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Education and Information to Improve Adherence to Screening for Breast, Colorectal, and Cervical Cancer—Lessons Learned during the COVID-19 Pandemic

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Simple Summary Screening for breast, colorectal, and cervical cancer is correlated with diagnosis at an earlier stage, less extensive surgery, and reduced mortality and fewer complications. Adherence rates to cancer screening are lower for individuals with low socio-economic conditions and educational attainment. These social disparities are only partially reduced by free screening through national initiatives. Education and information and appropriate expenditure for preventive care have the potentials to increase adherence to screening for colorectal, breast, and cervical cancer with the possibility of reduced cancer mortality. The findings of our study highlight the importance of the implementation of nationally organized screening programs for several other types of cancers that are often detected after the occurrence of symptoms. Nationally organized screening programs for several types of cancers, like esophageal, gastric, and pancreatic cancer, in regions with a high prevalence may increase the possibility of diagnosis at earlier stages and improved early and late results. Abstract The objective of this study was to determine the correlation between adherence to cancer screening programs and earlier diagnosis of the 14 most common types of cancers in the adult population, before and during the COVID-19 pandemic. National data concerning number of admissions and operations in Italy for adult patients admitted with oncologic problems during the COVID-19 pandemic (2020 to 2022) and in the pre-pandemic period (2015 to 2019) were analyzed. We selected 14 types of cancer that present the most common indications for surgery in Italy. This study included 1,365,000 adult patients who had surgery for the 14 most common types of cancer in the period 2015–2022, and interviews concerning adherence rates to screening for breast, colorectal, and cervical cancer were conducted for 133,455 individuals. A higher decrease in the number of operations for the 14 types of cancer (−45%) was registered during the first three acute phases of the pandemic, and it was more evident for screenable cancers like breast, colorectal, and cervical cancer (p < 0.001). During the first year of the COVID-19 pandemic, the number of screened individuals for breast, colorectal, and cervical cancer decreased by 33.8% (from 7,507,893 to 4,969,000) and the number of diagnoses and operations for these three types of cancer decreased by 10.5% (from 107,656 to 96,405). The increase and return to normality of the number of screened individuals in the last year of the pandemic (2022) and in the first post-pandemic year (2023) was associated with a return to the pre-pandemic levels of diagnoses and operations. The adherence rates were lower for individuals living in rural areas, with low socio-economic status, and unmarried persons; however, the most statistically significant factor for reduced adherence was a lower level of educational attainment. Free screening through nationally organized programs reduced social disparities. There were no significant differences between the pre-pandemic and pandemic periods for several types of cancers (stomach, esophagus, pancreas, liver) that are diagnosed for the occurrence of symptoms and for which nationally organized programs might increase the possibility of earlier diagnosis and improved clinical outcomes. Education, information, and appropriate expenditure for preventive care have the potential to reduce cancer mortality. Nationally organized screening programs for several types of cancers, which are often detected for the occurrence of symptoms, may increase the possibility of diagnosis at earlier stages.
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Citation: Gabriele, R.; Campagnol, M.;
Sapienza, P.; Borrelli, V.; Di Marzo, L.;
Sterpetti, A.V. Education and
Information to Improve Adherence to
Screening for Breast, Colorectal, and
Cervical Cancer—Lessons Learned
during the COVID-19 Pandemic.
Cancers 2024,16, 3042. https://
doi.org/10.3390/cancers16173042
Academic Editor: David Wong
Received: 30 July 2024
Revised: 27 August 2024
Accepted: 28 August 2024
Published: 31 August 2024
Copyright: © 2024 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and
conditions of the Creative Commons
Attribution (CC BY) license (https://
creativecommons.org/licenses/by/
4.0/).
cancers
Article
Education and Information to Improve Adherence to Screening
for Breast, Colorectal, and Cervical Cancer—Lessons Learned
during the COVID-19 Pandemic
Raimondo Gabriele , Monica Campagnol, Paolo Sapienza , Valeria Borrelli , Luca Di Marzo
and Antonio V. Sterpetti *
Department of Surgery, Policlinico Umberto I, Sapienza University, Viale del Policlinico, 00167 Rome, Italy;
raimondo.gabriele@uniroma1.it (R.G.); paolo.sapienza@uniroma1.it (P.S.); v.borrelli@policlinicoumberto1.it (V.B.);
luca.dimarzo@uniroma1.it (L.D.M.)
