Methicillin-resistant Staphylococcus aureus (MRSA) is a major environmental health concern in Pakistan. Therefore, the aim of the present study with 18 published studies was to assess the prevalence of MRSA in non-clinical settings in Pakistan based on different years from 2016 to 2022 and different locations.
For this, the relevant articles dealing with the prevalence of MRSA were analysed in Pub Me, Google Scholar, Research Gate, Science Hub and Google from 2016 to 2022. The statistical analyses were performed using STATA software (version 17) and Excel.
DEDICATION
to
my beloved father
I dedicate this work to my late father, Ch. Ghulam Rasool who has always been playing the role of a beacon light in my life. Every time, when I felt tough in my life, he took my hand and guided me towards the destination. He was, and he is still an inspiring person in my life because he was the person who not only showed me to differentiate between the right and wrong path, but also, he practised it himself and set an example for me.
Acknowledgement
I want to say a special hearty thanks to my worthy teacher Ms. Zainab Syed for her time and patience with me and the way how she guided and encouraged me at every step, when. This is which increased my passion and interest for developing my understanding and studying further in the fields of Microbiology.
A thanks goes to my husband as well, who helped me regarding language and grammar by taking time and showing patience and stood on my side all time.
Asia Gull A Norusta
List of Tables
Table 1.1 Taxonomy of Staphylococci
Table 1.2 Natural habitat of different Staphylococcal species
Table 1.3 Prevalence statistics of MRSA isolated from different food items in Karachi
Table 3.1 Number of articles obtained from searching international databases
Table 4.1 Main characteristics of the studies included in meta-analysis
List of Figures
Figure 4.1 Flow diagram of the selection criteria of the eligible studies
Figure 4.2 Forest plot of the prevalence of MRSA and its 95% confidence interval (CI) in non-clinical samples. The pooled was calculated using random-effect model. Ev/Trt= No. of MRSA positive isolates/ Total no. of samples.
Figure 4.3 Funnel plot of the meta-analysis on overall methicillin-resistant S. aureus (18 studies included, small study size)
Figure 4.4 Trends in MRSA prevalence and its 95% confidence interval (CI) in non-clinical samples based on the year in which the study was published.
Figure 4.5 Trends in MRSA prevalence and its 95% confidence interval (CI) in different provinces
Abstract
Methicillin - resistant Staphylococcus aureus(MRSA) is an important health concern as far as the environment of Pakistan is concerned.
Objectives
Therefore, the objective of present study of 18 published studies was to evaluate the prevalence of MRSA in non-clinical items in Pakistan based on various years from 2016 to 2022 and different locations.
Method
I searched the relevant articles that focused on the prevalence of MRSA in Pub Me, Google Scholar, Research Gate, Science Hub, and Google from 2016 to 2022. Statistical analyses were conducted using STATA software (version 17) and Excel.
Results
For this meta-analysis 380 searches were done. 100 articles were excluded due to their irrelevance and clinical based nature and 262 were excluded for reason of being about other countries. The mean quality score of the 18 eligible studies was 19.95 (range 15 to 22). The pooled prevalence of MRSA was 48.7% with 95% CI (26 – 71.4%). Significant heterogeneity values were observed in the prevalence rates of MRSA.
Publication bias was assessed for 18 studies and evaluation presented with significant Egger’s test (P = 0.87) and Kendall’s Tau test (P = 0.97). All the p-values were greater than 0.05 by suggesting no obvious publication bias. A subgroup analysis was also performed for the periods 2016 – 2022, where significant differences were observed.
Further a subgroup analysis was carried out to analyse MRSA prevalence in different provinces. The prevalence in Sindh with the value of 8.4% (95% CI 5-28.4) and 5.54% in KPK (95% CI: 4.6-27.9) was comparatively lower than that of in other provinces.
Discussion
The MRSA infections are causing economic and public health challenges and causing deaths. It is because of improper dosing and associated antimicrobial resistance. There exists a limited data on the rates of MRSA contamination in non-clinical items especially in health care setting and environment. In this meta-analysis study, total 18 published research articles from various medias were included. The prevalence rates of S. aureus and MRSA reported from different regions of Pakistan were evaluated during the period of 2016 – 2022. Overall, high prevalence of S. aureus (36.5%) and MRSA (15%) was observed in non-clinical samples. The pooled prevalence rate of MRSA was 48.7% with 95% CI (26 -71.4%).
The prevalence of MRSA is higher in Pakistan (10.8%) than in Europe (4.6%) for health care workers. The prevalence of MRSA for meat products and places in Pakistan is 35.7%, whereas it is 1.9% in USA. The prevalence of MRSA +ve for animals and their related environment in Pakistan is 20.3%, whereas it is 9.0% in India. The situation for the prevalence of MRSA for processed food in Karachi Pakistan with a mean of 8.4% is better than in Saudi Arabia with a mean of 17.0% for the same.
Conclusion
The prevalence rate of MRSA in Pakistan is increasing during the period from 2016 to 2022. The overall local increase is one of the reasons for the increasing prevalence rate of MRSA in Pakistan compared to other geographical locations. The second reason lies in the fact that Pakistan is a developing country and lack of proper handling, misuse of antibiotics, poor hygienic practices and inadequate infection control policies could be the contributing factors to high prevalence rates of MRSA.
1 Introduction
1.1 Staphylococcus
The term Staphylococcus, generally is used for all the species, refers to the cells habit of aggregating in grapelike clusters. In 1880, a Scottish Surgeon Sir Alexander Ogston identified micro-organisms in pus from an abscess, which he later called 'Staphylococci’. Staphylococcus is a combination of two Greek words, staphyle (bunch of grapes and Kokkos) and grains or berries i.e., bacteria occurring in grapelike cluster or berry. He used the most modern German microscopes and Koch's stains to study pus from abscesses and was first to grow Staphylococci in artificial cultures (hens' eggs) (Newsom, 2008). Itis a genus of Gram-positive, spherical bacteria, that is facultative anaerobic cocci with diameter 0.6-1.2 microns, non-spore forming and usually non capsulated, but some species such as S. aureus are capsulated (Newsom, 2008).
Staphylococci grow in foods as well as being present in animals (skin, nose, and mucous membranes). It can grow at 7 °C to approximately 48 °C, but its optimum temperature is 35 °C. It prefers pH range of 7.0–7.5, but it can grow as low as pH 4.5. Staphylococci can grow at low levels of water activity, for example, as low as 0.8 aw. So, it can be tolerant to high salts and sugar concentrations. The classification of Staphylococci is given in Table 1.1 below (Newsom, 2008):
Table 1.1: Taxonomy of Staphylococci
Tables are not included in the reading sample.
Species of Staphylococcus
There are currently 53 recognised species of Staphylococci and 28 subspecies most of which are found only in lower mammals. The most frequently Staphylococci human infection is associated with S. aureus , S. epidermidis and S. saprophyticus (Agency, 2007). The natural habitat of different Staphylococci species is depicted in Table 1.2 below:
Table 1.2: Natural habitat of different Staphylococcal species
Tables are not included in the reading sample.
These six species are considered as potential human pathogens in this genus. The first three are the most common isolates. S. aureus is often considered to be the most problematic of these three pathogens and is distinguished from the other two by being the only one able to coagulate plasma (Layeret al., 2006).
1.2 Staphylococcus aureus
Staphylococcus aureus is the major bacterial human pathogen that causes a wide range of clinical implications both in community-acquired as well as hospital-acquired settings. It is also the normal flora of skin and mucous membrane. S. aureus is the leading cause of skin and soft tissue infections, such as abscesses, boils, furuncles, and cellulitis. It can also cause pneumonia, endocarditis (infection of the inner lining of the heart chambers and heart valves), bone and joint infections. Thirty percent of human healthy population is affected by S. aureus as it asymptomatically colonizes skin of the human host (Gnanamaniet al., 2017).
S. aureus is armed with battery of virulence factors that facilitate to establish infections in the hosts and help it to survive in harsh conditions. This organism is popular for its ability to build up resistance against various antibiotics (Gnanamaniet al., 2017).
1.2.1 Microscopic characteristics of S. aureus
Under the light microscope, S. aureus appears in clusters resembling with bunch of grapes. They are gram -stained as non- motile, non- spore forming and capsulated Gram-positive cocci. The diameter of the cells ranges from 0.5 to 1.0 μ M. Under Transmission Electron Microscope (TEM) cells shows thick cells wall, distinctive cytoplasmic membrane, and amorphous cytoplasm. Scanning Electron Microscopy (SEM) reveals roughly spherical shaped cells with smooth surface (Bennettet al., 1986).
