Skip to main content
main-content

Tipp

Weitere Artikel dieser Ausgabe durch Wischen aufrufen

Erschienen in: memo - Magazine of European Medical Oncology 1/2020

Open Access 12.12.2019 | short review

Evidence-based follow-up in colorectal cancer—quo vadis?

verfasst von: MBA MCI, FEBS (HPB) Assoc. Prof. Priv.-Doz. Dr. Manuel Maglione, Assoc. Prof. Priv.-Doz. Dr. Alexander Perathoner

Erschienen in: memo - Magazine of European Medical Oncology | Ausgabe 1/2020

Summary

Colorectal cancer is the third most common and the third most lethal cancer disease in the western world. As most patients undergo treatment with curative intent at initial diagnosis, postoperative surveillance protocols have been established with the primary aim to detect possible disease recurrence in an early resectable stage. Various international guidelines recommend an intensive surveillance protocol over a 5-year time period. These guidelines are based on the reported significant benefit regarding overall patient survival, and on the observation that 90% of recurrences occur within the first 5 years following resection. Surveillance protocols include regular clinical examinations, measurement of the carcinoembryonic antigen, computed tomography scans and regular endoscopies. While there is plenty of evidence regarding the scheduling of endoscopies, the frequency of carcinoembryonic antigen measurements and computed tomography scans has been ever since under debate. The benefit of intensive compared to low frequency surveillance protocols regarding disease-specific survival has never been shown. Moreover, recent meta-analyses and randomized controlled trials challenge current guidelines. Intensive carcinoembryonic antigen assessment and computed tomography scan follow-up protocols seem to fail in generating better overall and disease-specific survival in colorectal cancer patients compared to less intensive surveillance strategies. This change over the last few decades parallels the treatment evolution of colorectal cancer from a primarily surgical to a multidisciplinary task. Instead of advocating a reduction of the follow-up intensity, these findings should stimulate the colorectal oncology field to move from a one-fits-all to a patient-centered surveillance.
Hinweise

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Introduction

Colorectal cancer (CRC) represents with an overall life time risk of 4.15% in women and 4.49% in men the third most common cancer diagnosed in the western world. Despite the fact that most of the diagnosed cancers can be detected in early stages and can be therefore treated with curative intent, it is the third leading cause of cancer-related deaths [1]. Advances in diagnostic tools, surgical techniques, neoadjuvant and adjuvant systemic treatments combined in multidisciplinary approaches have broadened the indication for curative intended treatment strategies. As a matter of fact, the risk of disease recurrence increased by up to 40% at the time of treatment because more patients with advanced stages undergo successful curative treatment; the majority of recurrences occur within the first 3 to 5 years [2]. Disease recurrence might manifest itself as locoregional recurrence, distal metastasis or as a metachronous colorectal primary.
Detecting the recurrent disease in an early, resectable stage with the aim to achieve a survival improvement is the major goal of postoperative CRC surveillance protocols. In addition, curative treatment approaches by implementation of multimodal strategies in patients presenting with liver-limited or lung-limited distant metastasis (in both cases >40% 5‑year survival) justify postoperative surveillance protocols for CRC [3, 4].
Other not less important goals include issues like identification of precancerous lesions which might represent precursors of metachronous CRC, diagnosis of surgery-related problems (e.g. incisional hernia, anastomotic stenosis), psycho-oncological support and last but not least audit of one’s own center’s data and potential impact of new therapeutic approaches [5].
Based on the observation that 90% of recurrences will occur within the first 3 to 5 years after treatment, major cancer societies like ESMO (European Society for Medical Oncology), ASCO (American Society of Clinical Oncology), NCCN (National Comprehensive Cancer Network) as well as the Austrian Society for Surgical Oncology (ACO ASSO) recommend 5‑year surveillance for CRC [6]. All the protocols resemble an intensive surveillance strategy built on four pillars: clinical examination, carcinoembryonic antigen (CEA), computed tomography (CT scans) and endoscopies performed at regular intervals.
The common intensive surveillance strategy relies on different meta-analyses and systematic reviews which showed that this strategy was associated with a better overall survival of patients following surgery for non-metastatic CRC compared to less intensive protocols [79]. However, many of the corresponding studies are outdated and have different shortcomings (e.g. small number of patients). A couple of recent methodologically high-quality trials have been published with consistent results showing that the expected survival benefit due to earlier detection of recurrence has not been achieved in intensive surveillance protocols. The various reduced frequency follow-up regimes analyzed by the most representative trials (COLOFOL study, GILDA study and FACS study) consisted of CT and CEA at 12 and 36 months, CEA only, CT only, CEA and CT, or symptom-based follow-up [1012]. The observation that the benefit of early detection of recurrence after curative treatment of CRC does not translate into improved cancer-specific survival definitely challenge current guidelines.