*Correspondence: antonio.sterpetti@uniroma1.it; Tel.: +39-649972188; Fax: 39-64997245
Simple Summary: Screening for breast, colorectal, and cervical cancer is correlated with diagnosis
at an earlier stage, less extensive surgery, and reduced mortality and fewer complications. Adher-
ence rates to cancer screening are lower for individuals with low socio-economic conditions and
educational attainment. These social disparities are only partially reduced by free screening through
national initiatives. Education and information and appropriate expenditure for preventive care have
the potentials to increase adherence to screening for colorectal, breast, and cervical cancer with the
possibility of reduced cancer mortality. The findings of our study highlight the importance of the
implementation of nationally organized screening programs for several other types of cancers that are
often detected after the occurrence of symptoms. Nationally organized screening programs for several
types of cancers, like esophageal, gastric, and pancreatic cancer, in regions with a high prevalence
may increase the possibility of diagnosis at earlier stages and improved early and late results.
Abstract: The objective of this study was to determine the correlation between adherence to cancer
screening programs and earlier diagnosis of the 14 most common types of cancers in the adult
population, before and during the COVID-19 pandemic. National data concerning number of
admissions and operations in Italy for adult patients admitted with oncologic problems during the
COVID-19 pandemic (2020 to 2022) and in the pre-pandemic period (2015 to 2019) were analyzed. We
selected 14 types of cancer that present the most common indications for surgery in Italy. This study
included 1,365,000 adult patients who had surgery for the 14 most common types of cancer in the
period 2015–2022, and interviews concerning adherence rates to screening for breast, colorectal, and
cervical cancer were conducted for 133,455 individuals. A higher decrease in the number of operations
for the 14 types of cancer (
45%) was registered during the first three acute phases of the pandemic,
and it was more evident for screenable cancers like breast, colorectal, and cervical cancer (p< 0.001).
During the first year of the COVID-19 pandemic, the number of screened individuals for breast,
colorectal, and cervical cancer decreased by 33.8% (
from 7,507,893 to 4,969,000
) and the number of
diagnoses and operations for these three types of cancer decreased by 10.5% (
from 107,656 to 96,405
).
The increase and return to normality of the number of screened individuals in the last year of the
pandemic (2022) and in the first post-pandemic year (2023) was associated with a return to the
pre-pandemic levels of diagnoses and operations. The adherence rates were lower for individuals
living in rural areas, with low socio-economic status, and unmarried persons; however, the most
statistically significant factor for reduced adherence was a lower level of educational attainment.
Free screening through nationally organized programs reduced social disparities. There were no
significant differences between the pre-pandemic and pandemic periods for several types of cancers
(stomach, esophagus, pancreas, liver) that are diagnosed for the occurrence of symptoms and for
which nationally organized programs might increase the possibility of earlier diagnosis and improved
clinical outcomes. Education, information, and appropriate expenditure for preventive care have the
potential to reduce cancer mortality. Nationally organized screening programs for several types of
Cancers 2024,16, 3042. https://doi.org/10.3390/cancers16173042 https://www.mdpi.com/journal/cancers
Cancers 2024,16, 3042 2 of 13
cancers, which are often detected for the occurrence of symptoms, may increase the possibility of
diagnosis at earlier stages.
Keywords: trends mortality rates; cancer; COVID-19 pandemic; screening
1. Introduction
The COVID-19 pandemic has brought reduced hospital/clinic visits and surgical
procedures. During the first year of the pandemic, the number of diagnoses of cancers
decreased by 10.5%; in the lockdown periods, the decrease reached 50% [
1
5
]. Screening of
the general population has been correlated with decreased mortality for breast, colorectal,
and cervical cancers. Organized screening has been associated with reduced mortality in
Europe. Cardoso et al. [
6
] and Ola et al. [
7
] found that organized screening programs for
colorectal cancer with fecal tests, especially when all eligible groups were covered, achieved
the highest utilization of the screening tests, with favorable survival rates for patients
with screen-detected colorectal cancer. These favorable results were also seen within each
stage—the five-year overall survival rates for patients with screen-detected stage I, II, III,
and IV cancers were 92.4% (95% CI 91.6–93.1), 87.9% (86.6–89.1), 80.7% (79.3–82.0), and
32.3 (29.4–35.2), respectively. The possibility that screening by sigmoidoscopy may reduce
colorectal cancer prevalence and mortality has been supported by Brenner et al. [
8
,
9
]. The
association between routine screening and reduced mortality for breast and cervical cancer
has become standard evidence [
10
,
11
]. It may appear unethical, but several lessons can be
derived from the COVID-19 pandemic, including the importance of screenings for breast,
colorectal, and cervical cancer and the negative consequences of their decrease.
