Received: 23 January 2022 Revised: 23March 2022 Accepted: 4 April 2022 DOI: 10.1002/pbc.29748 Pediatric Blood & Cancer The American Society of Pediatric Hematology/OncologyG LOBA L ONCO LOGY: R E S E A RCH ART I C L E Impact of COVID-19 in pediatric oncology care in Latin America during the first year of the pandemic Gabriela Villanueva1 Claudia Sampor2 Julia Palma3 Milena Villarroel3 Diana Valencia4,5 Mercedes García Lombardi6 Wendy Gomez Garcia7 Eva Lezcano Caceres8 Victoria Sobrero9 Lilia Garcia10 Victor Cabrera11 IvanMaza12 ThelmaVelasquez13 Cecilia Ugaz14 JacquelineMontoya Vasquez14 Rosdali Diaz Coronado14 Natalia Gonzalez15 Simone Aguiar16 Agustin Dabezies17 FlorenciaMoreno18,19 Susan Sardinas20 Yessika Gamboa21 EssyMaradiegue22 Ligia Fu23 Pascale Gassant24 KatiuskaMoreno25 Oscar Gonzales26 Magdalena Schelotto27 Sandra Luna-Fineman28,29 Celia Gianotti Antoneli30 Soad Fuentes-Alabi31,32 Silvana Luciani31 Andrea Cappellano33 Guillermo Chantada1,27,34 Liliana Vasquez31,35 1Pediatrics Hematology andOncology, Hospital Austral, Pilar, Argentina 2Service of Hematology/Oncology, Hospital J.P Garrahan, Buenos Aires, Argentina 3Pediatric Oncology, Hospital Luis CalvoMackenna, Santiago, Chile 4Pediatric Oncology, Hospital Universitario de Santander IMATOncomedica, Monteria, Colombia 5Pediatric Oncology, IMATOncomédica, Colombia 6Pediatric Oncology, Hospital de Niños Ricardo Gutierrez, Buenos Aires, Argentina 7Hematology-Oncology, Dr. Robert Reid Cabral Children’s Hospital, Santo Domingo, Dominican Republic 8Pediatric Oncology, Hospital Central Instituto de Prevision Social, Asunción, Paraguay 9Pediatric Oncology, Hospital Ramon Carrillo, San Carlos de Bariloche, Argentina 10Centro Universitario Contra el Cáncer UANL,Monterrey, Mexico 11Pediatric Oncology, Hospital Regional Río Blanco, Orizaba, Mexico 12Pediatric Oncology, Hospital Rebagliati, Lima, Peru 13Pediatric Oncology, UnidadNacional deOncología Pediátrica, Guatemala City, Guatemala 14Instituto Nacional de Enfermedades Neoplásicas, Lima, Peru 15Hospital Militar Nacional de Colombia, Bogotá, Colombia 16IOP/GRAACC/UNIFESP, São Paulo, Brazil 17Pediatric HematoOncology, MUCAM,Montevideo, Uruguay 18Registro Onco-Pediatrico Hospitalario Argentino (ROHA, Hospital based Pediatric Cancer Registry fromArgentina), Buenos Aires, Argentina 19Instituto Nacional del Cancer, Buenos Aires, Argentina 20Hospital del NiñoOvidio Aliaga Uria, La Paz, Bolivia 21Pediatric Oncology, Hospital Nacional de Niños, San José, Costa Rica 22Ministry of Health, Prevention of Cancer Directorate, Lima, Peru Abbreviations: COVID-19, coronavirus 2019 disease; HCE, healthcare expenditure; HIC, high-income countries; LATAM, Latin American; LMIC, low- andmiddle-income countries; NCDs, noncommunicable diseases; OR, odds ratio; PPE, personal protective equipment; SARS, severe acute respiratory virus; SCT, stem cell transplant; SLAOP, Latin American Society of Pediatric Oncology. Pediatr Blood Cancer. 2022;69:e29748. © 2022Wiley Periodicals LLC. 1 of 12wileyonlinelibrary.com/journal/pbc https://doi.org/10.1002/pbc.29748 https://orcid.org/0000-0002-6159-1882 https://orcid.org/0000-0002-9403-7415 https://orcid.org/0000-0002-1849-2256 https://orcid.org/0000-0003-2213-8919 https://orcid.org/0000-0003-0713-7651 https://orcid.org/0000-0002-9375-9336 https://orcid.org/0000-0002-9584-3208 https://wileyonlinelibrary.com/journal/pbc https://doi.org/10.1002/pbc.29748 2 of 12 VILLANUEVA ET AL. 23Hemato-Oncologia, Hospital Escuela Universitario, Tegucigalpa, Honduras 24Pediatric Oncology, Hôpital Saint - Damien, Port-au-Prince, Haiti 25Docente de pregrado de hematologia universidad laica Eloy Alfaro deManabi, Hospital Verdi Cevallos Balda - Hospital especialidades Portoviejo, Manabi, Ecuador 26Hospital Civil de Guadalajara Dr. Juan IMenchaca, Guadalajara, Jalisco, México 27Pediatric Oncology, Hospital Pereira Rossell, Montevideo, Uruguay 28University of Colorado School ofMedicine, Aurora, Colorado, USA 29Department for theManagement of Noncommunicable Diseases, Disability, Violence and Injury Prevention,World Health Organization, Geneva, Switzerland 30Universidade Nove the Julhio, São Pablo, Brazil 31Non-Communicable Diseases, Pan American Health Organization,Washington, District of Columbia, USA 32Pediatric Oncology, Hospital Nacional de Niños Benjamin Bloom y Fundacion Ayudame a Vivir Pro- Ninos con Cancer de El Salvador, San Salvador, El Salvador 33Department of Pediatric Neuro-Oncology, Instituto deOncologia Pediátrica - IOP/GRAACC/UNIFESP, São Paulo, Brazil 34Fundación Perez Scremini, Montevideo, Uruguay 35Facultad deMedicina, Centro de Investigación deMedicina de Precisión, Universidad de SanMartín de Porres, Lima, Perú Correspondence Gabriela Villanueva, Hospital Austral, Pediatrics Hematology andOncology, Pilar, Argentina. Email: gabrielavillanueva7@gmail.com Abstract Background: The ongoing coronavirus 