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Gastroenterology Unit, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, ItalyDepartment of Medical and Surgical Sciences, University of Bologna, Bologna, Italy
Gastroenterology Unit, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Bologna, ItalyDepartment of Medical and Surgical Sciences, University of Bologna, Bologna, Italy
The SARS-CoV-2 pandemic has had a huge impact on healthcare systems, resulting in many routine diagnostic procedures either being halted or postponed.
Aims
To evaluate whether the diagnoses of colorectal, gastric and pancreatic cancers have been impacted by the SARS-CoV-2 pandemic in Italy.
Methods
A survey designed to collect the number of histologically-proven diagnoses of the three cancers in gastroenterology services across Italy from January 1 to October 31 in 2017–2020. Non-parametric ANOVA for repeated measurements was applied to compare distributions by years and macro-areas.
Results
Compared to 2019, in 2020 gastric cancer diagnoses decreased by 15.9%, CRC by 11.9% and pancreatic by 9.9%. CRC distributions showed significant differences between all years, stomach cancer between 2018 and 2020 and 2019–2020, and pancreatic cancer only between 2017 and 2019. The 2019–2020 comparison showed fewer CRC diagnoses in the North (-13.7%), Center (-16.5%) and South (-4.1%), fewer stomach cancers in the North (-19.0%) and South (-9.4%), and fewer pancreatic cancers in the North (-14.1%) and Center (-4.7%), with an increase in the South (+12.3%). Distributions of CRC and gastric cancer were significantly different between all years in the North.
Conclusions
This survey highlights the concerning effects of the COVID-19 pandemic on the diagnostic yield of gastroenterology services for stomach, colorectal and pancreatic cancers in Italy.
The SARS-CoV-2 pandemic has had a rapid and dramatic effect on healthcare systems around the world. Due to the critical need to divert healthcare efforts to absorb the rapidly increasing number of COVID-19 patients, many activities have had to be quickly reorganized or reduced in order to accommodate the influx of patients. In Italy, during the first wave of the pandemic, which occurred between 1 March and 30 June 2020, many activities related to routine diagnostic procedures were either halted or postponed. In a recently published survey, up to 3% of routine endoscopic procedures were completely stopped, while the remaining ones were converted to emergency or oncological patient follow-ups [
]. A significant disruption in colon cancer screening programs occurred, including a complete suspension of both first (fecal immunochemical test) and second (colonoscopies) levels in some areas [
]. Furthermore, 13% excess mortality was registered in Italy between January and November 2020. Importantly, however, during the early months of the first wave of the pandemic (March-April), the number of deaths from any cause was 48,761 as opposed to 28,000 registered deaths from COVID-19 [
]. Recent estimates indicate that cancer of the colorectum, stomach and pancreas represent the second, sixth and seventh most frequent tumors, respectively, in both sexes in Italy in 2020 [
In this work we investigated whether in Italy the diagnosis of the three most incidental digestive cancers was impacted by the SARS-CoV-2 pandemic, by comparing the number of diagnoses made from January to October 2020 to those made during the same 10-month period in the previous three years.
2. Methods
We developed a web-based survey designed to assess the number of histologically-proven diagnoses of colorectal, gastric and pancreatic adenocarcinomas made in gastroenterology (GE) services across Italy.
The working group that formulated the survey was composed of the executive board of FISMAD (Italian Federation of Gastroenterological Societies) which included the presidents of the Italian Society of Gastroenterology and Digestive Endoscopy (SIGE, AB), the Italian Society of Digestive Endoscopy (SIED, LP), the Italian Association of hospital gastroenterologists and digestive endoscopists (AIGO, FM) together with the FISMAD president (EB) and one board member (LR).
A 9-question questionnaire (see supplementary information) was designed by the working group and administered through SurveyMonkey to the GE services across the country. The link to access the survey was emailed to all members affiliated to AIGO, SIED and SIGE.
The survey questions were aimed at assessing the number of diagnosed gastric, colorectal and pancreatic adenocarcinomas from January 1 to October 31 in 2017, 2018, 2019 and 2020. Ethics committee approval was not required for this type of survey. Data collection took place between 1 November 2020 and 22 January 2021.
2.1 Statistical analysis
The distributions of the number of diagnosed cancers were analyzed by plots (boxplots and bar charts), whereas summary statistics, across all 49 centers, were reported as the minimum, maximum, average, standard deviation and total number of cases aggregated by year (from 2017 to 2020) and by type (colorectal, gastric and pancreatic) of cancer. Similarly, a second descriptive analysis was conducted separately for each macro-area (North, Center and South).
