Risk Factors for Colonization with S.aureus and Methicillin Resistant Staphylococcus aureus Among Health Care Workers in Al-Batool teaching hospital for maternity and children in Diyala, Iraq

Background : Staphylococcus aureus coloniza-tion for the human nose representing a challenge that requires a cope with host defense and competing resident microor-ganisms. Objective: To evaluate the risk factors for in-fection with S. au-reus and MRSA among health care workers (HCWs) in Al-Batool teaching hospital for maternity and children in Diyala, Iraq. Patients and Methods: A total of 27 swabs were taken from HCWs in Al-Batool teaching hospital for ma-ternity and chil-dren in Diyala, Iraq (ATHMC) Standard microbi-ological proce-dures were used for diagnosis of S. aureus and Methicillin Re-sistant Staphylo-coccus aureus (MRSA). Results: Significant corre-lation was report-ed between age and colonization with S. aureus & MRSA. Inverse correlation was reported between education level and colonization with S. aureus and MRSA. Signifi-cant correlation was reported be-tween acne and colonization with S. aureus. Signifi-cant correlation was reported be-tween sinusitis, years of experi-ence, contact with farm animals and colonization with S. aureus and MRSA. Significant correlation was reported between ward of duty and colonization with MRSA. Conclusion: Colonization with S. aureus and MRSA inversely correlated with younger age group, education level of HCWs. Colonization with S. aureus and MRSA correlated with sinusitis, years of experience (5 -6); contact with farm animals. Colonization with S. aureus correlated with acne. Colonization with MRSA correlated with ward of duty at children care floor.


Introduction
The Staphylococcus aureus has a colonization of the human nose represents a challeng-ing impact that requires not only adherence to nasal epithelial cells but also competence to cope with host defense and competing resident microorganisms [1] . The continuous and heavy challenge of community-and hospital-acquired S. aureus infections poses a major threat for public health, mostly in children, pregnant women, and postpartum women [2].
Bloodstream infections with methicillinsusceptible(MSSA) and -resistant S.aureus (MRSA) raise of high-risk in hospitals death because the treatment requires fre-quent and prolonged hospitalization [3].At the same time, the hospital intensive care units represents the main site for MRSA, which is likely to cause and affect an outbreak [4].
S.aureus do not form spores or flagella, has possessed a capsule and produce gold-enyellow pigment, with decomposed mannitol [5] . Furthermore, it has also been found that plasma test coagulase, lactose fermentation, additionally the deoxyribonuclease ac-tivity is positive in S.aureus [6].Most of S.aureus possess alpha-hemolytic activity , forming a perfect transparent hemolytic ring around bacterial colonies, seen on a blood agar [7].
For the species identification, slide and tube coagulase test, and PCR-based tests are uti-lized and molecular methods for the detection of mecA are employed for MRSA [8]. S. aureus invades and adheres to host epithelial cells using a diversity of molecules that are collectively called microbial surface the components recognizing adhesive matrix mole-cules [9].
To evaluate the risk factors for infection with S.aureus and MRSA among health care workers(HCWs) in Al-Batool teaching hospital for maternity and children in Diyala, Iraq, (ATHMC).

Patients and Methods
The study was conducted at Al-Batool teaching Hospital for Maternity and Children (ATHMC), Diyala. The study was performed consistent with local regulations. Informed consent and consistent with the (Declaration of Helsinki) was obtained of the take samples from HCWs . The Clinical Research Ethics Committee approved the study at (ATHMC, Diyala, Iraq.

Study Participants
Current study was conducted, from March to November 2020 . The study included health care workers working in intensive care unit, children's care floor, Preterm care floor at ATHMC, Diyala. Iraq . Clinical and epidemiological data including: age, sex, smoking, using of hand disinfectants , education level , sinusitis , acne, years of experi-ence , ward of duty ,Contact with MRSA carriers, working with ambulant sector outside the work, contact with farm animals.

Study Samples
Nasal, mouth, and skin swabs from health care workers, were collected following a standardized protocol, inserting the swab tip from the places to be sampled and rotating and moving it for (five seconds) in each place.Transport swabs (AFCO, Origen Jordan) were used. The samples were submitted to microbiology laboratory of ATHMC, Diyala, Iraq .Isolation and diagnosis of S. aureus were based on ORIGINAL RESEARCH Published: 30 June 2023 Doi: 10.26505/DJM.24026850816 standard microbiological proce-dures, and methods and other interpretations were in accordance with the EUCAST guidelines [10].