2019 disease (COVID-19) pandemic strained medical systems worldwide. We report on the impact on pediatric oncology care in Latin American (LATAM) during its first year. Method: Four cross-sectional surveys were electronically distributed among pediatric onco-hematologists in April/June/October 2020, and April/2021 through the Latin American Society of Pediatric Oncology (SLAOP) email list and St Jude Global regional partners. Results: Four hundred fifty-three pediatric onco-hematologists from 20 countries responded to the first survey, with subsequent surveys response rates above 85%. More than 95% of participants reported that treatment continued without interrup- tion for new and active ongoing patients, though with disruptions in treatment avail- ability. During the first three surveys, respondents reported suspensions of outpatient procedures (54.2%), a decrease in oncologic surgeries (43.6%), radiotherapy (28.4%), stem cell transplants (SCT) (69.3%), and surveillance consultations (81.2%). Logistic regression analysis showed that at the beginning of the first wave, participants from countrieswith healthcare expenditure below7%weremore likely to report a decrease in outpatient procedures (odds ratio [OR]: 1.84, 95% CI: 1.19–2.8), surgeries (OR: 3, 95% CI: 1.9–4.6) and radiotherapy (OR: 6, 95% CI: 3.5–10.4). Suspension of surveil- lance consultations was higher in countries with COVID-19 case fatality rates above 2% (OR: 3, 95% CI: 1.4–6.2) and SCT suspensions in countries with COVID-19 inci- dence rate above 100 cases per 100,000 (OR: 3.48, 95% CI: 1.6–7.45). Paradoxically, at the beginning of the second wave with COVID-19 cases rising exponentially, most participants reported improvements in cancer services availability. Conclusion: Our data show the medium-term collateral effects of the pandemic on pediatric oncology care in LATAM, which might help delineate oncology care delivery amid current and future challenges posed by the pandemic. KEYWORDS COVID-19, healthcare delivery, Latin America, low- and middle-income countries, pediatric can- cer, survey mailto:gabrielavillanueva7@gmail.com VILLANUEVA ET AL. 3 of 12 1 INTRODUCTION Severe acute respiratory virus (SARS-CoV-2) outbreak resulting in coronavirus 2019 disease (COVID-19) caused an unprecedented pandemic that led tomore than 400million cases and close to 6million deaths around the world (dateMarch 7, 2022).1 More than 1 year into the pandemic, multiple measures were implemented by governments attempting to slow the spread of COVID-19 and to ameliorate the burden on their medical systems.2,3 These included home isolations, closing borders, schools, nonessential business, the use of personal protective equipment (PPE), and restricting travel within and between countries. The fear generated by the pandemic resulted in patients being unable or unwilling to seek medical care4 and patients were discouraged to come to the hospital, even those with chronic diseases, noncommunicable diseases (NCDs), cancer, or other major health problems. The pandemic exposed unprepared healthcare systems with limited PPE, limited ICU staff, and ventilators, which affected unprotected vulnerable populations.5 Initial cases of COVID-19 occurred in Latin America (LATAM) weeks after Europe and North America struggled with a steep first wave. This allowed LATAM coun- tries to implement early epidemiological actions and pre-emptively restrict their medical system’s nonessential use. Now, more than a year into the pandemic, the resulting economic and social impact are still unfolding. The development of multiple effective vaccines has provided some relief, though still only 24.2% of the world population is fully vaccinated, mainly in high-income countries (HIC),6 leaving most of the world exposed to new waves of COVID-19, with an increased risk for the development of highly contagious SARS-CoV-2 variants. The survival of pediatric oncology patients depends significantly on a functionalmedical systemthat allows for early diagnosis and referrals to tertiary care centers, timely initiation, coordination of care among multidisciplinary teams, and access to supportive care.7 Early studies showed that complications and mortality from COVID-19 were lower in pediatric patients compared to adults,8 and that pediatric oncol- ogy patients were not at elevated risk of poor outcomes as adult can- cer patients.9–11 However, a recent global study reporting the out- come of pediatric oncologic patients infected with COVID-19 from April 2020 to February 2021, showed that one-fifth of that popula- tion had a severe critical infection, and 3.8% died due to COVID-19, which is four times the mortality reported in the pediatric general population.12 A first report on the pandemic’s impact on pediatric cancer care delivery in LATAMwas published in April 2020 (before the firstwave in the region). This