Guideline

Ann Coloproctol 2024;40(2):89-113

pISSN: 2287-9714 • eISSN: 2287-9722
https://doi.org/10.3393/ac.2024.00059.0008

Colon cancer: the 2023 Korean clinical practice guidelines

for diagnosis and treatment
Hyo Seon Ryu1 , Hyun Jung Kim2,3 , Woong Bae Ji4 , Byung Chang Kim5 , Ji Hun Kim6 ,
Sung Kyung Moon7 , Sung Il Kang8 , Han Deok Kwak9 , Eun Sun Kim10 , Chang Hyun Kim11 ,
Tae Hyung Kim12 , Gyoung Tae Noh13 , Byung-Soo Park14 , Hyeung-Min Park11 , Jeong Mo Bae15 ,
Jung Hoon Bae16 , Ni Eun Seo17 , Chang Hoon Song18 , Mi Sun Ahn19 , Jae Seon Eo20 ,
Young Chul Yoon21 , Joon-Kee Yoon22 , Kyung Ha Lee23 , Kyung Hee Lee24 , Kil-Yong Lee25 ,
Myung Su Lee26 , Sung Hak Lee27 , Jong Min Lee28 , Ji Eun Lee29 , Han Hee Lee30 ,
Myong Hoon Ihn31 , Je-Ho Jang32 , Sun Kyung Jeon26 , Kum Ju Chae33 , Jin-Ho Choi34 ,
Dae Hee Pyo35 , Gi Won Ha36 , Kyung Su Han5 , Young Ki Hong37 , Chang Won Hong5 ,
Jung-Myun Kwak1 ; Korean Colon Cancer Multidisciplinary Committee
1
 ivision of Colon and Rectal Surgery, Department of Surgery, Korea University College of Medicine, Seoul, Korea
D
2
Department of Preventive Medicine, Korea University College of Medicine, Seoul, Korea
3
Institute for Evidence-based Medicine, Cochrane Collaboration, Seoul, Korea
4
Division of Colon and Rectal Surgery, Department of Surgery, Korea University Ansan Hospital, Ansan, Korea
5
Center for Colorectal Cancer, National Cancer Center, Goyang, Korea
6
Department of Pathology, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea
7
Department of Radiology, Kyung Hee University Hospital, Seoul, Korea
8
Department of Surgery, Yeungnam University College of Medicine, Daegu, Korea
9
Department of Surgery, Chonnam National University Hospital, Chonnam National University Medical School, Gwangju, Korea
10
Division of Gastroenterology and Hepatology, Department of Internal Medicine, Korea University College of Medicine, Seoul, Korea
11
Department of Surgery, Chonnam National University Hwasun Hospital, Chonnam National University Medical School, Hwasun, Korea
12
Department of Radiation Oncology, Nowon Eulji Medical Center, Eulji University, Seoul, Korea
13
Department of Surgery, Ewha Womans University College of Medicine, Seoul, Korea
14
Department of Surgery, Pusan National University Yangsan Hospital, Pusan National University School of Medicine, Yangsan, Korea
15
Department of Pathology, Seoul National University Hospital, Seoul, Korea
16
Division of Colorectal Surgery, Department of Surgery, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul,
Korea
17
Department of Radiology, Severance Hospital, Yonsei University College of Medicine, Seoul, Korea
18
Department of Radiation Oncology, Seoul National University Bundang Hospital, Seongnam, Korea
19
Department of Hematology-Oncology, Ajou University School of Medicine, Suwon, Korea
20
Department of Nuclear Medicine and Molecular Imaging, Korea University College of Medicine, Seoul, Korea
21
Department of General Surgery, Incheon St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea
22
Department of Nuclear Medicine and Molecular Imaging, Ajou University School of Medicine, Suwon, Korea
23
Department of Surgery, Chungnam National University Hospital, Chungnam National University College of Medicine, Daejeon, Korea
24
Department of Radiology, Seoul National University Bundang Hospital, Seongnam, Korea
25
Department of Surgery, Uijeongbu St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Uijeongbu, Korea

Received: January 20, 2024; Revised: March 11, 2024; Accepted: March 18, 2024
Correspondence to: Jung-Myun Kwak, MD, PhD
Division of Colon and Rectal Surgery, Department of Surgery, Korea University Anam Hospital, Korea University College of Medicine, 73 Goryeodae-ro,
Seongbuk-gu, Seoul 02841, Korea
Email: [email protected]

2024 Korean Society of Coloproctology

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/)
which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

www.coloproctol.org 89
 Ryu HS, et al.

26
Department of Radiology, Seoul National University Hospital, Seoul, Korea
27
Department of Hospital Pathology, Seoul St. Mary’s Hospital, College of Medicine, The Catholic University of Korea, Seoul, Korea
28
Department of Surgery, Yongin Severance Hospital, Yonsei University College of Medicine, Yongin, Korea
29
Department of Radiology, Soonchunhyang University Bucheon Hospital, Bucheon, Korea
30
Division of Gastroenterology, Department of Internal Medicine, Yeouido St. Mary’s Hospital, College of Medicine, The Catholic University of Korea,
Seoul, Korea
31
Department of Surgery, Soonchunhyang University Seoul Hospital, Soonchunhyang University College of Medicine, Seoul, Korea
32
Department of Surgery, Daejeon Eulji Medical Center, Eulji University, Daejeon, Korea
33
Department of Radiology, Jeonbuk National University Medical School, Jeonju, Korea
34
Center for Lung Cancer, Department of Thoracic Surgery, Research Institute and Hospital, National Cancer Center, Goyang, Korea
35
Department of Surgery, Samsung Medical Center, Sungkyunkwan University School of Medicine, Seoul, Korea
36
Research Institute of Clinical Medicine of Jeonbuk National University, Biomedical Research Institute of Jeonbuk National University Hospital,
Jeonju, Korea
37
Department of Surgery, National Health Insurance Service Ilsan Hospital, Goyang, Korea

Colorectal cancer is the third most common cancer in Korea and the third leading cause of death from cancer. Treatment outcomes
for colon cancer are steadily improving due to national health screening programs with advances in diagnostic methods, surgical
techniques, and therapeutic agents. The Korea Colon Cancer Multidisciplinary (KCCM) Committee intends to provide professionals
who treat colon cancer with the most up-to-date, evidence-based practice guidelines to improve outcomes and help them make deci-
sions that reflect their patients’ values and preferences. These guidelines have been established by consensus reached by the KCCM
Guideline Committee based on a systematic literature review and evidence synthesis and by considering the national health insurance
system in real clinical practice settings. Each recommendation is presented with a recommendation strength and level of evidence
based on the consensus of the committee.

