Abstract
Objectives:
Infections by invasive methicillin-resistant Staphylococcus aureus (MRSA) are associated with higher morbidity and mortality compared to methicillin-susceptible Staphylococcus aureus (MSSA) infections, and have increased significantly in both healthy children and children with chronic illnesses. In our study we aimed to estimate the prevalence of invasive MSSA and MRSA among invasive Staphylococcus aureus (S. aureus) infections in the pediatric population and measure the association between management outcomes and methicillin resistance in these infections.
Methods:
We conducted an observational, analytical, retrospective cross-sectional, chart-review study of pediatric patients (aged ≤16 years) admitted to King Khalid University Hospital in Riyadh, Saudi Arabia during 2019–2023 with invasive S. aureus infections.
Results:
We identified 85 patients with invasive S. aureus infections who met our inclusion and exclusion criteria; 65.9% of all included cases had MSSA infections. Additionally, MRSA infections accounted for 62.5% of all deaths (odds ratio [OR] = 3.68; p = 0.075) suggesting a trend toward higher mortality among MRSA patients. Of those infected with S. aureus, 31.8% required admission to the intensive care unit (ICU), with similar admission rates for both MSSA and MRSA, and both groups had a median hospital stay of 25 days.
Conclusion:
We estimated the prevalence of MRSA infections to be 34.1%. Our study showed a trend toward higher mortality among individuals with invasive MRSA infections than among those with MSSA infections. However, the findings regarding ICU admission rates and length of hospital stay were inconclusive.
Keywords: Methicillin-resistant Staphylococcus aureus, Pediatrics, Staphylococcus aureus
Introduction
Staphylococcus aureus (S. aureus) is a bacterium capable of causing a wide range of infections in individuals across all age groups. The infections range from mild soft tissue infections to invasive infections affecting the lung, bone, joints, bloodstream infections, and other normally sterile body parts [1]. The existing literature commonly defines invasive S. aureus infections as cases in which the bacterium is isolated from a normally sterile body site such as bone, cerebrospinal fluid, or blood [2].
Invasive methicillin-susceptible S. aureus (MSSA) and methicillin-resistant S. aureus (MRSA) infections are common in hospitalized patients and occur in community settings. Invasive MRSA infections have risen markedly among both healthy children and those with chronic conditions. This is a major public health concern because MRSA infections can be difficult to treat and may lead to serious complications, which may ultimately lead to death [3, 4]. Although epidemiological data among pediatric patients is limited, reports suggest an upward trend in both invasive and non-invasive MRSA infections in children [5].
Regarding sites of these invasive infections, most studies suggest that the lung is the most commonly affected (especially in patients with MRSA infections), followed by bloodstream [4, 6, 7]. However, these studies are limited by their sample sizes and reliance on older data. Another study found bones and joints to be the most common infection sites, followed by bloodstream infections; however, these results may not be generalizable, as the study was conducted at a single center [3].
The literature on infection outcomes is more consistent. Recent studies from developed countries revealed that patients with MRSA infections tend to have longer hospital stays and an increased likelihood of admission to a pediatric intensive care unit (ICU) than those with an MSSA infection [3, 7]. In contrast, studies from developing countries have not found any significant differences in the length of stay between MSSA and MRSA patients. However, this claim must be interpreted with caution, as one of the studies had a small sample size limited to children below the ages of 5, and another study excluded the ICU length of stay from the total hospitalization period [5, 8]. Despite some minor variations, the literature indicates longer ICU stays among patients with MRSA infection. Regarding mortality, a study from Utah reported a 3.6% mortality rate for MRSA infections, which was higher than that of patients with MSSA, while another study observed more complications in MRSA cases [3, 9].
Locally, there is limited literature on invasive S. aureus, particularly when focusing on the pediatric population. Among existing studies, a sizable proportion focuses on determining the prevalence of MRSA, but the results have been varied. For example, a 2020 systematic review reported MRSA prevalence among S. aureus strains in the Western, Central, and Eastern regions of Saudi Arabia as 42%, 32%, and 27%, respectively [10]. However, another meta-analysis referenced studies that estimated the national prevalence in Saudi Arabia to be closer to approximately 38% [11]. Older studies have reported broader S. aureus prevalence, ranging between 12% and 49% [10].