In order to compare the distributions of the number of diagnoses across years, we applied the non-parametric ANOVA for repeated measurements (Friedman test, p-values adjusted for Bonferroni correction), separately for each type of tumor and then for each macro-area. All statistical analyses were performed using R software (version 4.0.3).
3. Results
A total of 61 GE services replied to the survey (representing approximately 35% of all services in Italy) [
], with complete datasets available from 49. The distribution of the replies was: 32 from the North (65.3%), 6 from the Center (12.2%), and 11 from the South (22.4%).
Fig. 1 shows the cancer distribution across centers by year and type. For all the years, CRC was the most prevalent with also the largest variability across centers; gastric and pancreatic cancer distributions were more similar in terms of median level and variability (see also Table 1). Fig. 2 reports the total number of cases per year and separated by type. Between January 1 and October 31 2020, a total of 4234, 1308 and 1452 center-reported diagnoses of adenocarcinomas of the colorectum, stomach and pancreas, respectively were recorded.
Fig. 1Distribution (across centers) of the number of cancers separated by year and type.
Table 1Summary statistics (across all 49 centers) aggregated by type of cancer and year (min, max, average, standard deviation – SD -, total, absolute and relative percentage variation) and Friedman test for the number of colorectal, stomach and pancreatic cancer diagnoses per year.
Min, Max, Average refer to minimum, maximum, average and SD of number of cancers computed across all 49 centers with respect to the specific type of cancer at specific year;
Min, Max, Average refer to minimum, maximum, average and SD of number of cancers computed across all 49 centers with respect to the specific type of cancer at specific year;
Min, Max, Average refer to minimum, maximum, average and SD of number of cancers computed across all 49 centers with respect to the specific type of cancer at specific year;
Min, Max, Average refer to minimum, maximum, average and SD of number of cancers computed across all 49 centers with respect to the specific type of cancer at specific year;
the p-values are adjusted for Bonferroni correction.
Colorectal
2017
0
331
97.20
81.34
4763
2017 vs 2020 (p = 0.045); 2018 vs 2020 (p = 0.001); 2019 vs 2020 (p = 0.003)
2018
2
320
97.69
73.19
4787
24
0.50
2019
0
297
98.12
74.82
4808
21
0.44
2020
6
308
86.41
74.66
4234
−574
−11.94
Pancreas
2017
0
171
27.79
33.79
1306
2017 vs 2019 (p = 0.034)
2018
0
266
33.40
45.70
1570
264
20.21
2019
0
211
34.28
41.75
1611
41
2.61
2020
0
141
30.89
33.58
1452
−159
−9.87
Stomach
2017
0
105
31.04
26.33
1521
2018 vs 2020 (p = 0.014); 2019 vs 2020 (p = 0.010)
2018
1
126
30.98
25.80
1518
−3
−0.20
2019
0
116
31.76
26.29
1556
38
2.50
2020
1
101
26.69
20.60
1308
−248
−15.94
$ Min, Max, Average refer to minimum, maximum, average and SD of number of cancers computed across all 49 centers with respect to the specific type of cancer at specific year;
D is the absolute variation in the total number of cases compared to the previous year
Δ is the percentage relative variation in the total number of cases compared to the previous year.
# the p-values are adjusted for Bonferroni correction.
As reported in Table 1, compared to 2019, in 2020 the total number of stomach cancer diagnoses showed the highest reduction across Italy (−15.9%), followed by CRC (−11.9%) and pancreatic cancer (−9.9%).
When comparing the number of cases (of the 49 centers) across years, separately for each type of tumor, the following distributions were significantly different (see Table 1): for CRC, 2017 vs 2020 (p = 0.045), 2018 vs 2020 (p = 0.001) and 2019 vs 2020 (p = 0.003); for stomach cancer 2018 vs 2020 (p = 0.014) and 2019 vs 2020 (p = 0.01); and for pancreatic cancer, 2017 vs 2019 (p = 0.034).
We then considered the three major Italian macro-areas: the North, Center and South. The total number of cases by year, type and macro-area are reported in Fig. 3. Compared to 2019, the total number of diagnoses for colorectal cancer decreased in all three areas (see Table 2): North −13.7%, Center −16.5%, and South −4.1%. Stomach cancer, which had the highest diagnosis reduction at a national level in 2020 compared to 2019 (−15.9%, see Table 1), showed a different behavior when analyzed separately for each macro-area: while no changes were recorded in the South, in the North and Center 19.0% and 9.4% reductions, respectively were recorded. When considering pancreatic cancer, compared to 2019, in 2020 a 12.3% increase in diagnoses was recorded in the South, and 14.1% and 4.7% reductions were recorded in the North and Center, respectively.