The aim of our study was to analyze the number of admissions to hospital, the number
and type of surgical procedures, and the results for patients with oncologic problems,
during the pandemic years (2020 to 2022) in Italy. We analyzed the number of surgical
procedures performed for 14 common types of cancer in Italy. These data were compared to
those of the pre-pandemic period (2015–2019). This study aimed to confirm the importance
of cancer screening and to identify subgroups of patients with lower adherence rates
to screenings.
2. Methods
2.1. Study Design
1.
We analyzed the data concerning the number of admissions and operations in Italy
for patients admitted with oncologic problems during the COVID-19 pandemic (2020
to 2022) and in the pre-pandemic period (2015 to 2019). We selected 14 types of cancer
that present the most common indications for surgery in Italy.
2.
We analyzed the mortality rates in Italy during the pre-pandemic period (2015–2019)
and in the pandemic period (2020–2022) related or not to COVID-19 infection.
3.
A comparison was made between the characteristics (number/adherence) of preven-
tive screening for breast, colorectal, and cervical cancer during the pre-pandemic and
the pandemic periods.
The data about point 1 were extracted from the PNE (Programma Nazionale Esiti)
reports of the AGENAS (Agenzia Nazionale per i Servizi Sanitari Regionali) [
12
]. AGENAS
is a non-profit agency, part of the National Health Minister, supported by funds from the
Italian Government, which includes data from 1377 public and private hospitals, including
97% of hospital admissions in Italy.
The data about point 2 were extracted from the reports of the ISTAT (Italian Institute
for Statistics), ISS (Istituto Superiore Sanità), and EUROSTAT [1315].
ISTAT, ISS, and EUROSTAT are non-profit governmental public institutions. The
reports describe the mortality rates in Italy and in the European Union during the pre-
pandemic and pandemic periods.
Cancers 2024,16, 3042 3 of 13
The data about point 3 were based on the report of Italian National Institutions
concerning cancer and screening [1517].
All the patients gave written approved consent.
2.2. Data Analysis
The primary outcomes were changes in the number and type of operations performed.
The secondary outcomes were the 30-day mortality and morbidity rates after surgery.
IRB approval was not required for this study. All the patients gave written ap-
proved consent.
2.3. Statistical Analysis
The categorical variables are expressed as frequencies and percentages. The continuous
variables with normal distribution are expressed as mean and standard deviation. The
Student’s ttest and the chi square test were used where appropriate.
3. Results
3.1. Excess Mortality during the Pandemic Period (2020–2022)
During the three years of the pandemic, an excess mortality of 251,911 was registered.
In Italy, 73% of the excess deaths were related with the COVID-19 infection and 27%
occurred in patients who were COVID-19 negative. A similar trend was reported for all
countries in the European Union. The data about the more common reported causes for
excess of mortality for patients who were COVID-19 negative are available only for the
year 2020. In Italy, during the year 2020, the age-standardized mortality rate (
×
100,000) for
cardiovascular deaths was 281.1; for cancers, it was 227.0, and it was 100.7 for COVID-19.
In the year 2023, there was no excess mortality in Italy or in the European Union.
3.2. Reduced Number of Hospital Admissions and Surgeries for the 14 Analyzed Types of Cancer
Table 1shows the number of operations performed for the 14 analyzed types of cancer
in Italy. In the year 2020, 160,617 operations for the 14 analyzed types of cancer were
performed in Italy with a decrease of 10% (
18,000 operations) in comparison with the
expected number considering the trends from the previous five years. In the year 2021, a
decrease of 4% was registered (
6000 operations), whereas, in the last year of the pandemic
(2022), the number of operations was almost similar to that in the pre-pandemic period.
A higher decrease in the number of operations for the 14 types of cancer (
45%) was
registered during the first three acute phases of the pandemic (March–April 2020; October–
December 2020; January–March 2021) in which there was almost a complete cancellation of
screening and follow-up oncologic visits and reduced hospital admissions.