Clinical examination

Clinical examination, including recent medical history, is a routine procedure in every out-patient clinic regardless of the patients’ diseases. In CRC surveillance its role can be considered marginal regarding diagnosis of asymptomatic recurrences, and it might be even less in rectal cancer patients were radiation therapy does not allow any differential diagnosis between local recurrence and radiation consequences [13]. In this context, it should be mentioned that there is no evidence for performing regular fecal occult blood tests (FBOT).
The usefulness of regular examinations has to be seen in the possibility to address surgery-related problems, psychological and psychosocial issues [14] and also in the better adherence to the surveillance protocol if hospitals offer dedicated outpatient clinics for CRC [15].

Carcinoembryonic antigen

The carcinoembryonic antigen (CEA) is an oncofetal antigen produced by epithelial tumor cells in the digestive tract. In general, measurement of the tumor marker CEA is recommended every 3–6 months for 5 years [6]. It represents a cheap and safe test for the follow-up of colorectal cancer patients [16].
Elevated postoperative CEA is associated with a high probability of disease recurrence; however, negative CEA does not exclude tumor recurrence [17]. In fact, up to 40% of all recurrences of colorectal cancer do not have an accompanying increase of CEA [18]. The sensitivity of CEA testing ranges from 17 to 100%, while the specificity ranges from 66 to 98% in different studies [16]. A major disadvantage of CEA is the high rate of false positives (e.g. cigarette smoking), and there are also no clear data that confirm a significant impact on survival if assessed more frequently [16, 19]. Recently, a large randomized study showed that CEA screening provides an increased rate of surgical resection of recurrence compared with minimal follow-up. However, a survival advantage was not observed [10].

Imaging—computed tomography scan

The computed tomography (CT) scan is the imaging tool of choice in follow-up of CRC. Most guidelines recommend CT scans every 6–12 months for 3 or 5 years. However, the optimal frequency of CT imaging is not clear. Frequent use does not seem to be superior to less frequent use [11]. Ultrasound has a low sensitivity, magnetic resonance imaging is rather limited to the examination of the liver, positron emission tomography is indicated only in special cases, and endosonography may help only to detect local recurrence in rectal cancer. The major advantage of CT scans of the pelvis, abdomen and thorax is the early diagnosis of asymptomatic distant recurrence, which may still be resected with curative intent, especially in liver and lung [6, 20]. The FACS randomized clinical trial has shown that both CT and CEA were associated with an elevated rate of surgical treatment of recurrence, however, with no survival advantage. Interestingly the combination of CT and CEA did not seem to be superior to either alone [10].
Some experts argue that CT is associated with a relevant radiation exposure and a risk of new malignancies. Alternatively, chest x‑ray and abdominal ultrasound can be performed to detect liver or lung metastases; an ongoing French study will provide further clarity about whether this combination is equal to CT alone [21].

Endoscopy

In contrast to CEA measurement and CT scans, there is less contradictory evidence for the performance of surveillance endoscopies to diagnose synchronous and metachronous CRC as well as intraluminal recurrences. Considering the reported prevalence of up to 7% of synchronous CRC [22] preoperative colonoscopy in non-obstructive disease is mandatory. The high incidence of metachronous diseases within the first year in older studies as well as retrospective collected data reflect probably overlooked lesions at the time of initial CRC diagnosis and emphasize even more the importance of preoperative endoscopy [23]. It is generally recommended to perform the first colonoscopy within the first 3 to 6 months following surgery if preoperative colonoscopy was not possible [24].
While the recurrence risk decreases over time the estimated cumulative incidence of metachronous CRC persist with 0.35% per year following curative CRC resection [22]. This is the basis for recommending the first colonoscopy one year following CRC resection (or one year following early postoperative colonoscopy in initial obstructive disease), and in case of normal findings 3 years afterwards. The interval should be shortened in case of abnormal findings like dysplastic adenomas. After completed surveillance, colonoscopies should be repeated at regular intervals according to the national CRC screening protocols [24].

