Secondary Logo

Journal Logo

Online Articles: Original Articles

COVID-19-Related Reduction in Emergency Health Care Utilization Among Febrile Pediatric Oncology Patients

Kram, David E. MD, MCR*; Tooze, Janet A. PhD; Russell, Thomas B. MD*; McLean, Thomas W. MD*

Author Information
Journal of Pediatric Hematology/Oncology: April 2022 - Volume 44 - Issue 3 - p e649-e652
doi: 10.1097/MPH.0000000000002243
  • Free


The novel severe acute respiratory syndrome coronavirus (SARS-CoV-2) pandemic, caused by the coronavirus disease-19 (COVID-19), has disrupted daily life worldwide. Like other countries and states in the United States, North Carolina (NC) responded to this pandemic1 with various protective strategies to curb virus transmission, starting with a declaration of a state of emergency (Order 1162) on March 10, 2020, followed by restaurant and school closures and banning of mass gatherings, after which the governor ultimately issued Executive Order No. 121, a statewide Stay-at-Home Order on March 27, 2020.3 Hospitals prepared for a potential influx of critically ill patients by reducing elective procedures and surgeries, reallocating resources to care for COVID-19 patients, and preparing for an unprecedented health care emergency. National concern rose among individuals that visiting a health care facility would put them at increased risk for contracting COVID-19, resulting in vast reductions in health care utilization.4–10

Pediatric oncology patients undergoing chemotherapy for cancer are at risk for severe infections because of an acquired chemotherapy-induced immunocompromised state and the frequent presence in these children of central venous access devices (CVADs), which increase the risk for invasive bacterial infections.11–13 Guidelines for managing these patients recommend prompt evaluation at a health care facility, such as an emergency department (ED).14,15 Consequently, fever is among the most common reasons for ED visits among pediatric patients with cancer.16 Delayed or avoided evaluations in the setting of fever and possible neutropenia in pediatric oncology patients is associated with increased morbidity and mortality.17

During the first 10 weeks of the national pandemic, ED visits for life-threatening emergencies that necessitate immediate emergency care, including myocardial infarction, stroke, and hyperglycemic crisis dropped significantly,9 prompting calls for clear communication from public health and health care professionals to reinforce the significance of timely care and to reassure the public that EDs are maximally ensuring safety of their patients through infection prevention and control procedures. Fever in pediatric oncology patients is a similar potentially life-threatening medical emergency, and it is unclear how the pandemic has impacted the numbers of ED visits by this patient population. In this study, we sought to describe the extent to which the pandemic has impacted ED visit patterns among pediatric oncology patients with fever. We also sought to compare these results with national childhood vaccine rates.


Study Population and Data Collection

We analyzed data extracted from an IRB-approved internal database of pediatric ED encounters of pediatric oncology patients with CVADs who presented to the pediatric ED with fever (≥38.3°C once or ≥38.0°C twice in 1 h) corresponding to the time periods March 1 to July 31 for the years 2018 to 2020. Because the database was established for the purpose of quality improvement and the data were de-identified, consent and assent were not required. Data included demographic information, oncology diagnosis, and CVAD type. The ED at Brenner Children’s Hospital/Wake Forest Baptist Medical Center in Winston Salem, NC is a 24-bed level 1 trauma pediatric ED which sees ∼33,000 pediatrics patients every year. It is open 24 hours per day, 7 days per week, and is staffed by pediatric emergency medicine physicians.

We also extracted de-identified data of pediatric oncology clinic visits from the electronic medical record, as well as new pediatric oncology diagnoses and signed consents to the Children’s Oncology Group (COG) up-front registration and biology study, APEC14B1 Parts A and B from the time period September 1 to February 28 for the years 2018 to 2020. These 3 measures were used to compare overall patient volume in the 6 months leading up to the pandemic compared with the same time period in the previous year. Medical and demographic data were extracted from electronic medical records by retrospective chart review and entered into REDCap.

Statistical Analyses

The Mann-Whitney U test was used to evaluate differences in pediatric oncology clinic visits between September 2018 to February 2019 and September 2019 to February 2020 and in neutrophils and white blood cells count at ED encounter before and during the pandemic. The Student t test was used to evaluate a difference between the mean pediatric ED visits and age at presentation in 2018 and 2019 compared with 2020. χ2 tests were used to evaluate differences in the distribution of race, sex, ethnicity, disease, and admission of pediatric ED visits during the same time period, while the Fisher exact test was used to check for differences in patients’ CVAD type. Childhood vaccine data, which included percent change from 2019 to 2020, were obtained from the COVID-19 Research Database with their approval and plotted against the percent change in our ED visits from 2019 to 2020.5 All analyses were performed in SAS 9.4 (SAS Institute, Cary, NC).


