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Breast imaging hindered during covid-19 pandemic, in Brazil

ABSTRACT OBJECTIVE: To report the decrease in breast imaging after covid-19 pandemic, obtaining the number of mammograms performed in 2019 and 2020. Additionally, to investigate if there was an increase in the proportion of women undergoing mammography for diagnostic purposes, with palpable lesions. METHOD: This is a cross-sectional study, based on the number of mammograms performed by the Brazilian public health services, provided by DATASUS, an open access database. Mammograms from private institutions were not included. This study compares the number of mammograms performed in 2019 and 2020, in women aged 50–69 years, stratified by month, in each federal state, and the presence of palpable lumps (physician-reported). RESULTS: In total, 1,948,471 mammograms were performed in 2019 and 1,126,688 in 2020, for the population studied. These values represent a 42% decline. Monthly, a significant decreased is observed after April 2020. The results varied slightly according to federal state; yet the entire country was affected. Rondônia was the most affected state, with 67% decline. The proportion of women presenting palpable lumps increased from 7.06% on average in 2019 to 7.94% in 2020 (OR = 1.135, 95%CI 1.125–1.145, p = 0,001). DISCUSSION: The number of mammograms performed in 2020 declined considerably. Out of the women who presented for mammogram, the proportion of palpable lumps was significantly higher in 2020. Considering the detection rate of digital mammography, the loss of 800,000 exams means 4,000 undiagnosed breast cancer cases, by the end of 2020.


INTRODUCTION
In December 2019, Wuhan health authorities exposed that they were treating dozens of people with pneumonia, who tested negative for most viruses known to infect humans at the time, such as influenza, H1N1, and adenovirus. Typical symptoms included fever, cough, dyspnea, and headache; it often progressed to respiratory failure. The pneumonia outbreak was attributed to a virus: it was accompanied by leucopenia, diffuse pulmonary infiltrates, and no improvement with antibiotics. 1 Later, Wuhan researchers were able to isolate and sequence the genome of the virus, obtained from seven samples of critically ill patients, and they resulted 96% identical to a bat Coronavirus 1 .
The first cases and deaths outside China were reported in January. The World Health Organization (WHO) soon declared it a "Public Health Emergency of International Concern (PHEIC)" 2 , and named the disease as covid-19, an acronym for "Coronavirus disease 2019" 3 . As of January 2021, there have been approximately 95 million cases and 2 million deaths worldwide; Brazil is the third most affected country, with 8.5 million cases and 200 thousand deaths 4 .
Many authorities, governors and rulers followed Wuhan restrictive measures (known as total or partial "lockdown"), to contain the spread of the virus. On March 21 st , the Governor of São Paulo state João Doria decreed quarantine for all the 645 cities within the state 5 . He was then followed by other Governors. On March 17 th , the Brazilian National Health Agency (Agência Nacional de Saúde -ANS) recommended that "visits, exams or surgeries that do not apply as urgent" should be postponed 6 .
Breast cancer is the leading cause of death by cancer among women in Brazil, and the fifth among all causes (preceded by heart attack, pneumonia, diabetes, and chronic obstructive pulmonary disease) 7 . There are nearly 66,000 new breast cancer cases each year 8 . Globally, Brazil is still struggling to increase its survival rates. Even comparing to its neighbor Argentina, Brazil has much to improve. Global data reveals that, from 2010 to 2014, Brazil had breast cancer survival rates of 75.2%, compared to 84.4% in Argentina. Most European countries, as well as Japan, Australia, New Zealand, Canada, and the United States had five-year survival rates greater than 85% 9 .
In Brazil, the standard screening program for public health system is for women aged from 50 to 69 years, every two years 10 . Nevertheless, most private institutions prefer the recommendation from Brazilian Radiology College, to perform mammogram annually, after 40 years old, until good health 11 . It is estimated that screening coverage in Brazil, combining public and private care, is only 60% of the aimed population, approximately 12 .
This study reports the decrease in breast imaging after covid-19 pandemic, obtaining the number of mammograms performed in 2019 and 2020. Furthermore, it investigates if there was an increase in the proportion of women undergoing mammography for diagnostic purposes, with palpable lesions.

METHODS
This is a cross-sectional study, based on the number of mammograms performed by the Brazilian public health care, as provided by DATASUS, an open access database. Mammograms from private institutions were not included. Brazil has many private health services, whose data are not available at DATASUS.
When requesting for mammograms, after clinical history is obtained and physical exam completed, the physician or health care provider is supposed to answer the following questions on the cover of the request: 1. Does the patient have a lump in the breast?
In this study the number of mammograms will be the focus, especially those with answers "YES" for the first question -"Does the patient have a lump in the breast?", as reported by the physician or health care provider.
This study compares the number of mammograms performed in 2019 and 2020, at the Brazilian Unified Health System (SUS), in women aged from 50 to 69 years old -the main population from breast cancer screening in Brazil. The coverage of exams provided by SUS will be calculated, dividing that number from the population of women aged 50-69 years old. Then, the numbers will be stratified by month, in each federal state, and by the presence of palpable lumps. These will be named "YES" patients.
Tables and Graphs were built with Microsoft Office Excel ® . Odds Ratio values were obtained with the aid of Graph Pad Prism version 9 for MacOS; and they were considered significant if p < 0.05.