Additional aspects

It has to be highlighted that current international guidelines are based on data of patients operated on UICC stage II and III CRC. The expert guidelines do not particularly consider UICC stage I and IV because consistent data are missing. Over 95% of patients with UICC stage I are cured with surgery and do not need adjuvant chemotherapy. Consequently, the recurrence rate is minimal and intensive surveillance seems to be dispensable. In patients with UICC stage IV with an obvious high risk of recurrence of metastases, studies have demonstrated on the contrary that intensive 3‑monthly surveillance with CT after hepatic resection is reasonable and improves outcome [25]. Similarly, patients with hereditary syndromes (e.g. Lynch syndrome) also need more frequent surveillance to detect recurrence and additional tumor manifestations [26]. The follow-up of patients with rectal cancer has become particularly challenging because of new treatment options emerging recently. Local T1 tumor resection or watch and wait concepts demand an intensive follow-up approach (e.g. endoscopy every 3 months for 2 years) until representative data about less intensive surveillance are published.

Conclusion

Recent trials and meta-analyses challenge current CRC surveillance guidelines. Intensive approaches to surveillance are expensive, but facilitate early detection of recurrence after curative treatment of colorectal cancer. On the other hand, this benefit and less intensive approaches to surveillance do not seem to be inferior. However, the current recommendation is still an intensive surveillance protocol over a 5-year time period (Table 1). Reduced-frequency surveillance protocols should only be offered in the setting of clinical trials.
Table 1
Follow-up protocol of colorectal cancer patients at the Department of Visceral, Transplant and Thoracic Surgery at the Medical University of Innsbruck based on American NCCN Guidelines, European ESMO Guidelines and Austrian ACO-ASSO Guidelines
  
1st year
2nd year
3rd year
4th year
5th year
 
Months
3
6
9
12
15
18
21
24
27
30
33
36
39
42
45
48
51
54
57
60
Colon Carcinoma
CEA
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Clinical Examination
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Colonoscopy
(xa)
x
xb
CT scan
x
x
x
x
x
Rectal Carcinoma
CEA
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Clinical Examination
x
x
x
x
x
x
x
x
x
x
x
x
x
x
Colonoscopy
(xa)
x
xb
CT scan
(xc)
x
(xc)
x
x
x
x
Rectoscopyd
x
x
x
x
x
x
x
x
x
x
x
x
In case of curative treatment of distant metastases, CT scans are repeated in 6‑monthly intervals during the first 2 years and the surveillance period is prolonged for further 5 years
CEA carcinoembryonic antigen, CT computed tomography
aIf not performed preoperatively
bIf normal findings to be repeated regularly according to national screening protocols
cIn high-risk patients (G III, L pos, V pos)
dIn case of local excision or “watch & wait” strategy
Rather than encouraging a reduction of postoperative surveillance examinations the ongoing controversy should stimulate further evolution of patient-centered and stage-adapted surveillance protocols in the light of increasing knowledge of molecular, immunological and microbioma-associated aspects known to influence patients’ outcome.
Take-home message
Current guidelines recommend intensive surveillance postoperative protocols based on regular clinical examinations, measurements of CEA, CT scans and endoscopies. Recent data challenge these surveillance protocols and call for more patient-centered and stage-adapted protocols.

