Streptococcus pneumoniae is a major cause of disease in children and adults with associated high burden of morbidity and mortality. In 2015, the global mortality rate attributed to pneumococcal infection was 45 deaths (29-56) per 100,000 among children aged 1–59 months (1). The spectrum of clinical manifestations ranges from non-invasive disease such as otitis media, to invasive pneumococcal disease (IPD) such as meningitis and bacteremia. In a recent report on the global analysis of lower respiratory tract infections, pneumococcal pneumonia caused more deaths than all other etiologies combined accounting for 1,189,937 deaths in 2016 (2). Although there are >100 serotypes of S. pneumoniae (3, 4), only a limited number are responsible for most IPD. The introduction of vaccines played a role in reducing the burden of morbidity and mortality associated with common vaccine preventable infectious diseases (5, 6). Indeed, this has been demonstrable with pneumococcal conjugate vaccines (PCV), wherein the initial introduction of the seven-valent pneumococcal conjugate vaccine (PCV7) and the subsequent 13-valent vaccine (PCV13) have been effective in reducing the burden of pneumococcal disease in children and adults (7).

Antimicrobial resistance (AMR) is a major global health threat with ~700,000 attributable deaths annually and a projected increase to 10 million by 2050 (8). It has been suggested that by reducing the numbers of the target microbe (both antibiotic susceptible and resistant strains) in circulation, vaccination programs could be a promising additional weapon in the fight against AMR (6, 9). Furthermore, with fewer occurrences of clinical infections following vaccination, a drop in antibiotic utilization is expected which could reduce selection pressure and emergence of resistance strains. For S. pneumoniae, pneumococcal carriage has been described as a critical source of horizontal spread in the community and the effect of vaccination on reduction of nasopharyngeal colonization could also impact antibiotic resistance (10, 11). However, the occurrence of serotype replacement by non-vaccine serotypes and the association with antibiotic resistant pneumococcal strains could negate the expected reduction in AMR trends (7, 9, 10, 12). This highlights the need for surveillance of AMR in S. pneumoniae particularly the tracking of emergent trends after the onset of a PCV vaccination program.

The UAE is highly cosmopolitan with dynamic population movement of large numbers of expatriate residents and tourists from across the world. Hence the emergence and dissemination of AMR pathogens is a concern particularly with reports of novel and variant strains in circulation (13, 14). In the 2011–2013 Survey of Antibiotic Resistance (SOAR) in the Gulf States, susceptibility of S. pneumoniae to most of the antibiotics tested was found to be consistently lower in UAE compared to other countries in the region (15). An earlier report by Senok et al. (16) had identified a high level of penicillin resistance, elevated macrolide and fluoroquinolone resistance and the occurrence of multidrug resistance phenotypes among S. pneumoniae isolated between 2004 and 2006 from patients with community acquired respiratory tract infections in the UAE. In addition, despite the significant risk factors for pneumococcal disease in the Arabian Gulf region, and the calls for heightened pneumococcal surveillance, there remains a paucity of published literature on the burden of pneumococcal infections (17). Indeed, in the UAE, the only two published studies on pneumococcal burden are based on single center data obtained prior to the 2007 introduction of PCV-7 (18, 19). These studies showed a higher incidence rate of pneumococcal disease relative to developed countries (19) with S. pneumoniae as causative agent of 9% of community acquired pneumonia (18). To address this gap in the literature, this report describes S. pneumoniae epidemiology and antibiotic resistance trends in the UAE over a twelve-year period.

This study is a retrospective data analysis for the twelve-year period 2010–2021. This timeframe includes one year prior to the 2011 introduction of PCV-13 in the UAE. AMR trends in S. pneumoniae were assessed by analysis of routine patient care national level AMR surveillance data.

National surveillance programs are crucial for monitoring trends in pneumococcal disease and AMR patterns over time. We present the analysis of S. pneumoniae surveillance and AMR trends in the UAE over a period of 12 years (2010–2021). Our findings provide the first comprehensive epidemiological profile of pneumococcal disease in the UAE and the changing AMR trends which are of significance for clinical management. We demonstrate increased identification of S. pneumoniae in alignment with the increasing number of reporting sites over the data collection period. When normalized for number of study sites a sustained increasing trend of isolates per site observed from 2015 to 2019 which is consistent with global reports of rising pneumococcal disease burden (1, 23–25). The sharp decline observed in reported isolates in 2020 is suggestive of reduction in S. pneumoniae transmission during the first year of the COVID-19 pandemic. This could be attributable to the intense COVID-19 non-pharmacological interventions such as social distancing, masking and hand hygiene practices as well as the rapid change in healthcare-seeking behavior such as increased use of telemedicine and decreased hospital visits during the pandemic (26, 27). However, decreased testing and reporting during this period might have also resulted in the underestimation burden of pneumococcal disease.

