Antibiotic Overuse in a Contemporary Cohort of Children Hospitalized with Influenza, RSV, or SARS-CoV-2: A Retrospective Cohort Study

doi:10.21203/rs.3.rs-4614400/v1

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Antibiotic Overuse in a Contemporary Cohort of Children Hospitalized with Influenza, RSV, or SARS-CoV-2: A Retrospective Cohort Study

https://doi.org/10.21203/rs.3.rs-4614400/v1

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Background

Children hospitalized with viral respiratory tract infections (RTIs) are often prescribed antibiotics due to concern for bacterial co-infection, although most do not have concurrent bacterial infections. This unnecessary antibiotic treatment can lead to bacterial resistance and adverse events. The extent of antibiotic overuse in hospitalized children with community-onset viral RTIs has not been described in recent years. To identify antibiotic stewardship opportunities in this population, we quantified the extent of antibiotic overtreatment and determined predictors of antibiotic use among children hospitalized with influenza, respiratory syncytial virus (RSV), or SARS-CoV-2 (COVID-19).

Methods

We performed a single-center retrospective study evaluating antibiotic use and culture-confirmed bacterial co-infection among children and adolescents hospitalized with influenza, RSV, or COVID-19 between April 2020 and May 2023. Predictors of antibiotic treatment were determined using logistic regression.

Results

We included 1,718 patients (influenza: 188; RSV: 1,022; COVID-19: 535). Patients with RSV were younger and more likely to be in intensive care. Eight percent of patients had culture-confirmed bacterial co-infection. The proportion of children with culture-confirmed bacterial infection was low (8%) but the proportion receiving antibiotics was high and varied by virus (influenza: 60.6%, RSV:41.2%, COVID-19: 48.6%, p < 0.001). Independent predictors for receipt of antibiotics were elevated inflammatory markers, mechanical ventilation, and influenza infection. Among patients with the lowest severity of illness, 48% received ≥ 1 dose of antibiotics.

Conclusions

In children hospitalized with community-onset viral RTIs, antibiotic treatment is substantially higher than the burden of culture-confirmed bacterial infection, especially for influenza, suggesting antibiotic overuse and antibiotic stewardship opportunities.

antibiotic overuse

influenza

RSV

COVID-19

viral respiratory tract infection

The burden of pediatric hospitalizations for viral respiratory tract infections (RTIs) is substantial. In the U.S., over 22,000 children have been hospitalized with COVID-19 since 2020, 12,000–46,000 children are hospitalized with influenza each year, and up to 80,000 children < 5 years are hospitalized with RSV every year (1, 2, 3). Children hospitalized with viral RTIs are often treated with antibiotics due to concerns for bacterial co-infection, especially bacterial pneumonia, which can be preceded by viral infection (4, 5, 6). However, the majority of children with viral RTIs do not have concurrent bacterial infections, so this practice leads to unnecessary antibiotic treatment which, in turn, can lead to development of resistant bacteria and adverse events. Unlike in adults, the extent of antibiotic overuse in hospitalized children with community-onset viral RTI has not been well-quantified in recent years (4).

Several studies have found that although there were low rates of bacterial co-infection in adults hospitalized with COVID-19, up to 75% received antibiotics (5, 6, 8). Similarly, a large multicenter study evaluating children with critical illness from COVID-19 found that 7% of children had bacterial coinfection but 63% received antibiotics (5). Studies of antibiotic treatment among children hospitalized with influenza or RSV before the COVID-19 pandemic demonstrated that 60–90% received antibiotics (9, 10), but there were few evaluations of bacterial co-infection rates (11, 12, 13, 14). Furthermore, most prior studies of viral RTI do not quantify antibiotic use and may have overestimated bacterial co-infection burden because they interpreted any respiratory culture with bacterial growth as indicative of bacterial infection, although many positive respiratory cultures likely reflected colonization (15, 16, 17). We sought to quantify the extent of antibiotic overuse in a contemporary cohort of children hospitalized with viral RTI, in the context of an active hospital-based antibiotic stewardship program.

Sampling and Exclusion Criteria

We conducted a single center retrospective cohort study of all children and adolescents aged < 19 years old hospitalized at Monroe Carell Jr. Children’s Hospital at Vanderbilt, Nashville, TN who had a positive test for influenza, RSV, or COVID-19. Patients with RSV and influenza were hospitalized January 2021 to May 2023, and patients with COVID-19 were hospitalized April 2020 to February 2022. Patients were excluded if they were > 19 years of age or were not hospitalized.