In total, n=150 visits to the pediatric ED occurred by pediatric oncology patients presenting with fever during the analyzed periods between March 1 and July 31 for 2018, 2019, and 2020 (Table 1). During the time period in 2018, 65 encounters occurred; 60 occurred in 2019; 25 occurred in 2020. Compared with 2018, encounters for 2020 were decreased by 62%, and compared with 2019, encounters were decreased by 58%. The mean monthly visits were significantly different in 2018 and 2019 combined (12.7 visits) from 2020 (5 visits) (P=0.0007) (Table 1, Fig. 1).

TABLE 1 - Demographics and Clinical Data by Time Period
March-July 2018 and 2019, n (%) March-July 2020, n (%) P*
n 125 25
Sex 0.74
 Male 85 (68) 16 (64)
 Female 40 (32) 9 (36)
Race 0.26
 White 73 (58) 18 (72)
 Black 14 (11) 4 (16)
 Other 38 (30) 3 (12)
Ethnicity 0.63
 Hispanic or Latino 31 (25) 5 (20)
 Not Hispanic or Latino 94 (75) 20 (80)
Oncologic disease 0.79
 Hematologic malignancy 89 (71) 17 (68)
 Nonhematologic malignancy 36 (29) 8 (32)
CVAD 0.82
 Port-a-Cath 117 (94) 23 (92)
 Other 8 (6) 2 (8)
  Peripherally inserted central catheter 1 (1) 0
  Hickman catheter 4 (3) 3 (12)
  Peripheral IV 4 (3) 0
Admitted to Pediatric Oncology Inpatient Unit 0.01
 Yes 73 (58) 21 (84)
 No 52 (42) 4 (16)
Admitted to PICU 1.0
 Yes 5 (4) 1 (4)
 No 120 (96) 24 (96)
Fever before day of presentation 0.66
 Yes 7 (6) 2 (8)
 No 118 (94) 23 (92)
Deaths during hospitalization NA
 Yes 0 0
 No 125 (100) 25 (100)
Age, mean (SD) 6.8 (4.8) 5.7 (4.4) 0.29
White blood cell (×103 µL), mean (SD) 4.3 (4.6) 2.5 (3.2) 0.03
Neutrophils absolute (×103 µL), mean (SD) 2.8 (3.7) 1.5 (2.4) 0.03
*From Rao-Scott χ2 test for categorical variables and from t tests with standard errors constructed using Taylor series linearization for continuous variables.
CVAD indicates Central Venous Access Device; PICU, pediatric intensive care unit.

Monthly pediatric oncology emergency department (ED) visits for fever before and during the early part of the coronavirus disease-19 pandemic.

We found no differences in the distribution of race and sex and other demographics of ED patients in the years before the pandemic compared with 2020 (Table 1). A significantly higher percentage of patients were admitted during the pandemic, 84%, compared with 56% in the years before the pandemic. There were no differences in rates of PICU admission, duration of fever before presentation to the ED, or duration of admission for those admitted (Table 1). No deaths from infection were reported during these time periods.

In an effort to determine whether the Pediatric Oncology Program at Brenner Children’s Hospital saw fewer patients in the time period leading up to the pandemic, we compared clinic visits, new patient counts, and the number of consents to the standard up-front COG biology study from the 6 months leading up to the pandemic (September 2019 to February 2020) and compared these to the same 6-month period during the year prior (September 2018 to February 2019). Between September 2018 and February 2019, the Pediatric Oncology Clinic saw 1843 patients, the program diagnosed 35 new cancer patients, and obtained 18 COG APEC14B1 consents (Table 2). Between September 2019 and February 2020, the Pediatric Oncology Clinic saw 1883 patients, the program diagnosed 33 new cancer patients, and obtained 20 COG APEC14B1 consents. There was no significant difference in the number of clinic visits in that period in 2018 to 2019 and 2019 to 2020, P=0.42.

TABLE 2 - Pediatric Oncology Program Counts
September 2018-February 2019 September 2019-February 2020
Pediatric oncology clinic patients 1843 median=303.5 visits/month 1883 median=315.5 visits/month
Newly diagnosed cancer patients 35 33
COG APEC14B1 consents 18 20
COG indicates Children’s Oncology Group.

During the early phases of the pandemic in the spring and summer of 2020, national childhood vaccine rates also dropped as much as 60% from 2019.5 We plotted the percent change in our ED visits from 2019 to 2020 along with the percent change in national vaccine counts obtained from the COVID-19 Research Database.5 This revealed a larger drop in ED visits than in vaccines, but the shape of those changes through the early waves of the pandemic are very similar (Fig. 2).

