Bacterial culture and antibiotic resistance pattern in chronic rhinosinusitis among patients who underwent sinus surgery

Abstract

Objective

Chronic rhinosinusitis (CRS) is a common inflammatory condition affecting a large portion of the population worldwide. Bacterial infections are one of the causes of recurrence and treatment resistance in CRS. Our goal is to describe antimicrobial resistance patterns in patients with CRS who underwent functional endoscopic sinus surgery (FESS).

Methods

A retrospective chart review was conducted at King Abdulaziz University Hospital, which included 444 patients who underwent 444 FESS procedures between January 2014 and December 2018.

Results

A total of 98% of the patients underwent primary FESS. Of the 803 cultured samples, 611 (76%) yielded bacterial growth. The most frequently isolated organisms were Staphylococcus aureus (32%), Klebsiella pneumoniae (10.6%), and Pseudomonas aeruginosa (9.7%). Gram-positive organisms were most susceptible to vancomycin and ofloxacin.

Conclusion

A wide range of microorganisms were obtained from patients with CRS. The antibiotic resistance of microorganisms in CRS is an important issue because many of the pathogens are noted to be resistant to commonly used antibiotics.

Clinical trail

Not applicable.

Introduction

Chronic rhinosinusitis (CRS) is a common multifactorial inflammatory disease of paranasal sinuses; it persists for a minimum of 12 weeks and has significant adverse impact on patients’ quality of life. The common symptoms include nasal discharge, nasal obstruction, reduced sense of smell and facial pain [1]. According to a recent study approximately 5% of the global population is affected with CRS, and even at this proportion, it has imposed a significant socioeconomic burden to the healthcare systems in the form of reduced productivity, increased cost of care and recurrent medical visits [2].

CRS has a complex pathophysiology as it involves interplay of multiple variables such as the immune responses of host, microbial communities and environmental factors [3]. Traditionally, CRS was believed to be an infectious disease due to bacterial pathogens. However, the contemporary evidence suggest otherwise, CRS is now labelled as a chronic inflammatory condition in which sinonasal microbiome are major culprits rather than a specific pathogenic organism [4]. One researcher argued that the underlying mechanism for CRS is microbiota dysbiosis, a condition identified as an imbalance in the diversity and the composition of the microbiota [5].

Earlier studies suggested that the paranasal sinuses were sterile in healthy individuals; however, contemporary evidence using molecular techniques has demonstrated that the sinuses harbor a diverse microbiome even in health [6]. It has been reported that paranasal sinuses harbor diverse microbial ecosystem which plays a vital role in maintain mucosal homeostasis. Michalik (2024) reported that the balance of microbiota is disrupted in CRS which leads to chronic inflammation and impaired mucociliary clearance [4]. Despite this evidence, culture-based microbiology is still practiced in clinical settings to identify potential pathogenic microbe and to develop an antimicrobial therapy.

Furthermore, the role of bacteria in CRS remains unclear. It has been reported that bacterial colonization exacerbates the disease, but there is limited evidence which supports the role of bacteria in the initiation of CRS [1]. Therefore, the current treatment regimen of antibiotics in CRS is questioned. According to the European Position Paper on Rhinosinusitis and Nasal Polyps (2020), antibiotics are not recommended as first-line of treatment for CRS and it should be reserved primarily for acute exacerbations [7]. Moreover, a previous study has also reported inconsistent and minimal effect of antibiotic therapy in the outcome of CRS management [2].

Despite these debates, bacterial culture is still considered an important diagnostic tool in patients undergoing functional endoscopic sinus surgery (FESS) to gain an insight into the microbial profile and analyze the antibiotic resistance pattern. Besides, increased antibiotic exposure significantly increases the risk of antimicrobial resistance. In contrast to otitis media and acute bacterial rhinosinusitis, CRS has received relatively little attention in regard to the prevalence of antibiotic resistance. The goal of this study was to identify the most common organisms in CRS. We also aimed to identify the most sensitive and resistant antibiotics in our region to direct the medical management of CRS.