RESULTS
In total, 1,939,415 mammograms were performed in 2019 and 1,126,688 in 2020, for the studied population (Table 1). These values represent a 42% decline. SUS provided mammograms for 9.4% of women in 2019, and 5.3% in 2020. Table 2 shows the number of mammograms performed each month. It is observed that 2020 started well, with increased rates of mammography performed in January. Then, it declined slightly in February and March; and sharply from April forward, after restrictive measures were announced.    of mammograms (with or without palpable lumps), and the fraction of "YES" patients.
Although the total number of mammograms decreased, it is observed an increase in the proportion of patients with palpable lumps. In total, 7.06% of patients had palpable lumps in 2019, and 7.94% in 2020 (OR = 1.135, 95%CI 1.125-1.145, p = 0,001). Graph 1 shows the same data imaged.
Lastly, mammograms performed in each federal state were obtained. Results are presented in Table 3. The total numbers are slightly different from Table 2, because not every mammograms presented information about location.

DISCUSSION
The covid-19 pandemic has hindered breast cancer diagnosis in Brazil. The number of mammograms performed in 2020 declined considerably. Out of those women who did perform a mammogram examination, the proportion of palpable lumps was significantly higher in 2020. Based on this information, two assumptions can be done: that women postponed breast cancer screening; and that, even symptomatic, some may have chosen not to undergo mammogram or did not have access to it. Rondônia was the most affected state, with a 67% decrease in the number of mammograms performed. São Paulo, the most populated state, had overall 38% decline. Piauí stands as the least affected, with no decline at all. It is reasonable to exclude Amapá from any analysis: although it counted 37% more exams, it still has the lowest absolute number -probably due to documentation inaccuracies. The purpose of showing data from different states was not to determine whether one specific state had a statistically significant different outcome, but to show that the pandemic has affected the entire country. Southeast states (São Paulo, Rio de Janeiro, Minas Gerais, and Espírito Santo) have the best rates of screening coverage (67.9% compared to national 60%) 12 , but nevertheless they were as much, or even more, affected as other poorer states.
This study has pitfalls. A major concern is that it does not include data from private health care. If nationwide screening coverage is about 60%, and the population of women aged from 50 to 69 years old is close to 20 million, it is possible that more than 10 million mammograms performed are missing. Also, these data are dependent on the physician's ability to fill the request appropriately. On the positive side, the results fulfill the purpose to document how the pandemic affected breast cancer diagnosis, although partially.
It is controversial whether screening programs increase survival in low-income countries.
It is known that survival depends on tumor stage at diagnosis, with five-year rates of 99% for localized, 86% for regional, and 27% for distant disease 13 . Regular screening programs lower the rates of advanced disease at diagnostics 14 . A Cochrane meta-analysis showed significant increase in breast cancer survival with mammographic screening (RR 0.81, CI 0.74 to 0.87) 15 . However, studies were from Canada, the United States, United Kingdom, Sweden, and Scotland. In Brazil, unfortunately, the screening program has little effect at decreasing advanced disease and increasing survival. There are many other barriers to appropriate treatment. For example, the mean time between breast cancer presentation and biopsy on SUS is between 75-185 days 16 . Most operable cases are diagnosed in later stages (53.5% stage 2 and 23.2% stage 3) 17 . Some authors advocate that the best strategy for Brazil is prompt care for symptomatic patients 18 . However, a recent study found that, when diagnosed at early stages, survival rates in Brazil are greater than 90% 19 . This means that, despite all difficulties, Brazil's health authorities must not give up pursuing early detection for breast cancer.
Note that Graph 1 shows the effect of the "Outubro Rosa" campaign, to promote breast cancer awareness and screening. October is, indeed, the month with most mammograms performed throughout the year, and it had a positive effect in 2020 to relieve the pandemic scenario.
Considering that the average detection rate of breast cancers for digital mammography is 5/1,000 20 , the loss of 800,000 exams during the year of 2020 means 4,000 undetected breast cancers -and this value only addresses SUS patients. This represents a potential burden of advanced disease for the next years.
Worsening breast cancer rates of detection and survival will be a painful and costly side effect of the pandemic. ANS should exclude breast cancer screening and diagnosis from the postponement recommendation. It should be made clearer to the population that services related to the diagnosis and treatment of breast cancer are not considered as "consultations, exams or surgeries that do not apply as urgent." For the future, we may learn that breast cancer screening should never again be postponed, but adapted to any new crisis, pandemics, or situations.