Keywords: Colonic neoplasms; Diagnosis; Genetics; Therapy; Humans

INTRODUCTION METHODS

Colorectal cancer is the third most common cancer in Korea. It Methodology

accounts for 10.9% of all cancer deaths, the third highest mortality The guidelines were developed by both adapting previous guide-
rate among all cancers [1]. Treatment outcomes for colon cancer lines and de novo development through brainstorming by the
have steadily improved, with a 5-year survival rate of about 72% members of the development committee. These guidelines have 7
[2]. Various diagnostic and therapeutic approaches have been newly developed key questions (KQs) and 10 updated KQs select-
proposed in recent years. Personalized precision medicine based ed from the previous version. The systematic review followed the
on genetic information is also being pursued. However, the safety methodology outlined by Cochrane [3]. The GRADE (Grading of
and effectiveness of new treatments need to be verified. In addi- Recommendations Assessment, Development, and Evaluation)
tion, there are different views on optimal drug selection, timing, methodology was adopted to assess the quality of evidence and
treatment sequence, and duration, which need to be established determine the strength of the recommendation (SoR) [4].
based on scientific evidence. In recognition of the need for a mul-
tidisciplinary colorectal cancer guideline that reflects the latest Synthesis of evidence
knowledge in the Korean health insurance system and the actual Literature search
situation in the field, a multidisciplinary committee composed of A literature search was conducted through MEDLINE (PubMed)
experts from various medical departments specializing in colorec- using primary search terms derived through discussions with
tal cancer care was organized to develop evidence-based practice methodology experts (Supplementary Material 1). A systematic
guidelines for the diagnosis and treatment of colon cancer. literature search was conducted in MEDLINE, Embase, Cochrane,
and KoreaMed databases for articles updated since the references
used in the previous guideline version through August 2022 and
from inception until August 2022 for de novo KQs. The retrieved
articles were screened by applying inclusion and exclusion criteria

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 Ann Coloproctol 2024;40(2):89-113

in a PICOS (population, intervention, comparator, outcomes, and tation with a methodology expert and individual KQ members
study design) format by at least 2 committee members assigned to (Table 2).
each KQ. The literature selection process was reported according
to the PRISMA (Preferred Reporting Items for Systematic Reviews Formulation of recommendations
and Meta-Analyses) [5] flow diagram (Supplementary Fig. 1). Investigation of the values and preferences of the target population
A 19-question survey of health outcome priorities and preferences
Assessment of risk of bias was administered to 56 patients diagnosed and treated for colon
The quality of the literature was assessed independently by at least cancer of all stages.
2 reviewers for each KQ using assessment tools selected according
to the study design (Table 1) [6–10]. Discrepancies in the assess- Strength of recommendations
ment results were resolved by discussion. The results of the indi- Each KQ member developed draft recommendations and SoR
vidual evidence quality assessments are presented in Supplemen- based on the GRADE grid method by considering the strengths
tary Fig. 2 [11–220]. and limitations of the evidence, the magnitude and balance of
benefits and harms, patient values and preferences, physician bar-
Level of evidence riers, financial factors, and applicability in their practice setting
The level of evidence (LoE) was determined according to the using a summary of the evidence and the LoE [221] (Table 3).
GRADE group's criteria [4]. This assessment was done in consul-
Recommendation consensus
Table 1. Tools for assessing risk of bias The draft recommendations and SoR were discussed in a devel-
Study type Tool opment committee meeting and a consensus was reached through
Randomized controlled study Cochrane RoB 2 [6] a blind vote of all members conducted on August 28, 2023. The
Nonrandomized controlled study ROBINS-I [7]
internal committee recommendation grading process was attend-
Diagnostic study QUADAS-2 [8]
ed by at least 70% of all committee members. The committee’s de-
Cross-sectional study QUADAS-C [9]
Systematic review AMSTAR 2 [10] cision was deemed a consensus if at least 70% of the votes were
RoB, Risk-of-Bias Tool for Randomized Trials; ROBINS-I, Risk of Bias in cast on an individual item and at least 70% of the votes were in fa-
Nonrandomized Studies of Intervention; QUADAS, Quality Assessment vor. If less than 70% of the votes were in favor, the development
of Diagnostic Accuracy Studies; QUADAS-C, QUADAS-Comparative; committee members considered amendments and a second vote
AMSTAR, A Measurement Tool to Assess Systematic Reviews.
was taken.

Table 2. Level of evidence

Level of evidence Definition
High High evidence from a well-conducted RCT/meta-analysis with low risk of bias in study design and conduct, or from an ob-
servational study with no bias in study design or conduct and an effect size rated as very large
Moderate Evidence from an RCT/meta-analysis with bias in study design and conduct, or from an observational study with no bias in
study design or conduct and a large effect size
Low Evidence from an RCT/meta-analysis with study design and conduct flaws raised in more than one item, or from an observa-
tional study with no study design or conduct flaws
Very low Evidence from observational studies with study design and conduct flaws, case reports, or poorly systematized observational
studies
RCT, randomized controlled trial.

Table 3. Strengths of the recommendations and implications for clinical practice

Strength of recommendation Definition
Strong recommendation Strongly recommended in most clinical situations, given the benefits and harms of the treatment, level of evidence,
values and preferences, and resources
Conditional recommendation The use of these treatments may depend on the clinical situation or patient/societal values. They might be used se-
lectively or conditionally
Conditional against In some situations or conditions, implementation is not recommended because harms of the treatment may out-
weigh its benefits based on the clinical situation and/or patient/social value
Strong against It is not recommended in most clinical situations because the harms of the treatment outweigh the benefits, con-
sidering the clinical situation and/or patient/social value

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 Ryu HS, et al.

Endorsement process the direction of the recommendations and the SoRs.

External expert review
Twenty-three external experts in fields related to colon cancer di- Guideline update plan
agnosis and treatment who were not members of the development When high-quality evidence is reported on new diagnostic meth-
committee were selected to evaluate the recommendations and ods, drugs, and therapies, the guideline will be revised by adding
assess their acceptability. They reviewed the KQs, the objectivity new recommendations or revising or supplementing existing rec-
of the recommendation, the overall balance of benefits and harms ommendations. If new evidence is reported, the committee will
from the evidence assessment, recommendation direction and evaluate the evidence and discuss how to revise the recommenda-
SoR based on the strengths and limitations of the evidence. tions. If high-quality evidence is reported for un outcome with a
current recommendation, the committee will consider raising the
Public hearing LoE for that recommendation.
Public hearings were held to survey and incorporate feedback on

RESULTS

Recommendation Level of
Recommendation Method
strength evidence
Diagnosis
KQ 1. What imaging studies should be performed if liver metastases are suspected on Updated
abdominal computed tomography (CT) for staging in a patient with colon cancer?
   1-1. Liver magnetic resonance imaging (MRI) is recommended if metastases localized to the Do (strong) Low
liver are suspected or if liver resection is considered.
   1-2. When liver metastases are suspected in patients with colon cancer, positron emission Do (strong) Low
tomography (PET)-CT is recommended for radical treatment decisions.
KQ 2. Is the addition of PET-CT more effective than CT alone in patients with metastatic Updated
colon cancer?
   In patients with metastatic colon cancer, PET-CT is useful for detecting metastatic lesions not Do (strong) Very low
detected on contrast-enhanced CT. PET-CT is recommended for treatment decision-making
in metastatic colon cancer.
KQ 3. What tests can be considered for proximal colon evaluation in patients with left Updated
obstructive colon cancer where evaluating the proximal colon on preoperative colonoscopy
is difficult?
   In patients with left obstructive colon cancer where the proximal segment is difficult to evalu- Do (conditional) Very low
ate on preoperative colonoscopy, CT colonography, PET-CT, and completion colonoscopy
may be considered for proximal evaluation.
Intervention or surgery
KQ 4. Following the endoscopic resection of colorectal submucosal cancer (cT1N0M0) with a Updated
histopathologic diagnosis of completely resected (margin negative) submucosal adenocarci-
noma, what risk factors for lymph node metastasis should be considered for additional col-
ectomy?
   Further radical surgery should be considered in patients at high risk for lymph node metasta- Do (strong) Very low
sis, such as those with lymphovascular/perivascular involvement, poorly differentiated/undif-
ferentiated, deep submucosal invasion, and high-tier tumor budding, even if complete resec-
tion is achieved endoscopically.
KQ 5. Does D3 lymph node dissection or complete mesocolic excision/central vessel ligation De novo
contribute to reduced recurrence and improved survival in surgery for right-sided colorec-
tal cancer without distant metastases?
   D3 lymph node dissection or complete mesocolic excision/central vessel ligation is recom- Do (conditional) Very low
mended for nonmetastatic right-sided colon cancer.
KQ 6. Is the use of self-expanding metallic stents (SEMS) for preoperative decompression De novo
recommended in obstructive colon cancer?
   6-1. Preoperative stenting is not always recommended in operable obstructive right-sided co- Do not (conditional) Very low
lon cancer.
   6-2. Preoperative stenting in operable obstructive left-sided colon cancer may be considered in Do (conditional) Very low
selected cases.