When it comes to invasive infections specifically, the systematic review cited studies from the early 2010s showing only 9% of MRSA infections were invasive, whereas the rest were skin and soft tissue infections [10]. However, a study carried out across both Saudi Arabia and Lebanon reported that hospital-acquired MRSA pneumonia accounted for 55% of all MRSA cases and reported a mortality rate of 30-35% in Saudi hospitals owing to MRSA pneumonia [12]. This heterogeneity in study findings makes it difficult to accurately determine MRSA prevalence and assess its severity. Limited local data exists on the risk factors for invasive MRSA infection. A relatively old study suggested that certain chronic conditions may increase the prevalence of MRSA colonization and infection, but this area has not been explored in detail [10].
Local descriptive studies have documented a variety of invasive MRSA presentations. Two case series from 2017 and 2023, along with a literature review, describe invasive manifestations, such as bloodstream infections, infective endocarditis, osteomyelitis, pneumonia, lung abscesses, and brain abscesses. Most cases resolved without complications [13, 14].
This study was conducted to estimate the prevalence of invasive MSSA and MRSA infections among children diagnosed with S. aureus infections and to examine the association between methicillin resistance and management outcomes. We hypothesized that invasive MSSA infections would be more prevalent than invasive MRSA infections, while clinical outcomes such as mortality, median length of hospital stay, and ICU admission rates would be worse among patients with MRSA.
Methods
We conducted an observational, analytical, retrospective cross-sectional study conducted from October 2023 – November 2024, over 14 months, at King Khalid University Hospital (KKUH), Riyadh, Saudi Arabia, a tertiary teaching hospital with a capacity reaching up to 1200 beds. The population of interest was pediatric inpatients aged ≤16 years with an invasive S. aureus infection at KKUH between 2019 and 2023.
We used the single-proportion formula, we calculated that a sample size of 253 participants was required to sufficiently estimate the prevalence, assuming a confidence interval of 95% with a 5% margin of error and a proportion of (74/357) [3]. Furthermore, we added 20% extra to our target to account for potentially insufficient charts, raising the target sample size to 305 participants. However, as the actual number of eligible patients was lower, we included all patients who met the inclusion criteria. The inclusion criteria were pediatric patients aged ≤16 years with a positive S. aureus isolate from a sterile or potentially sterile body site (listed below), collected during 2019 2023 at KKUH. We excluded patients with non-invasive S. aureus infections, incomplete charts, and outpatients from the study. We obtained the patient list from the microbiology laboratory database at KKUH, and included pediatric patients aged ≤16 years from 2019 to 2023 with S. aureus isolates from blood, synovial fluid, bone, peritoneal fluid, pleural fluid, cerebrospinal fluid, pericardial fluid, or soft tissue. We included a maximum of one isolate per listed body site per patient.
We collected data from electronic health records at KKUH, including demographics and clinical characteristics: age, gender, type of infection, setting of acquisition (hospital- or community-acquired), comorbidities, isolate characteristics (site from which S. aureus was isolated and antibiotic resistance pattern), exposure variable (susceptibility to oxacillin (methicillin)), and outcome variables: length of hospital stay, ICU admission, length of stay in the ICU, and mortality.
Microbiological cultures were processed according to internal laboratory policies and procedures. Antimicrobial susceptibility testing was carried out using either the VITEK 2 (Biomerieux, Marcy-l’Étoile, France) or the Microscan Walkaway plus (Beckman Coulter city, California, United States).
Statistical analysis
We analyzed the data using SPSS statistical software 21.0 version for Windows operating system (IBM Inc., Chicago, IL, USA). Further, we also conducted descriptive and bivariate analyses. Descriptive analysis included frequencies, percentages, medians, and interquartile ranges. In the bivariate analysis, Pearson’s Chi-squared test and odds ratios were used to analyze categorical outcome variables. The Mann-Whitney U test was conducted to analyze quantitative outcome variables. A p-value of ≤0.05 was used to report the statistical significance of the results.
