Abstracts

Introduction

The COVID-19 pandemic has had consequences beyond the death due to the infection. In Brazil, since March 2020, states and municipalities have implemented policies to minimize the risk of transmission and have strengthened the health system capacity to treat COVID-19. Although of using slightly different approaches, most of the country adopted social distancing policies, with short- or long-term closures of non-essential businesses, schools, churches, and other activities and venues that lead to crowding ¹1. Silva LLS, Lima AFR, Polli DA, Razia PFS, Pavão LFA, Cavalcanti MAFH, et al. Social distancing measures in the fight against COVID-19 in Brazil: description and epidemiological analysis by state. Cad Saúde Pública 2020; 36:e00185020.. Moreover, due to the risk of infection, staff shortage and overwhelming COVID-19 cases, the use of most health services was restricted and non-essential procedures were postponed.

Studies conducted in high-income countries have reported sharp declines in health services visits, either for illness management or screening for diseases. Although later rescheduling are usually reported, current estimates suggest that some patients did not reschedule missed appointments, and the intensity of the decline and rescheduling varied according to the disease ²2. Wright A, Salazar A, Mirica M, Volk LA, Schiff GD. The invisible epidemic: neglected chronic disease management during COVID-19. J Gen Intern Med 2020; 35:2816-7.^,33. Papautsky EL, Hamlish T. Patient-reported treatment delays in breast cancer care during the COVID-19 pandemic. Breast Cancer Res Treat 2020; 184:249-54.^,44. Patt D, Gordan L, Diaz M, Okon T, Grady L, Harmison M, et al. Impact of COVID-19 on cancer care: how the pandemic is delaying cancer diagnosis and treatment for American seniors. JCO Clin Cancer Inform 2020; 4:1059-71.^,55. Ziedan E, Simon KI, Wing C. Effects of state COVID-19 closure policy on non-COVID-19 health care utilization. Cambridge: National Bureau of Economic Research; 2020. (NBER Working Paper Series; 27621).. Mehrotra et al. ⁶6. Mehrotra A, Chernew ME, Linetsky D, Hatch H, Cutler DA, Schneider EC. The impact of the COVID-19 pandemic on outpatient care: visits return to prepandemic levels, but not for all providers and patients. https://www.commonwealthfund.org/publications/2020/oct/impact-covid-19-pandemic-outpatient-care-visits-return-prepandemic-levels (accessed on Mar/2020).
https://www.commonwealthfund.org/publica... reported that the extent of rescheduling in the United States varied according to age and type of health insurance, with children presenting a smaller rescheduling, whereas Medicare patients showed a faster rescheduling. A survey conducted among breast cancer survivors in the United States reported that 44% of the subjects delayed their treatment, especially among younger patients ³3. Papautsky EL, Hamlish T. Patient-reported treatment delays in breast cancer care during the COVID-19 pandemic. Breast Cancer Res Treat 2020; 184:249-54.. Also in the United States, Ziedan et al. ⁵5. Ziedan E, Simon KI, Wing C. Effects of state COVID-19 closure policy on non-COVID-19 health care utilization. Cambridge: National Bureau of Economic Research; 2020. (NBER Working Paper Series; 27621). observed that State closure policies were associated with a decline in ambulatory visits, laboratory tests, and outpatient procedures, but these policies did not explain all the decline, and suggested that patient’s fear should be considered as another possible explanation.

Because delays in the care of chronic conditions may have short- and long-term consequences, ranging from late diagnosis to delays in starting treatment, it is important to assess the proportion of the population who failed to seek health care since the onset of the COVID-19 pandemic. We could not identify any population-based study from middle-income countries addressing this issue. We aimed to assess the proportion of the population in 133 Brazilian municipalities who had a health problem but failed to seek care or who failed to attend to a health service for a routine appointment examination, as part of the EPICOVID study, from March to August 2020 ⁷7. Hallal PC, Barros FC, Silveira MF, Barros AJD, Dellagostin OA, Pellanda LC, et al. EPICOVID19 protocol: repeated serological surveys on SARS-CoV-2 antibodies in Brazil. Ciênc Saúde Colet 2020; 25:3573-8..