study revealed that healthcare expenditure (HCE)was closely associatedwith higher proportions of disrupted pediatric onco- logic treatments.13 However, as the pandemic evolved, LATAMbecame one of the world’s hot spots, accounting for more than 30million cases andmore than 1million deaths. This study provides evidence from four cross-sectional surveys conducted throughout the first year of the pan- demic in LATAM, aiming to showhowpediatric cancer services adapted to several waves of SARS-CoV-2 infection and the disruptions of pedi- atric oncologic care delivery that resulted from them. 2 METHODS 2.1 Study design and participants We conducted four cross-sectional surveys of pediatric onco- hematologists throughout 20 LATAM countries during the first year of the COVID-19 pandemic. The participating countries include Argentina, Bolivia, Brazil, Chile, Colombia, Costa Rica, Cuba, Domini- can Republic, Ecuador, El Salvador, Guatemala, Haiti, Honduras, Mexico, Nicaragua, Panama, Paraguay, Peru, Uruguay, and Venezuela. The results of the first survey, performed in April 2020, have already been published.13 The survey was electronically distributed through the Latin American Society of Pediatric Oncology (SLAOP) (the Inter- national Society of Pediatric Oncology - SIOP-continental branch) email list in collaboration with St Jude Global and the Pan Amer- ican Health Organization (PAHO). For each country participating in the study, the national delegate from the SLAOP network was assigned to promote the survey among physicians. The distribution of the online forms included mailshots (through the email list of the SLAOP and the Central and South America Region Branch of St Jude Global - CASA). Surveys were carried out at four strategic moments during the pan- demic. The first one took place from April 12 to 19, 2020, during the firstwave of infections in Europe andNorthAmerica, but still few cases in LATAM. The second one took place from June 10 to 17, 2020, when cases were rising during the first wave in most LATAM countries. The third one was conducted from October 19 to 26, 2020, when the first wave started to resolve, and, finally, the fourth survey occurred from April 12 to 26, 2021, halfway through the region’s secondwave. 2.2 Survey questionnaires Each survey collected data on the individual perspectives of physicians (pediatric oncologist,medical directors, residents, and fellows)working in pediatric onco-hematology departments of public and private health institutions. We only included the group of professionals responsible for the treatment and coordination of care of patients with cancer to avoid high heterogeneity of answers. Each survey contained between 20 and 32 items and was developed to capture data about the disrup- tion and adaptation of pediatric cancer care at a specific time point, aiming to detect changes, as the pandemic evolved. Questions on the following topics were included: treatment suspension of newly diagnosed patients and active ongoing cases, chemotherapy protocol modifications, displacement or reduction of medical staff, suspension of outpatient procedures, cancer surgeries, radiation therapy sessions, bone marrow transplantation, and pal- liative care assessments and care. In addition, some questions were formulated to capture information about strategies implemented to provide continuity of care (telemedicine) and personal perspectives on the greatest impacts of the pandemic on patients’ care (delays in diagnosis, treatment abandonment, and out-of-pocket expenses). 4 of 12 VILLANUEVA ET AL. Health indicators and epidemiologic parameters of COVID-19, such as incidence rate, case fatality rate (number of COVID-19 deaths divided by the total number of cases, multiplied by 100) and HCE as a percentage of gross domestic product (GDP) from each coun- try were analyzed for potential association with the impact of treat- ment of children with cancer. All responses were anonymous and insti- tutional ethical review was not required. After data collection, each country delegate verified the authenticity and consistency of the data provided. 2.3 Statistical analysis Development indicators from each participating country were obtained from theWorld Bank Open Data platform.6 Data on COVID- 19 incidence and mortality beginning on February 28, 2020 (first COVID-19 case diagnosed in LATAM) to April 30, 2021 (day the last survey closed) were extracted from the data repository for the 2019 Novel Coronavirus Visual Dashboard operated by the Johns Hopkins University Center for Systems Science and Engineering (JHUCSSE).14 Respondent characteristics were reported using descriptive statis- tics. Categorical variableswere assessed by chi-square test. Univariate and multivariable logistic analyses were done for the following health- care factors: treatment of new patients, treatment of active/ongoing cases, suspension of outpatient procedures, suspension of oncologic surgeries, suspension of radiation therapy sessions, suspension of stem cell transplant (SCT), and suspension of surveillance consultations. We calculated crude odds ratios (OR) and variables associated with signifi- cant impact in amultivariable logistic regression analysis. Radiation therapy sessions and SCT proportions were calculated based on the total number of participants that reported having access to radiation therapy or SCT. Participants who reported no access to those services or answered “Do not know” were excluded. Significance was established when p-values were less than .05. Statistical analyses were performed using RStudio version 1.2.1335. 