1.2.2 Cultural characteristics of S. aureus
S. aureusiscatalase and coagulase positive . S. aureus grows readily on most bacteriologic media under aerobic or microaerophilic conditions. Colonies on solid media are round, smooth, raised, and shining. They form circular, smooth, shiny, and grey to deep golden yellow colonies on Mannitol Salt Agar with a diameter of about 2–3 mm. On blood agar, S. aureus produces β-haemolysis pattern (Turneret al., 2019).
1.3 Antibiotics Resistance
Antibiotics, also known as antibacterial are medications that destroy or slow down the growth of bacteria. They include a range of powerful drugs and are used to treat diseases caused by bacteria. Used properly, they can save lives. But there is a growing problem of antibiotic resistance. It happens when bacteria change and resist the effects of an antibiotic. Resistant bacteria may continue to grow and multiply in the presence of antibiotics (Roopeet al., 2019).
Antibiotic resistance occurs when an antibiotic has lost its ability to effectively control the growth of bacteria or kill them. In other words, the bacteria are "resistant" and continue to multiply in the presence of an antibiotic. This means that the antibiotic becomes less effective against that type of bacteria, as the bacteria has been able to improve its defences. Loss of ability of bacteria to the killing (bactericidal) or growth-inhibiting (bacteriostatic) properties of an antibiotic agent. When a resistant strain of bacteria is the dominant strain in an infection, the infection may be untreatable and life-threatening. Examples of bacteria that are resistant to antibiotics include methicillin-resistant Staphylococcus aureus (MRSA), penicillin-resistant Enterococcus (PRE), and multidrug-resistant Mycobacterium tuberculosis (MDR-TB) (Frieriet al., 2017).
1.3.1 Mechanism of Antibiotics Resistance
Antibiotic resistance is a natural phenomenon. Bacteria may become resistant in two ways:
1. By a genetic mutation
2. By acquiring resistance from another bacterium
Mutations are rare spontaneous changes of the bacteria's genetic material and thought to occur in about one in one million to one in ten million cells. Different genetic mutations yield different types of resistance. Some mutations enable the bacteria to produce enzymes that inactivate antibiotics, while other mutations eliminate the cell target at which antibiotics can attack. Any bacteria that acquire resistance genes, whether by spontaneous mutation or genetic exchange with other bacteria, could resist one or more antibiotics. Because bacteria can collect multiple resistance traits over time, they can become resistant to many different families of antibiotics. Environmentally, antibiotic resistance spreads as bacteria move from place to place. Bacteria can travel via airplane, water, wind, pets, and birds. People can pass the resistant bacteria to others by coughing, sneezing and contact with unwashed hands (Reygaert, 2018).
1.3.2 Types of Resistances
1.3.2.1 Intrinsic Antibiotic Resistance
Intrinsic resistance occurs when a bacterial specie became naturally resistant to a certain antibiotic or family of antibiotics, without the need for mutation or gain of further genes. This resistance mechanism mainly includes three aspects (Guoet al., 2020):
1. Outer Membrane Permeability
When the cell membrane permeability is lowered, the energy metabolism of the bacteria is affected, and drug absorption is reduced, leading to drug resistance. Resistance of S. aureus to aminoglycosides is caused by a decrease in membrane permeability and finally results in a decrease in drug intake (Guoet al., 2020).
2. Efflux Systems
The active efflux system of bacteria was discovered in 1980 by Ball and McMurry when studying the resistance of Escherichia coli to tetracycline. Scientist conducted many experiments on the active efflux system, which confirmed that the active efflux system is a normal physiological structure of bacteria and exists in sensitive strains. When induced by substrates in the environment for a long time, efflux system-encoding genes are activated and expressed, and the ability to efflux drugs is greatly enhanced, and leading to drug resistance. Active drug efflux systems play a role in resistance to multiple drugs. There are three types of multidrug-pumping proteins present on the S. aureus cell membrane: QacA, NorA, and Smr. These are important factor in MRSA (Guoet al., 2020).
3. Excessive Production of β-Lactamase
β-lactam antibiotics have a lethal effect on bacteria mainly through two mechanisms:
1. By binding to penicillin-binding protein (PBPs). It represses cell wall mucin synthesis, disrupts the cell wall, and leads to bacterial expansion and lysis.
2. By triggering the autolytic enzyme activity of the bacteria and resulted in autolysis and death.
Excessive secretion of β-lactamase by MRSA mainly reduces the effect of antibiotics through two mechanisms, which lead to MRSA resistant.
1. Hydrolysis mechanism, β-lactamase hydrolysed (break the, β-lactam ring) and inactivates β-lactam antibiotics.
2. A large amount of β-lactamase binds quickly and firmly to extracellular antibiotics, that prevent the antibiotics from reaching the intracellular space and therefore the antibiotics are not able to reach the target site (Lee & Park, 2016).
1.3.2.2 Acquired Antibiotic Resistance
Acquired resistance is achieved through the transfer of genetic material.Unlike intrinsic resistance, traits associated with acquired resistance are found only in some strains or subpopulations of each bacterial species. Acquired resistance results from successful gene exchange that may involve mutation or horizontal gene transfer through transformation, transduction, or conjugation (Reygaert, 2018). The strategies that bacteria use to develop acquired resistance are encoded on plasmids and may be classified into four mechanisms:
1. Decreased permeability of the cell wall to antibiotics.
2. Modification of enzymes to inactivate antibiotics.
3. Drug target site changes.
4. Efflux pumps that remove antibiotics from the cell.
5. Drug inactivation through enzymes is the predominant mechanism used by bacteria, and the expression of genes that encode these enzymes may be induced by medications (Clucket al.).
1.4 Antibiotic-Resistance in Staphylococcus Aureus
The history of the development and introduction of antibiotics, together with the often-rapid emergence of resistance in S. aureus, shows that this organism has a remarkable capacity for adapting to new types of antibiotics resistance. Consequently, there is a growing population of S. aureus that is resistant to traditional antibiotics and their derivatives. According to the sensitivity to antibiotic S. aureus can be divided into methicillin-sensitive Staphylococcus aureus (MSSA) and methicillin-resistant Staphylococcus aureus (MRSA). In recent decades, due to the evolution of bacteria and the misuse of antibiotics, the drug resistance of S. aureus has gradually increased, the infection rate of MRSA has increased worldwide, and treatment for MRSA has become more difficult. Accumulating proof has demonstrated that the resistance mechanisms of S. aureus are very complex, especially for MRSA, which is resistant to many kinds of antibiotics (Guoet al., 2020).
1.4.1 Methicillin Resistance in Staphylococcus Aureus (MRSA)
MRSA is a S. aureus that became resistant to β-lactam antibiotics due to mecA gene on its chromosomal DNA which they acquired from others. First MRSA was isolated in 1960 in England and became worldwide problem since 1970 (Hiramatsuet al., 2013).
The continuously high prevalence of (MRSA) throughout the world is a constant threat to public health, owing to the multi resistant characteristics of these bacteria. Methicillin resistance is phenotypically associated with the presence of the penicillin-binding protein 2a (PBP2a) not present in sensitive Staphylococci. This protein has a low binding affinity for β-lactam antibiotics. PBP2a is encoded by the mec A gene, which is in mec, a foreign DNA region (Brakstad & A. Mæland, 1997).
1.4.2 Community Associated MRSA
Community-associated MRSA infections (CA-MRSA) are MRSA infections in healthy people who have not been hospitalized or had any medical procedure (such as dialysis or any type of surgery) within the past year. Anyone can get CA-MRSA, but mostly have been seen among athletes, prisoners, military recruits, day-care attendees, injection drug users and other groups of people who live in crowded settings and routinely share contaminated items. Poor hygiene practices, such as lack of hand washing, may spread the bacteria easily. It begins as skin infections, first appear as reddened areas on the skin, can resemble pimples that develop into skin abscesses and boils causing fever, pus, swelling, and pain (Zafaret al., 2007).
1.4.3 Hospital Associated MRSA
Hospital-acquired MRSA are that S. aureus which isolates from patients after two or more than two days of their hospitalization, or after their recent surgery, dialysis, and residence in care facility within 1 year before the MRSA-culture date. The HA-MRSA is the result of a nosocomial infection, often acquired following a surgical or invasive medical procedure during a hospital stay. MRSA is spread by direct contact with an infected wound or from contaminated hands. People who are colonized MRSA but do not have signs of infection can spread the bacteria to others (Kavanagh, 2019).