Our findings show a male preponderance which may be a reflection of the demographic distribution of the UAE population but is also in keeping with reported literature from other studies (28, 29). The reasons for the male preponderance in pneumococcal disease are not fully understood hence further research is needed to elucidate the underlying factors as well as identify the potential implications for prevention and treatment strategies. The fact that most of our patients were in the pediatric age group is particularly relevant because nasopharyngeal carriage of S. pneumoniae is more prevalent in children compared to adults (30, 31). Indeed, nasopharyngeal isolates accounted for 22.7% of all isolates irrespective of specimen source and specifically for respiratory tract specimens, 44.4% of isolates were nasopharyngeal colonizers. Children are more likely to be colonized with S. pneumoniae due to their immature immune systems and increased exposure to respiratory pathogens and pneumococcal colonization contributes to the risk of IPD in children (24, 32). These findings underscore the need for targeted preventive measures to protect this vulnerable population (32). Vaccination against S. pneumoniae is particularly important in the pediatric population, as it has been associated with reduction in pneumococcal nasopharyngeal carriage leading to a reduced risk of IPD (33, 34).

Understanding the dynamics of pneumococcal disease and antimicrobial resistance is essential for developing robust intervention and treatment strategies. High levels of occurrence of nasopharyngeal carriage of S. pneumoniae can lead to the selection and spread of antibiotic resistant strains. Elevated levels of resistance to penicillin, macrolides and fluoroquinolone as well as the occurrence of multidrug resistance phenotype were reported in S. pneumoniae isolates in the UAE in a study carried out prior to the advent of the PCV vaccination program (16). In that report, of the 100 isolates identified between 2004 and 2006 only 57% were penicillin susceptible (16). Our findings which show high occurrence of penicillin resistant S. pneumoniae suggests that these isolates are now endemic in our setting. In contrast to the downward trend observed for beta-lactam antibiotics, resistance to quinolones, and macrolides showed an upward trend which is in keeping with findings from other countries in the region (35, 36). In Kuwait, the downward trend in penicillin resistance, has been shown to be associated with the introduction of the PCV and circulating serotypes (32, 35). The finding of similar trends of resistance for the two macrolide antibiotics aligns with previous report from the UAE which demonstrated high occurrence of level of cross-resistance between erythromycin and clindamycin (16). The ramifications of the increasing occurrence of S. pneumoniae MDR strains are immense including limitations on the effectiveness of antibiotics for the treatment of pneumococcal infections, which will further increase healthcare costs and the burden of disease. These findings underscore the need for continued surveillance and implementation of effective antibiotic stewardship programs to combat this growing AMR threat.

IPD and non-IPD differ in terms of their pathogenesis and clinical presentation. IPD is a severe and potentially life-threatening infection associated with invasion of sterile body sites while non-IPD is typically less severe and limited to non-sterile sites (37). The findings from this study represent the first insight into IPD burden in the UAE encapsulating the period post-commencement of the pneumococcal vaccination program. Expectedly, higher hospitalization with longer duration was observed for IPD patients. However, the high occurrence of MDR phenotype in both IPD and non-IPD isolates is a cause for concern as it suggests that emergence of resistant strains of S. pneumoniae is ongoing in our setting.

Our findings reveal the absence of data on S. pneumoniae serotypes circulating in our setting which is a limitation of the existing surveillance dataset. The emergence of non-vaccine serotypes and their increasing antimicrobial resistance is a reminder of the importance of ongoing surveillance to monitor changes in pneumococcal serotypes and their AMR patterns. Such data can inform the development of new and improved pneumococcal vaccines that provide coverage against a wider range of clinically relevant serotypes. We advocate for the urgent initiation of a national S. pneumoniae serotyping and genomic surveillance program as data from such initiative will be useful in guiding policy decisions for the introduction of new pneumococcal vaccines and vaccination schedules. In addition, such surveillance data will be useful for mapping genomic changes associated with serotype switching from vaccine pressure, as well as provide early warnings for emergence of resistance and the spread of global clones. The occurrence of a high percentage of missing data and information about specific population risk groups are limitations observed in this national AMR surveillance dataset. This highlights the need for continued provision of training to personnel at participating sites as well as expansion of the clinical parameters included in the dataset.

Our analysis of the national S. pneumoniae AMR surveillance data provides insights into the evolving patterns of pneumococcal disease and antimicrobial resistance in the UAE. The findings highlight the need for the introduction of a S. pneumoniae serotype surveillance program to guide the pneumococcal vaccination program, as well as continued AMR monitoring and targeted intervention measures to address the growing threat of antibiotic resistance.

The datasets presented in this article are not readily available because the National AMR Surveillance database managed by the UAE Ministry of Health and Prevention (MOHAP) contains confidential health information. Requests to access the datasets should be directed to https://mohap.gov.ae/.

Ethical approval for this study was provided by the Ministry of Health and Prevention Research Ethics Committee (MOHAP/DXB-REC/D.D.D/No.131/2021; MOHAP/DXB-REC/J.J.J./No. 86/2023), Dubai Scientific Research Ethics Committee (DSREC-GL17-2023), and Abu Dhabi Health Research and Technology Ethics Committee (DOH/ZHCD/2023/1316). The studies were conducted in accordance with the local legislation and institutional requirements. Written informed consent for participation was not required from the participants or the participants' legal guardians/next of kin in accordance with the national legislation and institutional requirements.

Conceptualization, data interpretation, and manuscript review and editing: AS, JT, NA, GM, CA, and DE. Data collection: AS, JT, NA, GM, CA, DE, and The UAE AMR surveillance consortium. Formal analysis and manuscript preparation: AS and JT. All authors have read and agreed to the published version of the manuscript.