From 2021 onwards, the institutional antibiotic stewardship team performed daily audit and feedback of antibiotics prescribed in inpatients; feedback was provided to treating providers via telephone or in person discussion. Audit and feedback were performed inconsistently during 2020 due to disruptions from the COVID-19 pandemic.

Data Collection

Medical records were reviewed to identify patients with positive viral antigen or PCR tests for influenza, RSV, or COVID-19 within 48 hours of hospitalization and to collect demographic and clinical characteristics including age, sex, race, microbiology results, hospital length of stay, laboratory results, and antibiotic administration. Race and ethnicity were both self-reported. Culture-confirmed bacterial infection was defined as growth of clinically significant bacteria (non-commensal species) indicative of bacterial co-infection from any specimen source including blood, urine, pleural fluid, cerebrospinal fluid, and respiratory secretions throughout the hospitalization. We also used a second, more stringent definition of culture-confirmed bacterial infection that excluded cultures of respiratory specimens. We did not collect information on presence of white blood cells (WBC) in respiratory cultures. Cultures with growth of common commensals, including diphtheroids, Micrococcus species, and coagulase-negative Staphylococci were considered colonizers and not bacterial infection. Patients with multiple viruses were excluded from multivariable logistic regression models.

Data Analysis

A univariable analysis was conducted using the entire sample to compare demographic and clinical variables by virus type, using Pearson's chi-squared for categorical characteristics, and Kruskal Wallis H test for continuous variables. After excluding patients with detection of multiple viruses, two different multivariable logistic regression models were developed a priori to identify predictors of 1) at least one dose of antibiotic treatment and 2) greater than 3 days of antibiotic treatment. The model included variables that were deemed clinically significant based on clinical judgement and were also found to be statistically significant in the univariable analysis. The logistic regression models included the type of virus, age, presence of elevated inflammatory markers [procalcitonin, PCT, (≥ 0.5 ug/mL) or C-reactive protein, CRP (≥ 50 mg/L)], intensive care unit (ICU) status, and whether the patient received mechanical ventilation. Patients who did not have inflammatory markers measured were assumed to have normal inflammatory markers in the multivariable analysis. Bacterial co-infection and antibiotic utilization percentages were determined by type of virus. Patients with a low severity of illness were defined as having normal inflammatory markers [PCT < 0.5 ug/mL or CRP < 50 mg/L], and not admitted to the ICU. Patients without inflammatory markers measured were excluded from severity of illness analyses. Analyses were done using Stata 17 (Stata Corp BE).

Demographic and clinical characteristics (Table 1)