3 RESULTS From 795 pediatric oncologists, medical directors, and resi- dents/fellows contacted, the response rate among all four surveys ranged between 43% and 57%. A total of 453 of 795 pediatric onco- hematologists from 20 countries responded to the first survey. The participation for subsequent surveys remained above 85% among the original respondents: 408 participants in June 2020 (90%), 386 inOctober 2020 (85.2%), and 389 in April 2021 (85.9%) (Table S1). In all four surveys, respondentswere pediatric oncologists (50%–59%), medical directors (31%), and residents/fellows (10%). Participants were affiliated to public hospitals (58%–63%), public–private (22%– 24%), or private (15%–17%). The most frequent facility type was children’s hospitals (41%), followed by general hospital (35%) and cancer centers (23%). The first three surveys took place during the beginning, peak, and resolution of the first wave in most participating countries, except for Uruguay, whose first wave started late in April 2021 (Figures 2 and 3). During those first three surveys, on average, respondents reported partial or complete suspension of outpatient procedures (54.2%), decreases in surgical services (43.6%), radiation therapy ses- sions (28.4%), SCT (69.3%), and off-therapy surveillance consultations (81.2%) (Table 1). Even though more than 95% of the participants sur- veyed reported that new and active patients received oncologic treat- ment during all four surveys, they also reported disruptions in treat- ment availability that conditioned the type of treatment they offered (Figures 1–3). Univariate logistic regression analysis was performed on each sur- vey. Factors, including incidence rate of more than 100 cases per 100,000, case fatality rate above 2%, and HCE less than 7%, were significantly associated with suspensions of some or all of the fol- lowing services: outpatient procedures, oncologic surgeries, patient surveillance, radiotherapy sessions, and SCT. In contrast, suspension of treatment of new and active ongoing patients was not, as physicians continue treating patients with the treatments modalities that were available. Multivariable logistic regression analysis showed that when COVID-19 cases were rising at the beginning of the first wave (June 2020), LATAM countries with an HCE below 7% were more likely to report a decrease in outpatient procedures (OR: 1.84, 95% CI: 1.19– 2.8) and surgeries (OR: 3, 95% CI: 1.9–4.6), controlling for other indi- cators of COVID-19 burden. In addition, suspension of radiation ther- apy sessions also increased in those countries with HCE less than 7% (OR: 6, 95%CI: 3.5–10.44). Surveillance consultationswere suspended in countries with a case fatality rate above 2% (OR: 3, 95% CI: 1.4– 6.2); and SCTwere suspended in countries where COVID-19 incidence rate was above 100 cases per 100,000 (OR: 3.48, 95% CI: 1.6–7.45) (Table S4). At the end of the first wave, in October 2020, the associa- tion between HCE and the suspension of outpatient procedures, surg- eries, radiotherapy sessions, and SCT suspensions remained, even as the first wave resolved and indicators of national burden of COVID-19 improved inmost countries (Table S5). In April 2021 (beginning of the second wave), with cases of COVID- 19 rising exponentially again in most countries, most participants reported an improvement in pediatric cancer services availability. Only 36% of respondents reported suspension of outpatient procedures (down from 50% in June 2020), 30.6% reported suspensions in surg- eries (down from 41% in June 2020), 16% suspension of radiotherapy sessions (down from 25.1% in June 2020), 37.5% suspension of SCT (down from 68.1% in June 2020); and 48.1% reported suspension of surveillance consultations (down from 80.7% in June 2020) (Table 1). In April 2021, only countries with HCE below 7% continued to have an increase in radiotherapy sessions suspension (OR: 3.16, 95% CI: 1.7– 5.89) and in SCT suspensions (OR: 7.16, 95% CI: 3.17–16.15), while other indicators of national COVID-19 burden did not show any asso- ciation (Table S6). At the beginning of the pandemic, 35.6% of participants reported