Conflict of interest

M. Maglione and A. Perathoner declare that they have no competing interests.
Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://​creativecommons.​org/​licenses/​by/​4.​0/​), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Literatur
1.
Zurück zum Zitat Ferlay J, Colombet M, Soerjomataram I, Dyba T, Randi G, Bettio M, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries and 25 major cancers in 2018. Eur J Cancer. 2018;103:356–87. CrossRef Ferlay J, Colombet M, Soerjomataram I, Dyba T, Randi G, Bettio M, et al. Cancer incidence and mortality patterns in Europe: estimates for 40 countries and 25 major cancers in 2018. Eur J Cancer. 2018;103:356–87. CrossRef
2.
Zurück zum Zitat Pfister DG, Benson AB, Somerfield MR. Clinical practice. Surveillance strategies after curative treatment of colorectal cancer. N Engl J Med. 2004;350(23):2375–82. CrossRef Pfister DG, Benson AB, Somerfield MR. Clinical practice. Surveillance strategies after curative treatment of colorectal cancer. N Engl J Med. 2004;350(23):2375–82. CrossRef
3.
Zurück zum Zitat Kanas GP, Taylor A, Primrose JN, Langeberg WJ, Kelsh MA, Mowat FS, et al. Survival after liver resection in metastatic colorectal cancer: review and meta-analysis of prognostic factors. Clin Epidemiol. 2012;4:283–301. PubMedPubMedCentral Kanas GP, Taylor A, Primrose JN, Langeberg WJ, Kelsh MA, Mowat FS, et al. Survival after liver resection in metastatic colorectal cancer: review and meta-analysis of prognostic factors. Clin Epidemiol. 2012;4:283–301. PubMedPubMedCentral
4.
Zurück zum Zitat Gonzalez M, Poncet A, Combescure C, Robert J, Ris HB, Gervaz P. Risk factors for survival after lung metastasectomy in colorectal cancer patients: a systematic review and meta-analysis. Ann Surg Oncol. 2013;20(2):572–9. CrossRef Gonzalez M, Poncet A, Combescure C, Robert J, Ris HB, Gervaz P. Risk factors for survival after lung metastasectomy in colorectal cancer patients: a systematic review and meta-analysis. Ann Surg Oncol. 2013;20(2):572–9. CrossRef
5.
Zurück zum Zitat Destri LG, Di Cataldo A, Puleo S. Colorectal cancer follow-up: useful or useless? Surg Oncol. 2006;15(1):1–12. CrossRef Destri LG, Di Cataldo A, Puleo S. Colorectal cancer follow-up: useful or useless? Surg Oncol. 2006;15(1):1–12. CrossRef
6.
Zurück zum Zitat Liu SL, Cheung WY. Role of surveillance imaging and endoscopy in colorectal cancer follow-up: quality over quantity? World J Gastroenterol. 2019;25(1):59–68. CrossRef Liu SL, Cheung WY. Role of surveillance imaging and endoscopy in colorectal cancer follow-up: quality over quantity? World J Gastroenterol. 2019;25(1):59–68. CrossRef
7.
Zurück zum Zitat Pita-Fernández S, Alhayek-Aí M, González-Martín C, López-Calviño B, Seoane-Pillado T, Pértega-Díaz S. Intensive follow-up strategies improve outcomes in nonmetastatic colorectal cancer patients after curative surgery: a systematic review and meta-analysis. Ann Oncol. 2015;26(4):644–56. CrossRef Pita-Fernández S, Alhayek-Aí M, González-Martín C, López-Calviño B, Seoane-Pillado T, Pértega-Díaz S. Intensive follow-up strategies improve outcomes in nonmetastatic colorectal cancer patients after curative surgery: a systematic review and meta-analysis. Ann Oncol. 2015;26(4):644–56. CrossRef
8.
Zurück zum Zitat Renehan AG, Egger M, Saunders MP, O’Dwyer ST. Impact on survival of intensive follow up after curative resection for colorectal cancer: systematic review and meta-analysis of randomised trials. BMJ. 2002;324(7341):813. CrossRef Renehan AG, Egger M, Saunders MP, O’Dwyer ST. Impact on survival of intensive follow up after curative resection for colorectal cancer: systematic review and meta-analysis of randomised trials. BMJ. 2002;324(7341):813. CrossRef
10.
Zurück zum Zitat Primrose JN, Perera R, Gray A, Rose P, Fuller A, Corkhill A, et al. Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial. JAMA. 2014;311(3):263–70. CrossRef Primrose JN, Perera R, Gray A, Rose P, Fuller A, Corkhill A, et al. Effect of 3 to 5 years of scheduled CEA and CT follow-up to detect recurrence of colorectal cancer: the FACS randomized clinical trial. JAMA. 2014;311(3):263–70. CrossRef
