Impact of COVID-19 Nonpharmaceutical Interventions on Pneumococcal Carriage Prevalence and Density in Vietnam

Nation, Monica Larissa; Manna, Sam; Tran, Hau Phuc; Nguyen, Cattram; Vy, Le Thi Tuong; Uyen, Doan Y; Phuong, Tran Linh; Dai, Vo Thi Trang; Ortika, Belinda D.; Wee-Hee, Ashleigh; Beissbarth, Jemima; Hinds, Jason; Bright, Kathryn; Smith‐Vaughan, Heidi; Nguyen, Thuong Vu; Mulholland, Kim; Temple, Beth; Satzke, Catherine

doi:10.1128/spectrum.03615-22

Cited by 14 publications

(7 citation statements)

References 26 publications

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“…However, incorporating a mechanism of reduced risk for developing an IPD due to the absence of circulation of common respiratory viruses led to similar estimates of the relative reduction in IPD incidence as reported in the EU/EEA for 2020 (Brueggemann et al, 2021; European Centre for Disease Prevention and Control and World Health Organization, 2022). This finding, coupled with the outcome of other studies that found a generally stable pneumococcal carriage prevalence in healthy individuals, both children and adults, during COVID-19 containment measures (Nation et al, 2023; Petrović et al, 2022; Rybak et al, 2022; Willen et al, 2022; Wyllie et al, 2023), supports the alternative hypothesis. This explanation accounts for the decreased incidence of IPD, rather than attributing it to reduced pneumococcal transmission, which resulted in a significant reduction in carriage according to the simulations (Smith and Opatowski, 2021).…”

Section: Discussionsupporting

confidence: 77%

“…This explanation accounts for the decreased incidence of IPD, rather than attributing it to reduced pneumococcal transmission, which resulted in a significant reduction in carriage according to the simulations (Smith and Opatowski, 2021). Furthermore, a study in Vietnam found that reductions in IPD associated with NPIs may be due to reductions in overall pneumococcal carriage density rather than carriage prevalence, driven by reductions in capsular pneumococcal carriage density frequently implicated in IPD (Nation et al, 2023). Considering that common respiratory viruses such as influenza increase pneumococcal carriage density, which contributes to transmission and disease, this hypothesis seems plausible (Alpkvist et al, 2015; Diavatopoulos et al, 2010; McCullers et al, 2010; Short et al, 2012; Wolter et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…Similar declines in bacterial disease during early waves of COVID-19 have been observed in the context of sentinel community-acquired infections in New Zealand (Duffy et al, 2021), IPDs in Taiwan (Chien et al, 2021) and Hong Kong (Teng et al, 2022), and lower respiratory tract infections in China (Chen et al, 2021). Yet, surprisingly, a growing number of studies have reported mostly stable pneumococcal carriage throughout the COVID-19 pandemic containment, including among infants in Belgium (Willen et al, 2022), children in Vietnam (Nation et al, 2023), Serbia (Petrović et al, 2022), France (Rybak et al, 2022), South Africa (Olwagen et al, 2023), and Israel (Dagan et al, 2023), adults in Connecticut (Wyllie et al, 2023), and households in Seattle (Bennett et al, 2023). In contrast, a study conducted in Denmark reported a decrease in pneumococcal carriage among older adults during the COVID-19 lockdown (Tinggaard et al, 2023).…”

Section: Introductionmentioning

confidence: 99%

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Revealing the drivers of antibiotic resistance trends inStreptococcus pneumoniaeamidst the 2020 COVID-19 pandemic: Insights from mathematical modeling