Methods

This retrospective study was conducted at King Abdulaziz University Hospital in Riyadh, Saudi Arabia and entailed a chart review of 444 patients who underwent 444 functional endoscopic sinus surgery (FESS) procedures performed between January 2014 and December 2024. The inclusion criterion was CRS that did not respond to maximum medical treatment. Patients were not stratified into CRS with nasal polyps (CRSwNP) and CRS without nasal polyps (CRSsNP) according to EPOS 2020 criteria, which represents a limitation of this study. Eligible patients were adults aged 18 years or older with a confirmed diagnosis of CRS based on EPOS criteria, defined as sinonasal symptoms persisting for at least 12 weeks supported by endoscopic or CT findings, whose condition had not responded to a full course of maximum medical therapy comprising systemic antibiotics and intranasal corticosteroids for a minimum of 12 weeks. Patients were excluded if their medical records were incomplete or lacked intraoperative culture data, if they had an immunocompromising condition other than diabetes mellitus, or if their primary diagnosis was other than CRS (for example, sinonasal neoplasm or allergic fungal rhinosinusitis). Regarding microbiological methods, specimens were collected intraoperatively using sterile swabs or tissue biopsies from the middle meatus and, where surgically accessible, from deeper sinus tissue. Samples were placed in Amies transport medium and transferred to the microbiology laboratory within two hours of collection. Organisms were identified by conventional culture and standard biochemical methods. Antibiotic susceptibility was determined by the Kirby-Bauer disk diffusion method, with results interpreted against Clinical and Laboratory Standards Institute (CLSI) breakpoints applicable at the time of testing. All cultures were aerobic, in keeping with the routine protocol of the institutional laboratory during the study period; anaerobic culture was not part of this protocol and was therefore not performed. This was a practical rather than a scientifically motivated exclusion, and its implications for the completeness of the microbiological profile are discussed in the Limitations section.

Of the total collected specimens, only 803 were processed for culture based on clinical relevance and laboratory selection criteria (e.g., suspected infection or adequate sample quality). The specimens were collected from the middle meatus and deep tissue and were sent for microbiology culture and antibiotic sensitivity testing. Only aerobic bacterial cultures were performed according to institutional laboratory protocols, and anaerobic cultures were not routinely conducted. The 444 patients contributed a total of 803 samples, giving a mean of 1.81 samples per patient, because specimens were taken from multiple sinus sites — including the middle meatus, maxillary, ethmoid, frontal, and sphenoid sinuses — in the same individual where the clinical picture warranted it. A sample was sent for culture processing when the operating surgeon documented endoscopic purulence or a clinical suspicion of active infection, and when the sample was of sufficient volume and quality for laboratory analysis; samples that were inadequate — for example dry swabs or those with probable surface contamination — were not processed. Because some patients contributed more than one sample, the sample rather than the patient served as the unit of microbiological analysis, and this is acknowledged as a limitation of the study design. It is also worth noting that this selection process may have concentrated the dataset toward more severely affected cases, and the microbial profiles described here may not fully reflect the spectrum of organisms encountered across the wider CRS surgical population.

The data were fed into the rhinology research data center to facilitate data management and analysis. Statistical analysis was performed using SPSS version 20 (IBM Corp., Armonk, NY, USA). Descriptive statistics were used to summarize the data. Categorical variables were presented as frequencies and percentages. Where applicable, chi-square tests were used to compare categorical variables, and a p-value of < 0.05 was considered statistically significant. Chi-square tests were used to compare the distribution of isolated organisms across subgroups defined by patient sex, diabetes status, and type of surgery. Where expected cell counts fell below five — as occurred in several comparisons involving the revision surgery subgroup, which comprised only nine patients — Fisher’s exact test was used in place of chi-square. The study was primarily descriptive in intent, and no continuous variable comparisons were undertaken. Given the large number of organism-antibiotic combinations examined, all inferential tests should be treated as exploratory and no correction for multiple testing was applied. It should also be acknowledged that, because some patients contributed more than one sample, the strict independence assumption of chi-square is not satisfied; the results are therefore best regarded as hypothesis-generating. Antibiotic resistance rates are expressed as the percentage of resistant isolates out of all isolates tested for a given organism-antibiotic pairing. Ethical approval to conduct this research was obtained from King Saud University Research Center.

Results

Of the 444 patients included in the study, 250 were male (56%) and 194 were female (44%). The mean age was 34 years. Diabetes was present in 64 (14%) of the patients. The majority (98%) underwent primary FESS and a small minority (2%) had revision FESS. The main patient characteristics are summarized in Table 1.

Table 1.

