Background: Staphylococcus aureus is a clinically significant pathogen that commonly causes community-acquired and nosocomial infections, especially in the hospital setting and is the most important risk factor for transmitting this pathogen [1]. In particular, the various manifestations of methicillin-resistant S. aureus (MRSA), are responsible for drastically lowered therapeutic options, serious courses of infection, and dramatically increased costs for prevention measures.
Ranking as the second most common cause of hospital acquired (nosocomial) bloodstream infections [2]. About 20% of patients undergoing surgery acquire at least one nosocomial S. aureus infection, leading to increased morbidity, mortality, hospital stay, and costs [2]. However, there is no any previous study conducted regarding this topic in Hargeisa, Somaliland.
Objectives: The main objective of this study was to determine the Carriage rate and Antimicrobial resistance Profile of Staphylococcus aureus Among Healthcare Workers at Edna Adan University Hospital.
Methods: Hospital-based cross-sectional was conducted on a total of 80 healthcare workers from July to August 2023 at EAUH. A simple random sampling technique was used and Samples were collected from HCWs at EAUH from July to August 2023. By using pre-moistened sterile cotton swabs and specimens were collected from the anterior nares and palms of the HCWs. The samples were collected by rotating the swabs gently two to three times on both nares of the study participants. Similarly, a second swab was used to collect specimen from both palms of the health care workers. Both swabs were cultured on blood agar and subculture onto Manitol Salt agar and incubated at 37 ℃ for 24 hrs.
Results: The overall prevalence of Staphylococcus aureus in this study was 20% (16/80) and methicillin-resistant Staphylococcus aureus was 7.5% (6/80). Carriage rate was highest among midwifes 7(29.2%) followed by nurses 5(26.3%) and doctors (3(17.6%) respectively. Similarly highest colonization rate of MRSA 3(60%) were observed among nurses and doctors 1(50%) followed by midwifes 2(28.6%). Length of healthcare service was significantly associated with MRSA colonization. Highest rate of resistance (100%) was found against Ampicillin, Cefoxitin (93.7%) Erythromycin (87.5%) and Gentamycin (68.75%) respectively. S. aureus was found to be highly sensitive to Doxycycline (100%) Ciprofloxacin (100%) and Clindamycin (87.5%). Similarly, MRSA was completely showed (100%) resistance against Cefoxitin and ampicillin.
Conclusion: The prevalence of Staphylococcus aureus and Methicillin-resistant Staphylococcus aureus are high in this study. The present study encourages the need for regular screening and surveillance among hospital staff and the environment to prevent MRSA transmission among health-care personnel and Molecular detection of highly resistant strains of MRSA are suggested.
S. aureus carriage, Healthcare workers, Hargeisa, Somaliland
Staphylococcus aureus is a clinically significant pathogen that commonly causes community-acquired and nosocomial infections, especially in the hospital setting and is the most important risk factor for transmitting this pathogen [1].
Ranking as the second most common cause of hospital acquired (nosocomial) bloodstream infections [2]. About 20% of patients undergoing surgery acquire at least one nosocomial S. aureus infection, leading to increased morbidity, mortality, hospital stay, and costs. Infections due to S. aureus strains could be caused by strains circulating in the community or present in hospital environments [3]. However S. aureus has also been known to colonize several sites of the human body in normal healthy people with the primary ecological niche being the anterior parts of the nares. From the anterior nares, S. aureus can be seeded in other extra-nasal sites which may include hands, pharynx, vagina, axillae, and skin that is either intact or inflamed. These sites may also be colonized without involvement of the anterior nares [4].
Carriage of S. aureus among healthcare workers (HCWs) has been documented to be a risk factor for transmission of the bacteria and the subsequent development of staphylococcal infections among patients in hospital settings and other health facilities [5]. Auto-infections among carriers also occur frequently [6]. The transmission of the bacteria from colonized or infected health care workers always occurs by direct contact or through fomites such as contaminated equipment or environment [7]. Increased Carriage of the bacteria on hands indicates poor hygiene practices among health care workers [8]. In addition, colonized HCWs provide a link through which cross transmission between community-acquired and hospital-acquired S. aureus occurs [9].