chemotherapy regimenmodifications due to drug shortages and 45.2% a significant decrease in access to blood products. Deeper into the VILLANUEVA ET AL. 5 of 12 F IGURE 1 Proportion of responses on childhood cancer treatments disruptions (total or partial suspensions) during the first year of COVID-19 pandemic in all participating Latin American countries pandemic (June–October 2020), chemotherapy availability improved as only 15% and 18% of participants reported chemotherapy short- ages. However, an average of 55% still reported decrease in access to blood products during the last three surveys (Table S7). As shown in Figure 4, participants reported that since the beginning of the pandemic, there were frequent delays in diagnosis (33%), fre- quent treatment abandonment (17.2%), and an increase in family out- of-pocket expenses (42.2%). Responses about access to SCT and radiation therapy varied within countries and between surveys. During all four surveys, on average, 48.5% of participants reported not having access to SCT and 15.4% of participants reported not having access to radiation therapy. Notably, during all four surveys, from 60% to 82% of respondents reported some percentage of hospital staff reduction due to COVID- 19 infection or quarantine, but only maximum of 3.75% reportedmore than a 50% staff reduction (in April 2020). In addition, a maximum of 1.5% of respondents reported more than 50% displacement of pedi- atric oncologist to work in other sectors of the hospital due to COVID- 19 (in June 2020) (Table 1). On average, 55% of participants had access to some form of telemedicine during the first year of the pandemic (including insti- tutional telemedicine platforms and nonprofessional communication channels such as WhatsApp, Facebook, or Zoom). In April 2021, more than 80% of participants reported that theywould like to have an insti- tutional telemedicine platform to follow their patients, as more than half of them (50.4%) had only access to nonprofessional communica- tion channels. By April 2021, 99 (25%) participants reported having contracted COVID-19, 298 (76%) reported being immunized with two doses of a SARS-CoV-2 vaccine, and 64 (16.4%)with only one dose. Only five par- ticipants (1.5%) refused to be vaccinated (Table S9). We did not find differences in type of suspensions of oncology care delivery based on type of hospital setting (oncologic hospital vs. chil- dren hospital vs. general hospital). 4 DISCUSSION The COVID-19 pandemic is an unprecedented global crisis that impacted pediatric cancer healthcare systems worldwide, with a greater effect on low- and middle-income countries (LMIC).2,3,12,15–17 One year into the pandemic, the initial fears and concerns have evolved alongwith treatment andprevention strategies forCOVID-19andmul- tiple effective vaccines havebeendeveloped in record time.As thepan- demic continues to unfold, our four surveys performed over the first year of the pandemic in LATAM show the medium-term effects on the care of pediatric cancer patients; and reveal how the medical systems and medical professionals adapted to the different healthcare crises that originated from the pandemic. Worldwide, the need to adapt to an uncertain future led to rationing of treatment delivery by suspensions of most pediatric 6 of 12 VILLANUEVA ET AL. F IGURE 2 South America. Proportion of responses on treatments disruptions (total or partial suspensions) per survey and per country, compared to number of COVID-19 cases per day in each country VILLANUEVA ET AL. 7 of 12 F IGURE 3 Central America. Proportion of responses on treatments disruptions (total or partial suspensions) per survey and per country, compared to number of COVID-19 cases per day in each country 8 of 12 VILLANUEVA ET AL. F IGURE 4 Effect of COVID-19 pandemic on treatment abandonment, delays in diagnosis, and increase in out-of-pocket expenses during the first year of the pandemic: 33% of participants reported that delays in diagnosis occurred very frequently; 17.2% of participants reported that treatment abandonment occurred very frequently during the pandemic; and 42.4% of participants reported an increase in family out-of-pocket expenses cancer services.13,16–18 A recent global study reported that 55.8% of children with cancer had modifications in their cancer-directed therapies during the pandemic. In India, a group reported 36.1% of 1146 pediatric patients with cancer experienced treatment delays after a country-wide lockdown. In alignment with these findings, our data show different levels of disruption of cancer services, such as suspension of SCT, radiotherapy sessions, oncologic surgeries, and chemotherapy modifications throughout the year. Specifically, from April 2020 to October 2020, most countries experienced the first wave with intense constraints imposed by government lockdowns. Therefore, the answers to our