INTRODUCTION

Colorectal cancer (CRC) corresponds to the third most common malignancy worldwide, with approximately two million new cases per year, and the second leading cause of cancer-related death in the world, with lung cancer being the first^1,2. In Brazil, according to the National Cancer Institute (INCA), it is expected that, for each year of the three-year period 2020-2022, 20,520 and 20,470 diagnoses of CRC will be registered in males and females, respectively. These values represent an estimated risk of 19.64 new cases per 100,000 men and 19.03 per 100,000 women³.

The incidence of CRC is known to be higher in people of African descent and increases with age and is typically diagnosed from the fifth decade of life onwards^4,5. In addition, in all age groups, men have a 1.5 times greater risk of having the disease than women⁵.

CRC corresponds to approximately 10.0% of all cancer diagnoses and deaths. In its early stages, it is asymptomatic or oligosymptomatic, with nonspecific symptoms, such as changes in bowel habits, weight loss, abdominal pain and digestive hemorrhage^6,2. Owing to these facts, the Ministry of Health (MH) recommends screening for the disease in people between 50 and 75 years of age without risk factors, through fecal occult blood testing (FOBT), which, if positive, should be complemented with colonoscopy (COL) or sigmoidoscopy⁷.

Colorectal polyps can be histologically classified according to their neoplastic potential: when hyperplastic, hamartomatous or inflammatory (pseudopolyps), they do not have a tendency to become malignant. The opposite is observed for adenomatous and serrated polyps⁸. Adenomas, in turn, can be subdivided according to the participation of the tubular and villous components in their constitution, as well as their degree of dysplasia, which can be low or high, the latter having a greater chance of evolving into CRC^9,10. Nearly all cases of CRC originate from adenomatous polyps¹¹. COL is considered the gold standard exam for detection and excision (polypectomy) of these lesions¹¹.

The first case of the disease caused by the SARS-CoV-2 Coronavirus (COVID-19) was first reported in November 2019 and classified as a pandemic in March 2020^12,13. COVID-19 has high transmissibility, in which airborne spread through droplets and aerosols, and contact with contaminated people and fomites are the most relevant routes of contagion^14,15. Thus, endoscopic examinations of the digestive system, which require a short physical distance between the patient and the professionals who perform them and promote exposure to potentially infectious biological samples, are considered high-risk procedures for viral contamination^16,17. Furthermore, the presence of SARS-CoV-2 has already been demonstrated in tissues such as the esophagus, stomach, duodenum and rectum of infected people¹⁸.

Faced with the fear of the imminent collapse of health systems, as a result of the high population demand for hospital equipment and human resources, the state of Goiás issued State Decree No. 9638, which declared a public health emergency and established the quarantine regime¹⁹. Following that, State Decree No. 9638 suspended all elective outpatient exams and procedures, with a few exceptions²⁰.

Added to this scenario was the fear of exposure to the coronavirus in health units, causing the population to undergo increasingly fewer routine screening investigations^21,22. Due to this, it is estimated that about 15,000 new cases of cancer were not detected each month in Brazil during the year 2020, representing a drop of 35.5% compared to 2019²³. With regard to CRC, it is estimated that around 263.8 thousand COL and 732 thousand FOBT failed to be performed²⁴.

Survival of patients with CRC is closely related to the early screening of the disease: after 5 years from the diagnosis, more than 90.0% of patients with stage I tumors are alive, while this rate is only 10.0% for stage IV adenocarcinomas²⁵.

Thus, in view of the high incidence of CRC, as well as its nonspecific symptoms and the possibility of being diagnosed early through COL to reduce morbidity and mortality, the current study aimed to assess the impact of the restriction measures brought into force in the context of the COVID-19 pandemic in the diagnosis of adenomatous polyps and CRC.

METHODS

This is a cross-sectional study that evaluated the colonoscopic findings of patients at a private clinic in the city of Goiânia, Goiás. The analysis began by adopting March 20, 2020, the date of the suspension of COL in the state of Goiás (March 20, 2020) (Goiás, 2020b), as a reference point. The exams were conducted between 20 March and 31 October, 2019, and between 20 March and 31 October, 2020. Data were collected from medical records including patient identification (name, gender, and age), colonoscopic findings, biopsy and/or polypectomy procedures, and corresponding histopathological findings.

All patients aged 18 years or older who underwent COL during the specified period were included. Examinations (COL an/or histopathology) lacking sufficient technical quality for diagnostic conclusions and patients with medical records that did not allow necessary data collection were excluded.

Variables were stratified and compared based on the year of COL performance (2019 vs 2020). Statistical calculations were performed using IBM® SPSS® software (Statistical Package for the Social Sciences), with a significance level of 5.0% (P<0.05). The study was approved by the Research Ethics Committee of the Pontifical Catholic University of Goiás.

RESULTS

719 (6.6%) out of the 10,951 exams performed during the study period were excluded. Our sample consisted of 10,232 (93.4%) individuals, divided into two groups, according to the year of COL performance. Group 1 consisted of 6,777 (66.2%) procedures performed in 2019 and group 2 consisted of 3,455 (33.8%) in 2020. Therefore, there was a 51.0% reduction in the total COL performed during the pandemic period. When the analysis is stratified by month, it is observed that there was a global decrease (P<0.001), with emphasis on the months of March and April, in which the percentages of reduction were 96.0% and 83.0%, respectively (Table 1).

