Clinicopathological characteristics of complicated colorectal cancers: a retrospective analysis over 10 years in two tertiary centers in Egypt

doi:10.21203/rs.3.rs-4921054/v1

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Clinicopathological characteristics of complicated colorectal cancers: a retrospective analysis over 10 years in two tertiary centers in Egypt

https://doi.org/10.21203/rs.3.rs-4921054/v1

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Background

The prognosis for emergency surgery for colorectal cancers (CRCs) and metastatic tumors was reported to be extremely poor. Our objective is to ascertain the clinical characteristics of patients who have been diagnosed with complications and metastases at two tertiary centers in Egypt.

Methods

a comparative retrospective study between complicated and non-complicated CRCs conducted in two tertiary centers in Egypt in 10 years.

Results

a total of 320 patients underwent surgery for CRC, of which 25% underwent emergency surgery (80 cases) and 240 (75%) patients underwent an elective one. There was a higher rate of complicated colon and non-complicated rectal cancer (P = 0.009). There was a significantly higher rate of positive L.Ns, positive LVI and PNI (P = 0.001), (P < 0.001) and (P < 0.001) respectively. In multivariate analysis, only the tumor site (right colon P = 0.010, left colon P = 0.022) as well as the LVI (P = 0.038) remained the most important predicting factors for complication. There was a significantly higher rate of OS in patients with T1 and T2 (P = 0.002), in patients with grade I and II (P = 0.005), node-negative and non-metastatic disease with (P = < 0.001) and (P = < 0.001) respectively.

Conclusion

Right and left colon cancers, along with positive lymphovascular invasion (LVI), are regarded as risk factors for surgical complications and metastases in cases of advanced stages, unfavorable grades, and node-positive tumors, leading to a poor prognosis.

CRC

complications

emergency

metastases

In recent years the incidence of colorectal cancers (CRCs) increased all over the world where it is reported to be the third most commonly diagnosed cancer. In the United States, it is considered the second most common cause of cancer-related deaths (1, 2). In Egypt, CRCs constitute 6.5% of all malignant tumors, in 2002–2003 it became the sixth recorded tumor according to the National Cancer Institute registry at Cairo University (3, 4).

Up to 15–30% of CRCs presented with large intestinal obstruction while 1–10% only presented with intestinal perforation. The sigmoid colon is the common site for obstruction (5). Emergency surgery with primary resection anastomosis for obstructed right colon cancer is the standard option of care however, the management of obstructed left-sided colon cancer is still a matter of debate either with one, two or three stages (6, 7).

Emergency surgery for complicated CRCs is reported to have a very bad prognosis than elective ones with a rate of 5-year survival between 12 and 31% in cases of obstruction and a high rate of recurrence in cases of perforation (8, 9). Papadimitriou et al., (1) concluded in their study that the advanced stage of the tumor was a prognostic risk factor for obstruction.

On the other hand, metastases due to CRCs remain the main cause of mortality where the liver is considered the primary site for metastases in up to 35–55% followed by the peritoneum where it develops in up to 1–15% and 20–50% in synchronous as well as metachronous CRCs respectively (10, 11). In addition, patients who have liver and/or peritoneal metastases will have a poorer prognosis than those who do not have (12).

This retrospective study aimed to identify the clinical characteristics of patients and the pathological features of the tumors presented with surgical complications as well as metastases in two tertiary centers in Egypt.

Study design:

It was a comparative retrospective study of all patients who underwent emergency surgery for complicated CRCs with or without metastases and those who underwent elective ones respectively that was conducted at the colorectal surgery unit (department of Surgery, Assiut University) and reviewing their postoperative data collected at the medical oncology and clinical oncology department at the main hospital and the South Egypt cancer institute (Assiut University) between 2013 and 2023.

The study was approved by the institutional review board of Assiut University Hospital (IRB: 04-2024-300345)

The study included all CRC patients operated on during the study period whose age was older than 18 years. Patients with familial cancer syndromes (hereditary nonpolyposis CRCs, familial adenomatous polyposis (FAP)) and patients known to have cancers on top of inflammatory bowel disease (IBD) were excluded.