Ethical approval for this study was granted by the Institutional Review Board (IRB) of King Saud University (IRB number: E-24-8471) prior to data collection. We collected data in a manner that ensured patient confidentiality and anonymity, wherein a code number was assigned to each participant. Patient data was not shared or collected outside hospital settings. All collected data remained confidential and was used for research purposes only.
Results
We identified a total of 95 patients aged 16 years or younger with positive cultures for S. aureus labeled to a sterile body site between 2019 and 2023. A total of 10 patients were excluded from our analysis because they met the exclusion criteria (5 patients were treated as outpatients, 4 patients had non-invasive S. aureus infections, and one patient had an insufficient chart). Among the remaining 85 patients, the prevalence of invasive MSSA was 65.9% (56 cases), whereas that of invasive MRSA was 34.1% (29 cases). The trends of MRSA and MSSA cases over the study period are presented in Figure 1. A total of 94 isolates of invasive S. aureus were identified for the 85 patients; the majority of which were from the blood, followed by soft tissues, body fluids, and bone (Table 1).
Figure 1.
Trends in invasive Staphylococcus aureus cases over the study period (N = 85).
Table 1.
Distribution of isolates in pediatric patients with invasive Staphylococcus aureus infections.
| MRSA† isolates | MSSA‡ isolatesn | All isolates | |
|---|---|---|---|
| n(%) = 53(56.38) | n(%) = 41(43.62) | N = 94 | |
| Body site | (within Each Variant) | (within the study population) | |
| Blood | 32 (60.4) | 28 (68.3) | 60 (63.8) |
| Body fluids§ | 8 (15.1) | 2 (4.9) | 10 (10.6) |
| Soft tissue* | 11 (20.8) | 5 (12.2) | 16 (17.0) |
| Bone | 2 (3.8) | 6 (14.6) | 8 (8.5) |
Methicillin-resistant Staphylococcus aureus,
Methicillin-susceptible Staphylococcus aureus,
body fluids include (Peritoneal fluid, Cerebrospinal fluid, Pleural fluid, and Synovial fluid).
Tissue include (Lung, Thigh, Scalp, Nasal sinuses, Foot, Neck, leg, and Back).
The median age of all children with invasive S. aureus infections was 6 years (interquartile range [IQR] = 10.75). Regarding gender distribution, there was a nearequal representation with a slight female predominance (51.8% of the study population). Most patients acquired the infection in a community setting, accounting for 63.5% of cases across both groups. Bacteremia was the most common infection type, followed by osteoarticular infections, pneumonia, and others (sinusitis, scalp infection, peritonitis, meningitis, lymphadenitis, infective endocarditis, appendicular abscess, and brain ventricular shunt infection). Comorbidities were classified into eight categories: nephrological, neurological, respiratory, cardiological, endocrine, gastrointestinal, hematological, and “other” (such as allergic, immunological, anatomical, or traumatic comorbidity). Neurological comorbidities were the most prevalent overall at 27.1%. Among patients with MSSA infections specifically neurological comorbidities accounted for 23.2% (n = 13), whereas in MRSA cases, the proportion was higher at 34.5% (n = 10). Nephrological comorbidities were the second most common, observed in 15.3% (n = 13) of patients. Of these, 19.6% (n = 11) were infected with MSSA, and 6.9% (n = 2) with MRSA infection. Patient demographics and clinical characteristics are summarized in Table 2.
Table 2.
Demographic, and clinical characteristics of pediatric patients with invasive Staphylococcus aureus infections.