As shown in
Significant difference p value= 0.024) and Inverse correlation (P value= 0.024)was re-ported between age group (22)(23)(24) year of HCWs and colonization with S.aureus.

Sex
As shown in Table (       reported between year of experience (1-2, 3-4) among HCWs in ATHMC and colonization with S.aureus . Significant difference (p value =0.003,) and correlation (p value = 0.003) respectively were reported between year of experience (5-6) among HCWs in ATHMC and colonization with S.aureus . The risk of getting s. aureus colonization was higher among those with (3-4) years of experience (2.5) compared with those of (1-2) years ,( 0.833 ).

Ward of Duty
As shown in Table (

Discussion
In the present study, significant differences and inverse correlations were reported between age group (22)(23)(24) years of health care workers and colonization with S. aureus and MRSA. The main group at risk for getting S. aureus colonization was (22)(23)(24) with (2.159) time compared with the same group of age MRSA colonization was (22)(23)(24), with (2.5) time in ATHMC.
Current results come in accordance with a study achieved among HCWs at Evliya Celebi hospital in Turkey by [14] , and [15,16] in Ethiopia and [17] in Egypt, and [18] in Spain and [19] in Iran , they stated that the age of HCWs play no role in infection with S.aureus or MRSA . Although there are differences in the main group at risk for getting S. aureus and MRSA infection they weren't significant nor had a correlation between the age of HCWs and infection with S. aureus and MRSA .
In current study, no correlation was reported between the sex as a risk factor for HCWs and colonization with S. aureus and MRSA for ATHMC which come in line with [21]in Iran, [22] in Nepal and [15] in Ethiopia , [18] in Spain [ ‫و‬ 17 ] in Egypt and [23] in Oman.
In current study ,S. aureus was detected mainly among females HCWs, (11.11%), and males, (7.40%) while MRSA was detected among females HCWs, (7.40%) compared with (3.70%) for males. These results come in accordance with that reported in Brazil by, [20], who reported that S.aureus was isolated from (26.5%) of females HCWs ver-sus(22.2%) for males HCWs without significant correlation between the sex of ORIGINAL HCWs and MRSA . Similar conclusion was recorded by [19] from Iran. Current results come in contrary with several studies around the world such as [22] who stated that colonization of MRSA was high among males (8.7%) than in females (4.3%) (p >0.05). Accordingly [24], reported higher MRSA colonization in males (7.2%) in comparison to females (5.8%) in Argentina , while [25] from Nepal ,reported that colonization was higher in fe-males (8.3%) in comparison to males (5.1%). The risk of getting S. aureus colonization among females HCWs in ATHMC was (1.061) versus (0.909) for males HCWs which come in agreement with [26] who stated that the risk of colonization of S.aureus was more frequent among males HCWs working at chil-dren hospitals in Bangladesh". "The risk of getting MRSA colonization among males HCWs in ATHMC (1.125) compared with (0.938) for females HCWs.
A study achieved by [14],in Turkey come agreement with current result. In Azadi teaching hospital in Kirkuk city\Iraq, [27] stated that the prevalence of S.aureus was higher in males (52.4%), versus (47.6%) for females on the other hand the prevalence of MRSA infection was (1.6%) for males versus for (1.2%) females including HCWs. While in current study MRSA was detected among females HCWs, (7.40%) versus (3.70%) for males . Here the variation may have attributed to the differences in the samples size and demographic distribution beside the quality of collected samples and differences in the quality of hospital environment as well as in the microbiological procedures that used for diagnosis and differences in the infection control measures in different countries . On the other hand [15,16,22] stated that ,sex play no role as risk factor for carriage rate of MRSA.
In the present study, S.aureus was detected among (11.11%) of nonsmoker health care workers compared with (7.40%) of smokers, while MRSA was detected among (3.70%) of smokers and (7.40%) of non-smoker healthcare workers. No correlation was reported between the smoking habit of HCWs and colonization with S. aureus and MRSA in ATHMC which come in line with that reported by [26,28]. The result of current study come in line with that reported by a study achieved in the college of dentistry at Karbala University, Iraq, who stated that non-smokers are more likely to have S.aureus infec-tions [29]. In contrary to the present result [22],stated that significant correlation was re-ported between smoking and S.aureus isolation from HCWs in Nepal and similar conclu-sion was reported in Taiwan [30]. In ATHMC, S. aureus was detected among (14.81%) of HCWs, who regularly use hand disinfectants versus (3.70%) who use hand disinfectants irregularly. MRSA was detected among (7.40%) of HCWs who claimed to regularly use hand disinfectant. No correlation was reported between the use of hand disinfectant among HCWs colonized with S. aureus or MRSA.