Table 1

Demographic and clinical characteristics of 1,718 pediatric patients by type of virus
Characteristic	Influenza (N = 188; 10.9%)^a	RSV (N = 1,022; 59.5%)^b	COVID-19 (N = 535; 31.1%)^c	Total (N = 1,718)^{d, e}
Demographics
Median age in years (range)	5.18 (0.02–17.68)	0.61 (0.11–18.43)	6.06 (0–18.96)	1.35 (0–18.96)
Male sex	108 (57.4%)	547 (53.5%)	278 (52.0%)	922 (53.7%)
Race
Asian	5 (2.66%)	6 (0.587%)	3 (0.561%)	14 (0.815%)
Black or African American	27 (14.4%)	142 (13.9%)	114 (21.3%)	279 (16.2%)
White	126 (67.0%)	673 (65.9%)	320 (59.8%)	1,104 (64.3%)
Other Race/Unknown	30 (16.0%)	201 (19.7%)	98 (18.3%)	321 (18.7%)
Ethnicity
Hispanic or Latino	42 (22.3%)	185 (18.1%)	100 (18.7%)	320 (18.6%)
Not Hispanic or Latino	81 (43.1%)	345 (33.8%)	150 (28.2%)	572 (33.3%)
Unknown	65 (34.6%)	492 (48.1%)	285 (53.3%)	826 (48.1%)
LOS, median days (range)	2.67 (0.39–57.55)	2.79 (0.01–98.46)	2.64 (0.06 -285.59)	2.75 (0.06-285.59)
Severity
ICU	55 (29.3%)	462 (45.2%)	117 (21.9%)	618 (36.0%)
Mechanical Ventilation	23 (12.2%)	108 (10.6%)	63 (11.8%)	187 (10.9%)
ECMO	2 (1.1%)	4 (0.39%)	4 (0.75%)	10 (0.58%)
Death	3 (1.60%)	16 (1.57%)	31 (6.23%)	48 (2.79%)
Symptomatic Respiratory Infection^f	124 (66.0%)	849 (83.1%)	359 (67.1%)	1298 (75.6%)
Microbiology
Bacterial Infection	15 (8.0%)	70 (6.9%)	55 (10.3%)	138 (8.0%)
Blood	5 (2.7%)	23 (2.3%)	18 (3.4%)	45 (2.6%)
Respiratory secretions	8 (4.3%)	34 (3.3%)	16 (3.0%)	57 (3.3%)
Urine	1 (0.53%)	11 (1.08%)	18 (3.36%)	30 (1.7%)
Other body fluid	1 (0.53%)	2 (0.20%)	2 (0.37%)	5 (0.29%)
Other	0	0	1 (0.19%)	1 (0.06%)^g
Inflammatory Markers
Inflammatory markers (PCT or CRP) measured	87 (46.3%)	305 (29.8%)	296 (55.3%)	671 (39.1%)
Elevated inflammatory markers [PCT (≥ 0.5 ug/mL) or CRP (≥ 50 mg/L)]^h	44 (50.6%)	124 (40.7%)	102 (34.5%)	264 (39.3%)
Very elevated inflammatory markers [PCT (> 1 ug/mL) or CRP (> 100 mg/L)]^h	29 (33.3%)	81 (26.6%)	51 (17.2%)	156 (23.2%)
PCT, median (range) [n = 426]	0.58 (0.06–100)	0.28 (0.06–100)	0.17 (0.06–100)	0.24 (0.06–100)
CRP, median (range) [n = 378]	38.65 (1 -295.3)	32.7 (0.2–367.6)	24.7 (0.2 -361.8)	30.9 (0.2–480)
Antibiotic Treatment
Received any antibiotics	114 (60.6%)	421 (41.2%)	260 (48.6%)	785 (45.7%)
Duration of antibiotics
No antibiotics	74 (39.4%)	601 (58.8%)	275 (51.4%)	933 (54.3%)
1–3 days	42 (22.3%)	185 (18.1%)	109 (20.4%)	331 (19.3%)
> 3 days	72 (38.3%)	236 (23.1%)	151 (28.2%)	454 (26.4%)
Antibiotics DOT median, range [n = 775]	5 (1–93)	4 (1–94)	5 (1–401)	4 (1–401)
^a Hospital admission from 12/20/2020–05/27/2023
^b Hospital admission from 04/01/2021–05/03/2023
^c Hospital admission from 04/06/2020-2/14/2022
^d Hospital admission from 04/06/2020–05/27/2023
^e 6 participants had influenza and RSV coinfection; 3 had influenza and COVID-19; 17 had RSV and COVID-19
^f ICD-10 diagnosis codes found in Supplemental Table 1
^g Cultured from a wound
^h Percent of those with PCT or CRP obtained
LOS, length of stay
ECMO, extracorporeal membrane oxygenation
PCT, procalcitonin
CRP, C-reactive protein
DOT, days of therapy

We included 1,718 pediatric patients (188 with influenza, 1,022 with RSV, 535 with COVID-19). Patient demographic and clinical factors varied by virus type (Table 1). Median age was lowest for patients with RSV and highest for patients with COVID-19 (0.61 years vs. 6 years, p < 0.001). Racial distribution varied significantly by virus; Black patients comprised 21.3% of patients with COVID-19, and lower percentages of patients with RSV and influenza, while white patients comprised two-thirds of patients with influenza but lower percentages of patients with RSV or COVID-19. A greater proportion of patients with RSV (45%) were in the ICU, than patients with influenza or COVID-19 (p < 0.001). Mortality was highest in patients with COVID-19 at 6.2% but was significantly lower for patients with influenza or RSV (p < .001). Inflammatory markers among patients in whom they were measured, were elevated in almost half of patients with influenza, in 40% of patients with RSV and 35% patients of COVID-19 (p < 0.001). The overall rate of bacterial co-infection was 8% when including respiratory cultures and 5.4% when excluding respiratory cultures. Positive cultures (of all specimen types including respiratory) occurred more commonly in patients with COVID-19 (10.3%) than those with RSV (6.9%) or influenza (8%) (p = 0.03). The median number of days from admission to collection of a positive bacterial culture was 3 (IQR = 2) and did not vary by virus type (p = 0.204).