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 Ann Coloproctol 2024;40(2):89-113

Recommendation Level of
Recommendation Method
strength evidence
Pathology
KQ 7. What is the appropriate number of lymph node examinations for proper lymph node Updated
staging of stage II and III colon cancer?
   For proper lymph node staging, the dissection and examinations of least 12 lymph nodes are Do (strong) Low
recommended for pathologic diagnosis.
KQ 8. Should microsatellite instability (MSI) testing be performed for all colon cancer pa- De novo
tients to screen for Lynch syndrome?
   MSI test is recommended for all patients with colon cancer to screen for Lynch syndrome. Do (conditional) Low
KQ 9. Is KRAS, NRAS, or BRAF gene testing necessary to determine targeted therapy for epi- Updated
dermal growth factor receptor (EGFR) as first-line chemotherapy in patients with metastat-
ic colon cancer?
  KRAS, NRAS, and BRAF genetic testing are recommended to determine the appropriateness of Do (strong) Moderate
EGFR-targeted therapy as first-line chemotherapy in patients with metastatic colon cancer.
Chemotherapy
KQ 10. Is adjuvant chemotherapy after curative resection necessary for high-risk stage II co- Updated
lon cancer patient?
   Adjuvant chemotherapy after surgery is recommended for high-risk stage II colon cancer pa- Do (conditional) Low
tients
KQ 11. Is 3 months of adjuvant chemotherapy with oxaliplatin oncologically safe for patients De novo
with stage III colon cancer compared to 6 months?
   11-1. Three months of adjuvant chemotherapy with oxaliplatin may be considered for patients Do (conditional) Low
with low-risk stage III (pT1–3N1) after colon cancer surgery.
   11-2. Three months of FOLFOX (folinic acid, fluorouracil and oxaliplatin) is not recommend- Do not (conditional) Low
ed as adjuvant chemotherapy in patients with high-risk stage III (pT4 or N2) after colon can-
cer surgery.
KQ 12. Does immunotherapy provide a better response rate in patients with metastatic colon De novo
cancer with MSI-high (MSI-H)/ MMR protein deficiency (dMMR) than conventional che-
motherapy?
   Immunotherapy is recommended for patients with MSI-H/dMMR metastatic colon cancer. Do (conditional) Low
KQ 13. In patients with locally advanced colon cancer, is the addition of neoadjuvant chemo- Updated
therapy oncologically superior to surgery alone?
   Neoadjuvant chemotherapy may be considered a treatment option for patients with locally ad- Do (conditional) Low
vanced colon cancer to reduce recurrence rates.
Resectable metastastic colon cancer
KQ 14. What is the appropriate treatment for patients with resectable colon cancer liver me- Updated
tastases?
   14-1. For theradical treatment of patients with a single colon cancer liver metastasis of 3 cm or Do (strong) Very low
less, hepatectomy is more effective than radiofrequency thermotherapy (RFA).
   14-2. In patients with resectable colon cancer liver metastases, simultaneous resection versus Do (conditional) Very low
staged resection is an option.
   14-3. In patients with resectable colon cancer liver metastases, either surgery after neoadjuvant Do (conditional) Very low
chemotherapy or upfront surgery can be considered.
KQ 15. Does pulmonary metastasectomy improve survival in patients with colon cancer lung Updated
metastasis?
   Pulmonary metastasectomy is considered for resectable colon cancer lung metastases. Do (conditional) Very low
KQ 16. Do cytoreductive surgery (CRS) and hyperthermic intraperitoneal chemotherapy De novo
(HIPEC) improve survival in patients with colon cancer with peritoneal metastases?
   CRS and selective HIPEC are recommended for patients with colon cancer with resectable Do (conditional) Low
peritoneal metastases
Unresectable metastatic colon cancer
KQ 17. Is second-line palliative chemotherapy recommended for improving survival and Updated
quality of life in patients with metastatic colon cancer after the failure of first-line pallia-
tive chemotherapy?
   Second-line palliative chemotherapy is recommended for patients with metastatic colon can- Do (conditional) Low
cer that have failed first-line palliative chemotherapy to improve survival and quality of life.

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 Ryu HS, et al.

DIAGNOSIS PET-CT has a higher diagnostic sensitivity for metastatic lesions

than contrast-enhanced CT (Supplementary Fig. 6) [44, 47, 52,
Topic: Diagnosis 60, 61, 63, 67, 71]. The concordance between PET-CT and con-
trast-enhanced CT for metastatic lesions ranges from 71% to 90%
KQ 1. What imaging studies should be performed if liver metas- for liver metastases, with the concordance being lower for extra-
tases are suspected on abdominal CT for staging in a patient with
hepatic metastases than for liver metastases [47, 58, 65, 75]. Addi-
colon cancer?
tional metastatic lesions can be detected by PET-CT. PET can also
Recommendation 1-1. detect secondary or synchronous colon cancer [57, 58, 60, 63, 67].
Liver MRI is recommended if metastases localized to the liver are PET-CT can detect additional extrahepatic metastases in 0.4 to
suspected or if liver resection is considered.
Strength of the recommendation: do (strong) 37.1% of cases compared to traditional diagnostics alone. PET-CT
Level of evidence: low results led to treatment changes in 6.8%–53.9% of colon cancer
patients [44, 47, 52, 57–75].
Recommendation 1-2.
When liver metastases are suspected in patients with colon cancer,
PET-CT is recommended for radical treatment decisions. Topic: Diagnosis
Strength of the recommendation: do (strong)
Level of evidence: low KQ 3. What tests can be considered for proximal colon evalua-
tion in patients with left obstructive colon cancer where evaluat-
ing the proximal colon on preoperative colonoscopy is difficult?
The resection of liver metastases can improve prognosis. Deter-
mining treatment intent and resectability is important [222]. Me- Recommendation 3.
In patients with left obstructive colon cancer where evaluating the
ta-analyses have indicated that MRI outperforms CT in detecting
proximal segment on preoperative colonoscopy is difficult, CT colo-
small metastatic lesions and characterizing indeterminate lesions nography, PET-CT, and completion colonoscopy may be considered
(Supplementary Figs. 3, 4) [11–18, 20–56, 223]. Therefore, MRI is for proximal evaluation.
the best option for accurately diagnosing liver metastases on a Strength of recommendation: do (conditional)
Level of evidence: very low
per-lesion basis. In situations where a treatment decision between
curative and palliative therapy is required, it is important to deter-
mine the presence or absence of distant metastases at the patient In patients with obstructive colorectal cancer where the proximal
level. PET-CT is recommended because of its high accuracy in colon could not be evaluated, CT colonography, PET-CT, and
per-patient analysis (Supplementary Fig. 5) [19, 40, 42–44, 46, 49, completion colonoscopy after stent insertion detected synchro-
50, 56]. PET-CT has the advantage of being able to accurately di- nous cancer in the proximal colon in 1.4%–15%, 4.1%– 9.7%, and
agnose distant metastases to organs other than the liver. For both 2.5%–10% of the cases, respectively, showing very high accuracy
MRI and PET-CT, patient value and preference surveys showed and leading to a change in the scope of surgery or a change in
that most patients were either in favor of additional testing or sup- treatment for those patients [76–83, 85–91, 224].
portive of it at the discretion of their physicians, indicating that CT colonography is a CT scan without the insertion of an en-
additional testing for an accurate diagnosis is supported by pa- doscope, which allows for the evaluation of the inner colon using
tients. computerized techniques. This technique can be useful when the
entire colon cannot be evaluated due to structural causes such as
Topic: Diagnosis colonic obstruction or other technical difficulties [225]. PET-CT
can detect suspected malignant lesions even when morphologic
KQ 2. Is the addition of PET-CT more effective than CT alone in variation is severe or direct histologic examination is difficult. In
patients with metastatic colon cancer?
addition to detecting proximal colorectal cancer, PET-CT can
Recommendation 2. help detect metastatic lesions. In addition, if a preoperative ab-
In patients with metastatic colon cancer, PET-CT is useful for de- dominal CT scan suggests a proximal colon lesion and a histolog-
tecting metastatic lesions not detected on contrast-enhanced CT.
ic diagnosis is needed for treatment planning, completion of the
PET-CT is recommended for treatment decision-making in meta-
static colon cancer. colonoscopy which refers to preoperative full colonoscopic evalu-
Strength of recommendation: do (strong) ation after effective stent placement with a small-diameter endo-
Level of evidence: very low scope should be considered. Its benefits may be significant.
Additional testing to evaluate the proximal colon should be