11.
Zurück zum Zitat Wille-Jørgensen P, Syk I, Smedh K, Laurberg S, Nielsen DT, Petersen SH, et al. Effect of more vs less frequent follow-up testing on overall and colorectal cancer-specific mortality in patients with stage II or III colorectal cancer: the COLOFOL randomized clinical trial. JAMA. 2018;319(20):2095–103. CrossRef Wille-Jørgensen P, Syk I, Smedh K, Laurberg S, Nielsen DT, Petersen SH, et al. Effect of more vs less frequent follow-up testing on overall and colorectal cancer-specific mortality in patients with stage II or III colorectal cancer: the COLOFOL randomized clinical trial. JAMA. 2018;319(20):2095–103. CrossRef
12.
Zurück zum Zitat Rosati G, Ambrosini G, Barni S, Andreoni B, Corradini G, Luchena G, et al. A randomized trial of intensive versus minimal surveillance of patients with resected Dukes B2‑C colorectal carcinoma. Ann Oncol. 2016;27(2):274–80. CrossRef Rosati G, Ambrosini G, Barni S, Andreoni B, Corradini G, Luchena G, et al. A randomized trial of intensive versus minimal surveillance of patients with resected Dukes B2‑C colorectal carcinoma. Ann Oncol. 2016;27(2):274–80. CrossRef
13.
Zurück zum Zitat Anthony T, Simmang C, Hyman N, Buie D, Kim D, Cataldo P, et al. Practice parameters for the surveillance and follow-up of patients with colon and rectal cancer. Dis Colon Rectum. 2004;47(6):807–17. CrossRef Anthony T, Simmang C, Hyman N, Buie D, Kim D, Cataldo P, et al. Practice parameters for the surveillance and follow-up of patients with colon and rectal cancer. Dis Colon Rectum. 2004;47(6):807–17. CrossRef
14.
Zurück zum Zitat Stiggelbout AM, de Haes JC, Vree R, van de Velde CJ, Bruijninckx CM, van Groningen K, et al. Follow-up of colorectal cancer patients: quality of life and attitudes towards follow-up. Br J Cancer. 1997;75(6):914–20. CrossRef Stiggelbout AM, de Haes JC, Vree R, van de Velde CJ, Bruijninckx CM, van Groningen K, et al. Follow-up of colorectal cancer patients: quality of life and attitudes towards follow-up. Br J Cancer. 1997;75(6):914–20. CrossRef
15.
Zurück zum Zitat Coebergh van den Braak RRJ, Lalmahomed ZS, Büttner S, Hansen BE, Ijzermans JNM, Group MS. Nonphysician clinicians in the follow-up of resected patients with colorectal cancer. Dig Dis. 2018;36(1):17–25. CrossRef Coebergh van den Braak RRJ, Lalmahomed ZS, Büttner S, Hansen BE, Ijzermans JNM, Group MS. Nonphysician clinicians in the follow-up of resected patients with colorectal cancer. Dig Dis. 2018;36(1):17–25. CrossRef
16.
Zurück zum Zitat Sørensen CG, Karlsson WK, Pommergaard HC, Burcharth J, Rosenberg J. The diagnostic accuracy of carcinoembryonic antigen to detect colorectal cancer recurrence—a systematic review. Int J Surg. 2016;25:134–44. CrossRef Sørensen CG, Karlsson WK, Pommergaard HC, Burcharth J, Rosenberg J. The diagnostic accuracy of carcinoembryonic antigen to detect colorectal cancer recurrence—a systematic review. Int J Surg. 2016;25:134–44. CrossRef
18.
Zurück zum Zitat Benson AB, Desch CE, Flynn PJ, Krause C, Loprinzi CL, Minsky BD, et al. 2000 update of American Society of Clinical Oncology colorectal cancer surveillance guidelines. J Clin Oncol. 2000;18(20):3586–8. CrossRef Benson AB, Desch CE, Flynn PJ, Krause C, Loprinzi CL, Minsky BD, et al. 2000 update of American Society of Clinical Oncology colorectal cancer surveillance guidelines. J Clin Oncol. 2000;18(20):3586–8. CrossRef
19.
Zurück zum Zitat Treasure T, Monson K, Fiorentino F, Russell C. The CEA Second-Look Trial: a randomised controlled trial of carcinoembryonic antigen prompted reoperation for recurrent colorectal cancer. BMJ Open. 2014;4(5):e4385. CrossRef Treasure T, Monson K, Fiorentino F, Russell C. The CEA Second-Look Trial: a randomised controlled trial of carcinoembryonic antigen prompted reoperation for recurrent colorectal cancer. BMJ Open. 2014;4(5):e4385. CrossRef
20.
