which it may act as disease – producing and help in transforming microbes among the students of 2-nd year Nursing department especially when they start training in health center during summer. These contaminated phones alsomay play an important role in the spreading of drug-resistant bacterial isolates. In order to reduce this potential risk, everyone should have an education about hygiene, comprehensive guidelines and strict hand wash. Also regular decontamination of mobile phones by appropriate cleaning of these device.

Conflict of interests :
The authors have not declared any conflict of interests.

Acknowledgements :
The author would like to thank the Middle Technical University / Technical Institute in Baquba and Al Tahrir Health center for offering critical administrative support in performing this study, also the author wishes to thank Ph. Dr. Israa Ibrahim Khalil especially for her financial support in microbial identification.