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 Ann Coloproctol 2024;40(2):89-113

considered in patients with obstructive colorectal cancer when Topic: Surgery

feasible, as the discovery of proximal lesions may alter the scope
of surgery. Failure to diagnose them may result in the need for KQ 5. Does D3 lymph node dissection or complete mesocolic ex-
cision/central vessel ligation contribute to reduced recurrence
secondary surgery or the failure of radical therapy.
and improved survival in surgery for right-sided colorectal can-
cer without distant metastases?
INTERVENTION OR SURGERY Recommendation 5.
D3 lymph node dissection or complete mesocolic excision/central
Topic: Surgery vessel ligation is recommended for surgery for nonmetastatic
right-sided colon cancer.
KQ 4. Following the endoscopic resection of colorectal submuco- Strength of recommendation: do (conditional)
sal cancer (cT1N0M0) with a histopathologic diagnosis of com- Level of evidence: very low
pletely resected (margin negative) submucosal adenocarcinoma,
what risk factors for lymph node metastasis should be considered
for additional colectomy? Meta-analysis studies showed that patients who underwent exten-
Recommendation 4. sive lymphadenectomy (D3 lymph node dissection or complete
Further radical surgery should be considered in patients at high risk mesocolic excision/central vessel ligation) had statistically signifi-
for lymph node metastasis, such as those with lymphovascular/peri- cant survival benefits over patients who did not undergo extensive
vascular involvement, poorly differentiated/undifferentiated, deep
lymphadenectomy, including longer overall survival (OS) (risk ra-
submucosal invasion, and high-tier tumor budding, even if com-
plete resection is achieved endoscopically. tio [RR], 0.78; 95% confidence interval [CI], 0.67–0.92), better
Strength of recommendation: do (strong) disease-free survival (DFS; RR, 0.68; 95% CI, 0.55–0.84), higher
Level of evidence: very low cancer-specific survival (CSS; RR, 0.27; 95% CI, 0.13–0.57), and
lower recurrence rate (RR, 0.55; 95% CI, 0.43–0.70) (Supplemen-
Submucosal cancers of the colon are those in which the infiltra- tary Fig. 8) [120–126, 128, 227–229]. However, meta-analysis
tion of cancer cells is confined to mucosal and submucosal layers. studies and prospective randomized clinical trials (RCTs) com-
The need for further radical resection has long been debated. A paring short-term postoperative outcomes between extensive
lymph node metastasis rate of around 10% has been reported lymphadenectomy and no extensive lymphadenectomy did not
[226]. Tumors are generally classified as high-risk for lymph node show significant differences in outcomes related to complications
metastasis if there is margin involvement, lymphovascular/vascu- such as anastomotic leakage, postoperative recovery, or reopera-
lar invasion, poorly differentiated/undifferentiated, deep submu- tion [230, 231]. D3 lymph node dissection or complete mesocolic
cosal involvement, or high-tier tumor budding, which has recent- excision/central vessel ligation is recommended as it has a lower
ly been reported to increase the risk of lymph node metastasis recurrence rate, a survival benefit, and minimal harm compared
[92–102, 104–113, 115–119]. The presence of each risk factor is to no extensive lymphadenectomy.
associated with a more than 3-fold increase in the odds ratio for Nonetheless, mandatory implementation of D3 lymph node
lymph node metastasis risk (Supplementary Fig. 7) [92–95, 97– dissection or complete mesocolic excision with central vessel liga-
102, 105–108, 110–112, 115, 116, 118, 119]. Therefore, we recom- tion may not be recommended for early-stage colon cancer pa-
mend radical resection with lymph node dissection in high-risk tients lacking preoperative lymph node metastases and exhibiting
patients with any 1 risk factor after endoscopic resection for sub- tumor invasion limited to the submucosal layer. Likewise, such
mucosal cancer and surveillance rather than further radical resec- procedures may be unsuitable for individuals at high surgical risk
tion in low-risk patients without all the above findings. due to advanced age or comorbidities.
Limited imaging tests are currently available to determine the
presence of lymph node metastases in colorectal cancer. When Topic: Intervention
deciding on further radical surgery, considering the patient’s gen-
KQ 6. Is the use of SEMS for preoperative decompression recom-
eral condition and risk of lymph node metastasis is recommend- mended in obstructive colon cancer?
ed. The decision should be made after full consultation with the
medical team and the patient. Recommendation 6-1.
Preoperative stenting is not always recommended in operable ob-
structive right-sided colon cancer.
Strength of recommendation: do not (conditional)
Level of evidence: very low

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Recommendation 6-2. PATHOLOGY