Fig. 3Total number of cancers by year, type and macro-area.
Table 2Summary statistics (across all 49 centers) aggregated by type of cancer and year (min, max, average, standard deviation – SD -, total, absolute and relative variation) and Friedman test for the number of colorectal, stomach and pancreatic cancer diagnosis per year and macro-area.
Min, Max, Average refer to minimum, maximum, average and SD of number of cancers computed across all 49 centers with respect to the specific type of cancer at specific year;
Min, Max, Average refer to minimum, maximum, average and SD of number of cancers computed across all 49 centers with respect to the specific type of cancer at specific year;
Min, Max, Average refer to minimum, maximum, average and SD of number of cancers computed across all 49 centers with respect to the specific type of cancer at specific year;
Min, Max, Average refer to minimum, maximum, average and SD of number of cancers computed across all 49 centers with respect to the specific type of cancer at specific year;
the p-values are adjusted for Bonferroni correction.
North
Colorectal
2017
38
331
116.31
86.89
3722
2017 vs 2020 (p = 0.015); 2018 vs 2020 (p<0.001); 2019 vs 2020 (p = 0.003)
2018
35
320
114.63
75.25
3668
−54
−1.45
2019
31
297
110.13
71.17
3524
−144
−3.93
2020
31
299
95.06
70.83
3042
−482
−13.68
Pancreas
2017
0
171
35.93
38.67
1078
2018
0
266
43.93
53.42
1318
240
22.26
2019
0
211
43.73
48.22
1312
−6
−0.46
2020
0
141
37.57
37.85
1127
−185
−14.10
Stomach
2017
6
105
40.63
26.43
1300
2017 vs 2020 (p = 0.011); 2018 vs 2020 (p<0.001); 2019 vs 2020 (p = 0.001)
2018
5
126
40.34
26.09
1291
−9
−0.69
2019
4
116
39.78
25.60
1273
−18
−1.39
2020
4
101
32.22
21.43
1031
−242
−19.01
Center
Colorectal
2017
0
100
39.50
36.86
237
2018
2
121
41.17
44.79
247
10
4.22
2019
0
178
53.50
65.27
321
74
29.96
2020
6
107
44.67
38.09
268
−53
−16.51
Pancreas
2017
0
25
7.67
9.50
46
2018
0
24
9.00
9.59
54
8
17.39
2019
0
41
10.67
15.63
64
10
18.52
2020
1
31
10.17
11.11
61
−3
−4.69
Stomach
2017
0
17
8.67
7.00
52
2018
1
26
12.00
9.65
72
20
38.46
2019
0
22
10.67
8.98
64
−8
−11.11
2020
2
18
9.67
5.82
58
−6
−9.38
South
Colorectal
2017
4
210
73.09
62.15
804
2018
6
205
79.27
62.84
872
68
8.46
2019
5
256
87.55
85.21
963
91
10.44
2020
6
308
84.00
95.85
924
−39
−4.05
Pancreas
2017
0
55
16.55
16.97
182
2018
0
50
18.00
18.29
198
16
8.79
2019
1
70
21.36
19.14
235
37
18.69
2020
0
73
24.00
22.92
264
29
12.34
Stomach
2017
0
60
15.36
16.51
169
2018
1
55
14.09
15.04
155
−14
−8.28
2019
0
90
19.91
24.87
219
64
41.29
2020
1
59
19.91
16.59
219
0
0.00
$ Min, Max, Average refer to minimum, maximum, average and SD of number of cancers computed across all 49 centers with respect to the specific type of cancer at specific year;
D is the absolute variation in the total number of cases compared to the previous year.
Δ is the percentage relative variation in the total number of cases compared to the previous year.
# the p-values are adjusted for Bonferroni correction.
By comparing the distributions across years separately for each type and macro-area, no significant differences were found in both the Center and Southern Italy for all cancer types (see Table 2). On the other hand, for northern Italy the following significant results were found: for CRC 2017 vs 2020 (p = 0.015), 2018 vs 2020 (p < 0.001) and 2019 vs 2020 (p = 0.003); for stomach cancer 2017 vs 2020 (p = 0.011), 2018 vs 2020 (p < 0.001) and 2019 vs 2020 (p = 0.001). No significant changes were found for pancreatic cancer in the North.