3.3. Heterogeneous Decrease in Surgical Operations
3.3.1. First Year of the Pandemic (2020)
The significant decrease of
10% for oncologic surgical interventions during the
first year of the pandemic (2020) had a statistically significant heterogeneous distribution
(p< 0.001).
The number of operations was similar in the pre-pandemic and post-pandemic periods
for specific pathologies, which are often diagnosed because of the occurrence of severe
symptoms and for which systematic screening is not performed in Italy. Surgery for
patients with cancer of the esophagus, pancreas, bladder, and ovary is often diagnosed by
investigative techniques to identify the cause of evident symptoms (dysphagia, jaundice,
hematuria, abdominal pain). This evidence implies that the medical system answered
promptly to the attention and worries of the patients, despite the inevitable difficulties
related with the prevention of the diffusion of the pandemic.
There was a statistically significant decrease in admissions and operations for patholo-
gies that are more often discovered in asymptomatic patients by screening programs, like
breast cancer, colon and rectal cancer, prostate cancer, and cervical cancer (Table 1).
Cancers 2024,16, 3042 4 of 13
Table 1. Number of patients who had surgery for 14 types of cancers in the pre-pandemic period (2015–2019) and in the pandemic period (2020–2021–2022) in Italy.
2015 2016 2017 2018 2019 Pre-Pandemic
Mean Annual 2020 2021 2022
Pandemic
Mean Annual
(% Difference) *
Esophagus 795 843 789 831 856 823 827 869 883 860 (+4.5%)
Stomach 6746 6557 6239 6146 5824 6302 5088 5075 4890 5018 (19%)
Gallbladder 890 917 840 837 771 851 713 731 736 727 (9%)
Liver 6408 6392 6303 6352 6610 6413 6195 5961 6126 6094 (7.7%)
Pancreas 2626 2648 2690 2809 2710 2697 2778 2766 2938 2827 (+2%)
Colon 27,019 26,784 26,849 27,127 26,233 26,802 23,078 24,796 25,542 24,472 (9.4%)
Rectum 7212 6844 6679 6668 6051 6691 5627 5615 5685 5642 (6.7%)
Kidney 10,935 11,002 11,129 11,736 11,907 11,342 10,665 11,676 12,481 11,607 (3.1%)
Prostate 18,952 18,972 18,673 20,270 20,688 19,511 17,115 18,645 21,324 19,028 (9.4%)
Bladder 5294 5302 5337 5201 5211 5269 5241 5101 5037 5126 (1.4%)
Breast 60,630 62,172 61,797 62,738 62,343 61,936 56,057 62,764 63,986 60,935 (2.5%)
Lung 11,454 11,590 12,039 12,458 12,782 12,065 11,637 12,083 12,808 12,176 (6.4%)
Uterus 11,743 12,036 12,044 11,961 12,349 12,027 11,643 12,103 12,106 11,951 (4.4%)
Ovary 4004 4042 3937 3978 4058 4004 3953 3909 4100 3987 (2.4%)
TOTAL 174,708 176,101 175,345 179,112 178,393 160,617
(10%) *
172,094
(4%) *
178,642
(0.5%) *
* The % mean difference with the expected number of operations on the basis of the trend in the five years before the pandemic.
Cancers 2024,16, 3042 5 of 13
Tables 27show the reduced number of asymptomatic patients who attended orga-
nized screening programs in Italy.
Table 2. Results of the national organized screening program for breast cancer in Italy before (2018–
2019) and during the pandemic (2020–2021).
2018 2019 2020 2021
Population of Italian women 50–69
years 8,695,338 8,670,039
Women 50–59 years 4,842,322 4,803,491
Women 60–69 years 3,853,016 3,866,548
Invitations 3,364,979 3,582,635 2,593,288 3,569,765
Attendance (%) 60.5 60.7 51.0 56.2
Number of mammograms 1,822,8511 1,876,721 1,242,415 1,937,375
Benign lesions 1036 952 741 1343
In situ ductal carcinoma 1069 1135 801 1316
Invasive carcinoma 8045 8300 6061 9845
Invasive carcinoma < 1 cm diameter 2409 2455 1781 2786
Table 3. The % of interviewed women who had a mammogram screening within the last two years
inside and outside the national organized system. Interviews made before (2017–2019) and during
the pandemic period (2020–2021) in Italy.