| Characteristics | MRSA† | MSSA‡ | All |
|---|---|---|---|
| 29 (34.12) | 56 (65.88) | N = 85 | |
| (within each variant) (within the study population) | |||
| Gender | |||
| Male | 16 (55.17) | 25 (44.64) | 41 (48.24) |
| Female | 13 (44.83) | 31 (55.36) | 44 (51.76) |
| Age | Median (Interquartile Range) | ||
| Age(Years) | 5 (10.8) | 6.5 (10.0) | 6 (10.8) |
| Type of infection | |||
| Bacteremia | 16 (55.2) | 30 (53.6) | 46 (54.1) |
| Pneumonia | 4 (13.8) | 3 (5.4) | 7 (8.2) |
| Osteoarticular infections | 4 (13.79) | 11 (19.6) | 15 (17.7) |
| Lower extremity soft tissue infections | 0 (0) | 4 (7.1) | 4 (4.7) |
| Surgical site infection | 0 (0) | 4 (7.1) | 4 (4.7) |
| Other infections§ | 5 (17.2) | 4 (7.1) | 9 (10.6) |
| Setting of acquisition | |||
| Community-acquired | 20 (69.0) | 34 (60.7) | 54 (63.5) |
| Hospital-acquired | 9 (31.0) | 22 (39.3) | 31 (36.5) |
| Comorbidities | |||
| None | 6 (20.7) | 17 (30.4) | 23 (27.1) |
| Any | 23 (79.3) | 39 (69.6) | 62 (72.9) |
| Nephrological | 2 (6.9) | 11 (19.6) | 13 (15.3) |
| Neurological | 10 (34.5) | 13 (23.2) | 23 (27.1) |
| Pulmonary | 5 (17.2) | 6 (10.7) | 11 (12.9) |
| Cardiological | 0 (0) | 8 (14.3) | 8 (9.4) |
| Endocrine | 4 (13.8) | 6 (10.7) | 10 (11.8) |
| Gastrointestinal | 3 (10.3) | 6 (10.7) | 9 (10.6) |
| Hematological | 5 (17.2) | 7 (12.5) | 12 (14.1) |
| Other* | 7 (24.1) | 10 (17.9) | 17 (20.0) |
Values are presented as numbers and percentages (%).
Methicillin-resistant Staphylococcus aureus,
Methicillin-susceptible Staphylococcus aureus,
Other infection types include (sinusitis, scalp infection, peritonitis, meningitis, lymphadenitis, infective endocarditis, appendicular abscess, and brain ventricular shunt infection).
Other comorbidities include (any metabolic/genetic, immunological, rheumatological, ophthalmological, anatomical, or traumatic comorbidities).
The antibiotic resistance profiles of the isolates showed similar patterns between the 2 groups, except for gentamicin, erythromycin, tetracycline, and trimethoprim/sulfamethoxazole. In MRSA infections resistance rates were as follows: gentamicin 24.1%, erythromycin and tetracycline 17.2% (n = 5), and trimethoprim/sulfamethoxazole 10.3%. In MSSA infections, antibiotic resistance was as follows: gentamicin 0%; erythromycin 34% tetracycline 5.4%; and trimethoprim/sulfamethoxazole 1.8% (Table 3).
Table 3.
Antibiotics resistance pattern in pediatric patients with invasive Staphylococcus aureus infections.
| MRSA* | MSSA† | All | ||
|---|---|---|---|---|
| 29 (34.12) | 56 (65.88) | N = 85 | ||
| Antibiotic | (within Each Variant) | (within the study population) | ||
| Oxacillin | 29 (100.0) | 0 (0) | 29 (34.1) | |
| Clindamycin | 4 (13.8) | 5 (8.9) | 9 (10.6) | |
| Erythromycin | 5 (17.2) | 19 (33.9) | 24 (28.2) | |
| Gentamicin | 7 (24.1) | 0 (0) | 7 (8.2) | |
| Daptomycin | 0(0) | 0 (0) | 0 (0) | |
| Vancomycin | 0(0) | 0 (0) | 0 (0) | |
| Tetracycline | 5(17.2) | 3 (5.4) | 8 (9.4) | |
| Trimethoprim Sulfamethoxazole | 3(10.3) | 1 (1.8) | 4 (4.7) | |
| Rifampicin | 1(3.5) | 0 (0) | 1 (1.2) | |
| Teicoplanin | 0 (0) | 0 (0) | 0 (0) | |
| Linezolid | 0(0) | 0 (0) | 0 (0) | |
Values are presented as numbers and percentages (%).
Methicillin-resistant Staphylococcus aureus,
Methicillin-susceptible Staphylococcus aureus.