1.5 Prevalence of MRSA Worldwide
According to the Centre for Disease Control and Prevention (CDC), about one in three people carry the S. aureus bacteria in their nose, and two out of 100 people carry MRSA. There are more than 80,000 cases of MRSA each year, and more than 11,000 people die from these infections. Although most of these cases occur in the hospital setting. MRSA infection is becoming a more widespread problem in the general community. People can become infected with MRSA after being in contact with an infected wound, or by sharing personal items like razors, toothbrushes, and towels that have touched infected skin (Hetemet al., 2016).
In 2014, the percentage of invasive MRSA isolates in Europe ranged from 0.9% in the Netherlands to 56% in Romania 17.4%. MRSA prevalence exhibits a north–south variation in Europe, with a higher proportion of resistant isolates in southern countries compared with northern countries. In Cyprus, Italy, Portugal, and Romania, more than 60% of healthcare-associated S. aureus infections were identified as MRSA (Hassounet al., 2017).
A study conducted in university hospital of Tehran, Iran reported MRSA prevalence of 22.5%. In U.K, Germany, Europe, and China, the MRSA prevalence ranges between 0.4-4.5%. In U.S and India is 6.6% and 8.5% respectively. The prevalence of MRSA infections, especially bacteraemia differs around the world (Shomaret al., 2021).
1.6 Prevalence of MRSA in Pakistan
There is not much data available regarding the prevalence of MRSA in Pakistan. The research papers read in local forums in Pakistan claimed around 35% MRSA in Pakistan (Aqibet al., 2017).
There was a difference in the MRSA frequency in different parts of the country according to a study arranged in 2002 in which regional laboratories of Pakistan were requested to participate; highest seen in Lahore (61%), closely followed by Karachi (57%), Rawalpindi Islamabad (46%), Peshawar (36%), Azad Kashmir (32%) and Quetta (26%) while minimum resistance was seen in Sukhur (2%).
Antibiotic resistance has become a major issue in the 21st century. Pakistan being one of only three polio-suffering countries is also suffering from bacterial resistance caused by poor use of Antibiotics. Being a third world country, Pakistan suffers from avoidable causes of antibiotic resistance but lacks the necessities which provides favourable environment to bacteria and produce resistance to its killer/inhibitor (Parveenet al., 2020).
1.7 MRSA in Environment
1.7.1 MRSA in Food
Staphylococci can survive under a wide range of environments e.g., on dry surfaces, high salt concentration and hospital set-ups. It can exist in air, dust, sewage, water, milk, food, on food equipment, environmental surfaces, humans, and animals.
It is transmitted through person to person contact as well as through inanimate objects. MRSA enter in a food set-up and contaminate the food products via human handlers or healthy nasal carriers. Food items made by hands without cooking are at high risk to carry Staphylococcal. However, air, dust, and food contact surfaces may also serve as vehicles in the transfer of Staphylococci in foods. According to research report published from Karachi, the prevalence statistics of MRSA in food items is listed in Table 1.3 below:
Table 1.3: Prevalence statistics of MRSA isolated from different food items in Karachi (Miraniet al., 2017)
Tables are not included in the reading sample.
1.7.2 MRSA in Milk
Use of antibiotics in food-producing animals has resulted in healthier and more productive animal. Disease incidence and mortality rates reduced in animals, and production of abundant quantities of nutritious for human. Despite these benefits, there is a considerable problem from public health, food safety. Development of antimicrobial resistance resulting from agricultural use of antibiotics that could impact treatment of diseases affecting the human population and become a significant global public health concern. MRSA prevalence in bovine milk 47% in China ,16.7% in Germany ,13.1% in India, 6.3% in Korea, 4% in USA (Javedet al., 2021).
1.7.3 MRSA on different hospital surfaces
A critical factor that allows the transmission of MRSA from a person to the environment and then to others, is the microorganism’s ability to survive on different types of surfaces under low humidity conditions (Jamilet al., 2018) . Wagenvoort and Penders 1997 reported the survival of MRSA for 175 days in hospital dust while an MSSA survived only for 4 weeks under the same conditions. MRSA can survive for one week on pure cotton and two weeks on cotton terry, while it lasts on polyester-cotton blend for less than one week (Wagenvoort & Penders, 1997). Polyester-cotton blends are most used in making different kinds of clothes including healthcare workers (HCWs) lab coats and scrubs. Thus, even within one day, the movement of the HCWs between different patients could promote transmission of MRSA from one patient to others in hospital (Jaradatet al., 2020).
1.7.4 MRSA in Public restrooms
Restrooms or washrooms are considered shared public spaces with pathogen transmission potential. Several studies documented the isolation of MRSA from restroom floors, handles, toilet seats, doorknobs, and water stopcock. In a study conducted during the Muslim pilgrimage (Hajj) season in Saudi Arabia, swabs were collected from doorknob surfaces of 224 toilets serving hundreds of thousands of people. Out of the 42 S. aureus strains identified, four were MRSA (Ahmed & Sirag, 2016).
1.7.5 MRSA in Schools and Universities
Environment of Schools and Universities contain many high-contact surfaces frequently touched by thousands of students and staff daily. In such environments, close physical contact, common shared spaces, and variable hygiene habits among students are some factors likely to contribute to the transmission of pathogens. MRSA have been isolated from a wide range of high-touch surfaces within schools and university environments such restrooms, lockers, elevators, dormitory fomites, and public computers (Robertset al., 2011).
1.8 Symptoms of MRSA Infection
The symptoms of a MRSA infection depend on the part of the body that is infected. For example, people with MRSA skin infections often can get swelling, warmth, redness, pus, and pain in infected skin. In most cases it is hard to tell if an infection is due to MRSA or another type of bacteria without laboratory test. Some MRSA skin infections can have a typical appearance and can be confused with a spider bite
MRSA infections can occur at various sites and may be serious, even life-threatening. Important MRSA infections include:
1. Bone infection (osteomyelitis)
2. Joint infection (septic arthritis)
3. Heart infection (endocarditis)
4. Pneumonia (Zelleret al., 2007)
1.9 Diagnosis and treatment of MRSA
Doctors diagnose MRSA by checking a tissue sample or nasal secretions for signs of drug-resistant bacteria. PCR is also a screening test for MRSA colonization in the nares, used to identify pneumonia patients at low risk for having MRSA (Parvezet al., 2018).
Antibiotics are the chosen line of treatment. However, repeated use of antibiotics has made MRSA resistant to methicillin, amoxicillin, penicillin, oxacillin, and cephalosporins and clindamycin. Invasive MRSA can be treated with trimethoprim-sulfamethoxazole, linezolid, and vancomycin (Parvezet al., 2018).
2 Literature Review
(Asghar Khanet al., 2016) conducted a study to determine the frequency of nasal carriage of methicillin resistant Staphylococcus aureusamong orthopaedic staff of Hayat Abad Medical Complex Peshawar from October 2011 till March 2012. They selected 73 (61 male & 12 females) orthopaedic staff members who come in regular contact with orthopaedic patients and regular employees of orthopaedic department. Mannitol fermentation and DNase test were used as selective media for the isolation of S. aureus. Antibiotic susceptibility testing was performed by modified Kirby-Bauer disc Diffusion. Resistance to Methicillin was detected by using Cefoxitin through disc diffusion test. Result of this study depicted that 72 out of 73 (98.6%) collected specimens were negative and only one was positive for S. aureus and MRSA. All female orthopaedic staff members were culture negative and one male orthopaedic staff was culture positive for MRSA. (Asghar Khan, DECEMBER 2016)
(Tariq, 2017) designed a study to evaluate carrier status of MRSA among dental health-care workers (HCWs) of Armed force Institute of Dentistry, Rawalpindi. The carriers could transmit infection when exposed to hospital setting during clinical work. Total 100 nasal samples were collected from HCWs including postgraduate trainees, house physicians, staff nurses and technicians by using cotton swabs moistened in sterile saline. Samples were inoculated on blood agar to look for β-hemolysis of S. aureus. Nutrient agar was used for the direct colony identification. Mannitol salt agar (MSA) and DNase were used as selective media for the isolation of S. aureus. Resistance to methicillin was detected by using cefoxitin through disc diffusion test. Result of this study showed that 35 (35%) samples were positive for S. aureusand 22 (22% overall & 63% of 35) out of these 35 samples were further positive forMRSA. They could be the potential risk factor for the transmission of nosocomial infection.