surveys reflect cautionary adaptation, as most medical systems organized to face unpredictable healthcare delivery crises. Not surprisingly, higher levels of treatment disruptions were reported in countries with HCE below 7%, and in countries with higher national burden of COVID-19, reflected by a higher incidence rate and case fatality rate above 2%. However, by April 2021, amid the secondwave in the region, the respondents’ answers reflected a better understanding of the effect of COVID-19 on children with cancer, a better preparedness of themedical system to safely deliver cancer care and the resilience of pediatric cancer professionals in the region, who were able to re-institute most cancer care services, in the midst of the pandemic. A recent questionnaire led by the World Health Organization on the impact of COVID-19 on NCD resources and services showed that 66% of participating countries (mainly upper-middle and high-income countries) includedNCD services in the list of national essential health services.19 However, in LMIC, access to quality cancer care was lim- ited even before the pandemic, as healthcare systems struggled with strained resources.20–22 The COVID-19 pandemic exacerbated the scarcity of these resources, and institutions reported decreases in financial support, as well as increased dependency on social organiza- tions to provide help in transportation and family accommodation dur- ing treatments.17 By April 2021, almost half of the participants in our surveys reported patients’ families experiencing increased economic burden of cancer care, including out-of-pocket expenses. This high- lights the overall increased social impact of the pandemic on cancer therapy delivery and financing. Essential drug shortage to treat oncologic pediatric patients is a multifactorial and an ongoing problem in LATAM.23 Issues with sup- ply, distribution, and procurement of chemotherapy agents worsened during the pandemic. For example, the total amount and type of chemotherapy agents needed were challenging to estimate given the fluctuations in number of patients with new oncologic diagnosis in- between COVID-19 waves. In addition, there were problems with dis- tribution of medications evenwithin the same country. Delayed diagnosis and treatment abandonment are well-described problems in LMIC. Treatment abandonment has been described as high as 20%–30% in some LATAM countries, though this problem did not affect all countries in the region equally.21,24 Early in the pan- demic, different studies reported a decrease of newly diagnosed chil- dren with cancer, delays in referral to tertiary centers,7,9,22,25 and increased treatment abandonment.7,9,15,22,25 By April 2021, our data show that one third of respondents reported persistent delays in diagnosis, and 17.2% reported treatment abandonment as a persis- tent problem, which might be related to an increase in the use of telemedicine as amodality to assure continuity of care, thoughwewere not able to corroborate that association. In addition, we cannot estab- lish if there was a difference in the rate of treatment abandonment before and during the pandemic, as we did not collect information at the patient level. Telemedicine (including video-, web-, and telephone-based inter- ventions) had been implemented pre-pandemic in malignant hema- tologic patients; and proved to be a feasible and acceptable form of intervention.26 The changing landscape of healthcare delivery created by the pandemic opened the opportunity to implement telemedicine to provide continuity of care to pediatric oncology patients.27,28 VILLANUEVA ET AL. 9 of 12 TABLE 1 Participant responses about treatment disruptions comparing the first wave (April–June–October 2020) and the beginning of secondwave in Latin America (April 2021) First wave Secondwave April 2020 June 2020 October 2020 April 2021 Total 453 408 (90%) 386 (85.2%) 389 (85.9%) Type of hospital setting Oncologic hospital 109 (24%) 99 (24%) 87 (22%) Children hospital 184 (40%) 269 (66%) 169 (44%) General hospital 160 (35%) 40 (10%) 130 (33%) Treatment of new patients Yes 429 (94.7%) 397 (97.6%) 382 (98.9%) 386 (99.2%) No 24 (5.3%) 11 (2.4%) 4 (1%) 3 (0.8%) Treatment of active/ongoing patients Yes 441 (97.3%) 402 (98.5%) 383 (99.2%) 387 (99.5%) No 12 (2.7%) 6 (1.5%) 3 (0.8%) 2 (0.5%) Chemotherapymodification: number of times chemotherapy regimensweremodified due to shortages <10 times 114 (25.1%) 10–20 times 26 (5.7%) >20 times 22 (4.8%) Nomodification 291 (64.2%) Current chemotherapy shortage situation Improved 45 (11%) 60 (15.5%) Unchanged 262 (64.2%) 234 (60.6%) Worsen 61 (15%) 69 (18%) Do not know 40 (9.8%) 23 (6%) Suspension of outpatient procedures Continue normally 189 (41.7%) 190 (46.6%) 189 (49%) 249 (64%) Partially suspended 241 (53.2%) 204 (50%) 196 (50.8%) 140 (36%) Completely suspended 23 (5%) 14 (3.4%) 1 (0.2%) 0 (0%) Suspension of cancer surgeries Continue normally 247 (54.5%) 241 (59%) 214 (55.6%) 270 (69.4%) Partially suspended 177 (39%) 154 (37.7%) 159 (41.2%) 116 (29.8%) Completely suspended 29 (6.4%) 13 (3.2%) 13 (3.4%) 3 (0.8%) Suspension of radiotherapy sessions Continue normally 250/372 (67.2%) 246/329 (74.7%) 236/323 (73%) 268/319 (84%) Partially suspended 97/372 (26%) 68/329 (20.6%) 83/323 (25.7%) 44/319 (13.8%) Completely suspended 25/372 (6.7%) 15/329 (4.5%) 4/323 (1.2%) 7/319 (2.2%) I do not have access to RT 81 67 51 52 Do not know ⋅⋅ 12 12 18 Suspension of SCT Continue normally 64/237 (27%) 79/248 (32%) 56/170 (33%) 118/189 (62.4%) Decrease but carried asmuch as possible 109/237 (46%) 113/248 (45.5%) 89/170 (52.3%) 63/189 (33.3%) Completely suspended 64/237 (27%) 56/248 (22.6%) 25/170 (14.7%) 8/189 (4.2%) Do not know/no SCT service 216 160 216 200 (Continues) 10 of 12 VILLANUEVA ET AL. TABLE 1 (Continued) First wave Secondwave April 2020 June 2020 October 2020 April 2021 Surveillance suspension Continue normally 48 (10.6%) 79 (19.4%) 102 (26.4%) 202 (51.9%) Partially suspended 250 (55.2%) 260 (63.7%) 265 (68.6%) 184 (47.3%) Completely suspended 155 (34.2%) 69 (17%) 19 (5%) 3 (0.8%) Suspension/modification palliative care Continue normally 366 (80.8%) 343 (84%) 314 (81.3%) ⋅⋅ Partially suspended 78 (17.3%) 61 (15%) 71 (18.4%) ⋅⋅ Completely suspended 6 (1.3%) 4 (1%) 1 (0.25%) Percentage ofmedical staff decreased (due to COVID-19 infection or quarantine) <10% 143 (31.5%) 164 (40.2%) 168 (43.5%) 209 (53.7%) 10%–50% 111 (24.5%) 128 (31.4%) 140 (36.2%) 74 (19%) >50% 17 (3.75%) 9 (2.2%) 8 (2%) 3 (0.8%) None 182 (40.17%) 107 (26.2%) 70 (18.1%) 103 (26.5%) Percentage ofmedical staff displaced <10% 90 (19.8%) 92 (22.5%) 87 (22.5%) 99 (25.4%) 10%–50% 23 (5%) 22 (5.4%) 34 (8.8%) 22 (5.6%) >50% 4 (0.9%) 6 (1.5%) 2 (0.5%) 0 (0%) None 336 (74.17%) 288 (70.6%) 263 (68.1%) 268 (68.9%) Changes in staff shift schedules Redistributed 338 (74.6%) 231 (56.6%) 200 (52%) ⋅⋅ Continue normally 115 (25.4%) 177 (43.4%) 186 (48%) ⋅⋅ Telemedicine Continue normally 69 (15.2%) 63 (15.4%) 68 (17.6%) 97 (25%) Increase 157 (34.6%) 178 (43.6%) 165 (43%) 107 (27.5%) No telemedicine 227 (50.1%) 167 (41%) 153 (39.6%) 185 (47.5%) Note: Percentage was calculated based on the total number of participants that reported having access to radiation therapy and bone marrow transplant. Participants who reported no access to those services or “Do not know” were excluded. Abbreviations: PPE, personal protective equipment; SCT, stem cell transplant. However, we were not able to demonstrate with our data what impact telemedicine had on suspensions of treatments and surveillance con- sultations. During all four surveys, on average, close to half of the par- ticipants reported not having access to telemedicine. By April 2021, 50.4% of participants reported only having access to nonprofessional communication channels, such as WhatsApp, Facebook, or Zoom, to provide continuity of care. Even though those communication channels worked in areas with poor internet connection, 84% of respondents reported interest in having a formal telemedicine platform to manage and follow patients. With multiple and effective vaccines developed, vaccine hesitancy, even among healthcare professionals, is one of the biggest challenges to control the pandemic.29 In LATAM, vaccine rollouts startedwith dif- ferent levels of success, as governments struggled to have access to vaccines. However, high-risk populations, including, healthcare profes- sionals, were prioritized initially. Our data by April 30, 2021 (beginning of the second wave) revealed that 76.6% of participants had received two doses of vaccine, 16.4% one dose, and only 1.5% refused the vac- cine, reflecting a high level of vaccine acceptance among pediatric oncologists in the region. However, the percentage of the general pop- ulation thatwas fully vaccinated at that time varied significantly. Coun- tries like Chile and Uruguay had similar percentage of their population fully vaccinated at that time as someHIC like theUnited States and the United Kingdom (35% and 19% vs. 34.2% and 21.9%, respectively). In contrast, the remaining LATAM countries had immunization rates that ranged from0% to 7% for two doses and 0% to 13% for one dose (Table S9).33 Multiple health organizations have recommended COVID-19 vac- cination to cancer patients.30–32 Children and adolescents undergoing cancer treatment are at higher risk for developing severe or fatal COVID disease, and even though there is paucity of data about the immune response generated by COVID-19 vaccines in immunosup- pressed patients, the risk of severe COVID-19 disease outweighs the risk of being vaccinated. VILLANUEVA ET AL. 11 of 12 Our study has several strengths and limitations. One of the biggest strengths of this study is its high and stable participation rate from 20 