The median length of hospital stay was 25 days across all patients, with no statistically significant difference between those with MRSA and MSSA infections (Table 4). Among patients diagnosed with S. aureus infections, 27 (31.8%) required ICU admission during their hospital stay. We found that the admission rates were similar, with no statistically significant association between the 2 groups. Nearly one-third of ICU admissions involved invasive MRSA infections, whereas the remaining two-thirds involved invasive MSSA infections. The median length of ICU stay was 12 days, with no statistically significant difference between the 2 groups (Table 4). Our data revealed an overall mortality rate among all patients with S. aureus infections of 9.4% (n = 8). Notably, MRSA infections contributed to 62.5% of the deaths, while MSSA infections accounted for the remaining 37.5 %. Results on death as an outcome showed a statistical trend toward higher mortality in MRSA cases, though not statistically significant (p = 0.075), with the odds of dying for patients with MRSA were 3.68 times higher compared to those for patients with MSSA (Table 4). Among patients who succumbed to mortality, the most common type of infection was bacteremia 50% (n = 4), followed by pneumonia 37.5%, and finally, a single case of peritonitis 12.5%. This pattern was similar for both MRSA (bacteremia [n = 2], pneumonia [n = 2], and peritonitis [n = 1]) and MSSA (bacteremia [n = 2], and pneumonia [n = 1]).
Table 4.
Management outcomes of pediatric patients with invasive Staphylococcus aureus infections.
| MRSA† | MSSA‡ | All | |||
|---|---|---|---|---|---|
| 29 (34.1) | 56 (65.9) | N = 85 | Odds ratio | ||
| Outcome | (within each variant) | (within the study population) | P-value | ||
| Mortality | |||||
| Died | 5 (17.24) | 3 (5.36) | 8 (9.41) | 3.68 | 0.075 |
| Alive | 24 (82.76) | 53 (94.64) | 77 (90.59) | ||
| ICU§ admission | |||||
| Admitted | 10 (34.48) | 17 (30.36) | 27 (31.76) | 1.21 | 0.699 |
| Not admitted | 19 (65.52) | 39 (69.64) | 58 (68.24) | ||
| Length of stay (Days) | Median (Interquartile Range) | p-value | |||
| Hospital length of stay | 27 (23) | 23.5 (32.25) | 25 (28) | 0.867 | |
| ICU§ length of stay | 14 (16) | 12 (23.5) | 12 (26.5) | 0.642 | |
Values are presented as numbers and percentages (%).
Methicillin-resistant Staphylococcus aureus,
Methicillin-susceptible Staphylococcus aureus,
Intensive care unit.
Discussion
It is difficult to compare our results with the existing literature due to the limited and often conflicting heterogeneous data. Two prominent studies analyzing the demographics of invasive S. aureus infections have reported highly different results: one conducted in Utah reported that 21% of infections were caused by MRSA, whereas a study from India found a significantly higher prevalence of nearly 85% [3, 8]. This discrepancy may stem from limited healthcare access in the second study, conducted in a developing country. Alternatively, this could reflect increased infection rates and inappropriate antibiotic use, both of which can drive antibiotic resistance. Another possible confounding factor across studies is small sample size, regardless of setting. Our findings align more closely with the Utah study, with a recorded MRSA prevalence of 34.1%. This similarity may be attributed to comparable healthcare infrastructure and adherence to treatment guidelines. Regarding demographic characteristics, previous studies consistently found no significant associations between MRSA infections and other factors (age and gender), a finding that is consistent with our results.
Few studies have examined the distribution of community-versus hospital-acquired infections, likely due to challenges in pinpointing infection origin, including incomplete histories as well as overlapping coinfections. One study reported that 45.7% of all infections were community-acquired, with a similar distribution between MRSA and MSSA [3]. In contrast, we found a higher proportion (65.5%) of community-acquired infections across both groups. This variation may stem from the referenced study distinguishing between “community acquired” and “community onset healthcare associated” infections, whereas we classified both under community-acquired acquisition.
