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Jamaoncology Bakouny 2021 L Letters Concept and design: Ortiz, Deshmukh. gland area of the United States (from March 2 to June 2, 2020),1 Acquisition, analysis, or interpretation of data: All authors. was compared with 3 control periods before and after the main Drafting of the manuscript: Ortiz, Colón-López, Deshmukh. Critical revision of the manuscript for important intellectual content: All authors. study period (the preceding 3 months from December 1, 2019, Statistical analysis: Ortiz-Ortiz, Tortolero-Luna, Torres-Cintrón, Deshmukh. to March 2, 2020; the same 3 months in the preceding year from Obtained funding: Ortiz, Colón-López, Deshmukh. March 2 to June 2, 2019; and the 3 months after the main study Administrative, technical, or material support: Ortiz, Wu, Deshmukh. period from June 3 to September 3, 2020). The percentage de- Supervision: Ortiz, Colón-López, Deshmukh. crease in screening tests and in diagnoses during the pan- ConflictofInterestDisclosures:DrOrtizreportedreceivinggrantsfromtheNational Institutes of Health during the conduct of the study; and personal fees from serving demic period compared with each of the control periods was as a consultant for Merck outside the submitted work. Dr Ortiz-Ortiz reported computed as percentage decrease = (Npandemic −Ncontrol)/ receiving grants from the Centers for Disease Control and Prevention (CDC) National Ncontrol. The 95% CIs were computed using the Clopper- Program of Cancer Registries and the National Cancer Institute (NCI) during the Pearson method using the DescTools package in R. All analy- conduct of the study; and grants from Abbvie Corp outside the submitted work. DrColón-LópezreportedrecevingpersonalfeesfromservingasaconsultantforMerck ses were performed using R, version 3.6.1 (R Foundation for & Co outside the submitted work. Dr Tortolero-Luna reported receiving grants from Statistical Computing) (eMethods in the Supplement). Ethi- the NCI and the CDC during the conduct of the study. Mr Torres-Cintrón reported cal approval for the study was provided by Brigham and Wo- receiving grants from CDC National Program of Cancer Registries during the conduct ofthestudy;andgrantsfromAbbVieCorpoutsidethesubmittedwork.DrDeshmukh men’s Hospital prior to commencement of data analysis, in- reportedreceivingpersonalfeesfromMerckIncoutsidethesubmittedwork.Noother cluding a waiver of the requirement for individual patient disclosures were reported. consent given the retrospective and noninterventional na- Funding/Support: This study was funded by U54 grant: 2U54CA096297-16, ture of the research. “Partnership for Excellence in Cancer Research between the University of Puerto Rico (UPR) and the University of Texas MD Anderson Cancer Center (MDACC)” and by award number NU58DP006318 from the National Program of Results | A total of 192 060 patients underwent screening dur- Cancer Registries of the Centers for Disease Control and Prevention to the ing the 4 screening periods. The overall mean (SD) age was 59.6 Puerto Rico Central Cancer Registry. (12.2) years, 58.6% of all patients were female, and 80.1% were Role of the Funder/Sponsor: The funding sources had no role in the design and non-Hispanic White. Overall, 15 453 patients (with 1985 ensu- conduct of the study; collection, management, analysis, and interpretation of ing diagnoses) had undergone 1 of the 5 cancer screening ex- the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication. aminations (low-dose computed tomography,Papanicolaou test, AdditionalContributions:RyanSuk,MS,UTHealthSchoolofPublicHealth,provided colonoscopy, prostate-specific antigen screening, or mammog- assistance with Figure 2. She was not compensated for her contribution. raphy) during the 3-month pandemic study period, compared 1. Deshmukh AA, Suk R, Shiels MS, et al. Incidence trends and burden of human with 51 944 patients (3190 diagnoses) during the subsequent 3 papillomavirus–associated cancers among women in the United States, months, 64 269 patients (3423 diagnoses) in the preceding 3 2001-2017. J Natl Cancer Inst. 2020;djaa128. doi:10.1093/jnci/djaa128 months, and 60 344 patients (2961 diagnoses) during the same 2. Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint 3 months of the preceding year (2019). The decrease in screen- regression with applications to cancer rates. Stat Med. 2000;19(3):335-351. doi:10.1002/(SICI)1097-0258(20000215)19:3<335::AID-SIM336>3.0.CO;2-Z ing tests was accompanied by decreases in ensuing diagnoses 3. Rosenberg PS, Check DP, Anderson WF. A web tool for age-period-cohort and was found across the 5 screening tests (Figure 1). The per- analysis of cancer incidence and mortality rates. Cancer Epidemiol Biomarkers Prev. centage of positivity of screening tests appeared to be higher dur- 2014;23(11):2296-2302. doi:10.1158/1055-9965.EPI-14-0300 ing the primary pandemic period compared with the 3 control 4. Burger EA, Smith MA, Killen J, et al. Projected time to elimination of cervical periods for mammographies (4.1% vs 1.9%-2.3%), prostate- cancer in the USA: a comparative modelling study. Lancet Public Health. 