As for patient gender, the majority were females (63.4%), corresponding to 64.7% of the sample in 2019 and 60.8% in 2020. Regarding the age group, it was noticed that 61.6% were aged 50 or over, and in 2019 this proportion was 63.8%, with a mean age of 53.5±14.0 years. In 2020, 57.2% of patients were within this range, with an average of 51.3±13.8 years (P<0.0001). Comparing the two analyzed periods, it can be seen that people who underwent COL in the pandemic year were significantly younger than those in the previous year (Table 2). It is also possible to observe that the greatest percentage drop in exams performed in 2020, compared to 2019, occurred in the age group aged 50 years or older, representing a deficit of 54.3% (Figure 1).

31.9% out of the 10,232 COL studied had at least one finding corresponding to a polyp (which can be either adenomatous or hyperplastic/inflammatory). When comparing the year 2019 (31.7%) with 2020 (32.3%), there was no statistically significant percentage difference (P=0.5646). The majority of the 3,267 polyps visualized were adenomatous (72.0%), this proportion was 78.3% and 68.8% in 2019 and 2020, respectively. This shows that, even with the absolute decrease in the number of exams performed during the lockdown period, adenomas represented a higher percentage of the total number of polyps found in 2020 than in 2019 (P<0.0001).

95.0% of the analyzed AP presented low-grade dysplasia and 5.0% high-grade dysplasia during the two years of the study. In 2019, the percentages of non-advanced and AP polyps were, respectively, 95.1% and 4.9%. Meanwhile, in 2020, these same proportions were 94.2% and 5.8%. However, the difference between the degrees of dysplasia was not statistically significant (P=0.34) (Table 3).

Furthermore, histological findings were obtained that confirmed the presence of tumor (CRC) in 1.2% (121) of the COL during the two analyzed periods. Of these tumors, 57 were found in 2020, representing 1.6% of the total number of exams in the same year. In 2019, 64 tumors were identified, which is equivalent to 0.9% of the COL performed in that year. From these data, it was noticed that the detection rate of adenocarcinomas by COL, during the pandemic, suffered a statistically significant increase (P=0.0018) (Table 3). Regarding gender, it is noticeable that most of the patients, in whom CRC was observed, are male (57.8% in 2019 and 59.6% in 2020); however, no statistical significance between 2019 and 2020 was found.

When evaluating the number of COL in which lesions (AP and/or tumor) were found, it can be seen that, during the lockdown period, there was a higher percentage of detection than when compared to the previous year (26.3% vs 21.1%) (P<0.001).

As for the referrals for performing COL, it was observed that the main five were: cancer prevention [4,663 (45.6%)], abdominal pain [1,297 (12.7%)], history of colonic polyps [943 (9.2%)], presence of gastrointestinal bleeding (melena, intestinal bleeding or hematochezia) [787 (7.7%)] and chronic diarrhea [466 (4.6%)]. When the referrals were evaluated according to the year of performance, it was noticed that cancer prevention [3,264 (48.2%) vs 1,399 (40.5%), P=0.000000001)] and hemorrhoidal disease [86 (1.3%) vs 17 (0.5%), P=0.0002)] were significantly more common in 2019. In 2020, the main referrals were abdominal pain [804 (11.9%) vs 493 (14, 3%), P=0.00005)], gastrointestinal bleeding [420 (6.2%) vs 367 (10.6%), P=0.000000001)] and change in bowel habits [244 (3.6%) vs 189 (5.5%), P=0.000008)] (Table 4).

DISCUSSION

This work aimed to evaluate the impact of the restrictive measures brought in force during the COVID-19 pandemic on the diagnosis of adenomas and CRC in a private clinic in the city of Goiânia. In 2020, there was a significant percentage reduction in the number of COL performed and in the average age of patients undergoing the exam. There was also a relevant increase in the detection of cancer and lesions (AP and CRC) per procedure performed in the year of the pandemic.

There was an evident 51.0% (P<0.001) reduction in the total COL performed in 2020, compared to 2019, with more significant monthly deficits in March and April. These findings corroborate other studies, which recorded significant declines in the number of procedures performed between March and May of the pandemic year^26,27.

Most patients were 50 years old or older (63.8% in 2019 vs 57.2% in 2020), which is in line with the MH guidelines for starting CRC screening⁷. In addition, a reduction was noticed in the average age in 2020 when compared to the previous year (53.5±14.0 years in 2019 vs 51.3±13.8 years in 2020, with P<0.0001), as well as a greater percentage decrease in the number of exams in those aged at least 50 years (-54.3%). This can be explained by the fact that the elderly correspond to a risk group for COVID-19²⁸. Thus, the fear of being infected probably impacted the decision of whether or not to perform the test during the quarantine period. In light of this, it is paramount to underscore that the incidence of colorectal cancer escalates with advancing age⁷. Consequently, the decrease in the average age and the reduction in the number of individuals aged over 50 undergoing the examination lead to a significant diminishment in the diagnosis of colorectal cancer and its precursors.