Kovacevic

Smith

Rahbé

et al. 2022

Preprint

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COVID-19 pandemic responses have dramatically modified the global ecological and epidemiological landscape of many infectious diseases. However, the pandemic’s impacts on antimicrobial resistance (AMR) are currently poorly understood and lack data. While surges in COVID-19 cases during the first wave of the pandemic may have exacerbated AMR, decreases in antibiotic use may have had the opposite effect. To disentangle how pandemic impacts such as lockdowns and modified antibiotic prescribing may affect AMR, we developed a mathematical model formalizing simultaneous transmission of SARS-CoV-2 and colonization with a bacterial pathogen across six pandemic scenarios. We used simulation to assess the effect of each scenario on the bacterial carriage prevalence, antibiotic resistance rate, and the invasive bacterial disease (IBD) incidence, using parameters based on the commensal community bacterium Streptococcus pneumoniae. Pandemic scenarios without community-wide lockdowns all resulted in a decrease in carriage prevalence of antibiotic-sensitive bacteria and an increase in the prevalence of antibiotic-resistant bacteria, while the addition of a population-wide lockdown resulted in a large reduction in colonization prevalence and IBD incidence for both strains (>70%). This translated to an increase in the antibiotic resistance rate across all scenarios to varying degrees, with lingering effects after the cessation of COVID-19 response measures. In the absence of lockdown, a population-wide surge in antibiotic prescribing coincident with the peak in SARS-CoV-2 infection resulted in the greatest increases in resistance rate (23%) and resistant IBD incidence (6%). Within-host interactions, SARS-CoV-2 variants, and population immunity are found to further drive the magnitude of pandemic impacts on resistant IBD incidence. Sensitivity analyses suggest that the extent of such impacts likely varies across different bacterial species. Although real-life scenarios are significantly more complicated, our findings suggest that COVID-19 pandemic responses may significantly impact antibiotic resistance in the community and support the need for monitoring resistance during pandemic waves.

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Section: Discussionsupporting

confidence: 77%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Revealing the drivers of antibiotic resistance trends inStreptococcus pneumoniaeamidst the 2020 COVID-19 pandemic: Insights from mathematical modeling

Kovacevic

Smith

Rahbé

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…Yet over the same time period, intriguingly, emerging data report persistent carriage of S . pneumoniae in the community across countries and age groups [ 44 – 46 ]. It has been suggested that reduced incidence of bacterial infection may thus be explained at least in part by concomitant prevention of other respiratory viruses like influenza [ 47 ], which have been shown to favour progression from bacterial colonization to disease [ 48 ].…”

Section: Discussionmentioning

confidence: 99%

Collateral impacts of pandemic COVID-19 drive the nosocomial spread of antibiotic resistance: A modelling study

Shirreff

Temime

et al. 2023

PLoS Med

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Background Circulation of multidrug-resistant bacteria (MRB) in healthcare facilities is a major public health problem. These settings have been greatly impacted by the Coronavirus Disease 2019 (COVID-19) pandemic, notably due to surges in COVID-19 caseloads and the implementation of infection control measures. We sought to evaluate how such collateral impacts of COVID-19 impacted the nosocomial spread of MRB in an early pandemic context. Methods and findings We developed a mathematical model in which Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2) and MRB cocirculate among patients and staff in a theoretical hospital population. Responses to COVID-19 were captured mechanistically via a range of parameters that reflect impacts of SARS-CoV-2 outbreaks on factors relevant for pathogen transmission. COVID-19 responses include both “policy responses” willingly enacted to limit SARS-CoV-2 transmission (e.g., universal masking, patient lockdown, and reinforced hand hygiene) and “caseload responses” unwillingly resulting from surges in COVID-19 caseloads (e.g., abandonment of antibiotic stewardship, disorganization of infection control programmes, and extended length of stay for COVID-19 patients). We conducted 2 main sets of model simulations, in which we quantified impacts of SARS-CoV-2 outbreaks on MRB colonization incidence and antibiotic resistance rates (the share of colonization due to antibiotic-resistant versus antibiotic-sensitive strains). The first set of simulations represents diverse MRB and nosocomial environments, accounting for high levels of heterogeneity across bacterial parameters (e.g., rates of transmission, antibiotic sensitivity, and colonization prevalence among newly admitted patients) and hospital parameters (e.g., rates of interindividual contact, antibiotic exposure, and patient admission/discharge). On average, COVID-19 control policies coincided with MRB prevention, including 28.2% [95% uncertainty interval: 2.5%, 60.2%] fewer incident cases of patient MRB colonization. Conversely, surges in COVID-19 caseloads favoured MRB transmission, resulting in a 13.8% [−3.5%, 77.0%] increase in colonization incidence and a 10.4% [0.2%, 46.9%] increase in antibiotic resistance rates in the absence of concomitant COVID-19 control policies. When COVID-19 policy responses and caseload responses were combined, MRB colonization incidence decreased by 24.2% [−7.8%, 59.3%], while resistance rates increased by 2.9% [−5.4%, 23.2%]. Impacts of COVID-19 responses varied across patients and staff and their respective routes of pathogen acquisition. The second set of simulations was tailored to specific hospital wards and nosocomial bacteria (methicillin-resistant Staphylococcus aureus, extended-spectrum beta-lactamase producing Escherichia coli). Consequences of nosocomial SARS-CoV-2 outbreaks were found to be highly context specific, with impacts depending on the specific ward and bacteria evaluated. In particular, SARS-CoV-2 outbreaks significantly impacted patient MRB colonization only in settings with high underlying risk of bacterial transmission. Yet across settings and species, antibiotic resistance burden was reduced in facilities with timelier implementation of effective COVID-19 control policies. Conclusions Our model suggests that surges in nosocomial SARS-CoV-2 transmission generate selection for the spread of antibiotic-resistant bacteria. Timely implementation of efficient COVID-19 control measures thus has 2-fold benefits, preventing the transmission of both SARS-CoV-2 and MRB, and highlighting antibiotic resistance control as a collateral benefit of pandemic preparedness.