Methods

The data used were from the fourth round of a repeated population-based serological survey conducted from August 24-27, 2020 in 133 Brazilian sentinel cities. The cities included Brasília, 26 state capitals and the largest municipalities in each of the country’s regions, as defined by the Brazilian Institute of Geography and Statistics (IBGE). Within each city, 25 urban census tracts were selected with probability proportionate to size, and 10 households were randomly sampled in each tract using households lists elaborated by the IBGE. In each household, all residents were enrolled using a smartphone app and one was randomly selected to be interviewed and tested for the presence of antibodies for SARS-CoV-2, using the WONDFO SARS-CoV-2 Antibody Test (Wondfo Biotech Co., https://en.wondfo.com.cn/). If the selected resident refused to provide a finger prick blood sample, a second household member was randomly selected. If this person also refused, the interviewers moved on to the next household. The next household to the right was also selected in case of absent residents. Further details on the study methodology have been previously published ⁷7. Hallal PC, Barros FC, Silveira MF, Barros AJD, Dellagostin OA, Pellanda LC, et al. EPICOVID19 protocol: repeated serological surveys on SARS-CoV-2 antibodies in Brazil. Ciênc Saúde Colet 2020; 25:3573-8..

The interview included a short questionnaire for collecting sociodemographic information (gender, age, schooling, race/skin color, household size, and household assets) and compliance with social distancing measures. The Brazilian race/skin color classification recognizes five groups based on the question: “How do you classify yourself regarding skin-color or race?”. The five response options are “white”, “mixed-race” (pardo), “black”, “yellow (Asian)”, and “indigenous”. Interviewers were instructed to check the “yellow” option when the subject mentioned being of Asian descent, and “indigenous” when any of the multiple indigenous nations were mentioned. The “mixed-race” category reflects mixed ancestry including European, African, and/or indigenous backgrounds. Socioeconomic position was assessed using a wealth index by analyzing household assets ⁸8. Barros AJD, Victora CG. Indicador econômico para o Brasil baseado no censo demográfico de 2000. Rev Saúde Pública 2005; 39:523-9.. The first component was divided into quintiles. The highest grade successfully completed was recorded as schooling level. The subjects were asked about the presence of the following chronic conditions: hypertension, diabetes, asthma, cancer, chronic kidney disease, heart disease, or other chronic condition.

Considering health services, the subjects were asked if, since the onset of the pandemic in March 2020, they had suffered from a health problem but did not seek care or failed to attend to a routine or screening examination. For positive answers, the reason for failing to seek care was also recorded.

The Stata 15 software (https://www.stata.com) was used for the analyses. Numbers were compared using the chi-square test. For ordinal variables, the p-value for linear trend and for heterogeneity were estimated and the one with the lower value was presented. Poisson regression with robust variance was used to estimate prevalence ratios, and all analyses controlled for the cluster-sampling design using svy prefix.

Interviewers wore individual protection equipment (aprons, gloves, surgical face masks, and shoe and hair covers) that were discarded as hospital waste after each interview. They were tested for COVID-19 prior to the field work and every two days thereafter. The study was approved by the Brazilian National Research Ethics Committee (process n. CAAE 30721520.7.1001.5313), with written informed consent form from all participants; for children and adolescents, consent was provided by parents or guardians.

Results

We interviewed 33,250 subjects in the fourth round of the seroprevalence survey. In this round, the response rate was 59.1%, and non-response was mostly due to whole families being away from home. Compared with the overall Brazilian population, men and young individuals were less likely to be interviewed. Concerning race/skin color, indigenous individuals were overrepresented in the studied sample, whereas the proportion of subjects who reported being white was lower than the national estimates (Table 1).

Table 2 shows that 11.8% (95% confidence interval - 95%CI: 11.4-12.1) of the individuals in the sample reported that since March 2020 they failed to seek care despite being ill, 17.3% (95%CI: 16.9-17.7) failed to attend to routine or screening examinations, and 23.9% (95%CI: 23.4-24.4) reported one or both outcomes. Concerning the main reason for not seeking care, 21.4% (95%CI: 20.4-22.5) reported that the service was closed, whereas 45.9% (95%CI: 44.6-47.1) reported being afraid of getting COVID-19 infection.

Women were more likely than men to not look for a health service, despite having a health problem or skipped a scheduled appointment. Regarding age, the risk of not seeking health care slightly increased for individuals aged 40-59 years and then declined, whereas for routine examination the risk of missing the visit increased steadily according to age. Wealth was inversely associated with the risk of not seeking care or failing to attend to a routine examination. The number of subjects who did not seek health services was higher in the North and Northeast regions. Finally, both outcomes were positively related to the number of previous chronic conditions (Table 3).