Neurological comorbidities were the most prevalent in our study population. This differs slightly from the study by Gerber and colleagues, which identified neuromuscular comorbidities as the most common [15]. One possible explanation for the high rate of neurological comorbidities in the current study is the sizable proportion of patients with syndromic conditions involving neurological abnormalities. Comorbidity distributions were similar between MRSA and MSSA groups, with 2 notable exceptions: cardiological and nephrological comorbidities were more prevalent in the MSSA group. This may be because cardiac and nephrological conditions do not typically require frequent antibiotic administration, thereby reducing the risk of acquiring resistant strains.
Antibiotic resistance, particularly in MRSA, remains a significant concern. Our study demonstrated a relatively similar resistance profile between the 2 groups, except for gentamicin, erythromycin, tetracycline, and trimethoprim/sulfamethoxazole antibiotics. We observed that gentamicin resistance was more prevalent in MRSA infections, whereas the Utah study reported clindamycin as the most common resistance [3].
Regarding mortality, one study reported a 3.6% mortality rate in patients with invasive MRSA infections, which was higher than that in MSSA cases [3]. In our study, MRSA accounted for 62.5% of all deaths, with a trend toward higher mortality (OR = 3.68; p = 0.075), though not statistically significant. A possible reason for this large difference could be the significantly smaller sample size and the higher proportion of blood isolates in our study population compared to the Utah study.3 Furthermore, in our study, the distribution of mortality over different types of infections differed somewhat from that reported in other studies. For example, we found that the most common types of infections in mortality cases were bacteremia (50%), pneumonia (37.5%), and peritonitis (12.5%), whereas another study identified osteoarticular infections (38%), central line-associated bloodstream infections (19%), and pneumonia (12%) as the leading causes of mortality [3]. The higher mortality from osteoarticular infections in that study may reflect the underlying patient population, which included a larger proportion of such infections.
Recent studies have indicated that MRSA infections are associated with longer hospital stays and an increased likelihood of ICU admission than those infected with MSSA [3, 7]. However, some studies from developing countries found no significant difference between MSSA and MRSA. We suggest that these claims should be interpreted with caution, due to smaller sample size and inconsistent definitions of hospital stay. For example, the study by Abqari et al [8] included only children under 5 years, while the study by Lalitha et al [6] did not include length of stay within the ICU as part of the total stay. In our study, we found no statistically significant differences in hospital or ICU length of stay between MRSA and MSSA groups. Several factors may explain this, including the small sample size of the study, a higher burden of comorbidities in the MSSA population, and the predominance of bacteremia in ICU admissions, which may have masked the effects of methicillin resistance on outcomes.
Study limitations
This study was limited by its small sample size, as we enrolled fewer patients than originally targeted. We also encountered issues with incomplete documentation in some patient charts due to insufficient reporting. Additionally, we excluded patients with positive cultures from non-sterile body sites, which may have led to underrepresentation of certain types of invasive infections. Finally, the single-center nature of this limits the generalizability. We propose expanding this research through larger, multi-center studies to obtain more generalizable data. Future studies should also explore harder-to-measure factors such as the impact of specific antibiotic therapy, treatment duration, and the relationship between infection sites and outcomes. Our study, limited as it may be, underscores the importance of monitoring and preventing drug resistance in microbial agents, we hope that it may influence stricter and more clear clinical guidelines with regards to empirical therapy.
In summary, we aimed to address the gaps in knowledge regarding the prevalence and outcomes of invasive S. aureus infections in pediatric patients. This is one of the few investigations focused on this topic in the region. We observed an MRSA prevalence of 34.1%, which is in agreement with the results of previous studies conducted under similar conditions. While our results on ICU admission rates and length of hospital stay were inconclusive, we identified a potentially important association between MRSA and higher mortality rates.
It is important to mention that unmeasured confounding factors such as treatment delays, source control differences, and variations in antibiotic selection may have influenced patient outcomes and were not fully accounted for in our analysis. Given the limitations of this study, these findings should be interpreted with caution. Nonetheless, they highlight the need for further investigations through well-powered, multicenter research.
Acknowledgements
We would like to acknowledge the Investigator support Unit (ISU), Prince Naif Health Research Center for the English language editing.
Conflict of Interest
The authors declare no conflict of interest.
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