Total Interviewed Women 28.072 Attendance to Screening Programs
2017–2019 2020–2021
Total
75%
Total
71%
AGE 50–59 77% 73%
AGE 60–69 73% 68%
Educational level *
1 65% 50%
2 73% 67%
3–4 78% 75%
5–8 82% 80%
Low income 60% 55%
Middle income 72% 65%
Good income 81% 77%
Italians 75% 72%
Non-Italians ** 70% 59%
* Educational level is based upon the International Standard Classification of Education (ISCED), 1997 version,
and refers to 1—pre-primary, primary education; 2—lower secondary education; 3–4—upper secondary and
post-secondary non-tertiary education; 5–8—tertiary education. ** Immigrants from low-income countries.
Cancers 2024,16, 3042 6 of 13
Table 4. Results of national screening program screening for colorectal cancer in Italy before
(2018–2019) and during the pandemic (2020–2021).
Colorectal Cancer Screening—Fecal Occult Blood Test
2018 2019 2020 2021
Italian population 50–69 years of age 17,123,098 17,233,176
Number invited 5,939,182 5,921,032 4,159,765 6,416,162
Attendance (%) 42.7% 40.5% 34.1% 38.7%
Number of tests 2,570,437 2,619,871 1,487,636 2,607,329
% of positive tests 4.8% 5.0% 5.5% 5.0%
No. of colonoscopies after positive test
97,604 105,592 60,754 99,100
Diagnoses of carcinoma 2418 2877 1402 2678
Diagnoses of large adenoma 14,870 17,356 10,286 16,000
% of endoscopic resections 17.9% 14.6% 19.3% 18.2%
Table 5. Screening for colorectal cancer (interviews of 51.706 persons aged 50–69 years).
Subgroups with Statistical Significance
at Univariate Analysis
% of Interviewed Persons
Who Had Timely
Screening
Inside the National
Organized Screening
Program
Outside the National
Organized Screening
Program
47% 39% 8%
Sex
Males 48% 39% 8%
Females 46% 39% 7%
Age
50–59 42% 34% 7%
60–69 52% 44% 8%
Education
1 37% 31% 6%
2 45% 39% 6%
3–4 49% 41% 8%
5–8 50% 38% 12%
Family income
Low 32% 26% 6%
Middle 41% 34% 7%
High 54% 46% 8%
Citizenship
Italian 47% 39% 8%
Immigrants (low-income countries) 43% 39% 4%
Cancers 2024,16, 3042 7 of 13
Table 6. Results of National Organization Screening Program for cervical cancer in Italy before
(2018–2019) and during the pandemic (2020–2021).
Screening Test 2018 2019 2020 2021
No. of Italian Women Aged 25–64 Years 16,183,088 16,190,022 16,191,04 16,232,654
Overall invited women for screening 3,966,409 3,835,318 2,598,295 3,426,660
Adherence to invitation (%) 41.7 40.7 34.2 39.2
Cytology 2,453,583 2,212,192 1,223,873 1,434,395
Adherence to invitation (%) 34.2 33.7 27.5 34.8
Diagnoses of CIN2+ for every
1000 examined women 4.6 5.0 5.5 4.5
HPV Test + Cytology 1,480,776 1,632,362 1,360,553 NA
Adherence to invitation (%) 48.5 45.2 37.6 NA
Diagnoses of CIN2+ for every
1000 examined women 5.6 6.4 6.8 NA
Number of total diagnoses for CIN2+ 7.177 7.625 5.228 NA
Table 7. Screening for cervical cancer (cytology or HPV + CYTOLOGY) (interviews of 53.677 women
aged 25–64 years).
Subgroups with Statistical
Significance at Univariate Analysis
% of Women Who Had
Timely Screening
Inside the National
Organized Screening
Program
Outside the National
Organized Screening
Program
79% 49% 30%
Age
25–34 74% 42% 32%
35–49 83% 47% 36%
50–64 78% 53% 25%
Education
1 60% 43% 17%
2 74% 51% 23%
3–4 81% 52% 31%
5–8 84% 47% 37%
Family Income
Low 67% 44% 23%
Middle 77% 48% 29%
High 84% 52% 32%
Citizenship
Italian 79% 48% 31%
Immigrants (low-income countries) 74% 55% 19%
We also documented a statistically significant reduction (p< 0.05), even if less evident,
in operations related with pathologies that are often diagnosed because of less vague
symptoms, implying a diagnostic course, which might have been deferred because of
the generalized fear of contamination and the tendency to defer diagnostics for less in-
validating symptom. Screening programs are not systematically performed in Italy for
these pathologies.