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“…A. Mice were euthanized at 6 days post co-infection for bacterial burden calculation in the nasal lavage (left) and blood [ 46 ]. Data were calculated as number of colony forming units (CFU) of Spn in nasal lavage and CFU/mL of blood (Data were log10 transformed, and values equal to 0 were regarded as undetectable).…”

Section: Resultsmentioning

confidence: 99%

IL-17RA promotes pathologic epithelial inflammation in a mouse model of upper respiratory influenza infection

Navaeiseddighi,

Tripathi,

Guo

et al. 2023

PLoS Pathog

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The upper respiratory tract (nasopharynx or NP) is the first site of influenza replication, allowing the virus to disseminate to the lower respiratory tract or promoting community transmission. The host response in the NP regulates an intricate balance between viral control and tissue pathology. The hyper-inflammatory responses promote epithelial injury, allowing for increased viral dissemination and susceptibility to secondary bacterial infections. However, the pathologic contributors to influenza upper respiratory tissue pathology are incompletely understood. In this study, we investigated the role of interleukin IL-17 recetor A (IL-17RA) as a modulator of influenza host response and inflammation in the upper respiratory tract. We used a combined experimental approach involving IL-17RA-/- mice and an air-liquid interface (ALI) epithelial culture model to investigate the role of IL-17 response in epithelial inflammation, barrier function, and tissue pathology. Our data show that IL-17RA-/- mice exhibited significantly reduced neutrophilia, epithelial injury, and viral load. The reduced NP inflammation and epithelial injury in IL-17RA-/- mice correlated with increased resistance against co-infection by Streptococcus pneumoniae (Spn). IL-17A treatment, while potentiating the apoptosis of IAV-infected epithelial cells, caused bystander cell death and disrupted the barrier function in ALI epithelial model, supporting the in vivo findings.

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Impact of COVID-19 Nonpharmaceutical Interventions on Pneumococcal Carriage Prevalence and Density in Vietnam

Abstract: The pneumococcus is a major cause of mortality globally. Implementation of NPIs during the COVID-19 pandemic led to reductions in invasive pneumococcal disease in many countries.

Cited by 14 publications

References 26 publications

Revealing the drivers of antibiotic resistance trends inStreptococcus pneumoniaeamidst the 2020 COVID-19 pandemic: Insights from mathematical modeling

Revealing the drivers of antibiotic resistance trends inStreptococcus pneumoniaeamidst the 2020 COVID-19 pandemic: Insights from mathematical modeling

Collateral impacts of pandemic COVID-19 drive the nosocomial spread of antibiotic resistance: A modelling study

IL-17RA promotes pathologic epithelial inflammation in a mouse model of upper respiratory influenza infection

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