The emergence of virulent and multidrug-resistant strains has increased the morbidity rates and impeded effective treatment of S. aureus infections. Notably among these resistance mechanisms is methicillin resistance (MRSA), which is due to acquisition of a mecA gene by S. aureus strains. This gene encodes for an alteration in the penicillin-binding proteins (PBP) leading to their decreased affinity for β-lactam antibiotics [10]. MRSA is usually spread by direct contact with an infected wound or from contaminated hands, usually those of healthcare providers [11]. The increasing prevalence of S. aureus , especially MRSA strains among HCWs worldwide is a growing public health concern. However, there is a limited information regarding the prevalence, risk factors and antimicrobial susceptibility patterns of S. aureus among HCWs in sub-Saharan African countries, including Somaliland. Therefore the knowledge on carriage rate among HCWs of S. aureus isolates and their antimicrobial resistance pattern provide the baseline data for infection control measures. The aim of this study was to assess the carriage rate and the antimicrobial susceptibility profile of S. aureus from the health care workers Edna Adan University Hospital in Somaliland.
The Edna Adan hospital was founded by Edna Adan Ismail, a famous lady in the context of Somalia and the world as well. The hospital located in Maroodi Jeex region, the capital city of Somaliland known as Hargeisa. EAUH is found in southern of Hargeisa. Based on census conducted in 2012, Hargeisa has a total population of 1.6 million (Central Statistics Department of Somaliland) The city has one referral Hospital, two general Hospitals, seven health care centers and five private Hospitals and other several private clinics.
The EAUH is one of the largest private hospitals in the city, which provides health services for the community especially, maternal and child health services, for patients from all parts of Somaliland and other neighborhood regions such as puntland, and southern Somalia.
A facility-based cross-sectional study was conducted from July to August 2023 in Edna Adan Hospital. Hargeisa, Somaliland. Health care workers at Edna Adan University Hospital that come in direct contact with patients were included in the study. Staffs not involved in the provision of direct healthcare services such as office workers and those have current disease compatible with S. aureus were excluded from the study.
All the HCWs working all the hospital departments were included in the study. Participants were recruited on a voluntary basis during their regular activities. An informed consent form was made available to each participant who also completed a question naira’s regarding demographic data. Such as sex, age, history of chronic diseases, recent use of antibiotics, level of education, profession and length of healthcare services.
Samples were collected from HCWs at EAUH from June to July 2023. By using pre-moistened sterile cotton swabs and specimens were collected from the anterior nares and palms of the HCWs. The samples were collected by rotating the swabs gently two to three times on both nares of the study participants. Similarly, a second swab was used to collect specimen from both palms of the health care workers. The samples were immediately processed within two hours and inoculated into blood agar and incubated at 37 °C for 48 hr. Colonies that were brown or white, beta-haemolytic and round, characteristic of S. aureus , were sub-cultured onto mannitol salt agar and incubated at 37 °C for 24 h. Again, Colonies that were golden yellowish in appearance on MSA were identified as S. aureus . Further identifications were done by gram stain and other biochemical tests such as Catalase and coagulase. Isolates that were Gram-positive, cocci-shaped, arranged in pairs and clusters, positive for catalase and coagulase were identified as S. aureus .
The bacteria was tested against different antimicrobial drugs using the Kirby-Bauer disc diffusion method [12]. The bacterial inoculum was prepared by making a saline suspension of isolated colonies from 24 h Mannitol salt agar plate and the suspension was adjusted with 0.5 McFarland turbidity standards by using sterile saline. A sterile cotton swab was dipped into the adjusted suspension and streaked on a Mueller-Hinton agar plate. Commercially available discs of 30 μg vancomycin, 5 μg ciprofloxacin, 10 μg gentamicin, 15 μg erythromycin, 30 μg amikacin, 10 μg Ampicillin, 30 μg Doxycycline and 2 μg clindamycin were used. The antimicrobial discs were placed firmly on the surface of the inoculated Mueller-Hinton agar plate by using sterile forceps and the plates were then incubated 37 °C. After 18h-24h of incubation, the plates were examined and the diameters of the zones of inhibition were measured. The Results were determined as susceptible, intermediate, and resistant according to the guidelines of the Clinical and Laboratory Standards Institute [13]. Identification of MRSA isolates was done using 30 μg cefoxitin antibiotic discs on Mueller-Hinton agar plate according to standard guidelines [13].