3.3.2. Second and Third Year of the Pandemic (2021–2022)
During the second and third year of the pandemic, hospital admissions and surgical
procedures for patients with cancers that are also detected by well-organized and planned
screening programs (breast, colon–rectum, cervical cancer) returned slowly to the pre-
pandemic levels, simultaneously with the return to almost-normal medical practice.
Cancers 2024,16, 3042 8 of 13
The number of admissions and surgical procedures for pathologies associated in
general with milder symptoms, which address a diagnostic course with radiological and
endoscopic tests, had a statistically significant decrease to reach the pre-pandemic levels
(p< 0.05).
Operations for patients with gallbladder cancer decreased significantly during the
three years of the pandemic, simultaneously with the statistically significant reduction in
open and laparoscopic cholecystectomies. Most diagnoses of gallbladder cancer are made
after a pathological examination of the gallbladder that was removed due to the presence
of stones.
3.3.3. Adherence to Screening for Breast, Colorectal, and Cervical Cancer
Attendance to screening decreased by 33.8% during the first year of the pandemic with
reduced numbers of diagnoses of cancers and adenomas: cancers were diagnosed at a more
advanced stage during the first year of the pandemic (
Supplementary Tables S1 and S2
).
Adherence to screening returned to the pre-pandemic levels during the second and third
years of the pandemic (2021–2022). Several factors were found to be correlated with reduced
adherence to screening, including unmarried status, younger age, living in rural areas, and
low economic status. Multiple regression analysis demonstrated that the most important
factor influencing attendance at cancer screening was the level of educational attainment
and the frequency of consultation with family doctors (Tables 3,5and 7). These disparities
were partially reduced by free screening organized by the Italian National System. Despite
significant differences related to the socio-economic status, the attendance rates were
inappropriately low either in the pre-pandemic or in the pandemic period.
3.3.4. Comparison with Other European Countries
Similarly to the case in Italy, in other EU countries, several factors were found to be
correlated with reduced adherence to screening, including unmarried status, younger age,
living in rural areas, low economic status. Again, the most significant factors were level of
educational attainment, expenditure for preventive care, and education and counseling,
including frequency of consultation and availability of family doctors (Figures 13).
Cancers 2024, 16, x FOR PEER REVIEW 8 of 12
Figure 1. Adherence rates to cervical cancer screening in Europe.
Figure 2. Adherence rates to mammogram breast cancer screening in Europe.
Figure 1. Adherence rates to cervical cancer screening in Europe.
Cancers 2024,16, 3042 9 of 13
Cancers 2024, 16, x FOR PEER REVIEW 8 of 12
Figure 1. Adherence rates to cervical cancer screening in Europe.
Figure 2. Adherence rates to mammogram breast cancer screening in Europe.
Figure 2. Adherence rates to mammogram breast cancer screening in Europe.
Cancers 2024, 16, x FOR PEER REVIEW 9 of 12
Figure 3. Adherence rates in Europe to colorectal cancer screening.
Figure 4. Expenditure for preventive care, education, and counseling in Europe (20122020). The
higher the level of expenditure for preventive care, education, and counseling, the higher the adher-
ence rates to cancer screening.
4. Discussion
Figure 3. Adherence rates in Europe to colorectal cancer screening.
Cancers 2024,16, 3042 10 of 13
Increased adherence to screening is significantly related to the implementation of orga-
nized programs. Considering only screening for colorectal cancer, the rate of participation
in screening programs differs significantly across European countries. The lowest participa-
tion is observed in countries in which organized, population-based screening programs
are not yet implemented. In 2019, 49% of people aged 50 to 74 reported that they had
never attended screening for colorectal cancer, with a lack of participation as high as 94%
in some countries and as low as 17% in others (Figure 2). The incidence of colorectal cancer
has decreased significantly in the last years (2000–2017) in countries with long-standing
screening programs and widespread population coverage, while it either remained stable
or increased in countries with no large-scale screening programs (Supplementary Table S3).