Zurück zum Zitat Chau I, Allen MJ, Cunningham D, Norman AR, Brown G, Ford HE, et al. The value of routine serum carcino-embryonic antigen measurement and computed tomography in the surveillance of patients after adjuvant chemotherapy for colorectal cancer. J Clin Oncol. 2004;22(8):1420–9. CrossRef Chau I, Allen MJ, Cunningham D, Norman AR, Brown G, Ford HE, et al. The value of routine serum carcino-embryonic antigen measurement and computed tomography in the surveillance of patients after adjuvant chemotherapy for colorectal cancer. J Clin Oncol. 2004;22(8):1420–9. CrossRef
21.
Zurück zum Zitat Lepage C, Phelip JM, Cany L, Faroux R, Manfredi S, Ain JF, et al. Effect of 5 years of imaging and CEA follow-up to detect recurrence of colorectal cancer: the FFCD PRODIGE 13 randomised phase III trial. Dig Liver Dis. 2015;47(7):529–31. CrossRef Lepage C, Phelip JM, Cany L, Faroux R, Manfredi S, Ain JF, et al. Effect of 5 years of imaging and CEA follow-up to detect recurrence of colorectal cancer: the FFCD PRODIGE 13 randomised phase III trial. Dig Liver Dis. 2015;47(7):529–31. CrossRef
22.
Zurück zum Zitat Kahi CJ, Boland CR, Dominitz JA, Giardiello FM, Johnson DA, Kaltenbach T, et al. Colonoscopy surveillance after colorectal cancer resection: recommendations of the US multi-society task force on colorectal cancer. Gastroenterology. 2016;150(3):758–68.e11. CrossRef Kahi CJ, Boland CR, Dominitz JA, Giardiello FM, Johnson DA, Kaltenbach T, et al. Colonoscopy surveillance after colorectal cancer resection: recommendations of the US multi-society task force on colorectal cancer. Gastroenterology. 2016;150(3):758–68.e11. CrossRef
23.
Zurück zum Zitat le Clercq CM, Winkens B, Bakker CM, Keulen ET, Beets GL, Masclee AA, et al. Metachronous colorectal cancers result from missed lesions and non-compliance with surveillance. Gastrointest Endosc. 2015;82(2):325–333.e2. CrossRef le Clercq CM, Winkens B, Bakker CM, Keulen ET, Beets GL, Masclee AA, et al. Metachronous colorectal cancers result from missed lesions and non-compliance with surveillance. Gastrointest Endosc. 2015;82(2):325–333.e2. CrossRef
24.
Zurück zum Zitat Rex DK, Kahi CJ, Levin B, Smith RA, Bond JH, Brooks D, et al. Guidelines for colonoscopy surveillance after cancer resection: a consensus update by the American Cancer Society and US Multi-Society Task Force on Colorectal Cancer. CA Cancer J Clin. 2006;56(3):160–7. quiz 85–6. CrossRef Rex DK, Kahi CJ, Levin B, Smith RA, Bond JH, Brooks D, et al. Guidelines for colonoscopy surveillance after cancer resection: a consensus update by the American Cancer Society and US Multi-Society Task Force on Colorectal Cancer. CA Cancer J Clin. 2006;56(3):160–7. quiz 85–6. CrossRef
25.
Zurück zum Zitat Gomez D, Sangha VK, Morris-Stiff G, Malik HZ, Guthrie AJ, Toogood GJ, et al. Outcomes of intensive surveillance after resection of hepatic colorectal metastases. Br J Surg. 2010;97(10):1552–60. CrossRef Gomez D, Sangha VK, Morris-Stiff G, Malik HZ, Guthrie AJ, Toogood GJ, et al. Outcomes of intensive surveillance after resection of hepatic colorectal metastases. Br J Surg. 2010;97(10):1552–60. CrossRef
26.
Zurück zum Zitat Giardiello FM, Allen JI, Axilbund JE, Boland CR, Burke CA, Burt RW, et al. Guidelines on genetic evaluation and management of Lynch syndrome: a consensus statement by the US Multi-society Task Force on colorectal cancer. Am J Gastroenterol. 2014;109(8):1159–79. CrossRef Giardiello FM, Allen JI, Axilbund JE, Boland CR, Burke CA, Burt RW, et al. Guidelines on genetic evaluation and management of Lynch syndrome: a consensus statement by the US Multi-society Task Force on colorectal cancer. Am J Gastroenterol. 2014;109(8):1159–79. CrossRef
Metadaten
Titel
Evidence-based follow-up in colorectal cancer—quo vadis?
verfasst von
MBA MCI, FEBS (HPB) Assoc. Prof. Priv.-Doz. Dr. Manuel Maglione
Assoc. Prof. Priv.-Doz. Dr. Alexander Perathoner
Publikationsdatum
12.12.2019
Verlag
Springer Vienna
Erschienen in
memo - Magazine of European Medical Oncology / Ausgabe 1/2020
Print ISSN: 1865-5041
Elektronische ISSN: 1865-5076
DOI
https://doi.org/10.1007/s12254-019-00553-4