Demographic data, underlying disorders, and type of surgery

Sex	Male Female	250(56%) 194(44%)
Mean age		34 years
Diabetes		64(14%)
Type of FESS	Primary Revision	435 (98%) 9 (2%)

Abbreviation: FESS, functional endoscopic sinus surgery

A total of 803 samples from 444 FESS procedures (primary and revision) were sent for culture and sensitivity analyses. Pathogens were isolated from 611 (76%) of these samples, while the remaining 24% of samples showed no bacterial growth. It is important to note that samples with no bacterial growth may still contain commensal organisms which are not reported in microbiology laboratory because they are considered clinically insignificant. About 77% of the total isolated pathogens were single organisms, but multi-pathogens accounted for 23% of the total isolated pathogens. Further details about samples and isolated pathogens are shown in Table 2.

Table 2.

Specimens collected and pathogens isolated

Specimenscollected	Total	803
PathogensIsolated	Total Nasal/Frontal Maxillary Sphenoid Ethmoid	611 − 298 (53%) − 122 (21%) − 66 (12%) − 80 (14%)
Pathogens isolated in patients with diabetes		128 (21%)
Pathogens isolated according to type of FESS	Primary Revision	596 (98%) 15 (2%)

Abbreviation: FESS, functional endoscopic sinus surgery

The most frequently isolated organisms were Staphylococcus aureus (n = 198, 32%), Klebsiella pneumoniae (n = 65, 10.6%), and Pseudomonas aeruginosa (n = 59, 9.7%). However, P. aeruginosa was the most frequently isolated organism in revision surgeries (7 of 15). The complete list of isolated pathogens is given in Table 3.

Table 3.

Pathogens isolated from the collected specimens

Organisms	Primary	Revision
Acinetobacter calcoanitratus	1
Citrobacter diversus	27
Citrobacter freundii 1	9
Enterobacter cloacae 1	33
Enterococcus species		3
Escherichia coli 1	32
Enterobacter aerogenes	21
Haemophilus influenza	7
Klebsiella aerogenes 1	5	4
Klebsiella oxytoca	22
Klebsiella pneumonia	65
Methicillin-resistant Staphylococcus aureus	9
Moraxella catarrhalis	3
Morganella morganii	2
Enterococcus species	3
Proteus mirabilis	4
Pseudomonas aeruginosa	52	7
Salmonella Serogroup G1	4
Serratia marcescens 1	14
Staphylococcus aureus 1	197	1
S. aureus Group B	2
Staphylococcus epidermidis 1	9
Staphylococcus species	1
Streptococcus Group A	13
Streptococcus Group B	28
Streptococcus pneumoniae	33
Total	596	15

The pathogens were tested for antibiotic susceptibility. Among the S. aureus isolates, the resistance rates to polymyxin B, penicillin G, and ampicillin were extremely high (100%, 95%, and 95%, respectively). However, the resistance rates were low to vancomycin (0%), gentamicin (0%), tetracyclines (11%), sulfamethoxazole-trimethoprim (9%), ofloxacin (5%), methicillin (4.8%), cefuroxime (11.7%), ciprofloxacin (7%), chloramphenicol (2.7%), and amoxicillin (8%).

For K. pneumoniae isolates, resistance rates to ampicillin (100%), cephalexin (28%), and amoxicillin (25%) were higher than 20%. However, the resistance rates of K. pneumoniae to ofloxacin (0%), gentamicin (0%), ciprofloxacin (0%), ceftriaxone (4.4%), sulfamethoxazole-trimethoprim (4%), and polymyxin B (3.8%) were much lower.

Among the S. pneumoniae isolates, there was high resistance to polymyxin B (100%), penicillin G (61%), gentamicin (100%), ampicillin (61%), and amoxicillin (61%). However, low rates of resistance to vancomycin (0%), ofloxacin (0%), cefuroxime (0%), ceftriaxone (0%), erythromycin (15%), and clindamycin (15%) were demonstrated. More details about the antimicrobial resistances of the frequently isolated pathogens are shown in Table 4.

Table 4.