The analysis of categorical data was done using SPSS version 23 software. S. aureus carriage was the dependent variable. Factors that could predispose to carriage of S. aureus among the health care workers such age, length of healthcare service, profession, presence of chronic debilitating conditions, history of antibiotic use and gender were the independent variables. Chi-square was used to analyze all the variables for significance and statistical significance was identified as p < 0.05.
The present study was approved by (office of postgraduate) Edna Adan University, and all experiments were performed in accordance with relevant guidelines and regulations. Participants’ information were anonymized prior to analysis and the confidentiality was assured by the researchers.
A total of 80 healthcare workers were recruited in the study and were screened for S. aureus carriage with a response rate of (100%). Among 80 healthcare workers, 16(20%) were positive for S. aureus . The age ranged between 20 and > 40 years (Mean age = 32.2 ± 8.22). 44(55%) were females and 36(45%) were males. The majority 24 (30%) of the health care workers were midwifes followed by 20(25%) were nurses. Regarding the length of the health care service of the participants, majority 38 (47%) had been working 1-5 years in the hospital (Table 1).
Table 1: Sociodemographic characteristics. View Table 1
As Table 2 depicted, the highest S. aureus carriers 2(66.6%) were observed among healthcare > 40-years-old followed by who were 30-39 years 8(22.2%), those who were females 10(22.7%) and those who were midwifes 7(29.2) followed by 5(26.3%) nurses.
Table 2: Distribution of S. aureus carriage by Age, Sex and profession. View Table 2
A total of 6 MRSA were isolated from 80 participants giving an overall colonization rate of (7.5%). Among the 36 males screened 6(16.6%) and 4(11.1%) were positive for S. aureus and MRSA respectively, when compared to 10(22.7%) 2(4.5%) of the 44 females screened. Similarly highest colonization rate of MRSA 3(60%) were observed among nurses and doctors 1(50%) followed by midwifes 2(28.6%). Conversely, No MRSA carriage was detected among the anesthesiologists and laboratory technicians (Table 3, Table 4 and Table 5).
Table 3: Distribution of S. aureus and MRSA carriage among the health professions. View Table 3
Table 4: Potential factors associated with MRSA Colonization among the HCW at EAUH. View Table 4
Table 5: Antimicrobial susceptibility profile of the isolated S. aureus. View Table 5
The antimicrobial susceptibility patterns were performed for the S. aureus isolates against antimicrobials using conventional dis diffusion. All S. aureus isolates were completely sensitive to Ciprofloxacin (100%), Doxycycline (100%) and (87.5%) sensitive to Clindamycin. Hence these drugs were found to be the most effective drugs against S. aureus in the study area. However, highest resistant was detected to Ampicillin (100%) followed by Erythromycin (87.5%), Gentamycin (68.75%) and Amikacin (56.25%) respectively (Table 6).
Table 6: Antimicrobial susceptibility pattern of MRSA (n = 6). View Table 6
This study reports the carriage rate for S. aureus among HCWs at the Edna Adan University Hospital. Edna Adan Hospital is one of the largest Maternity hospital in Somaliland. The overall carriage rate of S. aureus among health care workers was found to be 20%.
The findings of this study is comparable similar study done in India where the carriage rate of S. aureus was (20.7%) [14]. And Oman (20.5% [15]. However, similar studies have reported higher carriage rate of S. aureus in other developing countries than we have reported in this study. Such as Gabon (29%) [16], Ethiopia (28.8) [17], Principe (23.7%) [18] and Egypt (29.%) [19]. conversely, lower findings of S. aureus colonization rate have been reported from Madagascar (11%) [20], Yekatit 12 hospital, Ethiopia (14.3%) [21] and Nigeria (17.3%) [22]. The difference of carriage rate of S. aureus among HCW might due to variations of microbiological procedures, sampling techniques, study populations, infection control and preventive measures and rationale antibiotic usage which varies from hospital to hospital.