4. Discussion
The aim of our study was to assess whether under the SARS-CoV-2 pandemic, the diagnoses of digestive cancers with a high impact on the population such as colorectal, stomach and pancreatic adenocarcinomas, had been affected. Compared to 2019, in 2020 we found a 11.9% reduction in the total number of diagnoses of CRC, a 15.9% reduction in stomach cancer diagnoses, and 9.9% reduction in pancreatic cancer diagnoses. Importantly, at a national level CRC and stomach cancer showed significant differences when comparing data between 2020 and 2019 and 2018. Considering data from the three macro-areas, we found that in northern Italy, compared to 2019, the total number of CRC, stomach and pancreatic cancer diagnoses decreased by 13.7%, 19.0% and 14.1%, respectively. Comparing the diagnosis distributions across years, in 2020 in the North, only CRC and stomach cancer were significantly different from the previous years, while no differences were found in the Center and South for any cancer.
Our analysis might reflect differences in the areas that were affected by COVID-19, in particular during the first phase of the pandemic in which the North had a dramatic spread of infection associated with a high mortality, while in the Center-South the spread was much lower [
Mortality impacts of the coronavirus disease (COVID-19) outbreak by sex and age: rapid mortality surveillance system, Italy, 1 February to 18 April 2020.
]. Importantly, during the early months (March-April) of the first phase of the epidemic, the greater impact of mortality in the cities in Northern Italy was only partially (66%) explained by the deaths notified as COVID-19 [
Our data confirm the anticipated negative effect that the SARS-CoV-2 pandemic has had on highly-impacting diseases such as cancers. There were fewer diagnoses of CRC throughout the country, which were more pronounced and significant in the North. Data on CRC also reflect the difficulties of screening programs which had to be halted across Italy. Data published by the Italian National Screening Observatory (ONS) and including information from 1 January 2020 to 30 September 2020, estimated a 4.7 standard month screening delay across the country with peaks of 7.1 and 8.4 months (Lombardy and Calabria, respectively). Importantly, the ONS estimated that 1168 CRC and 6700 advanced adenomas had not been carried out across the country, though under normal circumstances they would have been [
The fact that these diagnoses were not carried out could have an impact on disease stage and mortality. In fact, recent data on delays from colorectal cancer screening showed a possible 12% increase in mortality for delays beyond 12 months [
]. This was also echoed by two different studies from Hong Kong and the UK, indicating that missing diagnoses due to surges in SARS-CoV-2 would lead to increased mortality [
Impacts of the coronavirus 2019 pandemic on gastrointestinal endoscopy volume and diagnosis of gastric and colorectal cancers: a population-based study.
The data presented show how reductions in the volume of specialized GE diagnostic activities due to the COVID-19 pandemic have led to a substantial number of diagnoses not being carried out of the three “big killers”, namely stomach, colorectal and pancreatic cancers. These effects of the COVID-19 pandemic could drastically impair the protective effect of CRC screening that has been accumulated over two decades, and reverse the positive trends observed for colorectal and stomach cancers. In fact, between 2008 and 2016, 1.4 and 1.2% reductions were recorded in colorectal cancer incidence in men and women annually, respectively. In addition, considering the colorectal cancer screening age-target (50–69 years), 4.1% and 3.0%, yearly reductions were recorded respectively, highlighting the important effect of screening programs on colorectal incidence; a lower trend has also been recorded for stomach cancer (−1.9% and −1.4% in men and women) [
Data from the present survey highlight the need for an urgent response to this critical situation by decision-makers at different institutional levels, with adequate actions aimed at restoring the level of activity necessary to meet the epidemiological needs and make up for the accumulated delay, both in routine GE diagnostic activity and CRC screening program.
The GE workforce was already inadequate to meet the needs of specialized health care in 2014 [
]. Consequently, with the COVID-19 pandemic, it is imperative that an appropriate, efficient and stable allocation of resources is carried out, which is truly commensurate with healthcare needs.
We acknowledge some limitations. First of all, our study does not cover the entire Italian healthcare system. However, considering that according to Ministry data in 2014 there were 174 gastroenterology services in Italy [
], our survey captured data from approximately one third of them. We thus believe that our sample provides a significant nationwide representation of the diagnostic activities of digestive cancers during the COVID-19 pandemic. Furthermore, our study does not assess the impact of the COVID-19 pandemic on the cancer-related mortality. We can reasonably assume that the significant proportions of missed diagnoses will affect the disease stage and, in turn, the number of deaths (as discussed above), but more studies will be needed in the near future to assess this aspect.
In conclusion, this survey highlights the concerning effects of the COVID-19 pandemic on GE diagnostic activities related to stomach, colorectal and pancreatic cancers. These data should support appropriate and timely decision making and planning of support for GE in the months and years to come.
Declaration of Competing Interest
The authors of the manuscript and the researchers involved in the study declare no conflict of interest.
Funding
Luigi Ricciardiello is funded by Fondazione AIRC per la ricerca sul cancro, IG 21723.