In all European countries, the most significant correlation between adherence to
screening was related with the level of expenditure for preventive care, education, and
counseling (Figure 4). Expenditure for preventive care, education, and counseling imply
several positive actions, including the prevention of obesity, control of diabetes, appropriate
diet, and implementation of adequate cancer screening programs. The expenditure for
preventive care allows national and local initiatives, addressing the importance of screening,
and an adequate number of counseling centers and a higher number and availability of
family doctors.
Cancers 2024, 16, x FOR PEER REVIEW 9 of 12
Figure 3. Adherence rates in Europe to colorectal cancer screening.
Figure 4. Expenditure for preventive care, education, and counseling in Europe (20122020). The
higher the level of expenditure for preventive care, education, and counseling, the higher the adher-
ence rates to cancer screening.
4. Discussion
Figure 4. Expenditure for preventive care, education, and counseling in Europe (2012–2020). The
higher the level of expenditure for preventive care, education, and counseling, the higher the adher-
ence rates to cancer screening.
4. Discussion
During the pandemic period, namely during the acute phases, deferrable surgeries
were rarely performed, and patients asked for medical advice only for severe symptoms
and were subsequently operated on, if needed. As consequence, there was an increased
number of emergency operations, for cancers diagnosed at a more advanced stage [15].
The pandemic confirmed the importance of organized screening programs for cancer
of the breast, colon–rectum, and cervix [
18
22
]. Reduced screening was associated with
a lower number of diagnoses and operations, as well as with the diagnosis of cancer at
more advanced stages. Reduced adherence to screening programs included all levels of the
Cancers 2024,16, 3042 11 of 13
population, and it was more evident for people with lower educational attainment, those
with a lower family income, and immigrants from low-income countries [
23
25
]. Timely
treatment may have been less accessible to vulnerable patient populations.
Free screening through the Italian National System reduced social disparities either
before or during the pandemic. However, still, the overall adherence rates were lower than
expected even in individuals with higher educational attainment and family income, and
social disparities persisted despite the free screening [26,27].
Proper education and information about the importance of preventive care may in-
crease the adherence to cancer screening programs. Valid information requires several
forms of communication including general and location-specific considerations. The first
form of communication should be a commitment from national institutions, including
mass-media campaigns and teaching in schools, universities, and workplaces; the second
aspect, probably the most difficult and effective, should be reserved to local communities,
including clinicians, nurses, and small hospitals. Family doctors play a major role in this
setting. Almost 90% of the individuals with low educational attainment and a lower family
income attended screening because of the advice of family doctors.
In this context, a close collaboration between policy makers, health care providers and
physicians is fundamental, assuring a good cost-effectiveness ratio for health spending.
Another observation relates to the similar number of operations performed before
and during the pandemic for specific forms of cancer for which an organized screening
program in Italy has not yet been implemented. This evidence supports the concept that,
for these types of cancers, the diagnosis is based mainly on the occurrence of symptoms,
with a consequent delay in treatment and diagnosis at later stages [
28
31
]. Thus, it is
conceivable to introduce screening in Italy for specific types of cancers in regions with
high prevalence of the disease. Screening for gastric cancer and esophageal cancer has led
to earlier diagnosis, less invasive treatment, and improved survival rates in several East
Asian countries.
5. Conclusions
Education and information and appropriate expenditure for preventive care have
the potential to increase adherence to screening for colorectal, breast, and cervical cancer
with the possibility of reduced cancer mortality. The findings of our study highlight the
importance of the implementation of nationally organized screening programs for several
other types of cancers that are often detected after the occurrence of symptoms. Nationally
organized screening programs for several types of cancers, like esophageal, gastric, and
pancreatic cancer, in regions with a high prevalence may increase the possibility of diagnosis
at earlier stages an improved early and late results.
Supplementary Materials: The following supporting information can be downloaded at https://www.
mdpi.com/article/10.3390/cancers16173042/s1, Table S1: Pathology of Breast Cancer: 9706 patients
who did not receive pre-operative neoadjuvant; Table S2: Pathology of Colorectal Cancer: 8287 pa-
tients who did not receive pre-operative neoadjuvant; Table S3. Mortality rates from colorectal cancer
for individuals 50–74 years of age.
