Prevalence and risk factors of upper gastrointestinal cancers missed during endoscopy: a nationwide registry-based study

Wladyslaw Januszewicz; Klaudiusz Witczak; Paulina Wieszczy; Magda Socha; Maryla H. Turkot; Urszula Wojciechowska; Joanna Didkowska; Michal F. Kaminski; Jaroslaw Regula

doi:10.1055/a-1675-4136

Endoscopy, Table of Contents

Endoscopy 2022; 54(07): 653-660
DOI: 10.1055/a-1675-4136

Original article

Prevalence and risk factors of upper gastrointestinal cancers missed during endoscopy: a nationwide registry-based study

Wladyslaw Januszewicz

¹Department of Gastroenterology, Hepatology and Clinical Oncology, Centre of Postgraduate Medical Education, Warsaw, Poland

²Department of Oncological Gastroenterology, Maria Sklodowska-Curie National Research Institute of Oncology, Warsaw, Poland

,

Klaudiusz Witczak

³Department of Analyses and Strategy, Ministry of Health of the Republic of Poland, Warsaw, Poland

,

Paulina Wieszczy

¹Department of Gastroenterology, Hepatology and Clinical Oncology, Centre of Postgraduate Medical Education, Warsaw, Poland

⁴Institute of Health and Society, University of Oslo, Oslo, Norway

,

Magda Socha

³Department of Analyses and Strategy, Ministry of Health of the Republic of Poland, Warsaw, Poland

,

Maryla H. Turkot

¹Department of Gastroenterology, Hepatology and Clinical Oncology, Centre of Postgraduate Medical Education, Warsaw, Poland

,

Urszula Wojciechowska

⁵Department of Epidemiology and Cancer Prevention, Maria Sklodowska-Curie National Research Institute of Oncology, Warsaw, Poland

,

Joanna Didkowska

⁵Department of Epidemiology and Cancer Prevention, Maria Sklodowska-Curie National Research Institute of Oncology, Warsaw, Poland

,

Michal F. Kaminski

¹Department of Gastroenterology, Hepatology and Clinical Oncology, Centre of Postgraduate Medical Education, Warsaw, Poland

²Department of Oncological Gastroenterology, Maria Sklodowska-Curie National Research Institute of Oncology, Warsaw, Poland

⁴Institute of Health and Society, University of Oslo, Oslo, Norway

,

Jaroslaw Regula

¹Department of Gastroenterology, Hepatology and Clinical Oncology, Centre of Postgraduate Medical Education, Warsaw, Poland

²Department of Oncological Gastroenterology, Maria Sklodowska-Curie National Research Institute of Oncology, Warsaw, Poland

› Author Affiliations

Abstract

Background A significant proportion of upper gastrointestinal cancers (UGICs) remain undetected during esophagogastroduodenoscopy (EGD). We investigated the characteristics and risk factors of UGICs missed during endoscopy.

Methods In this nationwide registry-based study, we analyzed two large Polish datasets (National Health Fund and National Cancer Registry) to identify individuals who underwent EGD and were subsequently diagnosed with UGIC. Cancers diagnosed < 6 months after EGD were defined as “prevalent” and those within ≥ 6– < 36 months as “missed.” We compared the characteristics of missed and prevalent cancers, and analyzed the risk factors for missed UGICs in a multivariable regression model.

Results We included 4 105 399 patients (mean age 56.0 years [SD 17.4]; 57.5 % female) who underwent 5 877 674 EGDs in 2012–2018. Within this cohort, 33 241 UGICs were diagnosed, of which 1993 (6.0 %) were missed. Within esophageal neoplasms, adenocarcinomas were more frequently missed than squamous cell cancers (6.1 % vs. 4.2 %), with a relative risk of 1.4 (95 % confidence interval [CI] 1.1–1.8, P = 0.01). Most gastric cancers were adenocarcinomas, of which 5.7 % were classified as missed. Overall, a higher proportion of missed UGICs than prevalent cancers presented at an advanced stage (42.2 % vs. 36.2 %, P < 0.001). Risk factors for missed UGICs included initial EGD performed within primary (vs. secondary) care (odds ratio [OR] 1.3, 95 %CI 1.2–1.5), female sex (OR 1.3, 95 %CI 1.2–1.4), and higher comorbidity (Charlson comorbidity index ≥ 5 vs. 0; OR 6.0, 95 %CI 4.7–7.5).

Conclusions Among UGICs, esophageal adenocarcinomas were missed most frequently. Missed cancers occur more frequently within the primary care sector and are found more often in women and individuals with multiple comorbidities.