(Salmanet al., 2018) conducted a study to determine the frequency and drug susceptibility pattern of MRSA among HCWs (Health Care Workers) of a tertiary care Nishtar hospital, Multan, Pakistan. They selected 225 HCWs (78 males & 147 females) including laboratory staff, doctors, nurses, and paramedical staff for their study. HCWs having no signs of infections and any other systemic disease were included in this study. Nasal samples were collected using sterile swab and processed in the laboratory for MRSA, MSSA and for antimicrobial sensitivity of S. aureus. Of the collected samples, 54 (24%) nasal flora were positive for S. aureus & 21 out these 54 (39%) were positive for MRSA.
( Arif Maqsood Ali, 2020 ) designed a study to determine the percentage of HCW’s (Health Care Workers) having MRSA carriage at Rawalpindi Institute of Cardiology, Rawalpindi. Nasal and throat specimens were collected from 200 HCWs (48 males & 152 females) working in hospital. Specimens were collected from 91 HCWs working in intensive care unit, 53 from operation theatre, 33 from cardiac surgical ward, 12 from surgical private ward and 11 from paediatrics department. S. aureus were identified by colony morphology, gram staining and biochemical tests. MRSA were identified by observing zone of inhibition around cefoxitin disc on Mueller Hinton Agar (MHA). Result of the study indicated that 13 workers were positive for S. aureus, and all these were also MRSA positive.
(Syedet al., 2021) conducted a cross-sectional study to determine the nasal carriage of S. aureus and MRSA among healthcare workers in a tertiary care setting Islamabad, Pakistan. They collected 210 nasal swabs using cotton swabs moistened in sterile saline. Mannitol fermentation and DNase were used as selective media for the isolation. Antibiotic susceptibility test was performed by modified Kirby-Bauer disc Diffusion method. Resistance to methicillin was detected by using cefoxitin through disc diffusion test. According to the result, 52 /210 (24.76%) nasal swabs had S. aureus growth, and 15 out of 52 (28.85%) were MRSA positive. There was no association of infection with age, gender, duration of job and smoking. The frequency of nasal carriage of MRSA amongst healthcare workers was regardless of the nature of their professional engagement.
(Shoaibet al., 2021) designed a cross sectional study to investigate the effect of ablution on MRSA nasal colonisation. It was conducted at the department of Pathology, King Edward Medical University Lahore. They collected 220 samples: 110 from ablution performing healthcare workers and 110 from non-ablution performing healthcare workers. In gathered data, females were the dominant participants; 140 (64%) and majority of the participants 91 (41%) were from the surgical ward. A total of 117 (53%) participants had more than five years of working experience at the hospital. The collected specimens were processed at the Microbiology department for microscopy and culture. The positive cultures were taken and processed for the identification of Staphylococcus aureus i.e., confirmation by colony morphology, gram staining, catalase, DNase, coagulase test and results were recorded. Isolated S. aureuswere screened for MRSA by using cefoxitin disc. According to the study result was as: 43 were positive for S. aureus (11 from ablution performing group and 32 from non-ablution performing group). 25 were positive for MRSA (9 from ablution performing group and 16 from non-ablution performing group). Females from the non-ablution performing group were harbouring 63% more MRSA in their nose as compared to ablution performing group. This study exhibited that MRSA colonisation was significantly higher in non-ablution performing group as compared to ablution performing group. Regular nasal washing or ablution performance is a simple, easy, effective, and inexpensive way to reduce the risk of MRSA.
(Parveenet al., 2020) conducted a cross sectional study to evaluate prevalence of MRSA colonization among healthcare-workers and effectiveness of decolonization regimen in ICU (Intensive Care Unit) of a Tertiary Care Hospital, Lahore, Pakistan. They screened total 46 samples and after the detection of colonies of S. aureusin samples, five days decolonization regimen of nasal mupirocin ointment and chlorhexidine-based body wash were used to check the effectiveness of this regimen. According to the result of this study, a significant relationship was found between the prevalence of MRSA colonization and profession and gender. Out of total 46 participants, 18 were found positive for S. aureus and 6 were found positive for MRSA. MRSA colonization was found highest in nurses i.e., 66.67%. 16.67% MRSA prevalence was seen in doctors and 16.67% in respiratory therapists respectively. The success rate of treatment regimen was 83.33%. Prevalence of MRSA was found higher, but effectiveness of decolonization treatment regimen is like the worldwide success rate.
(Jamilet al., 2020) conducted a cross sectional study to determine colonization of Staphylococcus aureus in nasal cavities of healthy individuals from district Swabi, KPK, Pakistan. They collected 200 nasal samples (139 males & 61 females) from healthy students of Swabi University during October 2016 and April 2017. Kirby Bauer disk diffusion test method was used for antibiotic susceptibility. Of the collected samples, S. aureus was detected in 41 (20.5%) samples. Amongst them, 27 (65.85%) strains were isolated from male participants and 14 (34.14%) from female participants. However, No MRSA was detected among these isolated samples.
(Farmanullahet al., 2018) arranged a study to investigate the prevalence ofStaphylococcus aureusin the environment of Khyber Teaching Hospital Peshawar Pakistan. They collected 200 samples from the walls, air, floor and inanimate objects from the burn ward, surgical ward, and operation theatre. From these collected samples 64 (32%) were positive for Staphylococcus aureus. 37 out of these 64 (58.7%) were found positive for MRSA.
(Asifet al., 2017) managed a cross sectional study to estimate the frequency of MRSA in the nasal carriage of hospital employees at the General Hospital Lahore. They collected 380 samples from October 2015 to January 2016 from different clinical wards. Identification of S. aureus was done using colony morphology and Gram staining. Biochemical tests (catalase & coagulase test) were also employed for the confirmation of S. aureus. By using Cefoxitin disk, MRSA was identified. Result of this study was that 89 out of 380 nasal samples were found positive for S. aureus and 31 out these 89 (34%) were found further positive for MRSA, whereas males of age group 50 had highest ratio of MRSA in their nasal cavities.
(Syedet al., 2018) conducted a study for detection and molecular characterization of methicillin-resistant S. aureus from table eggs in Haripur, Pakistan. Total 300 egg samples were collected from different areas of Haripur, Pakistan from December 2015 to May 2016. Microbial detection was carried out from three parts of the egg, the inner membrane, egg white, and egg yolk. Identification of the strains was done using microbiological and biochemical tests, including microscopy, catalase, coagulase, DNase tests as well as mannitol fermentation on mannitol salt agar. The result of this study confirmed 64 (21.3%) positive for S. aureus , whereas 33 eggs (51.6%) out of 64 eggs were found positive for MRSA .
(Shoaibet al., 2022) designed a study to investigate the epidemiology and genetic relatedness of mecA gene in S. aureus isolated from pets, immediate individuals in contact with pets, and veterinary clinic environments. They collected 300 samples from different veterinary hospitals (Lahore, Narowal, Quetta, Faisalabad, Bahawalpur) of Pakistan. Collected samples were subjected to microbiological and biochemical examination for the isolation of S. aureus. MRSA was investigated phenotypically by using oxacillin disk diffusion assay and genotypically targeting mecA gene by PCR. Result of this study was overall 101 (33.7%) positive for S. aureus & MRSA.
(Shoaibet al., 2020) designed a study to diversify epidemiological pattern and antibiogram of mecA gene in Staphylococcus aureus isolated from pets, pet’s owners, pet’s personals, and the environment of animal treatment sites at Faisalabad, Pakistan. Total 384 samples were collected from nose and ear of dogs, cats, humans, and environmental sites (115 dogs, 115 cats, 96 pet owners & 58 environment of hospital). The collected samples were shifted to the laboratory of Institute of Microbiology, University of Agriculture Faisalabad. The identification of S. aureus was done by mannitol sugar fermentation and colony morphology. The overall 79.2% (304 out of 384) of collected samples were found positive for S. aureus. In cats 84.3%, dogs 81.7%, humans 72.9%, and environment sites 77.6% isolates were positive for S. aureus . Identification of MRSA was done by oxacillin disc diffusion test and the result was positive for 127 for MRSA out of 304. The mecA MRSA gene were found higher in dogs (33.91%) as compared to cats (30.4%).