2020;5 specific antigen screenings (22.7% vs 9.9%-13.2%), colonosco- (4):e213-e222. doi:10.1016/S2468-2667(20)30006-2 pies (1.3% vs 0.7%-0.9%), and Papanicolaou tests (11.6% vs 6.5%- 5. Centers for Disease Control and Prevention. BRFSS prevalence & trends data. Published 2020. Accessed September 3, 2020. https://www.cdc.gov/brfss/ 10.0%), but not for low-dose computed tomography scans (0.8% brfssprevalence/ vs 0.7%-0.8%). The percentage decreases in screening were pro- 6. Lei J, Ploner A, Elfström KM, et al. HPV vaccination and the risk of invasive nounced across all screening tests, compared with all 3 control cervical cancer. N Engl J Med. 2020;383(14):1340-1348. doi:10.1056/NEJMoa1917338 periods, and ranged from –60% to –82% (Figure 2A). The per- centage decreases in diagnoses resulting from the cancer screen- Cancer Screening Tests and Cancer Diagnoses ing tests, compared with all 3 control periods, were also pro- During the COVID-19 Pandemic nounced (–19% to –78%; Figure 2B). Assuming the same number Oncology patient care may be disrupted secondary to corona- of patients (64 269) would have otherwise been screened dur- virus disease 2019 (COVID-19) through delays in diagnostic in- ing the pandemic period as in the previous 3 months, approxi- vestigations and surgical procedures, as well as delayed can- mately 1438 cancerous and precancerous lesion diagnoses (1985 cer diagnoses because of reduced cancer screening. This study vs 3423 diagnoses) were “missed” during the primary pan- assesses the number of pa- demic period. Supplemental content tients undergoing cancer screening tests and of ensu- Discussion | This study reports a significant decrease in the num- ing cancer diagnoses during the COVID-19 pandemic in the larg- ber of patients undergoing screening tests for cancer and in the est health care system in the northeastern United States, Mas- number of ensuing diagnoses of cancerous and precancerous le- sachusetts General Brigham. sions during the COVID-19 pandemic in 1 health care system in the Northeastern United States. We found that, from June to Sep- Methods | This study comprised four 3-month periods. One pe- tember 2020, there was a significant recovery in the number of riod, during the first peak of the pandemic in the New En- screening tests and ensuing diagnoses, to almost prepandemic 458 JAMA Oncology March 2021 Volume 7, Number 3 (Reprinted) jamaoncology.com © 2021 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 09/28/2021 Letters Figure 1. Changes in the Numbers of Cancer Screening Tests and Ensuing Diagnoses A B Subsequent 3 mo Pandemic group All tests Positive test results Cancer screening test Cancer screening test Mammography Mammography PSA PSA Colonoscopy Colonoscopy Papanicolaou test Papanicolaou test Low-dose CT scan Low-dose CT scan 0 10 000 20 000 30 000 0 10 000 20 000 30 000 Screening tests, No. Screening tests, No. C Preceding 3 mo D Same 3 mo in 2019 Cancer screening test Cancer screening test Mammography Mammography PSA PSA Colonoscopy Colonoscopy Papanicolaou test Papanicolaou test Low-dose CT scan Low-dose CT scan 0 10 000 20 000 30 000 0 10 000 20 000 30 000 Screening tests, No. Screening tests, No. Changes in the numbers of cancer screening tests and ensuing diagnoses by cancer screening test and screening period during the primary pandemic study period compared with3controlperiods(subsequent3months,preceding3months,andsame3monthsintheprecedingyear).CTindicatescomputedtomography;PSA,prostate-specificantigen. Figure 2. Percentage Decreases in the Numbers of Screening Tests and Ensuing Diagnoses Subsequent 3 mo Preceding 3 mo Same 3 mo in 2019 A Screening tests 0 –10 –20 –30 –40 –50 –60 –70 Change in cancer screening tests, % –80 –90 Mammography PSA Colonoscopy Papanicolaou Low-dose test CT scan Cancer screening test B Screening tests with diagnoses of cancerous or precancerous lesions 60 40 20 0 Percentage decreases during the primary pandemic study period –20 compared with 3 control periods –40 (subsequent 3 months, preceding 3 months, and same 3 months in the –60 preceding year) in the number of Change in cancer diagnosis, % screening tests (A) and in the number –80 of screening tests leading to –100 diagnoses of cancerous or Mammography PSA Colonoscopy Papanicolaou Low-dose precancerous lesions (B). Error bars test CT scan indicate 95% CIs. CT indicates Cancer screening
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