A study achieved by [31] in among Indian HCWs confirmed that, (51.61%) of HCWs were positive for MRSA and after the use of an alcohol-based hand sterilization a total of (9.68%), HCWs were remained positive for MRSA. This corresponds with cur-rent study, and the possibility for persistence of MRSA as well as direct contact with contaminated surfaces such as walls, tools, patients skin and clothes beside the role of the length of the nails of HCWs (especially females) which is a reason for not fully sanitizing the hand despite using sterilization. Current study come in contrary with [15,16],who stated that hand washing practice among HCWs have no role in minimizing of infection with S.aureus and MRSA. On the other hand the contentious exposure of gloves and gown of HCWS for contamination with S.aureus and other pathogens especially during health care activities and exposure to the contaminated secretions [32],which facilitate the second line of problem as the HCWs will be the source for contamination for patients and hospital environment [33,34] .Another source for contamination was the mobile phone which was used even at duty that permit the possibility of cross contamination and failure of safety precautions [35]".
In current study, S.aureus was recovered from (14.81%) of HCWs who have a diploma in health care, compared with (3.70%) among those who have a Bachelor of nursing .
In ATHMC, MRSA was isolated from (7.40%), of HCWs in had a diploma in health care, and (3.70%) with a bachelor of nursing. " No significant correlation was reported between education level among HCWs , which come in line with that reported by [36,37] while inverse correlation was reported be-tween education level among HCWs and colonization with S. aureus and MRSA in ATHMC". "The risk for colonization with S.aureus among those having a diploma in health care was (1.250), while the risk for colonization with MRSA among those having a diploma in health care was(1.500 )time in ATHMC .These results come in agreement with [38],who stated that nurses was at 2.58 times higher than other HCWs for getting MRSA.
On the other hand [39],reported that the risk for nursing staff of being colonized with MRSA was almost two-fold higher than for medical staff and three-fold higher than for other healthcare staff . Results of current study come in partial agreement with [14],in turkey and [40] in Gaza Strip-Palestine and [41] in Saudi Arabia , stated that the education level play no role in infection with S.aureus and MRSA among HCWs. The possible explanation for high isolation rate of S. aureus and MRSA from those with diploma in health care may attributed to their adhesion with patients and entry for different hospital wards during their shift, change of patients dressing and continuous exposure for several possible sources for infection .
In current study, S.aureus was in (14.81%) of HCWs have no sinusitis versus (3.70%) suffering from sinusitis, while MRSA was in (3.70%) of HCWs who have no sinusitis .
Significant correlations was reported between sinusitis among HCWs and colonization with S. aureus, and marginal correlation was reported between sinusitis among HCWs and colonization with S. aureus and MRSA, in ATHMC. These results come in accord-ance with [39] and in contrary with that reported by [36] who stated that there was no significant correlation between S. aureus and MRSA colonization and sinusitis among HCWs. In the present study, S.aureus was isolated from (11.11%) of HCWs , who have no acne versus (7.40%) suffering from acne, while MRSA was isolated from (7.40%) of HCWs who do not suffer from acne. Significant correlations were reported between acne among HCWs colonization with S. aureus, in ATHMC which come in line with that re-ported by [38],who stated that acne represent a important risk factor for MRSA coloniza-tion among HCWs.
In the present study, in ATHMC. S. aureus was from (11.11%) of HCWS have (1-2) years of experience compared with (3.70%) for those with(3-4),(5-6) years of experience, while MRSA was isolated equally from (3.70%) of HCWs have (1-2),(3-4),(5-6) years of experience. Significant correlation respectively were reported between years of experience (one, two) among HCWs and colonization with S.aureus which come in agreement with In ATHMC, No correlation respectively was reported between years of experience (1-2, 3-4) among HCWs and colonization with S.aureus and MRSA, while significant correla-tion was reported between years of experience (5-6) among HCWs colonized with S.aureus and MRSA which come in line with [16,36,41] .