Antimicrobial resistance of frequently isolated pathogensto different antimicrobial agentsin patients with chronic rhinosinusitis

	Staphylococcus aureus		Klebsiella pneumonia		Streptococcus pneumoniae		Streptococcus Group A		Staphylococcus epidermidis
Sensitive vs. resistant	S	R	S	R	S	R	S	R	S	R
Vancomycin	72	0	0	0	11	0	3	0	5	0
Tetracycline	73	9	0	0	9	3	6	0	5	0
Sulfamethoxazole Trimethoprim	20	2	24	1	0	0	0	0	1	0
Penicillin G	4	77	0	0	5	8	6	0	1	4
Polymyxin B	0	73	25	1	0	10	0	4	1	4
Ofloxacin	53	3	26	0	8	0	2	0	3	0
Norfloxacin	3	0	5	0	0	0	0	00	0	0
Nafcillin	0	0	2	0	0	10	0	0	0	0
Methicillin	79	4	0	0	0	0	0	0	3	1
Meropenem	4	0	13	1	0	0	0	0	0	0
Imipenem	5	0	16	0	0	0	0	0	0	0
Gentamicin	75	0	29	0	0	10	0	4	0	0
Cefoxitin	35	0	20	2	0	0	0	0	4	1
Cefixime	3	0	2	0	0	0	0	0	2	0
Erythromycin	68	15	0	0	11	2	6	0	2	2
Cefazolin	1	1	3	0	0	0	0	0	0	0
Cefuroxime	46	5	26	2	13	0	6	0	3	0
Cefotaxime	0	0	14	0	0	0	0	0	0	0
Ceftriaxone	10	0	28	1	13	0	2	0	2	0
Cephradine	54	29	0	1	5	8	6	0	1	4
Cephalexin	1	1	18	8	0	1	0	0	0	0
Clindamycin	69	13	0	0	11	2	6	0	4	1
Ciprofloxacin	40	3	28	0	1	0	2	0	2	0
Chloramphenicol	72	2	24	3	10	0	4	0	5	0
Ceftazedime	1	1	26	0	2	0	0	0	1	0
Aztreonam	1	0	19	0	0	0	0	0	0	0
Ampicillin	4	79	0	29	5	8	6	0	1	5
Amoxicillin	23	2	21	7	5	8	4	0	1	0

P. aeruginosa was most sensitive to imipenem (100%), ciprofloxacin (100%), amikacin (100%), ceftazidime (96%), gentamicin (91.4%) and piperacillin (90%), while it was completely resistant to chloramphenicol (100%) and indicated high rates of resistance to ticarcillin (45%) and carbenicillin (41.6%). The antibiotic susceptibility of P. aeruginosa that was isolated from study participants is demonstrated in Fig. 1.

Fig. 1.

Antibiotic susceptibility of P. aeruginosa that was isolated from study participants

Discussion

The role of microbiologic pathogens is controversial in the pathophysiology and failure of medical treatment for CRS. In the present study, bacterial pathogens were isolated from 76% of cultured samples with S. aureus (n = 198, 32%), K. pneumoniae (n = 65, 10.6%), and P. aeruginosa (n = 59, 9.7%) were most frequently identified microbes. The findings of present study align with previous culture-based studies, but it is pertinent to be cautious with interpretation with in the evolving pathophysiology of the sinonasal microbiota.

The most important findings of present study are the predominance of S. aureus (32%), which is consistent with previous studies reporting the same bacteria in severe CRS and refractory disease [8, 9]. Couple of studies reported biofilm formation and superantigen as the underlying mechanism through which S. aureus may contribute to the inflammation and resistance to treatment [10, 11]. However, Cho et al. (2020), argued that the exact role of S. aureus is still unclear because it may act as a pathogen or commensal organism depending on the microbial interactions and host immune status [8]. Therefore, the culture-based approaches are limited in their distinction between pathogenicity and colonization.

One notable finding of current study was relatively high prevalence of Gram-negative bacteria, specifically, K. pneumoniae (10.6%) and P. aeruginosa (9.7%). Recent studies also support the findings of present study and reported large number of Gram-negative isolates in CRS, specifically in patients with prolonged antibiotic exposure or prior surgery experience [12, 13]. Moreover, P. aeruginosa was frequently reported in present study among cases with revision surgeries. This supported previous evidence that surgical intervention may select for resistant organisms [14]. These assertions are clinically significant owing to association of P. aeruginosa with poor surgical outcomes, persistent infection and biofilm formation [15].

Another important finding of present study is the strong antibiotic resistance among commonly isolated pathogens. For instance, S. aureus showed high level resistance to penicillin and ampicillin which is consistent with global trends of beta-lactam resistance [16]. However, S. aureus demonstrated higher susceptibility to vancomycin and gentamicin which aligns with regional and international data [17]. Similarly, high resistance was observed in K. pneumoniae for ampicillin, but sensitivity improved to aminoglycosides and fluoroquinolones [18]. These patterns of antibiotic resistance outline the need for culture-directed therapy and antibiotic stewardship in the management of CRS.