(Rashidet al., 2021) conducted a study to analyse the presence of enterotoxigenic MRSA in salted sea fish from Gwadar. Total 50 freshly preserved salted fish samples were collected from Gwadar Baluchistan. The samples were processed for MRSA in Food Microbiology and Bioprocess Technology Laboratory Department, University of Baluchistan, Quetta. Biochemical testing was done for confirmation of S. aureus followed by 16SrRNA and nuc genes amplification. The samples were also processed for mecA, SEA and SEB. In their study, they found that 13 out of 50 collected samples were positive for S. aureus and MRSA as well.
(Javedet al., 2022) studied epidemiology and molecular characterization of S. aureus causing bovine mastitis in water buffaloes from the Hazara division of Khyber Pakhtunkhwa, Pakistan from August 2019 to January 2020. All 35 districts of the Hazara division were included in the study. Eleven buffalo farms were chosen in each district for sampling. On each farm, five buffaloes were selected for a total of 400 milking water buffaloes. Milk samples were cultured on mannitol salt agar (MSA) plates. S. aureus were identified mannitol fermentation, gram staining and DNase. Antibiotic susceptibility was assessed using antimicrobial disk diffusion. Result of this study depicted that among 400 collected samples, 102 were S. aureus positive, whereas only 20 out of 102 (19.6%) were found positive for MRSA.
(Aqibet al., 2017) designed a study to determine the prevalence of MRSA, and in-vitro therapeutic response of various antibiotics against MRSA in bovine milk. They collected 900 (50% from cattle and 50% from buffalo) samples of milk from various Tehsils of District Faisalabad. For the identification of S. aureus, milk samples were checked using biochemical tests and later confirmation of MRSA was done using oxacillin disk sensitivity test. Among the collected samples, 495 samples were found positive for S. aureus and 168 out of 495 were identified positive for MRSA.
(Miraniet al., 2017) conducted a study on the prevalence of Staphylococci in commercially processed food products in Karachi-Pakistan. They adopted cross-sectional survey method to determine the prevalence of Staphylococcus aureus and Methicillin Resistant Staphylococcus aureus (MRSA). They collected 1012 samples from different food processing industries during 2013 to 2016. Of the collected samples, 367 samples were found positive for S. aureus, and 85 samples amongst 367 samples were positive for MRSA.
(Sadiqet al., 2020) conducted a study on the prevalence of MRSA in Slaughterhouses and meat shops in Islamabad-Rawalpindi, Pakistan. They collected 300 samples (200 from working area, knives, hooks, butcher’s hands, and beef, 60 from chicken and mutton and 40 from nasal and rectal swabs). By performing Biochemical tests and gram staining, 150 out of 300 samples were S. aureus positive.Disc diffusion and specific gene detecting such as 16SrRNA, nuc, mecA, Spa and coa tests showed all 150 positive samples were resistant to four tested antibiotics i.e., Neomycin, Methylcytidine, Ciprofloxacin and Tetracycline. mecA gene was detected in 107 (71%) isolates confirming them as MRSA. This was the first study on the molecular identification of MRSA in meat samples from Pakistan. The high prevalence of MRSA in meat samples demand for implementation of proper hygienic practices and procedures during slaughtering, transport and marketing of meat and meat products to prevent the spread of these bacteria to the human population.
3 Methods
3.1 Guideline
This meta- analysis based review study was carried out according to the guidelines of “Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRIMA)” (Pageet al., 2021).
3.2 Quality Assessment
The qualities of all included studies were evaluated in accordance with the checklist of “Strengthening the Reporting of Observational studies in Epidemiology (STROBE)” (Von Elmet al., 2014) , which contains 22 essential items. The overall score ranged from 0-22. Article was given one point when the criteria for the desired item was fulfilled. The studies scoring <8 points were considered as poor-quality study.
3.3 Literature Search
An online search of 5 International database sources i.e., Pub Med, Google Scholar, Research Gate, Science-Hub, and Google was carried out to identify relevant studies reported from Pakistan about the prevalence rates of MRSA in non- clinical samples between January 1, 2012, to July 31, 2022. Total 380 searches were carried out. The reference list of the searched studies was further reviewed for any relevant publication. The duplicate article found using the above-mentioned databases were removed using EndnoteX7 (Thomson Reuters, New York, NY, USA). The searched sources of 380 articles are given in Table 3.1 below:
Table 3.1: Number of articles obtained from searching international databases
Tables are not included in the reading sample.
3.4 Key Words
The following keywords were searched: Staphylococcus aureus, MRSA (Methicillin-Resistant Staphylococcus Aureus), Antibiotics-Resistant Prevalence, Environment of Pakistan, Surrounding, Milk, Meat and Health-care workers (HCWs)
3.5 Eligibility Criteria for Studies
All human studies published from 2016 to 2022 in English Language that evaluated MRSA (Processed
Pre-valence) in the environment including food, meat, milk products, pets, pet’s surrounding, environment of hospitals were eligible for inclusions.
3.6 Inclusion Criteria
The eligible studies were selected for inclusion in this meta-analysis when the following criteria was met:
1. Full-text articles available in English language.
2. Studies reported from different regions of Pakistan.
3. Cross-sectional studies.
4. Sample size provided.
5. Samples assessed for S. aureus and MRSA prevalence. Non-clinical samples collected from hospital staff and environment, pets, slaughterhouses, milk, and meat shops.
3.7 Exclusion Criteria
Studies were excluded based on following exclusion criteria:
1. Duplicated data or review articles and conference abstracts.
2. Articles without full text.
3. Articles reported from regions other than Pakistan.
4. Samples from clinical ill patients.
3.8 Data Extraction
The following relevant information were extracted from the included studies: Author’s name, year of study, publishing year, place of study, number of samples, type of samples, S. aureus positive number, MRSA positive number (isolate number), phenotypic and genotypic methods used for identification and environment of sample of study.
3.9 Publication Bias
Risk of publication bias was analysed using Begg test.
3.10 Statical Analysis
Meta analysis was performed to determine the pooled prevalence of MRSA and 95% confidence interval (CI) using OpenMeta analyst (Brown University, Providence, USA). Heterogeneity of the studies were determined using Q test and the I 2 statistic. P < 0.10 suggests heterogeneity among study parameters. The I2 statistic was used to quantify the degree of heterogeneity, with values of 25%, 50%, and 75% suggesting low, medium and high degrees of heterogeneity, respectively (Johnson & Whisman, 2013). We used a random-effect model by the DelSimonian-Laird (DL method to analyse data with substantial amounts of heterogeneity (I 2 > 50%) (Buccheri & Sharifi, 2017). The prevalence and 95% confidence interval were determined by Jackson method of DelSimonian-Laird (DL) model for MRSA.
4 Results
4.1 Selection of Studies
For this meta-analysis, total 380 articles were identified in the initial search. Out of these 380 searches, 100 articles were excluded because of their irrelevance and clinical based nature. Case report, conference abstracts and review articles were also excluded. 262 articles were excluded for reason of being about other countries and not having full text. Eighteen relevant articles were selected because they met the inclusion criteria, and their full text were reviewed. The flow diagram of the selection process of the included studies is shown in Figure 4.1.
Figures are not included in the reading sample.
Figure 4.1: Flow diagram of the selection criteria of the eligible studies
4.2 Characteristics of the eligible Studies
Of the included 18 articles, 1 to 10 focused on the prevalence of S. aureus & MRSA contamination environment of hospitals, 11 on table eggs, 12 & 13 on pets, person, and environment, 14 on salted sea fishes, 15 and 16 on milk, 17 on commercially processed food products and 18 on working area of slaughterhouses and meat shops. The included studies were from the 4 provinces of Pakistan: Punjab, Sindh, Baluchistan, Khyber Pakhtunkhwa (KPK) and from Islamabad Capital Territory (ICT). All the included studies reported S. aureus prevalence whereas MRSA prevalence was reported in 17 studies. The mean quality score of the 18 eligible studies was 19.95 (range, 15 to 22). The detailed characteristics and quality scores of the included studies are summarized in Table 4.1 below.
Table 4.1: Main characteristics of the studies included in meta-analysis
Tables are not included in the reading sample.
4.3 Pooled MRSA Prevalence
Of the included 18 studies, 2006 (36.5%) S. aureus positive isolates were recovered. Methicillin resistance was recorded in 799 (15%) isolates out of 5500 total samples. The pooled prevalence of MRSA was 48.7%, 95% CI (26–71.4%). Significant heterogeneity values were observed in the prevalence rates of MRSA across included studies with a heterogeneity value (Tau^2= 0.234, P = <0.001, I2 of 99.65%), as shown in Figure 4.2.