Contradictory result reported by [42],who stated that HCWs with few years of experience were more susceptible for colonization with S.aureus and MRSA. The possible explanation for the correlation between the years of experience and the colonization/infection rate of S.aureus may have attributed to the continuous exposure for microbs due to the heavy duty especially at the first years of occupation as a medical staff that required adhesion with clinical cases furthermore the limited awareness about personal protection during the routine work which is usually noticed with those of limited years of experience .
In current study, In ATHMC S.aureus was isolated from HCWs on the Children's care floor, (11.11%), followed by HCWs in the Intensive care unit (7.40%), while MRSA was from HCWs on the children's care floor, (11.11%). These results come in approximate of that recorded in Sultan Qaboos University hospital in Oman, where the prevalence of MRSA reach up to 9.1% in neonate intensive care unit however they reported a high prevalence in surgery unit 21.4% [23].
No correlation was reported between ward of duty and colonization with S. aureus and MRSA in ATHMC. Which come in accordance with that reported in Iran by [21] and in Oman by [23].
Significant correlations were reported between wards of duty on the children's care floor for HCWs colonization with MRSA in ATHMC. One of the reasons that lead to high rates on the children's floor is the basic design of the building that is not designated as a hospital and the large number of children admitted at a ward that exceeds the basic capacity of the rooms, which certainly leads to cases of contamination and crosscontamination .
This lead to subsequent spread of the pathogens from one place to another, whether in the hospital environment or to the skin of the coming patient. This happened due to the lack of awareness of the necessity to perform hand disinfection with alcoholic solutions to reduce the number of germs and thus the possibility of transmission of the pathogens to the medical staff and to the largest possible number if we take into account the fre-quent use of tools such as tables and desks on which the mobile phone or papers are placed of the patient, which is very likely to contain pathogenic germs. In a study achieved by [16], they stated that there was no significant relationship between specialties and S. aureus or MRSA infection .
In the present study, in ATHMC. S. aureus was isolated from (18.51%) of HCWs who assumed that they do not have contact with MRSA carriers, while MRSA was iso-lated from (7.40%) of HCWs who assumed that they do not have contact with MRSA carriers, with no significant correlation for S. aureus and MRSA in ATHMC. These result come in line with that reported by [38],stated that contact with MRSA carrier with or without protective clothes have no effect on the possibility of colonization among HCWs. Current results indicate the limited awareness about the presence of s. aureus and MRSA around in hospital and their critical role in serious consequences for patient and medical staff equally.
In current study, S. aureus was isolated from (14.81%) of HCWs who do not work in the ambulant sector versus (3.70 %) of those working in the ambulant sector outside the work.
These results come in agreement with [38,43] ,they stated that working in ambulant sector outside the work represent a considerable risk for getting S.aureus /MRSA and then transmitted to the patient and /or hospital environment.
In ATHMC, S. aureus (13.33%) of HCWs hospitals that do not have contact with farm animals versus (10%) that have contact with farm animals, the risk of getting S.aureus colonization among HCWs who have contact with farm animals (3.500) times. These results come in agreement with [44],who stated ,that the German HCWs how have direct or indirect contact with calves and /or pigs have 10 fold possibility of getting S.aureus. Current results come in agreement with [38,43]. In the other hand ,the possibil-ity of cross-transmission from farm or even pets animals to human leads to form a status of transient to stable colonization especially if they have sinusitis or dermatitis among HCWs who have contact with these animals [39] ,and subsequently they act as a vector for transmission of S.aureus /MRSA to the following patients during their ward duty [43].

Conclusions
Inverse correlation was reported between younger age group , education level of HCWs and colonization with S.aureus and MRSA .Significant correlation was reported between age group (28)(29)(30) year of HCWs in ATHMC and colonization with MRSA. Significant correlation was reported between sinusitis , years of experience (5-6)years ,contact with farm animals and colonization with S.aureus and MRSA .Significant correlation was reported between acne and colonization with S.aureus .Significant correlation was reported between ward of duty at children care floor and colonization with MRSA.

Recommendations
Take care for the role of health care workers in the transmission of S.aureus and MRSA for the patients and hospital environment.