Despite these results, there is an ongoing debate regarding the role of bacteria in CRS pathogenesis. For instance, previous studies have verified that CRS is a microbial dysbiosis, in which the composition and diversity of sinonasal microbiome is changed [8, 19]. Furthermore, recent advancement in molecular techniques have also contested the earlier assumptions of sterility in sinuses [20, 21]. Therefore, the presence of bacteria in CRS does not necessarily indicate causation, and culture results must be interpreted cautiously within the broader context of host–microbe interactions.

In a recent study, the authors compared the standard hospital culture (SHC) to the DNA sequencing analysis for pathogen detection in CRS individuals [22]. The most common organisms recognized through SHC were P. aeruginosa and S. aureus, each identified in 10 cultures. The DNA sequencing analysis, meanwhile, revealed that S. epidermidis was the single most commonly identified organism, detected in 13 cultures. S. epidermidis is generally considered part of the normal sinonasal microbiota rather than a true pathogen; therefore, its identification in this study likely reflects laboratory reporting practices rather than true pathogenicity. The authors concluded that the reliability of pathogen detection among CRS patients depends principally on the applied technique. Thus, DNA sequencing analysis may demonstrate more accuracy than SHC, especially in cases of chronic resistant polymicrobial infections.

In this study, Gram-positive organisms (i.e., S. aureus and S. pneumoniae) and CNS were most susceptible (100%) to vancomycin. These pathogens were also susceptible to ofloxacin, with 95% sensitivity for S. aureus and 100% sensitivity for S. pneumoniae and CNS. More recently, a study by Vandelaar et al. showed that among all samples collected from 134 patients, the highest prevalence of bacterial taxa was for Streptococcus spp. (31.1%), followed by Pseudomonas spp. (20.0%), S. aureus (20.0%), and S. epidermidis (11.9%) [9].

In 2016, a cross-sectional study was carried out in Iran to determine the antibiotic resistance pattern of the bacteria causing CRS [23]. Gram-negative bacteria had the highest rate (76.47%) of multi-drug resistance, with Enterobacter spp. being the predominant isolate (70.37%). In addition, about 74% of the Gram-negative bacteria had multi-drug resistance, with S. aureus being the most frequently reported pathogen (90%).

Recently, a study obtained middle meatus swabs and tissue samples during sinus surgery in 18 patients: five cases with CRS with nasal polyps, five cases with diffuse CRS without nasal polyps, five cases with unilateral purulent maxillary CRS, and three cases with healthy mucosa [24]. Upon examination, the most commonly cultured organism from the swabs were P. acnes, S. epidermidis, Corynebacterium spp., and S. aureus. In addition, gene analysis detected no definite variation in the bacterial community of the control group versus CRS cases of unilateral purulent maxillary CRS and CRS with nasal polyp, but there was a significant difference between healthy samples and CRS samples without polyps.

Although antibiotics constitute a major aspect of CRS management, especially in cases of exacerbated conditions, there are hazardous issues of drug misuse, such as financial burden and risk of developing Clostridium difficile colitis. Further and more importantly, it may lead to drug resistance, which results in extended hospital admission and has an associated high mortality rate. Additionally, standard microbiology laboratory practices typically report only clinically significant pathogens while omitting commensal organisms. This reporting bias may explain the relatively low prevalence of organisms such as Staphylococcus epidermidis in this study. Notably, molecular studies have demonstrated that S. epidermidis is one of the most abundant commensal organisms in the sinonasal cavity and may even exert protective effects by inhibiting pathogenic bacteria [25, 26]. Therefore, its classification as a pathogen in culture-based studies should be interpreted with caution.

Variability in microbiological findings across studies may also be attributed to differences in sampling techniques, patient populations, and diagnostic methodologies. Culture-based methods, although widely used in clinical practice, have limited sensitivity and fail to detect non-culturable or fastidious organisms [22]. In contrast, next-generation sequencing provides a more comprehensive understanding of microbial diversity but is not yet routinely available. This discrepancy contributes to inconsistencies in reported microbiological profiles and highlights the need for integrating molecular diagnostics into future research.