Figures are not included in the reading sample.
Figure 4.2: Forest plot of the prevalence of MRSA and its 95% confidence interval (CI) in non- clinical samples. The pooled prevalence was calculated using random-effect model. Ev/Trt= No. of MRSA positive isolates/ Total no. of samples.
4.4 Publication Bias
Publication bias was assessed for 18 studies. The evaluation presented visual asymmetry of the funnel plot (Figure 4.3) with significant Egger’s test (P= 0.87) and Kendall’s Tau test ( P = 0.97). All the P- values are greater than 0.05, suggesting that there was no obvious publication bias.
Figures are not included in the reading sample.
Figure 4.3: Funnel plot of the meta-analysis on overall methicillin-resistant S. aureus (18 studies included, small study size)
4.5 Trends in MRSA Prevalence from 2016 - 2022
To analyse the trends for changes in the prevalence of MRSA in more recent years, a subgroup analysis was performed for the periods (2016 – 2022). Significant differences were observed in the prevalence of MRSA infection by year, with the prevalence rate of 1% in 2016 which increased to 12% in 2017 and then 14% in 2018. In 2020, there was a surge at the peak of 23%. A decline was seen in 2021 where the prevalence was only 11% however then again, an increase in prevalence at the 17% was seen in 2022. The increasing and decreasing trends of MRSA and their corresponding 95% CIs are shown in Figure 4.4.
Figures are not included in the reading sample.
Figure 4.4: Trends inMRSAprevalence and its 95% confidence interval (CI) innon- clinical samples based on the year in which the study was published
4.6 Prevalence of MRSA in Different Provinces
A subgroup analysis was carried out to analyze MRSA prevalence in different provinces i.e., KPK, Punjab, Sindh, Baluchistan, and ICT. The prevalence of MRSA was highest in Baluchistan 26% (95% CI: 1.5-36.9) followed by ICT 23.92% (95% CI: 4.1-31.8) and Punjab 18.66% (95% CI: 11.7-36.2). The prevalence was comparatively lower in Sindh 8.4% (95% CI 5-28.4) and KPK 5.54% (95% CI: 4.6-27.9) (Figure 4.5).
Figures are not included in the reading sample.
Figure 4.5:Trends inMRSAprevalence and its 95% confidence interval (CI) indifferent provinces
5 Discussion
The MRSA infections are posing economic and public health challenges and are the leading cause of deaths because of improper dosing and associated antimicrobial resistance which is making this pathogen a superbug (Zorganiet al., 2009). Worldwide, limited data exists on the rates of MRSA contamination in non- clinical items present in health care setting and environment. This meta-analysis was performed to systematically analyze the rates of S . aureus and MRSA contamination in non- clinical items in the hospital setting and related environment and evaluate different subgroups which can influence the results of the included studies. In this meta- analysis study, total 18 published research articles from PubMed, Google scholar, Sci-hub and ResearchGate were included. The prevalence rates of S. aureus and MRSA reported from different regions of Pakistan during the time-period 2012-2022 was evaluated. Overall, high prevalence of S. aureus (36.5%) and MRSA (15%) was observed in the non- clinical samples. The pooled prevalence rate of MRSA was 48.7%, 95% CI (26 –71.4%).
The prevalence rate of MRSA in Pakistan is higher than that reported in Kenya (18.3%) (Omuseet al., 2012), however, it is comparable to study conducted in Libya (39%) (Zorganiet al., 2009).
A study was conducted on health care workers in the European region, where total samples of 726 were taken and it showed a mean of for the prevalence of MRSA of 4.6% (Sassmannshausen, 2016). The present study in hand gave a mean for the prevalence of MRSA 10.8% in Pakistan. It shows that the environment in Europe for health care workers is healthier than in Pakistan.
A study was conducted on various kinds of meat (turkey, pork, beef & chicken) in USA, where total samples of 3’520 were taken and it showed a mean for the prevalence of MRS of 1.9% (Beilei, 2016) as compared to present study (35.7%). It shows that the environment of USA for meat in slaughterhouses and shops is much better than in Pakistan for the same.
A study was conducted on animal handlers and their environment in southern province Karnataka of India, where total samples of 666 were taken and it showed a mean for the prevalence of MRSA of 9.0% (Venugopal, 2019). The present study in hand gave a mean of MRSA 20.3% in Pakistan for the same area. It shows that the environment in India based on this Indian study for animals and their surroundings is healthier than in Pakistan. However, the mean of 20.3% for MRSA is based on 5 various studies in the period of 2017 to 2022 and the mean of 9.0% in Karnataka was from only one study in 2019.
A study was conducted on processed food products in Saudi Arabia, where total numbers of samples were 150 (Mashael, 2021). This study gave a result of 17.0% for the prevalence of MRSA for the same. When we compared the result of present study of mean of processed food in Karachi, Pakistan, it was observed that the rate for prevalence of MRSA in Pakistan for the same was 8.4% with the total samples of 1012. This showed the level of hygienic handling in Pakistan is better than in Saudi Arabia.
The increasing prevalence rates of MRSA can be attributed to the following reasons: First, the overall local increase in the prevalence of MRSA in Pakistan as compared to other geographic location. Secondly Pakistan is a developing country therefore lack of proper handling, misuse of antibiotics, poor hygienic practices, and inadequate infection control policies can also contribute to high prevalence rates of MRSA.
To check the trends in MRSA prevalence, subgroup analysis was caried out in different years in which the studies were published. According to the results of the study, it was found that prevalence of MRSA had increased over the period. It is worrisome that prevalence rate of MRSA in 2016 was 1% and then in 2020, it was at 23%. A decline was seen in 2021 where the prevalence was only 11% however then again, an increase in prevalence at the 17% was seen in 2022. The possible reasons for the emergence of MRSA in recent years can be improved diagnostics, and inadequate antibiotics administration Therefore, the importance of hospital environmental sterilization should be practiced (Diazet al., 2018).
The prevalence rate of MRSA varies considerably among different provinces. The prevalence of MRSA was highest in Baluchistan 26% (95% CI: 1.5-36.9) followed by ICT 23.92% (95% CI: 4.1-31.8) and Punjab 18.66% (95% CI: 11.7-36.2). The prevalence was comparatively lower in Sindh 8.4% (95% CI 5-28.4) and KPK 5.54% (95% CI: 4.6-27.9). The difference can be due to different reporting guidelines.
Significant differences were observed in the included studies resulting in high degree of heterogeneity (Tau^2= 0.234, P = <0.001, I2 of 99.65%). The funnel plot depicted visual asymmetry suggesting publication bias may be due to poor reporting or due to small study size.
This meta- analysis has several limitations. First, some of the important articles may have lost because we only included the articles which reported sample size. Secondly, articles that didn’t reported sampling type and study year also limited the subgroup analysis. Thirdly, amongst the 18 included articles, sampling type, sample size, study year and study location were different which has also impacted our results. Finally, the number of articles included in our meta-analysis was very small. Despite the limitations of this meta-analysis, it is the first meta-analysis about the pooled prevalence rates of MRSA contamination in non-clinical samples throughout Pakistan.
6 Conclusion and Recommendation for further Research
6.1 Conclusion
It can be concluded that the prevalence rate of MRSA is increasing in Pakistan over the years from 2016 to 2022. Overall, there was a high prevalence ofS. aureus(36.5%) and MRSA 15%. The pooled prevalence rate was 48.7% with CI of 95%. The results and discussion as well as the comparison of the study showed that the prevalence rate of MRSA in Pakistan is even high than that of in Kenya and Libya.
The study in hand showed that the prevalence rates of MRSA were increasing on various local places in Pakistan in the years from 2016 to 2022, which is causing the high rate of prevalence of MRSA in Pakistan overall. Being a developing country, Pakistan is facing many other challenges like improper handling, misuse of antibiotics, poor hygienic practices, and inadequate infection control policies. All these facts are contributing to high prevalence rates of MRSA.
A comparison of the prevalence of MRSA for different provinces showed that the prevalence rate of MRSA was the highest with 26% in Baluchistan and the lowest with 5.54% in KPK. It can be one of the reasons that KPK was more developed than Baluchistan in the previous years.