Women accounted for the majority of the sample in both years analyzed (64.7% in 2019 vs 60.8% in 2020). It is observed that, even with a higher risk of developing CRC, the proportion of males undergoing COL is lower than that of females, which can be explained by the routine gynecological examinations, which include performing FOBT for CRC screening in all patients over 50 years of age²⁹. In turn, despite representing the minority of the studied population (35.3% in 2019 vs 39.2% in 2020), men were proportionally subjected to more tests during the pandemic than in 2019 (P=0.0001). Furthermore, it is interesting to note that, among the patients who received CRC diagnoses, 58.7% were male, a finding compatible with the INCA data and other studies^3,5.

With regard to the detection of polyploid lesions, there was no statistical significance in the comparison between the years 2019 and 2020, which shows that, proportionally, a similar number of findings corresponding to polyps was found in the two periods investigated. These same results were described in the studies by Hinterberger et al. (2021)³⁰ and Holland et al. (2022)²⁶. However, after analyzing the biopsies, there was an increase in the proportion of adenomas found in 2020 (78.3%) when compared to 2019 (68.8%) (P<0.0001). On the other hand, other studies did not find a statistically significant difference in the detection of adenomatous polyps^26,31. Regarding the degree of dysplasia, during the pandemic, the percentages of adenomas with low-grade and high-grade dysplasia were respectively 94.2% and 5.8%, and, in the previous year, 95.1% and 4.9% (P=0.3435). Despite this, there was an absolute decrease of 584 non-advanced adenomas and 22 advanced adenomas in 2020.

Our work showed an increase in the cancer detection rate per procedure (0.9% in 2019 vs 1.6% in 2020, with P=0.0018), as well as a higher percentage of lesion screening (CRC and adenomatous polyps) (21.1% in 2019 vs 26.3% in 2020, with P<0.0001). These data are consistent with other studies^26,27,31. However, as fewer COL and, therefore, polypectomies were performed in 2020, lower absolute numbers of tumors and adenomas were found. Therefore, significant diagnostic losses are believed to have occurred, which has already been reported in the literature^26,27,30.

It is estimated that 4.0% of all non-advanced adenomatous polyps can become advanced adenomas and 3.1% of these can progress to CRC⁹. Considering the year 2019, during which 73 advanced adenomatous polyps and 1,407 non-advanced adenomatous polyps were recorded, if these polyps had not been removed, four of them could have progressed to CRC. The same calculation, when applied in 2020, is equivalent to three cases. This demonstrates that, even with a higher proportion of adenoma diagnoses in 2020, there was an absolute decrease in the amount of prevented CRC.

When the reasons for performing COL were evaluated, it was observed that the main reason was cancer prevention [4,663 (45.6%)] in both years. However, according to the year of the procedure, it was noticed that this indication was statistically more significant in 2019 [3,264 (48.2%) vs 1,399 (40.5%), P=0.000000001)]. In 2020, abdominal pain [804 (11.9%) vs 493 (14.3%), P=0.00005)], gastrointestinal bleeding [420 (6.2%) vs 367 (10.6%), P=0.000000001)] and changes in bowel habits [244 (3.6%) vs 189 (5.5%), P=0.000008)] stood out as the main referrals. This shows that people undergoing COL in the pandemic year were mostly symptomatic, while routine CRC screening was likely hampered by fear of contamination by SARS-CoV-2.

Non-invasive screening methods, such as FOBT and fecal immunohistochemical tests (FIT) with higher positivity limits, have been proposed by many authors as a solution to meet the need to retake patients at risk, as well as prioritization by sex, age and history screening^26,32,33. Thus, colonoscopic surveillance would be reserved for cohorts with the greatest expected benefit³³.

As a direct consequence of the decrease in CRC diagnoses during the pandemic, several studies have pointed to delays in starting treatment and an increase in the number of advanced cases and disease-related mortality^25,34,35. However, more studies are still needed on this topic in the Brazilian population. In the same respect, Morris et al. (2021)²⁵, highlights the importance of creating a rapid system of data records to effectively inform the real situation of health services during critical periods, such as the pandemic.

Despite the work presenting some limitations, such as the fact that the sample only included elective COL performed in a single private clinic in the city of Goiânia, it is noteworthy that the findings are compatible with those found in other studies.

CONCLUSION

There was a significant decrease in the number of COL performed in 2020 compared to 2019, which can be attributed to fear of COVID-19 infection and restrictions. Despite the reduction in overall procedures, there was a notable increase in the detection rate of cancer and adenomatous polyps per procedure in 2020, suggesting a higher proportion of symptomatic patients seeking medical attention. In spite of the increased detection rate per procedure, the absolute number of tumors and adenomas found decreased in 2020, potentially resulting in diagnostic losses and fewer cases of prevented CRC.

In summary, the findings suggest that the COVID-19 pandemic had a significant impact on CRC screening and diagnosis patterns, highlighting the need for adapted strategies to ensure continued access to essential preventive healthcare services during similar crises in the future.

REFERENCES

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