There are some important limitations in this study. The first limitation is that it was performed in a single institution, and therefore we cannot generalize our results. However, our relatively large sample size could minimize any discrepancies in the results when compared with other regional studies. Another limitation is that participants’ antibiotic use prior to surgery is unknown and could have altered the microbial pattern. This could be easily prevented by instructing patients to not use antibiotics for a sufficient period before FESS. Furthermore, the lack of phenotypic classification of CRS (CRSwNP vs. CRSsNP) limits the ability to assess microbiological differences between disease subtypes. Additionally, the absence of anaerobic cultures may have resulted in underestimation of anaerobic pathogens. Several additional limitations deserve more detailed consideration. As a retrospective chart review, the study is susceptible to incomplete or inconsistent documentation, and cultures are likely to have been sent selectively in more severely affected cases, which may have skewed the microbial profile toward organisms associated with complicated or refractory disease. Prior antibiotic use is perhaps the most consequential uncontrolled variable in this study. Because all patients had CRS that had failed maximum medical treatment, the overwhelming majority will have received at least one — and often multiple — antibiotic courses before undergoing surgery. Antibiotic exposure suppresses susceptible strains and selects for resistance, so the resistance rates reported here, and particularly the high rates of penicillin and ampicillin resistance seen across several organisms, may reflect the cumulative effect of this selective pressure rather than underlying regional epidemiology. Future work should prospectively capture antibiotic histories and, where the data allow, compare microbiological profiles between antibiotic-exposed and antibiotic-naive patients. The multiple-samples-per-patient issue also has implications beyond the statistical ones already noted: because the sample rather than the patient was the unit of analysis, the dataset over-represents patients from whom several specimens were taken, and ideally the analyses would be revisited using generalised estimating equations or a mixed-effects model that accounts for within-patient clustering. Without such reanalysis, the inferential results remain exploratory. The absence of anaerobic cultures further limits the completeness of the microbiological picture. Anaerobic organisms — among them Peptostreptococcus, Fusobacterium, and Prevotella species — have been detected in up to 30 to 40% of CRS cases when appropriate methods are used, and their exclusion here means the true burden of anaerobic infection is likely underestimated. As noted earlier, this reflected routine institutional practice rather than a deliberate methodological choice, and future studies should incorporate anaerobic culture as standard.

Overall, while this study reinforces the relevance of culture-based microbiology in identifying bacterial pathogens and guiding antimicrobial therapy, it also underscores its limitations in capturing the complexity of CRS. Future research should aim to integrate culture-based findings with molecular microbiome analysis and clinical phenotyping to develop more targeted and personalized treatment strategies.

Conclusion

This descriptive study of CRS microbiology, along with present and future similar studies, provides a basis for interpretation that will improve data accuracy and medical practice. This is especially important in Saudi Arabia and the Gulf states, where there is almost no literature on this topic.

With the increasing rates of resistance, we recommend culture-directed antibiotic therapy for patients with CRS whenever possible and use of a single broad-spectrum antibiotic when there are no available sensitivity tests. We also recommend avoiding beta lactam antibiotics (especially penicillin and ampicillin), given that Gram-positive organisms in this study and many others have shown high rates of resistance. That said, these recommendations need to be read alongside the study’s methodological constraints. The high resistance rates to beta-lactam antibiotics observed in this cohort likely reflect, at least in part, the heavy prior antibiotic exposure inherent to a treatment-refractory surgical population, and it would be premature to use these figures to guide empirical prescribing without corroboration from prospective or population-based data. Culture-directed therapy remains the most defensible approach whenever it is available, but in practice clinicians will need to weigh culture findings against each patient’s individual antibiotic history and disease phenotype before deciding on treatment.

We also recommend further studies of CRS microbiology and antibiotic resistance, especially in Saudi Arabia, where there is insufficient literature to establish a management plan. Furthermore, there is wide variation among the microbiologic components in patients with CRS around the world.

Author contributions

T.A.: methodology, and writing manuscript. F.A.: data collection, and data analysis. S.A.: manuscript review, data collection and editing.

Funding

This study is supported via funding from Prince sattam bin Abdulaziz University project number (PSAU/2025/R/1447).

Data availability

The data supporting the conclusions of this study are not publicly accessible due to privacy considerations but may be requested from the corresponding author.

Declarations

Human ethics and consent to participate

This study was approved by research committee and the Internal Review Board (IRB) at King Saud University Research Center. All participants received an information sheet regarding the study purpose, type of data which will be collected, and the voluntary nature of participation. A consent form was obtained from all participants. All procedures involving human participants were performed in accordance with the ethical standards of the Declaration of Helsink.

Competing interests

The authors declare no competing interests.