Concerning the reasons for not seeking care, closure of health services was less frequently reported among the wealthiest, while fear of getting COVID-19 infection was positively associated with wealth. Subjects who self-reported being white were more likely to mention being afraid of getting COVID-19 infection as a reason for failing to seek care. The number of chronic conditions was not associated with fear of getting COVID-19 infection as a reason for failing to seek care, whereas closure of health services was more frequently reported among those with one or more preexisting chronic condition (Table 4).

Discussion

In the fourth round of a large population-based serological survey of prevalence of antibodies against SARS-CoV-2, we observed that about one out of four subjects either failed to seek care due to a health problem or missed a routine examination. Among these subjects, about half did not attend to a health service for fear of getting COVID-19 infection, whereas the closure of health services was reported by two out of ten subjects. The likelihood of not seeking care was higher among women, the poorest, those living in the North or Northeast regions and those who reported having preexisting chronic conditions.

In the United States, Ziedan et al. ⁵5. Ziedan E, Simon KI, Wing C. Effects of state COVID-19 closure policy on non-COVID-19 health care utilization. Cambridge: National Bureau of Economic Research; 2020. (NBER Working Paper Series; 27621). reported that state closure policies and suspension of non-elective medical procedures were not the major explanation for the decline in seeking health care, and suggested that patients’ fear of COVID-19 infection should be considered as an alternative explanation. By asking about reasons for not seeking care, we could identify that fear of getting COVID-19 infection was the main factor for avoiding health care, but public policies related to the pandemic also affected the use of health services. Individuals who failed to attend to a health service may look for it in the future. Studies conducted in high-income countries have reported a later rescheduling, but it seems that the analysis is incomplete ²2. Wright A, Salazar A, Mirica M, Volk LA, Schiff GD. The invisible epidemic: neglected chronic disease management during COVID-19. J Gen Intern Med 2020; 35:2816-7.^,33. Papautsky EL, Hamlish T. Patient-reported treatment delays in breast cancer care during the COVID-19 pandemic. Breast Cancer Res Treat 2020; 184:249-54.^,44. Patt D, Gordan L, Diaz M, Okon T, Grady L, Harmison M, et al. Impact of COVID-19 on cancer care: how the pandemic is delaying cancer diagnosis and treatment for American seniors. JCO Clin Cancer Inform 2020; 4:1059-71.^,55. Ziedan E, Simon KI, Wing C. Effects of state COVID-19 closure policy on non-COVID-19 health care utilization. Cambridge: National Bureau of Economic Research; 2020. (NBER Working Paper Series; 27621).. A study conducted in Italy ⁹9. Lazzerini M, Barbi E, Apicella A, Marchetti F, Cardinale F, Trobia G. Delayed access or provision of care in Italy resulting from fear of COVID-19. Lancet Child Adolesc Health 2020; 4:e10-1., evaluating cases of delayed access to health care, identified that fear of COVID-19 infection was the main reason for not seeking care. The delay in seeking health care may have current or future negative consequences, as shown by a modelling study based on data from the National Health Service (United Kingdom) on the impact of COVID-19 on cancer diagnosis delay and cancer survival ¹⁰10. Maringe C, Spicer J, Morris M, Purushotham A, Nolte E, Sullivan R, et al. The impact of the COVID-19 pandemic on cancer deaths due to delays in diagnosis in England, UK: a national, population-based, modelling study. Lancet Oncol 2020; 21:1023-34.. Compared with pre-pandemic figures, the authors suggested that the mortality rate would increase from 7.9 to 9.6% for breast cancer, 15.3 to 16.6% for colorectal cancer, and 5.8 to 6% for esophageal cancer ¹⁰10. Maringe C, Spicer J, Morris M, Purushotham A, Nolte E, Sullivan R, et al. The impact of the COVID-19 pandemic on cancer deaths due to delays in diagnosis in England, UK: a national, population-based, modelling study. Lancet Oncol 2020; 21:1023-34..