Preoperative stenting in operable obstructive left-sided colon cancer
may be considered in selected cases.
Topic: Pathology
Strength of recommendation: do (conditional)
Level of evidence: very low
KQ 7. What is the appropriate number of lymph node examina-
tions for proper lymph node staging of stage II and III colon can-
cer?
Meta-analysis studies showed a lower rate of stoma formation in
the SEMS group of patients with right-sided obstructive colon Recommendation 7.
For proper lymph node staging, the dissection and examinations of
cancer than in the emergency surgery (ES) group (Supplementary at least 12 lymph nodes are recommended for pathologic diagnosis.
Fig. 9) [129–136]. However, most studies had few cases of stoma Strength of recommendation: do (strong)
formation in each group. Thirty-day mortality was lower in the Level of evidence: low
SEMS arm, and there was no significant difference in the open
conversion rate (Supplementary Fig. 9) [129–136]. In terms of on- There are limitations in that each previous study had a different
cologic outcomes, 3-year DFS was higher in the SEMS arm (RR, patient population and that the number of lymph node examina-
1.23; 95% CI, 1.02–1.49; P = 0.03), while no significant difference tions was decided according to various self-criteria, making it dif-
in 5-year DFS or 5-year OS (Supplementary Fig. 10) [129, 131– ficult to conduct a comprehensive analysis. However, most studies
135]. The serious complication of bowel perforation may occur classified patients based on 12 lymph nodes. Thus, the present
during SEMS insertion, although it is not frequent. In many cases meta-analysis was performed based on 12 lymph nodes. The me-
of right-sided colon cancer, primary anastomosis without stoma ta-analysis showed a significant reduction in overall mortality
creation is possible without preoperative decompression. In clini- (hazard ratio [HR], 0.78; 95% CI, 0.72–0.85) with increases in the
cal practice, SEMS insertion is limited by the patient’s visit time, number of lymph nodes dissected (Supplementary Fig. 13) [154,
emergency level, and the human and material resources of the in- 158, 162–164]. Lee et al. [158] found reductions in the recurrence
stitution. Because the benefits of the procedure do not outweigh rate with increasing numbers of lymph nodes dissected (HR, 0.59;
the harm it may cause and the resources it requires, SEMS inser- 95% CI, 0.41–0.85). However, their study was limited by very low
tion for preoperative decompression is not always recommended quality of evidence. Patient values and preferences surveys also
for surgically curable obstructive right-sided colon cancer. suggest that patients would prefer to have more than 12 lymph
In patients with left-sided obstructive colon cancer, the SEMS nodes removed, as curing and minimizing recurrence are top pri-
group showed significantly lower rates of stoma formation and orities in colon cancer treatment.
overall complication but higher primary anastomosis rates than
the ES group (Supplementary Fig. 11) [137, 138, 140–153]. Re- Topic: Pathology
garding oncologic outcomes, the recurrence rate in the SEMS
group was significantly higher than in the ES group (RR, 1.39; 95% KQ 8. Should MSI testing be performed for all patients with co-
lon cancer to screen for Lynch syndrome?
CI, 1.09–1.78; P = 0.006) when data were analyzed by including
only RCTs. Three-year DFS, 5-year DFS, 3-year OS, and 5-year OS Recommendation 8.
showed substantial heterogeneity, although no significant differ- MSI test is recommended in all patients with colon cancer to screen
for Lynch syndrome.
ences were seen between the 2 groups (Supplementary Fig. 12)
Strength of recommendation: do (conditional)
[137, 138, 141, 142, 145, 146, 148–152, 232]. While SEMS insertion Level of evidence: low
has demonstrated superiority over ES in short-term outcomes such
as the stoma formation rate, overall complications, and primary Microsatellite instability (MSI) testing can detect abnormalities in
anastomosis rate in patients with left-sided obstructive colon can- the number of microsatellites repeats in the sequences of patients
cer, there are concerns about recurrence. A significant difference in with Lynch syndrome or sporadic tumors. It has a theoretical sen-
the recurrence rate depending on the occurrence of perforation sitivity of 100% for colon cancer caused by Lynch syndrome. In a
was reported in a SEMS group [135]. In operatively curable ob- meta-analysis, patients with positive MSI accounted for approxi-
structive left colon cancer, SEMS insertion may be considered by mately 11% of all colon cancer patients and approximately 22% of
experienced interventionists in selected patients, as adequate pre- all colon cancer patients who met the revised Bethesda guidelines
operative decompression with SEMS insertion increases the likeli- criteria and required genetic testing to confirm Lynch syndrome
hood of primary anastomosis without creating a stoma. (Supplementary Fig. 14A, B) [165–173]. Among patients ulti-

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 Ann Coloproctol 2024;40(2):89-113

mately diagnosed with Lynch syndrome after screening with MSI testing are > 95%. Thus, the likelihood of misusing targeted thera-
testing and genetic testing for confirmation, 22% did not meet the pies due to incorrect genetic testing results is low. Although there
revised Bethesda guidelines criteria (Supplementary Fig. 14C) is a cost associated with the test, 96% of patients agreed with test-
[165–167, 169, 173]. ing in a survey on patient values and preferences. A 2012–2013
In a survey of patient values and preferences, 59% of patients survey of more than 300 oncologists in 5 European countries
agreed with the use of MSI testing to screen for Lynch syndrome, found that 99.3% of the physicians performed KRAS genetic test-
30% preferred their physician’s judgment, and 7% preferred genet- ing before using anti-EGFR antibody [234].
ic testing to confirm Lynch syndrome without screening.
CHEMOTHERAPY
Topic: Pathology
Topic: Chemotherapy
KQ 9. Is KRAS, NRAS, or BRAF gene testing necessary to deter-
mine targeted therapy for EGFR as first-line chemotherapy in KQ 10. Is adjuvant chemotherapy after curative resection neces-
patients with metastatic colon cancer? sary for high-risk stage II colon cancer patients?
Recommendation 9. Recommendation 10.
KRAS, NRAS, and BRAF genetic testing are recommended to deter- Adjuvant chemotherapy after surgery is recommended for high-risk
mine the appropriateness of EGFR-targeted therapy as first-line stage II colon cancer patients.
chemotherapy in patients with metastatic colon cancer. Strength of recommendation: do (conditional)
Strength of recommendation: do (strong) Level of evidence: low
Level of evidence: moderate

Meta-analysis results in this study confirmed a difference in pro- High-risk stage II colon cancer is defined as having at least one of
gression-free survival (PFS) with the use of anti-EGFR antibody in the following risk factors: T4 tumor, bowel obstruction or perfo-
both KRAS wide type (WT) and mutant type (MT) tumors. In ration, lymphatic or vascular invasion, perineural invasion, lymph
KRAS WT, the use of anti-EGFR antibody was associated with PFS node yield of fewer than 12, poorly differentiated tumor, and pos-
benefits (HR, 0.66; 95% CI, 0.58–0.74) and OS (HR, 0.76; 95% CI, itive margins. In high-risk stage II colon cancer, when comparing
0.67–0.86). In MT tumors, the use of targeted therapy adversely af- the adjuvant chemotherapy group to the surgery alone group, a
fected PFS (HR, 1.22; 95% CI, 1.06–1.41) with no significant dif- statistically significant increase in OS was seen (HR, 0.62; 95% CI,
ference in OS. The survival benefit of using anti-EGFR antibody 0.46–0.95) but no significant difference in DFS (HR, 0.76; 95% CI,
based on KRAS testing was 24% for OS and 22% to 34% for PFS 0.57–1.02) or recurrence-free survival (RFS; HR, 1.01; 95% CI,
(Supplementary Fig. 15A, B) [174, 175, 177, 178]. Targeted therapy 0.79–1.29) (Supplementary Fig. 16A–C) [181–187, 235]. One pro-
had PFS benefits in NRAS WT tumors (HR, 0.72; 95% CI, 0.58– spective study reported adverse effects of adjuvant chemotherapy
0.89) and OS (HR, 0.77; 95% CI, 0.64–0.93), while in NRAS MT, after surgery for high-risk stage II colon cancer that included ele-
there was no significant difference in PFS or OS (Supplementary vated alanine aminotransferase and aspartate aminotransferase
Fig. 15C) [176]. The survival benefit of using anti-EGFR antibody levels, decreased appetite, diarrhea, and nausea (Supplementary
with NRAS testing was 23% for OS and 28% for PFS. Fig. 16D) [186]. However, the number of events was low. In addi-
Analyses showed that BRAF WT had superior PFS and OS in tion, such risks were not thought to outweigh the survival benefit.
patients treated with targeted therapies compared to MT (Supple- Curing and minimizing recurrence were top priorities for patients
mentary Fig. 15D) [179, 180]. However, these studies did not in the survey, with 86% of all respondents agreeing that they
compare outcomes with and without targeted therapies. Thus, the would accept the adverse effects of chemotherapy to improve sur-
survival benefit associated with BRAF testing and using targeted vival outcomes.
therapies is unknown. An analysis of randomized studies of RAS-
WT/BRAF-MT patients found no difference in OS or PFS with or Topic: Chemotherapy
without anti-EGFR antibody treatment [233]. These results sug-
gest that BRAF genetic testing can be used as a rationale for avoid- KQ 11. Is 3 months of adjuvant chemotherapy with oxaliplatin
oncologically safe for patients with stage 3 colon cancer com-
ing targeted therapies in BRAF MT patients undergoing first-line pared to 6 months?
chemotherapy.
The sensitivity and specificity of both RAS and BRAF genetic

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 Ryu HS, et al.