- Elisa STASI, Gastroenterologia ed Endoscopia Digestiva, Ospedale “Vito Fazzi”, Lecce.
- Giovanni SERIO, U.O.C. Anatomia Patologica, Ospedale “Vito Fazzi”, Lecce.
- Luigi Maria MONTALBANO, U.O.C Gastroenterologia ed Endoscopia Digestiva, Ospedali Riuniti “Villa Sofia-Cervello”, Palermo.
- Vincenzo Giorgio MIRANTE, SC Gastroenterologia ed Endoscopia Digestiva, Dipartimento Oncologico e Tecnologie Avanzate, Azienda USL-IRCCS di Reggio Emilia.
- Osvaldo BURATTINI, U.O.C. Gastroenterologia ed Endoscopia Digestiva IRCCS “S. de Bellis”, Castellana Grotte, Bari.
- Simona ATTARDO, Unità di Gastroenterologia ed Endoscopia Digestiva, Azienda Ospedaliera-Universitaria di Novara, Ospedale “Maggiore della Carità”, Novara.
- Stefano BARGIGGIA, Gastroenterologia ed Endoscopia digestiva, Clinica “San Carlo”, Paderno Dugnano, Milano.
- Manuele DINCA, U.O.S. Gastroenterologia, Ospedali Riuniti di Padova Sud “Madre Teresa di Calcutta”, Padova.
- Guido MISSALE, U.O.C. Endoscopia Digestiva e Interventistica, ASST Spedali Civili, Università degli Studi di Brescia.
- Costanza ALVISI, U.O.S.D. Endoscopia Digestiva ASST, Pavia.
- Francesco BROGLIA, U.O.S.D. Endoscopia Digestiva e Gastroenterologia, ASST Lodi.
- Luca FERRARIS, U.O. Gastroenterologia, ASST Valleolona, Varese.
- Maria Cristina CONTI BELLOCCHI, U.O.S.D. Endoscopia Diagnostica Interventistica del pancreas, AOUI Verona.
- Carmelo LUIGIANO, U.O.D. Endoscopia Digestiva, ASST “Santi Paolo e Carlo”, Presidio Ospedaliero San Paolo, Milano.
- Socrate PALLIO, U.O.S.D. Endoscopia Digestiva, Azienda Ospedaliero-Universitaria di Messina, Policlinico “Gaetano Martino”, Messina.
- Carlo MANFRINI, Servizio Endoscopia Digestiva, Ospedale "Pederzoli", Peschiera Del Garda, Verona.
- Rosamaria BOZZI, Centro di Gastroenterologia ed Endoscopia Digestiva, ASL Benevento.
- Davide CHECCHIN, U.O.C. Gastroenterologia, Ospedale HUB di Mestre, Venezia.
- Thomas TOGLIANI, S.S.D. di Gastroenterologia ed Endoscopia Digestiva, ASST Poma Mantova.
- Antonietta D'ERRICO, U.O. Anatomia e Istologia Patologica, IRCCS Azienda Ospedaliero Universitaria di Bologna Sant'Orsola-Malpighi; Dipartimento di Medicina Specialistica, Diagnostica e Sperimentale, Università di Bologna.
- Franco BAZZOLI, U.O. Gastroenterologia, IRCCS Azienda Ospedaliero-Universitaria di Bologna, Policlinico Sant'Orsola-Malpighi; Dipartimento di Scienze Mediche e Chirurgiche, Università di Bologna.
−Orazio LA BIANCA, U.O.C. Endoscopia Digestiva, Azienda Ospedaliera Universitaria “San Giovanni di Dio e Ruggi d'Aragona” di Salerno - Ospedale “Amico Gaetano Fucito”, Mercato San Severino, Salerno.
- Debora BERRETTI, S.O.C. Gastroenterologia Azienda Sanitaria Universitaria del Friuli Centrale, Udine.
Mortality impacts of the coronavirus disease (COVID-19) outbreak by sex and age: rapid mortality surveillance system, Italy, 1 February to 18 April 2020.
Impacts of the coronavirus 2019 pandemic on gastrointestinal endoscopy volume and diagnosis of gastric and colorectal cancers: a population-based study.
During the height of the coronavirus disease 2019 (COVID-19) pandemic, caused by the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2), many healthcare facilities needed to focus on screening for and treating patients with known or suspected COVID-19 [1]. This resulted in the diversion of healthcare workers and resources leading to the stop of colorectal cancer (CRC) primary screening and an alarming reduction in endoscopy activity during the COVID-19 pandemic, affecting and changing the daily practice of gastrointestinal endoscopy (both diagnostic and therapeutic) and will do so for the foreseeable future.
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