It can be concluded from the results and discussion from the last chapter that the prevalence of rate of MRSA in Pakistan (10.8%) is higher than the rate of the prevalence MRSA in Europe, that is 4.6% for the same field, health care workers. That indicates that there are more measures are needed for the health care workers to reduce the risk of MRSA in Pakistan.
The results and discussion as well as the comparison of the study on various kinds of meat in the USA threw light on the very high ratio of MRSA in Pakistan. It was in Pakistan 35.7% and in the USA just 1.9%. This result leaded us to think over the hygienic standards in slaughterhouses and meat shops in Pakistan. That is naturally a matter of special attention, for which strong measures are needed in Pakistan for the health of our community and environment.
A comparison regarding animals and their environment of Karnataka India with Pakistan showed a mean of MRSA in Pakistan with a value of 20.3%, whereas it was in India only 9.0%. It is important to note that both countries belong to South Asia and people of the both the country have almost similar culture and mentality. However, the lower rate of MRSA of 9.0% showed that the hygienic conditions for animals and animals related environment are better in India than those of in Pakistan. It again indicates that some measures are needed in this field as well.
A comparison of the prevalence of MRSA for the processed food in Karachi, Pakistan with the processed food in Riyadh, Saudi Arabia gave us the information that the hygienic conditions in Karachi, Pakistan for the processed food is better than for the same in Riyadh, Saudi Arabia. The prevalence rate of MRSA was 8.4%, whereas it was for the same in Saudi Arabia 17.0%.
6.2 Recommendations for the further Research
A deep analysis of the prevalence of MRSA in slaughterhouses and meat shops in Pakistan can also be done by comparing it with the presence of MRSA in slaughterhouses and meat shops in the advanced countries of the world. This comparison and result could lead us to reduce the prevalence of MRSA in slaughterhouses and meat shops in Pakistan.
Further research is suggested to find the prevalence of MRSA on animals and animal related environment in Pakistan by comparing the results with the western countries. This could answer us not only the high rate of MRSA in our country but also can be helpful in finding solution to reduce it by following the example of the best.
References
Agency, H. P. (2007). Identification of Staphylococcus species, Micrococcus species and Rothia species. National Standard Method BSOP ID 7, issue 2.
Ahmed, O. B., & Sirag, B. (2016). Microbial contamination of door knobs in public toilets during Hajj. Asian J Sci Tech, 7, 3676-3679.
Aqib, A. I., Ijaz, M., Anjum, A. A., Malik, M. A. R., Mehmood, K., Farooqi, S. H., & Hussain, K. (2017). Antibiotic susceptibilities and prevalence of Methicillin resistant Staphylococcus aureus (MRSA) isolated from bovine milk in Pakistan. Acta tropica, 176, 168-172.
Arif Maqsood Ali, A. M. K. a. A. B. H. (2020). Methicillin Resistant Staphylococcus aureus Nasal Carriage among Health Care Workers at Rawalpindi Institute of Cardiology, Rawalpindi, Pakistan. ournal of Infectious Diseases and Medicine, 5(2). doi: 10.37421/jidm.2020.5.141
Asghar Khan, K. J., Iqbal, M. J., & Siraj, M. (2016). FREQUENCY OF NASAL CARRIAGE OF METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS IN ORTHOPAEDIC STAFF. KJMS, 9(3), 324.
Asif, A., Javed, I., Mushtaq, S., & Anwar, S. (2017). Nasal carriage of methicillin resistant staphylococcus aureus among tertiary care hospital employees in a non-outbreak setting. Pakistan Journal of Pathology, 28(4).
Beilei. (2016). MRSA and multidrug-resistant Staphylococcus aureus in U.S. retail meats. National Library of Medicine , 289-297.
Farmanullah, K., Bashir, A., Jawad, A., Han Sang, Y., & Shumaila, B. (2018). Investigation of Staphylococcus aureus, prevailing in the environment of Khyber Teaching Hospital, Peshawar, Pakistan.
Bennett, R., Yeterian, M., Smith, W., Coles, C., Sassaman, M., & McClure, F. (1986). Staphylococcus aureus identification characteristics and enterotoxigenicity. Journal of Food science, 51(5), 1337-1339.
BRAKSTAD, O. G., & A. MÆLAND, J. (1997). Mechanisms of methicillin resistance in staphylococci. Apmis, 105(1‐6), 264-276.
Cluck, D., BCIDP, A., & Singleton, A. Understanding Antimicrobial Resistance.
Diaz, R., Afreixo, V., Ramalheira, E., Rodrigues, C., & Gago, B. (2018). Evaluation of vancomycin MIC creep in methicillin-resistant Staphylococcus aureus infections—a systematic review and meta-analysis. Clinical Microbiology and Infection, 24(2), 97-104.
Frieri, M., Kumar, K., & Boutin, A. (2017). Antibiotic resistance. Journal of infection and public health, 10(4), 369-378.
Gnanamani, A., Hariharan, P., & Paul-Satyaseela, M. (2017). Staphylococcus aureus: Overview of bacteriology, clinical diseases, epidemiology, antibiotic resistance and therapeutic approach. Frontiers in Staphylococcus aureus, 4(28), 10.5772.
Guo, Y., Song, G., Sun, M., Wang, J., & Wang, Y. (2020). Prevalence and therapies of antibiotic-resistance in Staphylococcus aureus. Frontiers in cellular and infection microbiology, 10, 107.
Hassoun, A., Linden, P. K., & Friedman, B. (2017). Incidence, prevalence, and management of MRSA bacteremia across patient populations—a review of recent developments in MRSA management and treatment. Critical care, 21(1), 1-10.
Hetem, D. J., Derde, L. P., Empel, J., Mroczkowska, A., Orczykowska-Kotyna, M., Kozińska, A., Hryniewicz, W., Goossens, H., Bonten, M., & group, M. W. s. (2016). Molecular epidemiology of MRSA in 13 ICUs from eight European countries. Journal of Antimicrobial Chemotherapy, 71(1), 45-52.
Hiramatsu, K., Ito, T., Tsubakishita, S., Sasaki, T., Takeuchi, F., Morimoto, Y., Katayama, Y., Matsuo, M., Kuwahara-Arai, K., & Hishinuma, T. (2013). Genomic basis for methicillin resistance in Staphylococcus aureus. Infection & chemotherapy, 45(2), 117-136.
Jamil, J., Zaman, K., Ullah, S., Ali, I., & Kalsoom. (2020). Colonization of Staphylococcus aureus in nasal cavities of healthy individuals from district Swabi, KP, Pakistan. JPMA. The Journal of the Pakistan Medical Association, 70(7), 1154-1158.
Jamil, B., Gawlik, D., Syed, M. A., Shah, A. A., Abbasi, S. A., Müller, E., Reißig, A., Ehricht, R., & Monecke, S. (2018). Hospital-acquired methicillin-resistant Staphylococcus aureus (MRSA) from Pakistan: molecular characterisation by microarray technology. European Journal of Clinical Microbiology & Infectious Diseases, 37(4), 691-700.
Jaradat, Z. W., Ababneh, Q. O., Sha’aban, S. T., Alkofahi, A. A., Assaleh, D., & Al Shara, A. (2020). Methicillin resistant Staphylococcus aureus and public fomites: a review. Pathogens and Global Health, 114(8), 426-450.
Javed, M. U., Ijaz, M., Fatima, Z., Anjum, A. A., Aqib, A. I., Ali, M. M., Rehman, A., Ahmed, A., & Ghaffar, A. (2021). Frequency and Antimicrobial Susceptibility of Methicillin and Vancomycin-Resistant Staphylococcus aureus from Bovine Milk. Pakistan Veterinary Journal, 41(4).
Javed, S., McClure, J., Syed, M. A., Obasuyi, O., Ali, S., Tabassum, S., Ejaz, M., & Zhang, K. (2022). Epidemiology and molecular characterization of Staphylococcus aureus causing bovine mastitis in water buffaloes from the Hazara division of Khyber Pakhtunkhwa, Pakistan. PloS one, 17(5), e0268152.
Kavanagh, K. T. (2019). Control of MSSA and MRSA in the United States: protocols, policies, risk adjustment and excuses. Antimicrobial Resistance & Infection Control, 8(1), 1-8.
Layer, F., Ghebremedhin, B., Moder, K.-A., Konig, W., & Konig, B. (2006). Comparative study using various methods for identification of Staphylococcus species in clinical specimens. Journal of clinical microbiology, 44(8), 2824-2830.