Recommendation 11-1. Fig. 18B) [194]. Quality of life was significantly better in the pem-
Three months of adjuvant chemotherapy with oxaliplatin may be brolizumab arm (Supplementary Fig. 18C) [193]. Phase II studies
considered for patients with low-risk stage III (pT1–3N1) after co- and retrospective studies also showed improved survival with im-
lon cancer surgery.
munotherapy in patients with MSI-H/dMMR metastatic colon
Strength of recommendation: do (conditional)
Level of evidence: low cancer. PFS rates of 13 months and OS of 47 months were report-
ed with pembrolizumab or nivolumab, whereas PFS of 6 to 7
Recommendation 11-2. months and OS of 13 to 28 months were reported with a conven-
Three months of FOLFOX is not recommended as adjuvant chemo-
therapy for patients with high-risk stage III (pT4 or N2) after colon tional chemotherapy [195, 239–242].
cancer surgery. In the Keynote-177 study, the incidence of grade 3 or higher
Strength of recommendation: do not (conditional) treatment-related adverse events was also significantly lower in the
Level of evidence: low
pembrolizumab arm (22% vs. 66%; RR, 0.30; 95% CI, 0.22–0.42)
(Supplementary Fig. 18A) [194]. The CheckMate 142 and Key-
Meta-analysis showed that in patients with stage III colon cancer, note-164 studies also reported less frequent adverse events in the
3 months of adjuvant chemotherapy significantly reduced the in- pembrolizumab arm than in the conventional chemotherapy arm
cidence of peripheral neuropathy without compromising OS [195, 239]. Thus, immunotherapy can reduce treatment harm and
compared to 6 months of adjuvant chemotherapy (Supplementary improve survival and quality of life, consistent with patient values.
Fig. 17A, B) [188, 192, 236, 237]. While RFS was not significantly However, in Korea, immunotherapy for metastatic colon cancer
different between 3 or 6 months of CAPOX (capecitabine and ox- is not covered by national health insurance. In addition, it is ex-
aliplatin) or FOLFOX in patients with low-risk stage III, 3 months pensive, resulting in economic inequalities. For this reason, we
of FOLFOX led to inferior outcomes in patients with high-risk reached a consensus with a conditional recommendation. If the
stage III (HR, 1.37; 95% CI, 1.11–1.69) (Supplementary Fig. 17C) national health insurance system changes its policy in the future,
[189–191, 238]. Therefore, adjuvant chemotherapy for 3 months the SoR may be upgraded.
is preferred for patients with low-risk stage III, showing a signifi-
cant reduction in peripheral neuropathy without affecting surviv- Topic: Chemotherapy
al outcome. In high-risk stage III, FOLFOX showed a clear disad-
vantage in RFS despite a reduction in peripheral neuropathy. KQ 13. In patients with locally advanced colon cancer, is the ad-
dition of neoadjuvant chemotherapy oncologically superior to
Therefore, FOLFOX for 3 months is not recommended given its surgery alone?
oncologic hazard.
Recommendation 13.
Neoadjuvant chemotherapy may be considered a treatment option
Topic: Chemotherapy in patients with locally advanced colon cancer to reduce recurrence
rates.
KQ 12. Does immunotherapy provide better response rates in Strength of recommendation: do (conditional)
patients with metastatic colon cancer with MSI-H/dMMR than Level of evidence: low
conventional chemotherapy?

Recommendation 12. A randomized phase III study has compared 6 weeks of neoadju-
Immunotherapy is recommended for patients with MSI-H/dMMR
vant chemotherapy followed by surgery to 18 or 24 weeks of adju-
metastatic colon cancer.
Strength of recommendation: do (conditional) vant chemotherapy following surgery in patients with colon can-
Level of evidence: low cer clinically staged as T3–4, N0–2, or M0 on imaging studies.
The study found that residual disease or recurrence rates at 2
Keynote-177, a randomized phase III study, compared immuno- years were significantly lower in the neoadjuvant chemotherapy
therapy (pembrolizumab) with conventional chemotherapy (FOLF- group (16.9% vs. 21.5%; RR, 0.72; 95% CI, 0.54–0.98), although
OX or FOLFIRI [folinic acid, fluorouracil, and irinotecan] ± beva- there was no difference in OS or CSS (Supplementary Fig. 19A)
cizumab or cetuximab) [194]. PFS (HR, 0.59; 95% CI, 0.45–0.79) [196]. No statistically significant differences in postoperative com-
and the overall response rate (RR, 1.36; 95% CI, 1.02–1.81) were plications, including anastomotic leakage and intra-abdominal
significantly improved in the pembrolizumab arm (Supplementary abscess were seen (Supplementary Fig. 19B) [196]. In a survey of
Fig. 18A, B) [194]. However, OS was not significantly different be- patient values and preferences, 36% agreed with preoperative che-
tween the 2 groups (HR, 0.74; 95% CI, 0.53–1.03) (Supplementary motherapy and 59% said it depended on their surgeon’s judgment.