Percent change in emergency department (ED) visits and childhood vaccines in the early part of the coronavirus disease-19 2020 pandemic compared with the same time period in 2019.


In the days and weeks following the declaration of COVID-19 as a North Carolina statewide emergency on March 10, 2020, there was a significant decrease in pediatric ED visits of pediatric oncology patients with fever at our institution. This finding is consistent with other reports on the substantial reduction in pediatric and adult health care utilization across the country during the pandemic,4–8 and exhibits a nearly identical pattern with the national drop in childhood vaccination rates during the same time period.

The cause of the significant decrease in ED visits for these patients might be explained by many pandemic-related factors, including lack of exposure to other non-COVID-19 communicable diseases, fear of exposure to COVID-19 at a health care facility, or the misinterpretation of fever as a nonemergency during a time when the public health recommendations were to minimize non-urgent health care. Febrile neutropenia episodes in children with cancer yield positive blood cultures ∼25% of the time,18 with the majority of the remainder of the cases having a either documented viral etiology or no identified cause at all. As the state-mandated school closures and shelter-in-place orders likely led to a substantial decrease in the spread of other non-COVID-19 communicable diseases, pediatric cancer patients with CVADs may have simply had fewer exposures, contracted fewer viral infections, and had fewer febrile episodes.

However, of concern is the possibility that parents opted not to seek medical attention for febrile episodes in their children with cancer, either because they were afraid of exposing their children to COVID-19 in a health care facility, or perhaps because they did not want to add burden to an already over-burdened hospital, instead electing to observe their children at home. Regarding the fear of exposure, Lazzerini and colleagues recently reported 12 pediatric cases in Italy where parents reported avoiding seeking medical attention for fear of infection with SARS-CoV-2. Two children had acute leukemia, one of which presented after 7 days of very high fever and the other with prolonged symptoms of profound anemia; one of them died several days after hospitalization.19 The other children in the cohort also presented with advanced diseases, with 3 of them ultimately dying of various treatable disease, including acute onset type 1 diabetes, bacterial pneumonia, and sepsis. A similar health care avoidance occurred during the Severe Acute Respiratory Syndrome (SARS) epidemic in Taiwan because of fear of contracting SARS.20 Regarding the avoidance of over-burdening the hospital, the general message from public health and health care professionals was to stay home, and indeed included canceling routine or non-urgent medical visits. This practice probably accounts for the reduction in national childhood vaccination rates. It is possible that families misunderstood the urgency and threat that a fever represents in their children with cancer and thought they were following stay-at-home recommendations and orders. Anecdotally, our on-call physicians have received fewer after-hour calls during the pandemic, suggesting that families may be more reluctant to call or seek medical advice for other reasons in addition to fever.

The findings in this report are subject to several limitations. This was a single center study, had relatively small numbers, and was observational in nature. Thus, the results may not be generalizable. In addition, a formal attempt to study fever incidence at home and/or parental decision making in the face of fever during the early pandemic was not undertaken. This information could potentially further explain the dramatic drop in ED visits during this time period.

The early months of the pandemic were understandably filled with fear and uncertainty. Health care professionals, including pediatric oncologists, could not predict the how a pediatric oncology patient would fare should they contract SARS-CoV-2. However, through the first year of the pandemic, we are better prepared for this next year: COVID-19 vaccines are increasingly available; nationally, the shortage of personal protective equipment has been addressed; we are more familiar with COVID-19-specific infection prevention and control procedures; there is widespread use of personal masks among health care workers and the public; there is the awareness that children and young people have less severe acute COVID-19 than adults21; and we have increasing data about pediatric cancer patients and COVID-19. The Pediatric Oncology COVID-19 Case Report, a national registry created by researchers at the University of Alabama at Birmingham, has documented 857 cases of pediatric cancer patients with COVID-19 as of April 20, 2021.22 In children with a hematologic malignancy who contracted COVID-19, 32% were asymptomatic, and the most frequent symptom was fever (44%). They report a 2% death rate in these patients. In children with solid tumors included in this registry, 43% were asymptomatic, with a total death rate of 5%. These mortality rates, especially the rate associated with solid tumors, are notably higher than other reports on children without cancer.21 These data are both empowering and potentially concerning, and should be taken into account when counseling families.

As we emerge from the first year of the pandemic, newly armed with more widely available COVID-19 vaccines, but face potential new challenges related to new SARS-CoV-2 variants and vaccine hesitancy, close attention should be given to consistent communication with pediatric cancer patients and their families about the life-threatening nature of fever. Specifically, that fever in a pediatric oncology patient requires prompt medical attention, along with reassurance that hospitals are adhering to the Centers for Disease Control and Prevention’s recommendations to minimize exposure and nosocomial spread of this highly contagious virus.