As a prognostic factor for complicated CRCs, epidemiological, clinical and tumor factors were analyzed. The following factors were reviewed: age, sex, comorbidities and pre-operative diagnosis according to the site of the tumor and, presence or absence of liver or peritoneal metastases. Furthermore, the tumor factors were also analyzed as the pathological stage and grade of the tumor as well as the lympho-vascular and perineural invasion (PNI)

For comparison, patients were classified into two main groups: the complicated group (means CRCs associated with obstruction or perforation) whether there were metastases or not, and the non-complicated one (CRC patients underwent surgery in an elective basis without metastases or with intraoperative detection of metastases).

Diagnosis of obstructed as well as perforated CRCs was established according to the preoperative images and the post-operative histopathological reports. On the other hand, elective CRC diagnosis was obtained by reviewing the preoperative imaging, diagnostic colonoscopy, and pre-operative diagnosis of endoscopic biopsy.

Definitions and interventions:

Radical resection (R0) was defined as a central ligation (high tie) of the vascular pedicle of the tumor with en block resection of the tumor and the draining area of lymph nodes. Palliative surgery means decompression of the dilated colon by the creation of a stoma due to tumor obstruction or bypass surgery.

Emergency surgery means obstructed or perforated CRC and it was performed within the first 24 hours after admission while elective surgery was the radical surgery after colorectal preparation, and it was conducted within three to four days after admission.

The tumor is considered metastatic when hepatic and or peritoneal deposits are detected either preoperatively by image or intraoperatively during tumor evaluation (on emergency or elective basis)

Tumors proximal to the splenic flexure were considered as right-sided cancers while those distal to it a left-sided tumors. All resections were performed either as one-stage procedure (primary resection anastomosis) in cases of elective resections or as two two-stage procedures or bypass surgery in cases of emergency procedures. Right or extended right colectomy was performed for right-sided tumors, while left or extended left colectomy, anterior resection, low anterior resection (with or without diverting ileostomy), and Hartmann's colostomy was performed for left-sided cancers.

Statistical Analysis:

All statistical calculations were done using SPSS (statistical package for the social science; SPSS Inc., Chicago, IL, USA) version 22. Data were statistically described in terms of mean ± standard deviation (± SD), or median and range when not normally distributed, frequencies (number of cases), and relative frequencies (percentages) when appropriate. Comparison of quantitative variables was done using Mann Whitney U test as the data were not normally distributed. For comparing categorical data, Chi-square (χ2) test was performed. Fisher Exact test was used instead when the expected frequency was less than 5. Odds ratio (OR) with a 95% Confidence Interval (CI) and Logistic Regression was calculated for the prediction of the development of complications. Kaplan-Meier’s method with log-rank test was used for the calculation of overall survival analysis. P-value set significant at 0.05 level.

At the study period between 2013 and 2023, 320 patients underwent surgery for CRCs. Two hundred eighty-three (88.4%) were younger than 65 years old with a median age of 45 (18–96) years old and a male predominance. Abdominal pain constitutes the common presentation (41.9%) followed by chronic constipation (29.7%), bleeding per rectum (29.7%), and intestinal obstruction (12.5%). Other sporadic presentations are shown in Table 1. Adenocarcinoma was the predominant histopathology (80.8%) while squamous cell carcinoma reported in 3 (0.9%) cases only. The site, the grade, and the TNM stage of the tumors were shown in Table 1.