98 https://doi.org/10.3393/ac.2024.00059.0008
 Ann Coloproctol 2024;40(2):89-113

Given the lack of evidence for neoadjuvant chemotherapy in on the effectiveness and side effects of those modalities.
nonmetastatic colon cancer and the limitations of the radiologic Whether simultaneous resection is more effective than staged
diagnosis of lymph node metastases, overtreatment in node-nega- resection remains inconclusive, with both approaches being used
tive patients is a concern. Thus, patients selection should be done in real-world practice. OS and DFS were not significantly different
carefully. between simultaneous versus staged resection. Simultaneous re-
Although neoadjuvant chemotherapy has an unclear survival section was not associated with a higher risk of complications
benefit, it was shown to reduce recurrence rates. In a comparison compared to staged resection in a prospective randomized study
of groups that did and did not receive neoadjuvant chemotherapy, (Supplementary Fig. 21) [197, 198, 204, 209]. Patient values and
no significant differences were found in terms of postoperative preferences surveys also showed that minimizing recurrence
complications, overall treatment duration, or cost, supporting the (43.0%) and the surgeon’s judgment (39.3%) were the most im-
option of preoperative chemotherapy in select patients with local- portant factors in deciding the timing of surgery. Clinically, the
ly advanced colon cancer to reduce recurrence rates. decision between simultaneous and staged resection can be made
selectively based on clinical settings.
RESECTABLE METASTATIC COLON CANCER No statistical difference in 3-year DFS, 5-year DFS, or 5-year
OS was found in a comparison of surgery after neoadjuvant che-
Topic: Resectable liver metastases motherapy versus upfront surgery (Supplementary Fig. 22A) [84,
200, 201, 206–208]. Postoperative complications tended to be
KQ 14. What is the appropriate treatment for patients with re-
higher in the surgery after neoadjuvant chemotherapy group than
sectable colon cancer liver metastases?
in the upfront surgery group. However, the difference did not ap-
Recommendation 14-1. pear to be significant, although some studies reported the con-
For the radical treatment of patients with a single colon cancer liver trary results (Supplementary Fig. 22B) [201, 202, 206–208]. In a
metastasis of 3 cm or less, hepatectomy is more effective than RFA.
Strength of recommendation: do (strong) survey of patient values and preferences, 26.8% responded that
Level of evidence: very low they would like to reduce the extent of surgery by receiving neo-
adjuvant chemotherapy, and 51.8% agreed that it was up to their
Recommendation 14-2.
surgeon. Surgery after neoadjuvant chemotherapy has the advan-
In patients with resectable colon cancer liver metastases, simultane-
ous resection versus staged resection is an option. tage of confirming chemosensitivity. However, it may make it
Strength of recommendation: do (conditional) more difficult to locate the lesion and increase the risk of postop-
Level of evidence: very low erative complications. There is no difference in benefits or risks.
Recommendation 14-3. Thus, either treatment can be chosen depending on the patient’s
In patients with resectable colon cancer liver metastases, either sur- condition.
gery after neoadjuvant chemotherapy or upfront surgery can be
considered.
Strength of recommendation: do (conditional) Topic: Resectable lung metastases
Level of evidence: very low
KQ 15. Does pulmonary metastasectomy improve survival in pa-
tients with colon cancer lung metastasis?
All previous studies comparing hepatectomy and RFA were all ret-
rospective. Because RFA was performed in high-risk patients, the Recommendation 15.
results regarding treatment complications and survival outcomes Pulmonary metastasectomy is considered for patients with resect-
able colon cancer lung metastases.
should be cautiously interpreted [199, 203, 205]. The local recur-
Strength of recommendation: do (conditional)
rence rate was significantly lower in the resection group than in the Level of evidence: very low
RFA group (RR, 0.14; 95% CI, 0.05–0.38) (Supplementary Fig. 20)
[199, 203, 205]. Although few major complications have been re- Studies on pulmonary metastasectomy for colon cancer are scarce
ported, it is difficult to conclude treatment-related harms due to because the patient population is heterogeneous, with different
bias in subject selection. Given the local recurrence rate, resection indications for local and systemic treatment depending on the
is the treatment of choice for resectable colon cancer liver metasta- number and extent of metastases at diagnosis. Two treatments are
ses. Other modalities such as RFA, stereotactic body radiation often combined in practice. Nevertheless, pulmonary metastasec-
therapy, microwave ablation, and cryoablation may be considered tomy for colon cancer is widely performed in clinical practice. A
depending on surgical risk. However, there is insufficient evidence meta-analysis showed a trend toward better survival in patients

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 Ryu HS, et al.

who underwent lung resection compared to patients treated UNRESECTABLE METASTATIC COLON
without surgical resection (RR, 0.72; 95% CI, 0.51–1.03; P = 0.07) CANCER
(Supplementary Fig. 23A) [211–213], although the difference was
not statistically significant. Median survival was significantly lon- Topic: Palliative chemotherapy
ger in patients who underwent resection than in patients treated
KQ 17. Will second-line palliative chemotherapy improve surviv-
without surgical resection (RR, 0.76; 95% CI, 0.01–1.42; P = 0.02)
al and quality of life in patients with metastatic colon cancer after
(Supplementary Fig. 23B) [210, 211]. the failure of first-line palliative chemotherapy?
Pulmonary metastasectomy can be considered if the primary
lesion has already been resected or is planned to be resected, pul- Recommendation 17.
Second-line palliative chemotherapy is recommended for patients
monary function is good, the risk of lung resection is low, and with metastatic colon cancer that have failed first-line palliative che-
pulmonary metastatic lesions are resectable. motherapy to improve survival and quality of life.
Strength of recommendation: do (conditional)
Level of evidence: low
Topic: Resectable peritoneal metastasis

KQ 16. Do CRS and HIPEC improve survival in patients with co- In metastatic colorectal cancer patients with disease progression
lon cancer with peritoneal metastases?
after first-line palliative chemotherapy, treatment with irinotecan
Recommendation 16. significantly improved survival compared with best supportive
CRS and selective HIPEC are recommended for patients with colon care (RR, 1.7; 95% CI, 1.24–2.35) (Supplementary Fig. 26A) [216].
cancer with resectable peritoneal metastases.
Chemotherapy was also associated with fewer tumor-related side
Strength of recommendation: do (conditional)
Level of evidence: low effects and better quality of life, although it showed side effects
(Supplementary Fig. 26B, C) [216]. In patients with metastatic co-
Patients with colorectal cancer with peritoneal metastases typical- lon cancer who have failed first-line palliative chemotherapy, the
ly are not expected to survive more than one year without treat- priority in deciding on second-line palliative chemotherapy is to
ment. However, even palliative chemotherapy can improve medi- improve survival and quality of life. Therefore, second-line che-
an survival from 12 months to 16 months [243]. Several studies motherapy should be considered for patients with metastatic col-
demonstrated a significant survival benefit for patients who un- orectal cancer.
derwent CRS followed by HIPEC compared to palliative chemo-
therapy (HR, 0.55; 95% CI, 0.32–0.95) (Supplementary Fig. 24A) CONCLUSION
[215, 217–220]. When the incidence of grade 3 or higher compli-
cations was compared, no significant difference was seen between These guidelines emphasize the importance of a personalized
CRS followed by HIPEC and palliative chemotherapy (Supple- treatment plan based on a multidisciplinary approach to the man-
mentary Fig. 24B) [219]. agement of colon cancer that takes the patient’s values, preferenc-
However, the results recently reported from a phase III trial and es, and the evolving landscape of diagnostic and treatment options
prospective study that analyzed the effectiveness of CRS followed into consideration.
by HIPEC versus CRS alone in colorectal cancer with peritoneal The recommended surgical technique for nonmetastatic
metastases showed no additional survival benefit in patients who right-sided colon cancer is complete mesocolic excision/central
received CRS with oxaliplatin-based HIPEC compared to the CRS vessel ligation to reduce recurrence and improve survival out-
alone group (Supplementary Fig. 25A) [214, 244]. In a compari- comes. At least 12 lymph nodes should be examined for lymph
son of grade 3 or higher complications between the 2 groups, no node staging. In the management of obstructive colon cancer, de-
difference in the rate of complications within 30 days was seen compression with preoperative stenting is not always necessary
(Supplementary Fig. 25B) [214]. Therefore, in patients with colon for right-sided colon cancer. However, it is recommended for
cancer with resectable peritoneal metastases, CRS should be the left-sided colon cancer for adequate decompression with SEMS
cornerstone of treatment. The effectiveness of HIPEC remains insertion. Adjuvant chemotherapy is recommended for patients
unclear. Considering that high morbidity and mortality are asso- with high-risk stage II and III after surgery. In low-risk stage III, 3
ciated with CRS, it is important to select candidates who might months of adjuvant chemotherapy with oxaliplatin may also be
achieve the best outcomes. considered.
For metastatic colon cancer, liver MRI or PET is recommended