Regarding the colonization rate of MRSA among the healthcare workers in the current study, we found that the MRSA colonization rate was 7.5%. Higher burden of MRSA colonization rate was found among the females (22.7%) which is comparable with similar study conducted in Dar Al salam Hospital, Tanzania where the carriage rate among female HCW was 45.5% [23]. It is However. Contradicts from similar study conducted in Tikur Anbessa Hospital, Ethiopia (39.3%) [24] In which high carriage rate of MRSA was observed among males. However, the carriage rate of MRSA among HCW in the current study was higher than studies conducted in India (2.5%) [25] Ethiopia (5.8%) [26] and Kenya where no MRSA carriage was found among the healthcare workers [27]. But lower than similar studies done in elsewhere like Egypt (13.5%) [28], Ethiopia (12.7%) [26], Libya (19%) [29] and Tanzania (15.6%) [30]. The variations could be therefore, as a result of difference in microbiological procedures such as incubation period of the culture during antimicrobial sensitivity testing and local adherence of antibiotics usages among the healthcare workers.
In addition, highest colonization rate of MRSA 3(60%) were observed among nurses and doctors 1(50%) followed by midwifes 2(28.6%). Which is coincides with similar study conducted in Harar, Eastern Ethiopia where nursing and doctors carriage of MRSA were reported 15.3%, 11.1% respectively [31]. GAZA strip, where nursing and doctors carriage of MRSA were also observed (30.4%) and (16%) respectively [32].
These findings could be attributed by the increased physical contact of nurses and doctors with patients in the study area.
The present study assessed results to help to know the impact on the carriage rate of MRSA with the duration of length of healthcare services which has a significant difference. Similar effects had been made in a study carried out at tertiary and regional hospitals in Dar Salaam, Tanzania [30] although, the difference was not statistically significant. In fact due to dealing with patients for a longer period of years may increase the risk of exposure to total colonization.
The present study showed that there was no significant association between carriage of MRSA with sex (p = 0.085), Age (p = 0.503), history of hypertension (p = 0.241), history of diabetics (p = 0.124), recent use of antibiotics (p = 0.682), profession (p = 0.440). But it is, however length of healthcare services (p = 0.033 ) was highly significant associated with colonization rate of MRSA which is comparable with similar study done in Ethiopia [31]. Furthermore, relatively high carriage rate of MRSA colonization were observed among the males than females in the current study which is in agreement with those reported in Saudi Arabia [33]. But incomparable with similar study conducted in Ethiopia where females were more colonized by MRSA than males [34].
Understanding of antimicrobial resistance profile of the isolates is an important tool in the successful treatment of infections caused by S. aureus and prevention of outbreaks caused by MRSA in hospital settings. In this study high proportions (100%), (87.5%), (68.75%) and (56.25%) of S. aureus were resistant to Ampicillin, Erythromycin, Gentamycin and Amikacin respectively. The greater resistance offered by S. aureus against commonly used antibiotics could be attributed to many such as misuse and overuse of antibiotics.
In the present study, All S. aureus isolates were completely sensitive to Ciprofloxacin (100%), Doxycycline (100%) and (87.5%) sensitive to Clindamycin. Therefore, lower susceptibility of these drugs were reported from studies on healthcare workers in Ethiopia [26]. Resistance rates among MRSA isolates towards Gentamycin, Amikacin, Erythromycin and Doxycycline were significantly higher compared to those observed in S. aureus . These findings are similar to that reported in previous study conducted in the same settings [23].
The carriage rate of S. aureus and colonization of MRSA among the healthcare workers in Edna Adan University Hospital was relatively high, particularly among midwifes, nurses and doctors. The length of healthcare services was found to be significantly associated with colonization of MRSA. The study emphasizes the need for regular surveillance of hospital staff in the hospital environment to prevent S. aureus and MRSA transmission among health-care personnel, visitors, attendants and patients. Strict adherence to infection control practices is essential to limit the spread of MRSA through frequent hand-washing habits before, after and even in between every patient visit or medical procedures.
HM was involved in the conception, design, report writing analysis and the interpretation, KH involved specimen collection and manuscript writing. All authors read and approved the final manuscript.
A uthors declare that they have no competing interest.
The author(s) received no financial support for the research.
Not applicable.
The present study was approved by (office of postgraduate) Edna Adan University, and all experiments were performed in accordance with relevant guidelines and regulations. Participants’ information were anonymized prior to analysis and the confidentiality was assured by the researchers.
Not applicable.
We are thankful to Edna Adan University Hospital and the healthcare workers for their kind support and cooperation during the study period.