Author Contributions: R.G.: data collection, data analysis, visualization, validation, and writing—rev-
iewing original draft; M.C.: data collection, data analysis, visualization, validation, and
writing—reviewing
original draft; P.S.: data collection, data analysis, visualization, validation, supervision; and
writing—re
-
viewing original draft; V.B.: data collection, data analysis, visualization, validation, and writing—re-
viewing original draft; L.D.M.: data collection, data analysis, visualization, validation, supervision,
and writing—reviewing original draft; A.V.S.: conceptualization, data collection, data analysis, visu-
alization, validation, supervision, and writing—original draft. All authors have read and agreed to
the published version of the manuscript.
Funding: This research received no external funding.
Institutional Review Board Statement: IRB approval was obtained from the university ethical board
(330215 July 2023). This study was conducted according to the rules dictated by the Helsinki Declaration.
Cancers 2024,16, 3042 12 of 13
Informed Consent Statement: Consent statement was waived because analysis of national data.
Data Availability Statement: Data are available on request by antonio.sterpetti@uniroma1.it.
Conflicts of Interest: The authors have no conflicts of interest to declare.
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... The disparity highlights the potential influence of cultural norms, healthcare system structures, and public health approaches on screening behaviors across different global regions. While the COVID-19 pandemic likely contributed partially to the low screening participation observed [44,45], this finding nonetheless highlights a critical gap in preventive healthcare utilization and underscores the pressing need for a more nuanced examination of factors affecting cervical cancer screening uptake within the Singaporean context, potentially drawing insights from successful global practices. ...
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Article
Importance Advanced-stage breast cancer rates vary by race and ethnicity, with Black women having a 2-fold higher rate than White women among regular screeners. Clinical risk factors that explain a large proportion of advanced breast cancers by race and ethnicity are unknown. Objective To evaluate the population attributable risk proportions (PARPs) for advanced-stage breast cancer (prognostic pathologic stage IIA or higher) associated with clinical risk factors among routinely screened premenopausal and postmenopausal women by race and ethnicity. Design, Setting, and Participants This cohort study used data collected prospectively from Breast Cancer Surveillance Consortium community-based breast imaging facilities from January 2005 to June 2018. Participants were women aged 40 to 74 years undergoing 3 331 740 annual (prior screening within 11-18 months) or biennial (prior screening within 19-30 months) screening mammograms associated with 1815 advanced breast cancers diagnosed within 2 years of screening examinations. Data analysis was performed from September 2022 to August 2023. Exposures Heterogeneously or extremely dense breasts, first-degree family history of breast cancer, overweight/obesity (body mass index >25.0), history of benign breast biopsy, and screening interval (biennial vs annual) stratified by menopausal status and race and ethnicity (Asian or Pacific Islander, Black, Hispanic/Latinx, White, other/multiracial). Main Outcomes and Measures PARPs for advanced breast cancer. Results Among 904 615 women, median (IQR) age was 57 (50-64) years. Of the 3 331 740 annual or biennial screening mammograms, 10.8% were for Asian or Pacific Islander women; 9.5% were for Black women; 5.3% were for Hispanic/Latinx women; 72.0% were for White women; and 2.0% were for women of other races and ethnicities, including those who were Alaska Native, American Indian, 2 or more reported races, or other. Body mass index PARPs were larger for postmenopausal vs premenopausal women (30% vs 22%) and highest for postmenopausal Black (38.6%; 95% CI, 32.0%-44.8%) and Hispanic/Latinx women (31.8%; 95% CI, 25.3%-38.0%) and premenopausal Black women (30.3%; 95% CI, 17.7%-42.0%), with overall prevalence of having overweight/obesity highest in premenopausal Black (84.4%) and postmenopausal Black (85.1%) and Hispanic/Latinx women (72.4%). Breast density PARPs were larger for premenopausal vs postmenopausal women (37% vs 24%, respectively) and highest among premenopausal Asian or Pacific Islander (46.6%; 95% CI, 37.9%-54.4%) and White women (39.8%; 95% CI, 31.7%-47.3%) whose prevalence of dense breasts was high (62%-79%). For premenopausal and postmenopausal women, PARPs were small for family history of breast cancer (5%-8%), history of breast biopsy (7%-12%), and screening interval (2.1%-2.3%). Conclusions and Relevance In this cohort study among routinely screened women, the proportion of advanced breast cancers attributed to biennial vs annual screening was small. To reduce the number of advanced breast cancer diagnoses, primary prevention should focus on interventions that shift patients with overweight and obesity to normal weight.