We observed that the highest number of subjects who failed to seek health care were in the North and Northeast regions of Brazil. We expected this result because these regions showed the highest seroprevalence ¹¹11. Hallal PC, Hartwig FP, Horta BL, Silveira MF, Struchiner CJ, Vidaletti LP, et al. SARS-CoV-2 antibody prevalence in Brazil: results from two successive nationwide serological household surveys. Lancet Glob Health 2020; 8:e1390-8. and hospital case-fatality ¹²12. Baqui P, Bica I, Marra V, Ercole A, van der Schaar M. Ethnic and regional variations in hospital mortality from COVID-19 in Brazil: a cross-sectional observational study. Lancet Glob Health 2020; 8:e1018-26. at the time of the survey. Moreover, in Manaus, capital of the State of Amazonas, a large mortality rate due to respiratory diseases and other causes was observed in the first weeks of the pandemic ¹³13. Orellana JDY, Cunha GM, Marrero L, Horta BL, Leite IC. Explosion in mortality in the Amazonian epicenter of the COVID-19 epidemic. Cad Saúde Pública 2020; 36:e00120020., which could indicate a collapse of the health care system. Our result could also be due to lower access and use of health services that were presented before the pandemic. Stopa et al. ¹⁴14. Stopa SR, Malta DC, Monteiro CN, Szwarcwald CL, Goldbaum M, Cesar CLG. Use of and access to health services in Brazil, 2013 National Health Survey. Rev Saúde Pública 2017; 51 Suppl 1:3s., using data from the Brazilian National Health Survey, reported that people living in the South and Southeast regions had greater access to health services than residents in the other regions of Brazil. This difference can be explained by a greater offer of health services, both public and private, as well as the socioeconomic level of the population ¹⁵15. Viacava F, Bellido JG. Health, access to services and sources of payment, according to household surveys. Ciênc Saúde Colet 2016; 21:351-70.. Medina et al. ¹⁶16. Medina MG, Giovanella L, Bousquat A, Mendonça MHM, Aquino R; Comitê Gestor da Rede de Pesquisa em Atenção Primária à Saúde da Abrasco. Primary healthcare in times of COVID-19: what to do? Cad Saúde Pública 2020; 36:e00149720. suggest the need for a more territorialized, community-based, and home-based approach on primary health care to face any epidemic. This approach could accurately identify those people who are failing to seek health care during the pandemic and consequently failing to treat other diseases. Medina et al. also indicated the need to strengthen primary care to fight epidemics, guaranteeing services that have a more territorialized, community-based and home-based approach, aiming to achieve greater success in dealing with health crises and maintaining the continuity of care for other pre-existing conditions.

The COVID-19 pandemic is more critical for indigenous and the poorest ¹⁷17. Horta BL, Silveira MF, Barros JD, Barros FC, Hartwig FP, Dias MS, et al. Prevalence of antibodies against SARS-CoV-2 according to socioeconomic and ethnic status in a nationwide Brazilian survey. Rev Panam Salud Pública 2020; 44:e135.^,1818. Rodrigues EPS, Abreu IN, Lima CNC, Fonseca DLM, Pereira SFG, Dos Reis LC, et al. High prevalence of anti-SARS-CoV-2 IgG antibody in the Xikrin of Bacajá (Kayapó) indigenous population in the brazilian Amazon. Int J Equity Health 2021; 20:50., and our study suggests that these individuals are also more likely to not seek care for other health conditions during the pandemic. This association continued after controlling for regions of the country as a confounding factor, since poor and indigenous Brazilians are concentrated in the North and Northeast. Lately, socioeconomic and health inequalities have diminished in Brazil, but not all ethnic groups have benefited from such advances, and wide inequalities in health and nutrition among Brazilian indigenous populations have been reported ¹⁹19. Campos MB, Borges GM, Queiroz BL, Santos RV. Diferenciais de mortalidade entre indígenas e não indígenas no Brasil com base no Censo Demográfico de 2010. Cad Saúde Pública 2017; 33:e00015017.^,2020. Horta BL, Santos RV, Welch JR, Cardoso AM, Santos JV, Assis AMO, et al. Nutritional status of indigenous children: findings from the First National Survey of Indigenous People's Health and Nutrition in Brazil. Int J Equity Health 2013; 12:23.. The negative consequences of delaying care or diagnosis of some conditions may increase social and health inequalities in the near future.

Acknowledgments

To the Brazilian Association of Collective Health (Abrasco), the “Fazer o Bem Faz Bem” Program (JBS S.A.), and the Itaú Educational and Cultural Foundation.

References

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