Full Text

References

References
1 International Agency for research on cancer (IARC). Cancer today. Cancer fact sheets. Accessed: Dec 18 2019 https://gco.iarc.fr/today/fact-sheets-cancers
2 Smyth EC, Lagergren J, Fitzgerald RC. et al. Oesophageal cancer. Nat Rev Dis Prim 2018; 3: 17048
3 Njei B, Mccarty TR, Birk JW. Trends in esophageal cancer survival in United States adults from 1973 to 2009: a SEER database analysis. J Gastroenterol Hepatol 2016; 31: 1141-1146
4 Asplund J, Kauppila JH, Mattsson F. et al. Survival trends in gastric adenocarcinoma: a population-based study in Sweden. Ann Surg Oncol 2018; 25: 2693-2702
5 Menon S, Dhar A, Hoare JM. et al. How commonly is gastric cancer missed at endoscopy: a UK primary care based study. Gastrointest Endosc 2012; 75: AB139
6 Hosokawa O, Tsuda S, Kidani E. et al. Diagnosis of gastric cancer up to three years after negative upper gastrointestinal endoscopy. Endoscopy 1998; 30: 669-674
7 Raftopoulos SC, Segarajasingam DS, Burke V. et al. A cohort study of missed and new cancers after esophagogastroduodenoscopy. Am J Gastroenterol 2010; 105: 1292-1297
8 Pimenta-Melo AR, Monteiro-Soares M, Libânio D. et al. Missing rate for gastric cancer during upper gastrointestinal endoscopy: a systematic review and meta-Analysis. Eur J Gastroenterol Hepatol 2016; 28: 1041-1049
9 Wang YR, Loftus EV, Judge TA. et al. Rate and predictors of interval esophageal and gastric cancers after esophagogastroduodenoscopy in the United States. Digestion 2016; 94: 176-180
10 Cho YS, Chung IK, Kim JH. et al. Risk factors of developing interval early gastric cancer after negative endoscopy. Dig Dis Sci 2015; 60: 936-943
11 Hernanz N, Rodríguez de Santiago E, Marcos Prieto HM. et al. Characteristics and consequences of missed gastric cancer: a multicentric cohort study. Dig Liver Dis 2019; 51: 894-900
12 Rodríguez de Santiago E, Hernanz N, Marcos-Prieto HM. et al. Rate of missed oesophageal cancer at routine endoscopy and survival outcomes: a multicentric cohort study. United Eur Gastroenterol J 2019; 7: 189-198
13 Yalamarthi S, Witherspoon P, McCole D. et al. Missed diagnoses in patients with upper gastrointestinal cancers. Endoscopy 2004; 36: 874-879
14 Chadwick G, Groene O, Hoare J. et al. A population-based, retrospective, cohort study of esophageal cancer missed at endoscopy. Endoscopy 2014; 46: 553-560
15 Menon S, Trudgill N. How commonly is upper gastrointestinal cancer missed at endoscopy? A meta-analysis. Endosc Int Open 2014; 02: E46-E50
16 Zdrowia M, Polskiej R, Zdrowia M. et al. Sprawozdanie z działalności narodowego funduszu zdrowia za 2011 rok. [2011 National Health Fund activity report]. Accessed: Dec 18 2019 https://www.nfz.gov.pl/bip/dzialalnosc-nfz/
17 Tyczyński JE, Démaret E, Parkin DM. , eds. Standards and guidelines for cancer registration in Europe: the ENCR recommendations: volume I. Lyon: International Agency for Research on Cancer; 2003
18 Didkowska J, Wojciechowska U, Czaderny K. et al. Cancer in Poland in 2017. Accessed: Dec 18 2019 http://onkologia.org.pl/wp-content/uploads/Nowotwory_2017.pdf
19 Fritz A, Percy C, Jack A. et al. International classification of diseases for oncology. 3rd. edition Geneva: World Health Organization; 2000
20 Lauren P. The two histological main types of gastric carcinoma: diffuse and so-called intestinal-type carcinoma. An attempt at a histo-clinical classification. Acta Pathol Microbiol Scand 1965; 64: 31-49
21 Cheung D, Evans T, Lawrence G. et al. OC-013 How often is upper gastrointestinal cancer missed during endoscopy?. Gut 2013;
22 Cheung D, Menon S, Hoare J. et al. Factors associated with upper gastrointestinal cancer occurrence after endoscopy that did not diagnose cancer. Dig Dis Sci 2016; 61: 2674-2684
23 Chadwick G, Groene O, Riley S. et al. Gastric cancers missed during endoscopy in England. Clin Gastroenterol Hepatol 2015; 13: 1264-1270
24 Arnold M, Soerjomataram I, Ferlay J. et al. Global incidence of oesophageal cancer by histological subtype in 2012. Gut 2015; 64: 381-387
25 Fujita S. Biology of early gastric carcinoma. Pathol Res Pract 1978; 163: 297-309
26 Khalil Q, Gopalswamy N, Agrawal S. Missed esophageal and gastric cancers after esophagogastroduodenoscopy in a midwestern military veteran population. South Med J 2014; 107: 225-228
27 Woodland H, Winters D, Colleypriest B. PTH-016 How often do we miss upper gastrointestinal tumours at gastroscopy?. Gut 2017; 66: A212
28 Tai FWD, Wray N, Sidhu R. et al. Factors associated with oesophagogastric cancers missed by gastroscopy: a case–control study. Frontline Gastroenterol 2020; 11: 194-201
29 Gavric A, Hanzel J, Zagar T. et al. Survival outcomes and rate of missed upper gastrointestinal cancers at routine endoscopy: a single centre retrospective cohort study. Eur J Gastroenterol Hepatol 2020; 32: 1312-1321
30 Hosokawa O, Hattori M, Douden K. et al. Difference in accuracy between gastroscopy and colonoscopy for detection of cancer. Hepatogastroenterology 2007; 54: 442-444
31 Kaminski MF, Regula J, Kraszewska E. et al. Quality indicators for colonoscopy and the risk of interval cancer. N Engl J Med 2010; 362: 1795-1803
32 Corley DA, Jensen CD, Marks AR. et al. Adenoma detection rate and risk of colorectal cancer and death. N Engl J Med 2014; 370: 1298-1306
33 Januszewicz W, Wieszczy P, Bialek A. et al. Endoscopist biopsy rate as a quality indicator for outpatient gastroscopy: a multicenter cohort study with validation. Gastrointest Endosc 2019; 89: 1141-1149
34 Farhadi A, Fields JZ, Hoseini SHB. The assessment of esophagogastroduodenoscopy tolerance a prospective study of 300 cases. Diagn Ther Endosc 2001; 7: 141-147
35 Hazeldine S, Fritschi L, Forbes G. Predicting patient tolerance of endoscopy with conscious sedation. Scand J Gastroenterol 2010; 45: 1248-1254

Supplementary Material

Supplementary material