LATAM countries with pediatric oncology programs. However, responses are subjective, as surveys solicited pediatric oncologists’ insights on the impact of the pandemic and on the barriers to cancer care delivery. There is a disparity in the number of participants from different countries throughout all four surveys, and the calculated pro- portion of answers at each time point is conditioned by the number of participants per country. Therefore, it is difficult to compare countries’ data within and between surveys. However, as most LATAM countries shared a similar infectionwave pattern during the first year of the pan- demic,we believe the information collected ismeaningful. Another lim- itation is that we cannot provide real measurements of the level of dis- ruption and expenses. As the pandemic unfolds, real-time research to determine the main factors that affect medical care delivery to pedi- atric oncology patientswill help better delineate areas of improvement and needs in every country. In conclusion, our data show differences between participants’ responses during the first and second waves of COVID-19 in LATAM. During the first wave, treatment disruptions (suspension of SCT, radio- therapy sessions, outpatient procedures, surveillance consultations, and surgeries) were prevalent. In addition, in countries with high COVID-19 burden and HCE below 7%, pediatric oncologists reported more extreme disruptions at the peak of the first wave. Nonetheless, all countries reported an improvement and recovery of pediatric can- cer services during the secondwave. CONFLICT OF INTEREST Guillermo Chantada receives fees from Bayer and Elea-Phoenix (Argentina) and participates on the data safety monitoring board or advisory board for Bayer (Larotrectinib). Sandra Luna-Fineman receives personal fees fromRiverboat Study (Research intoVisual end- points and Rb Health outcomes - 5R01CA225005-03 - salary sup- port), WHO NCD Childhood Cancer - consultant (salary support), St Jude Global consultant, St Jude Children’s Research Hospital, Global Retinoblastoma studies (salary support). Sandra Luna-Fineman is also a SLAOP Board member and works at the Retinoblastoma Advisory Committee, St Jude Global Alliance, St Jude Children’s Research Hos- pital. All the remaining authors declare no conflicts of interest. DATA AVAILABILITY STATEMENT The data that support the findings of this study are available from the corresponding author upon reasonable request. ORCID GabrielaVillanueva https://orcid.org/0000-0002-6159-1882 CeciliaUgaz https://orcid.org/0000-0002-9403-7415 RosdaliDiazCoronado https://orcid.org/0000-0002-1849-2256 EssyMaradiegue https://orcid.org/0000-0003-2213-8919 Sandra Luna-Fineman https://orcid.org/0000-0003-0713-7651 GuillermoChantada https://orcid.org/0000-0002-9375-9336 LilianaVasquez https://orcid.org/0000-0002-9584-3208 REFERENCES 1. World Health Organization. WHO Coronavirus Disease (COVID-19) Dashboard. World Health Organization. Accessed August 7, 2022. https://covid19.who.int 2. Graetz D, Agulnik A, Ranadive R, et al. 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Pediatr Blood Cancer. 2022;69:e29748. https://doi.org/10.1002/pbc.29748 https://doi.org/10.1177/1178632920984161 https://doi.org/10.1177/1178632920984161 https://www.who.int/publications-detail-redirect/9789240010291 https://www.who.int/publications-detail-redirect/9789240010291 https://doi.org/10.1200/JCO.2014.60.6376 https://doi.org/10.1200/JCO.2014.60.6376 https://doi.org/10.1097/MOP.0b013e32835c1cbe https://doi.org/10.1007/s10147-021-01971-3 https://doi.org/10.1007/s10147-021-01971-3 https://doi.org/10.1016/S1470-2045(21)00517-9 https://doi.org/10.1016/S1470-2045(21)00517-9 https://doi.org/10.1016/S2352-4642(19)30296-2 https://doi.org/10.3332/ecancer.2021.1172 https://doi.org/10.2196/29619 https://doi.org/10.2196/29619 https://doi.org/10.23750/abm.v91i3.9849 https://doi.org/10.2217/fon-2020-0324 https://doi.org/10.2217/fon-2020-0324 https://doi.org/10.1007/s10654-020-00671-y https://doi.org/10.5694/mja2.51444 https://doi.org/10.5694/mja2.51444 https://www.who.int/publications-detail-redirect/WHO-2019-nCoV-vaccines-SAGE_recommendation-BNT162b2-2021.1 https://www.who.int/publications-detail-redirect/WHO-2019-nCoV-vaccines-SAGE_recommendation-BNT162b2-2021.1 https://www.cancer.gov/about-cancer/coronavirus/coronavirus-cancer-patient-information https://www.cancer.gov/about-cancer/coronavirus/coronavirus-cancer-patient-information https://ourworldindata.org/covid-vaccinations https://doi.org/10.1002/pbc.29748 Impact of COVID-19 in pediatric oncology care in Latin America during the first year of the pandemic Abstract 1 | INTRODUCTION 2 | METHODS 2.1 | Study design and participants 2.2 | Survey questionnaires 2.3 | Statistical analysis 3 | RESULTS 4 | DISCUSSION CONFLICT OF INTEREST DATA AVAILABILITY STATEMENT ORCID REFERENCES SUPPORTING INFORMATION