The data, technology, and services used in the generation of the childhood vaccine research findings were generously supplied pro bono by the COVID-19 Research Database partners, who are acknowledged at


1. Dong E, Du H, Gardner L. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect Dis. 2020;20:533–534.
2. Declaration of a State of Emergency to Coordinate Response and Protective Actions to Prevent the Spread of COVID-19. Available at: Accessed October 28, 2020.
3. Executive Order No. 121: Stay at Home Order and Strategic Directions for North Carolina in Response to Increasing COVID-19 Cases. 2020 Available at: Accessed October 28, 2020.
4. Fact Sheet: Service Use among Medicaid & CHIP Beneficiaries age 18 and Under during COVID-19. Available at: Accessed October 28, 2020.
5. Martin K, Kurowski D, Given P, et al. The impact of COVID-19 on the use of preventative health care. Available at: Accessed June 11, 2021.
6. Taquechel K, Diwadkar AR, Sayed S, et al. Pediatric asthma health care utilization, viral testing, and air pollution changes during the COVID-19 pandemic. J Allergy Clin Immunol Pract. 2020;8:3378–3387.e11.
7. Santoli JM, Lindley MC, DeSilva MB, et al. Effects of the COVID-19 pandemic on routine pediatric vaccine ordering and administration—United States, 2020. MMWR Morb Mortal Wkly Rep. 2020;69:591–593.
8. Bramer CA, Kimmins LM, Swanson R, et al. Decline in child vaccination coverage during the COVID-19 pandemic—Michigan Care Improvement Registry, May 2016-May 2020. MMWR Morb Mortal Wkly Rep. 2020;69:630–631.
9. Hartnett KP, Kite-Powell A, DeVies J, et al. Impact of the COVID-19 pandemic on emergency department visits—United States, January 1, 2019-May 30, 2020. MMWR Morb Mortal Wkly Rep. 2020;69:699–704.
10. Lange SJ, Ritchey MD, Goodman AB, et al. Potential indirect effects of the COVID-19 pandemic on use of emergency departments for acute life-threatening conditions—United States, January-May 2020. MMWR Morb Mortal Wkly Rep. 2020;69:795–800.
11. Jiang M, Li C-L, Pan C-Q, et al. The risk of bloodstream infection associated with totally implantable venous access ports in cancer patient: a systematic review and meta-analysis. Support Care Cancer. 2020;28:361–372.
12. Pizzo PA. Management of fever in patients with cancer and treatment-induced neutropenia. N Engl J Med. 1993;328:1323–1332.
13. Pizzo PA. Fever in immunocompromised patients. N Engl J Med. 1999;341:893–900.
14. Lehrnbecher T, Robinson P, Fisher B, et al. Guideline for the management of fever and neutropenia in children with cancer and hematopoietic stem-cell transplantation recipients: 2017 update. J Clin Oncol. 2017;35:2082–2094.
15. Klastersky J, de Naurois J, Rolston K, et al. Management of febrile neutropaenia: ESMO Clinical Practice Guidelines. Ann Oncol. 2016;27(suppl 5):v111–v118.
16. Mueller EL, Sabbatini A, Gebremariam A, et al. Why pediatric patients with cancer visit the emergency department: United States, 2006-2010. Pediatr Blood Cancer. 2015;62:490–495.
17. Salstrom JL, Coughlin RL, Pool K, et al. Pediatric patients who receive antibiotics for fever and neutropenia in less than 60 min have decreased intensive care needs. Pediatr Blood Cancer. 2015;62:807–815.
18. Alali M, David MZ, Danziger-Isakov LA, et al. Pediatric febrile neutropenia: change in etiology of bacteremia, empiric choice of therapy and clinical outcomes. J Pediatr Hematol Oncol. 2020;42:e445–e451.
19. Lazzerini M, Barbi E, Apicella A, et al. Delayed access or provision of care in Italy resulting from fear of COVID-19. Lancet Child Adolesc Health. 2020;4:e10–e11.
20. Chang HJ, Huang N, Lee CH, et al. The impact of the SARS epidemic on the utilization of medical services: SARS and the fear of SARS. Am J Public Health. 2004;94:562–564.
21. Swann OV, Holden KA, Turtle L, et al. Clinical characteristics of children and young people admitted to hospital with covid-19 in United Kingdom: prospective multicentre observational cohort study. BMJ. 2020;370:m3249.
22. The Pediatric Oncology COVID-19 Case Report. Available at: Accessed May 18, 2021.

pediatric; oncology; fever; neutropenia; COVID-19

Copyright © 2021 Wolters Kluwer Health, Inc. All rights reserved.