Antibiotic Treatment

Although few patients had culture-confirmed bacterial infections, 45.7% of patients received at least one dose of antibiotics and 26.4% received > 3 days of antibiotics (Fig. 1). Antibiotic treatment varied by virus type. Among patients with influenza, 60.6% received at least one antibiotic dose, and 38% received > 3 days of antibiotics. In contrast, only 23% of patients with RSV and 28% of patients with COVID-19 received > 3 days of antibiotics (p < 0.001).

The percent of patients receiving antibiotic treatment was higher in ICU than non-ICU locations and higher among those with very elevated inflammatory markers vs. normal inflammatory markers (Fig. 2). Among a subgroup of patients with low severity of illness, 7.3% had culture-confirmed bacterial infection including respiratory cultures, while 48.1% received at least 1 dose of antibiotic and 20.8% received > 3 days of antibiotics; these percentages did not differ significantly by virus type.

Predictors of Antibiotic Treatment

Independent predictors of receiving > 3 days of antibiotic treatment were elevated inflammatory markers, being on mechanical ventilation, and having a diagnosis of influenza (Table 2). The same variables were independent predictors for receiving at least 1 dose of antibiotics. Patients with elevated inflammatory markers were significantly more likely to receive antibiotics than those without elevated inflammatory markers (OR 4.45, 95% CI 3.28 to 6.05) when adjusted for mechanical ventilation, influenza diagnosis, and age (Table 2).

Table 2

Multivariable analysis to determine predictors of receiving > 3 days of antibiotic therapy.
Characteristic	Odds Ratio	95% CI	P-Value
Age	1.02	0.99–1.04	0.224
Elevated CRP (> 50 mg/L) or PCT (> 0.5 ug/L)	4.46	3.28–6.05	< 0.001
Mechanical Ventilation	7.36	4.82–11.24	< 0.001
ICU	1.21	0.90–1.63	0.201
Influenza	2.02	1.36–2.99	< 0.001
COVID	1.14	0.82–1.57	0.445

In this large contemporary cohort of children hospitalized with influenza, RSV, or COVID-19, we found that the percent of patients with bacterial co-infection was low, while the percent of patients receiving antibiotic treatment was high. Overall, the proportion of patients prescribed antibiotics for > 3 days was 46%, which is 4–6 times greater than the proportion that had culture-confirmed bacterial infections. This difference between antibiotic treatment and bacterial infection burden was greatest among patients with influenza and with elevated inflammatory markers in both ICU and non-ICU settings.

Notably, among patients with the lowest severity of illness, in whom bacterial infection was least likely, any antibiotic treatment was administered to 48.1% of patients and > 3 days of antibiotics were given to 20.8% of patients, suggesting antibiotic overtreatment. For this group of patients, clinicians could consider withholding or promptly deescalating antibiotics. In contrast, for patients with high severity of illness, it is appropriate to initiate empiric and/or targeted antibiotic treatment.

The rates of antibiotic use seen in our study are similar to those reported in earlier, studies, suggesting that antibiotic prescribing practices have not changed in recent years despite greater provider and public awareness of the importance of antibiotic stewardship (9, 18, 19). We observed that the proportion of patients receiving antibiotics was highest for patients with influenza (> 60%) and lowest for patients with RSV (41%). Previous studies spanning over 20 years have noted antibiotic use in 49–58% of children and adults diagnosed with influenza (9, 18, 19). The antibiotic utilization percentage we observed among patients with RSV is also comparable to findings from previous studies, in which 33–57% of children hospitalized with RSV who did not have a culture-confirmed bacterial infection were administered antibiotics (10, 20).

While the low bacterial co-infection rate we observed is supported by recent adult and pediatric studies of patients with COVID-19, it contrasts with some earlier studies of influenza and RSV that reported higher bacterial co-infection rates of 27–40% (15, 16, 17). This discrepancy may be due to fact that some earlier studies defined bacterial co-infection largely based on positive bacterial culture results from non-sterile sites such as sputum or respiratory secretions and used bacterial colony count thresholds that are not validated for diagnosis of bacterial pneumonia (15, 16, 17, 21). Additionally, these studies found that S. pneumoniae and S. aureus, were the most commonly isolated bacterial pathogens among children with viral RTI (16, 17). Though growth of these organisms from respiratory specimens may have reflected bacterial co-infection in some patients, they may have reflected colonization of the respiratory tract in others (22).