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 Ann Coloproctol 2024;40(2):89-113

to determine resectability and radical treatment decision. MSI Author contributions

testing and KRAS, NRAS, or BRAF gene testing are required when Conceptualization: HSR, JMK, HJK, WBJ, BCK, JHK, SKM; Data
considering various treatment options. Resection may be consid- curation: all authors; Formal analysis: HJK; Funding acquisition:
ered for resectable liver or lung metastases. CRS and selective JMK; Investigation: all authors; Methodology: HJK, WBJ; Project
HIPEC are recommended for resectable peritoneal metastases. administration: JMK, HJK; Visualization: all authors; Writing–
Immunotherapy provides better response rate than conventional original draft: all authors; Writing–review & editing: HSR, JMK.
chemotherapy in metastatic colon cancer patients with MSI-H/ All authors read and approved the final manuscript.
dMMR.
Supplementary materials
ARTICLE INFORMATION Supplementary Material 1. Literature search terms for each key
questions (KQs).
Disclaimer Supplementary Fig. 1. PRISMA (Preferred Reporting Items for
The 2023 Colon Cancer Korean Clinical Practice Guidelines are Systematic Reviews and Meta-Analyses) flowchart for each key
intended to guide the clinical practice of colon cancer based on questions (KQs).
published medical evidence for diagnosis and treatment. In actual Supplementary Fig. 2. Risk of bias assessment for each key ques-
clinical practice, the specific treatment of various clinical situa- tions (KQs) using QUADAS-2 (Quality Assessment of Diagnostic
tions may differ from these guidelines. The guidelines should not Accuracy Studies 2), QUADAS-C (QUADAS-Comparative),
interfere with or limit them. These guidelines do not have legal ROBINS-I (Risk of Bias in Nonrandomized Studies of Interven-
status. They are not binding. Users are responsible for patient out- tion), and Cochrane RoB 2 (Risk-of-Bias Tool for Randomized
comes in actual clinical practice. Trials 2).
Supplementary Fig. 3. Forest plots of (A) per-patient and (B)
Conflict of interest per-lesion sensitivity and specificity of computed tomography for
Je-Ho Jang is an Editorial Board member of Annals of Coloproctol- detecting liver metastasis.
ogy, but was not involved in in the peer reviewer selection, evalua- Supplementary Fig. 4. Forest plots of (A) per-patient and (B)
tion, or decision process of this article. To identify other potential per-lesion sensitivity and specificity of magnetic resonance imag-
conflicts of interest for all members who participated in the devel- ing for detecting liver metastasis.
opment of guidelines, we examined whether they were employed Supplementary Fig. 5. Forest plots of (A) per-patient and (B)
by a related company, received sponsorship or honoraria of more per-lesion sensitivity and specificity of FDG positron emission to-
than KRW 10 million, conducted research funded by a specific mography–computed tomography for detecting liver metastasis.
institution or pharmaceutical company or received rights to eco- Supplementary Fig. 6. Forest plots of sensitivity and specificity of
nomic benefits, or had intellectual property rights such as patents (A) positron emission tomography–computed tomography and
or royalties in the last 2 years. No potential conflict of interest rel- (B) computed tomography for detecting metastatic lesions.
evant to this article was reported. Supplementary Fig. 7. Forest plots for the association between
lymph node metastasis and (A) lymphovascular invasion, (B) dif-
Funding ferentiation, (C) depth of invasion ( ≥ 1,000 μm), and (D) tumor
This guideline was developed with research funding provided by budding.
the National Cancer Guidelines Initiative, and the financial sup- Supplementary Fig. 8. Forest plots of 3- and 5-year (A) recur-
port had no direct or potential influence on the content or process rence rate, (B) disease-free survival, (C) overall survival, and (D)
of the guideline. The multidisciplinary committee, which includ- cancer-specific survival in extensive lymphadenectomy (D3
ed representation from 13 relevant societies, was independent of lymph node dissection or complete mesocolic extension/central
financial support. This work was also supported by the Research vessel ligation) versus no extensive lymphadenectomy for
Fund of National Cancer Center (Goyang, Korea) (No. NCC- right-sided colon cancer.
2112570-3). Supplementary Fig. 9. Forest plots of (A) the stoma formation
rate, (B) 30-day mortality, and (C) open conversion rate in self-ex-
Acknowledgments panding metallic stents versus emergency surgery for right-sided
The authors thank the Korean Cancer Management Guideline obstructive colon cancer.
Network (KCGN) for the technical support. Supplementary Fig. 10. Forest plots of (A) the R0 resection rate,

https://doi.org/10.3393/ac.2024.00059.0008 101
 Ryu HS, et al.

(B) 3-year disease-free survival, (C) 5-year disease-free survival, Supplementary Fig. 21. Forest plots of (A) oncologic outcomes
and (D) 5-year overall survival in self-expanding metallic stents and (B) postoperative complications in simultaneous versus
versus emergency surgery for right-sided obstructive colon cancer. staged resection in patients with resectable colon cancer liver me-
Supplementary Fig. 11. Forest plots of (A) the stoma formation tastases.
rate, (B) primary anastomosis rate, (C) overall complication rate, Supplementary Fig. 22. Forest plots of (A) oncologic outcomes
and (D) 30-day mortality in self-expanding metallic stents versus and (B) postoperative complications in upfront surgery versus
emergency surgery for left-sided obstructive colon cancer. surgery following neoadjuvant chemotherapy in patients with re-
Supplementary Fig. 12. Forest plots of (A) 3-year disease-free sectable colon cancer liver metastases.
survival (DFS), (B) 3-year overall survival (OS), (C) 5-year DFS, Supplementary Fig. 23. Forest plots of (A) overall survival and
(D) 5-year OS, and (E) recurrence rate in self-expanding metallic (B) median overall survival in patients with pulmonary metasta-
stents versus emergency surgery for left-sided obstructive colon sectomy with resectable colon cancer pulmonary metastases.
cancer. Supplementary Fig. 24. Forest plots of (A) overall survival and
Supplementary Fig. 13. Forest plot of overall and disease-free (B) adverse events in patients with colorectal cancer peritoneal
survival in lymph node yields of more than 12 versus less than 12. metastasis receiving cytoreductive surgery and hyperthermic in-
Supplementary Fig. 14. Forest plots of (A) microsatellite instabil- traperitoneal chemotherapy versus palliative chemotherapy.
ity/mismatch repair deficiency positivity, (B) positivity for revised Supplementary Fig. 25. Forest plots of (A) overall survival and
Bethesda guidelines for Lynch syndrome in colon cancers, and (C) (B) adverse events in patients with colorectal cancer peritoneal
false-negative rate of revised Bethesda guidelines in genetically metastasis receiving cytoreductive surgery and hyperthermic in-
confirmed Lynch syndrome patients. traperitoneal chemotherapy versus cytoreductive surgery alone.
Supplementary Fig. 15. Forest plots of progression-free survival Supplementary Fig. 26. Forest plots of (A) overall survival, (B)
(PFS) and overall survival (OS). (A) PFS and (B) OS according to quality of life, and (C) adverse events in second-line palliative
KRAS status. (C) PFS and OS according to NRAS status. (D) PFS chemotherapy for metastatic colon cancer after failure of first-line
and OS according to BRAF status. palliative chemotherapy.
Supplementary Fig. 16. Forest plots of (A) disease-free survival, Supplementary materials are available from https://doi.org/
(B) recurrence-free survival, (C) overall survival, and (D) adverse 10.3393/ac.2024.00059.0008.
effects in patients receiving adjuvant chemotherapy versus no ad-
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