Lee, Y.-D., & Park, J.-H. (2016). Phage conversion for β-lactam antibiotic resistance of Staphylococcus aureus from foods. Journal of Microbiology and Biotechnology, 26(2), 263-269.
Mashael. (2021). The prevalence of Staphylococcus aureus and Methicillin Resistant Staphylococcus aureus in Processed Food Samples in Riyadh, Saudi Arabia . JPAM, 91-99.
Mirani, Z. A., Aqeel, A., & Naz, S. (2017). Prevalence of staphylococci in commercially processed food products in Karachi-Pakistan. Journal of Microbiology and Infectious Diseases, 7(02), 83-87.
Newsom, S. (2008). Ogston's coccus. Journal of hospital Infection, 70(4), 369-372.
Omuse, G., Kariuki, S., & Revathi, G. (2012). Unexpected absence of meticillin-resistant Staphylococcus aureus nasal carriage by healthcare workers in a tertiary hospital in Kenya. Journal of hospital Infection, 80(1), 71-73.
Page, M. J., McKenzie, J. E., Bossuyt, P. M., Boutron, I., Hoffmann, T. C., Mulrow, C. D., Shamseer, L., Tetzlaff, J. M., Akl, E. A., & Brennan, S. E. (2021). The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Systematic reviews, 10(1), 1-11.
Parveen, S., Saqib, S., Ahmed, A., Shahzad, A., & Ahmed, N. (2020). Prevalence of MRSA colonization among healthcare-workers and effectiveness of decolonization regimen in ICU of a Tertiary care Hospital, Lahore, Pakistan. Advancements in Life Sciences, 8(1), 38-41.
Parvez, M. A. K., Ferdous, R. N., Rahman, M. S., & Islam, S. (2018). Healthcare-associated (HA) and community-associated (CA) methicillin resistant Staphylococcus aureus (MRSA) in Bangladesh–Source, diagnosis and treatment. Journal of Genetic Engineering and Biotechnology, 16(2), 473-478.
Reygaert, W. C. (2018). An overview of the antimicrobial resistance mechanisms of bacteria. AIMS microbiology, 4(3), 482.
Roberts, M., Soge, O., No, D., Helgeson, S., & Meschke, J. (2011). Characterization of Methicillin‐resistant Staphylococcus aureus isolated from public surfaces on a University Campus, Student Homes and Local Community. Journal of applied microbiology, 110(6), 1531-1537.
Roope, L. S., Smith, R. D., Pouwels, K. B., Buchanan, J., Abel, L., Eibich, P., Butler, C. C., Tan, P. S., Walker, A. S., & Robotham, J. V. (2019). The challenge of antimicrobial resistance: what economics can contribute. Science, 364(6435), eaau4679.
Rashid, N., Shafee, M., Iqbal, S., Samad, A., Khan, S., Hasni, M., Rehman, Z., Ullah, S., Rehman, F., & Khan, G. (2021). Enterotoxigenic methicillin resistant Staphylococcus aureus contamination in salted fish from Gwadar Balochistan. Brazilian Journal of Biology, 83.
Sadiq, A., Samad, M., Basharat, N., Ali, S., Saad, Z., Khan, A. N., Ahmad, Y., Khan, A., & Khan, J. (2020). Methicillin-Resistant Staphylococcus aureus (MRSA) in Slaughter Houses and Meat Shops in Capital Territory of Pakistan During 2018–2019. Frontiers in Microbiology, 11, 577707.
Salman, M. K., Ashraf, M. S., Iftikhar, S., & Baig, M. A. R. (2018). Frequency of nasal carriage of Staphylococcus Aureus among health care workers at a Tertiary Care Hospital. Pakistan journal of medical sciences, 34(5), 1181.
Sassmannshausen. (2016). MRSA Prevalence and Associated Risk Factors amoung Health-Care Workers in Non-outbreak Situations in the Dutch-German EUREGIO. Frontiers.
Shoaib, M., Aqib, A., Ali, M., Ijaz, M., Sattar, H., Ghaffar, A., Sajid Hasni, M., Bhutta, Z., & Ashfaq, K. (2022). Kulyar MF-eA and Pu W (2022) Tracking Infection and Genetic Divergence of Methicillin-Resistant Staphylococcus aureus at Pets, Pet Owners, and Environment Interface. Front. Vet. Sci, 9, 900480.
Shoaib, M., Rahman, S. U., Aqib, A. I., Ashfaq, K., Naveed, A., Kulyar, M. F.-e.-A., Bhutta, Z. A., Younas, M. S., Sarwar, I., & Naseer, M. A. (2020). Diversified Epidemiological Pattern and Antibiogram of mecA Gene in Staphylococcus aureus Isolates of Pets, Pet Owners and Environment. Pakistan Veterinary Journal, 40(3).
Shoaib, N. F., ul Ain, Q., Iqbal, K., & Asif, M. (2021). Effect of ablution on methicillin resistant staphylococcus aureus (MRSA) nasal colonization in healthcare workers. Journal of the Pakistan Medical Association, 71(5), 1472-1475.
Shomar, R. T. A., Ramlawi, A., Abu-Dan, R., & Elmanama, A. A. (2021). Antimicrobial Resistant Coliforms in Tap Water with Low Free Residual Chlorine Levels in Two Hospitals: Case Study in Gaza, Palestine. Journal of Water Resource and Protection, 13(10), 767-777.
Syed, F., Akhtar, N., Arif, M. A., Ramzan, A., Niazi, R., ubaid Hasnain, S., Hanif, M. D., Asghar, S., & Naheed, A. (2021). A cross sectional study to assess nasal carriage of methicillin resistant Staphylococcus aureus in healthcare professionals in a tertiary care hospital. Journal of the Pakistan Medical Association, 71(1), 205-209.
Syed, M. A., Shah, S. H. H., Sherafzal, Y., Shafi-ur-Rehman, S., Khan, M. A., Barrett, J. B., Woodley, T. A., Jamil, B., Abbasi, S. A., & Jackson, C. R. (2018). Detection and molecular characterization of methicillin-resistant Staphylococcus aureus from table eggs in Haripur, Pakistan. Foodborne pathogens and disease, 15(2), 86-93.
Tariq, A. (2017). Carrier Status of Methicillin-Resistant Staphylococcus Aureus (MRSA). Journal of Rawalpindi Medical College, 21(3), 244-247.
Turner, N. A., Sharma-Kuinkel, B. K., Maskarinec, S. A., Eichenberger, E. M., Shah, P. P., Carugati, M., Holland, T. L., & Fowler, V. G. (2019). Methicillin-resistant Staphylococcus aureus: an overview of basic and clinical research. Nature Reviews Microbiology, 17(4), 203-218.
Venugopal, N. (2019). Molecular detection and typing of MRSA and methicillin-resistant coagulase-negative staphylococci isolated from cattle, animal handlers and their environment from Karnataka, Southern Province of India. Veterinary World , 1760-168.
Von Elm, E., Altman, D. G., Egger, M., Pocock, S. J., Gøtzsche, P. C., Vandenbroucke, J. P., & Initiative, S. (2014). The Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) Statement: guidelines for reporting observational studies. International journal of surgery, 12(12), 1495-1499.
Wagenvoort, J., & Penders, R. (1997). Long-term in-vitro survival of an epidemic MRSA phage-group III-29 strain. Journal of hospital Infection, 4(35), 322-325.
Zafar, U., Johnson, L. B., Hanna, M., Riederer, K., Sharma, M., Fakih, M. G., Thirumoorthi, M. C., Farjo, R., & Khatib, R. (2007). Prevalence of nasal colonization among patients with community-associated methicillin-resistant Staphylococcus aureus infection and their household contacts. Infection Control & Hospital Epidemiology, 28(8), 966-969.
Zeller, J. L., Burke, A. E., & Glass, R. M. (2007). MRSA infections. JAMA, 298(15), 1826-1826.
Zorgani, A., Elahmer, O., Franka, E., Grera, A., Abudher, A., & Ghenghesh, K. (2009). Detection of meticillin-resistant Staphylococcus aureus among healthcare workers in Libyan hospitals. Journal of hospital Infection, 73(1), 91-92.
- Citation du texte
- Asia Gull A Norusta (Auteur), 2022, Environmental burden of MRSA in Pakistan. A meta-analysis of prevalence in non-clinical samples (2016-2022), Munich, GRIN Verlag, https://www.grin.com/document/1434398
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