Patient demographic and clinical factors differed by virus type, which may have influenced medical management and could explain why antibiotic treatment differed by virus. Hospitalized patients with RSV were significantly younger and less likely to receive antibiotics than patients with influenza. Clinicians may have been more likely to avoid antibiotics in patients hospitalized with RSV because these children were most commonly infants with bronchiolitis and were not as acutely ill as the patients with influenza. This hypothesis is supported by the fact that ICU admission was more common among patients with RSV than patients with influenza, but rates of mechanical ventilation were similar between the groups, likely because many infants with RSV received supplemental oxygen but did not require mechanical ventilation.

We determined that several variables were independent predictors for receipt of antibiotic treatment, including having influenza, requiring mechanical ventilation, and having elevated inflammatory markers. Antibiotic treatment of patients with influenza may stem from widespread clinician awareness of reports of influenza-associated Gram-positive bacterial pneumonia and the associated high mortality (23, 24, 25). Mechanical ventilation is a predictor likely because it is a surrogate for severe illness in which antibiotic treatment may be warranted. High inflammatory markers is likely strongly associated with antibiotic treatment because of clinician confidence that these tests indicate bacterial infection. However, these tests, especially CRP, have low specificity and low positive predictive value (PPV) for bacterial infection and can be elevated in viral infections (26). Providers should be wary about prescribing antibiotics based solely on the results of inflammatory markers, without consideration of the clinical context.

Strengths of our study are the large sample size, use of a stringent definition of bacterial co-infection, and evaluation of a contemporary cohort. Our study also has limitations, including its single center, retrospective nature, which may reduce its generalizability. However, our study corroborates findings of antibiotic overuse seen in earlier studies (5, 6, 7). Additionally, because bacterial pneumonia is not often confirmed by culture and we did not collect information about abnormal chest radiographs, we may have underestimated the occurrence of bacterial pneumonia. However, it is unlikely that almost half of patients (the proportion who received antibiotics) developed bacterial pneumonia after RTI (27). We identified subjects based on positive viral test results, determined symptomatic respiratory tract infection based on diagnosis codes, and did not confirm presence of respiratory symptoms through chart review. It is possible that antibiotic treatment was given for infections other than pneumonia (eg. acute otitis media), which we were not able to ascertain. In addition, antimicrobial stewardship interventions were inconsistently implemented throughout 2020 due to the COVID-19 pandemic.

Despite these limitations, we demonstrate in a contemporary cohort that unnecessary antibiotic use persists in hospital settings, as the antibiotic treatment burden far exceeds bacterial co-infections for children hospitalized with influenza, RSV, or COVID-19. Antibiotic stewardship programs should encourage clinicians to withhold or promptly deescalate antibiotics, particularly for children hospitalized with low severity of viral RTI, in whom bacterial infection is very rare and stewardship interventions may have higher acceptance.

Ethics approval and consent to participate: Not applicable. This study was approved with a waiver of consent by the Vanderbilt University IRB (#232179).

Consent for publication: Not applicable.

Availability of data and material: The datasets generated and analysed during the current study are not publicly available but are available from the corresponding author on reasonable request.

Competing interests: The authors declare that they have no competing interests.

Funding: M.K. is a recipient of the Pediatric Infectious Diseases Society’s SUMMERS award.

Authors' contributions: M.K. performed data collection and analysis and prepared the manuscript. N.J.T supervised data analysis. A.B.K. assisted with data collection and analysis of the patients with COVID-19. R.B supervised data collection, analysis, and manuscript preparation. All authors read and approved the final version of the manuscript.

Acknowledgements: Not applicable.

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No competing interests reported.

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Antibiotic Overuse in a Contemporary Cohort of Children Hospitalized with Influenza, RSV, or SARS-CoV-2: A Retrospective Cohort Study

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Abstract

Background

Methods

Results

Conclusions

Figures

Background

Methods

Sampling and Exclusion Criteria

Data Collection

Data Analysis

Results

Demographic and clinical characteristics (Table 1)

Antibiotic Treatment

Predictors of Antibiotic Treatment

Discussion

Declarations

References

Additional Declarations

Supplementary Files

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