Table 1

Clinicopathological characteristics of CRC cases.
Clinic-pathological characteristics	N = 320
Age (years)
• Mean ± SD	46.10 ± 14.23
• Median (range)	45 (18–96)
• < 65 years	283	(88.4)
• ≥ 65 years	37	(11.6)
Sex
• Male	165	(51.6)
• Female	155	(48.4)
Clinical presentation
• Abdominal pain	134	(41.9)
• Constipation	95	(29.7)
• Bleeding per rectum	95	(29.7)
• Intestinal obstruction	40	(12.5)
• Changing bowel habit	10	(3.1)
• Diarrhea	10	(3.1)
• Vomiting	13	(4.1)
• Others
• Accidentally discovered	1	(0.3)
• Recurrent anorectal carcinoma	1	(0.3)
• Recurrent cancer colon	14	(4.4)
• Abdominal wall mass	1	(0.3)
• Recurrent sigmoid cancer	1	(0.3)
• Weight loss	7	(2.2)
• Low back pain	1	(0.3)
Pathology
• Adenocarcinoma	257	(80.8)
• Mucin adenocarcinoma	48	(15.1)
• Signet ring adenocarcinoma	10	(3.1)
• Squamous cell carcinoma	3	(0.9)
Tumor grade
• Well-differentiated	48	(15.1)
• Moderate differentiated	223	(70.1)
• Poorly differentiated	44	(13.8)
• Undifferentiated	3	(0.9)
Tumor site
• Right colon	70	(21.9)
• Left colon	73	(22.8)
• Rectum	177	(55.3)
T stage
• T2	47	(14.7)
• T3	199	(62.2)
• T4	73	(22.8)
• Tx	1	(0.3)
N stage
• N0	91	(28.4)
• N1	122	(38.1)
• N2	92	(28.7)
• N3	12	(3.8)
• Nx	3	(0.9)
M stage
• M0	208	(65.0)
• M1	112	(35.0)
Received radiotherapy	143	(45.0)
K-Ras
• Wild	56	(28.0)
• Mutant	15	(7.5)
• Not needed or not available	129	(64.5)
Emergency
• No emergency	240	(75.0)
• Emergency	80	(25.0)

Quantitative data are presented as mean ± SD or median (range), and qualitative data are presented as number (percentage).

Regarding the surgical interventions, 25% of patients underwent emergency surgery (80 cases) while elective surgery was done for 240 (75%) patients. Furthermore, Neoadjuvant radiotherapy was delivered to 143 patients out of the total cases (45%). All demographics of the studied cases are shown in Table 1.

Table 2

reports the clinicopathological characteristics between complicated and non-complicated CRC cases. There was no significant difference between complicated and non-complicated cases regarding the age, sex, tumor grade, tumor stage, and the type of K-ras gene. Moreover, there was a higher rate of complicated colon (right 27.2% and left 26.5%) cancer and non-complicated rectal cancer (63.3%) with a significant difference (P = 0.009). In addition, the complicated cases after surgery have a significantly higher rate of positive harvested L.Ns ( 80.1%), positive lymph-vascular invasion (LVI) ( 63.7%), and positive PNI (58.1%) with a p-value of P = 0.001, P < 0.001 and P < 0.001 respectively.

Table 2

Comparison between clinicopathological characteristics between complicated and non-complicated colorectal cancer cases
Clinicopathological characteristics	Non-complicated (n = 169)		Complicated (n = 151)		P value
Age (years)					0.739
• Mean ± SD	45.85 ± 13.96		46.38 ± 14.58
• Median (range)	45 (18–96)		46 (19–90)
• < 65 years	147	(87.0)	136	(90.1)	0.389
• ≥ 65 years	22	(13.0)	15	(9.9)
Sex					0.387
• Male	91	(53.8)	74	(49.0)
• Female	78	(46.2)	77	(51.0)
Tumor grade					0.244
• Well to moderate differentiated	146	(87.4)	125	(82.8)
• Poorly differentiated and undifferentiated	21	(12.6)	26	(17.2)
Tumor site					0.009
• Right colon	29	(17.2)	41	(27.2)
• Left colon	33	(19.5)	40	(26.5)
• Rectum	107	(63.3)	70	(46.4)
T stage					0.315
• Early (T2)	28	(16.6)	19	(12.6)
• Advanced (T3 + T4 + Tx)	141	(83.4)	132	(87.4)
N stage					0.001
• Negative (N0)	61	(36.1)	30	(19.9)
• Positive (N1, N2, N3, Nx)	108	(63.9)	121	(80.1)
Lymphovascular invasion (LVI)	45	(30.2)	79	(63.7)	< 0.001
Perineural invasion (PNI)	39	(26.2)	72	(58.1)	< 0.001
K-Ras*					0.500
• Wild	13	(86.7)	43	(76.8)
• Mutant	2	(13.3)	13	(23.2)

* the remaining cases don’t have K-Ras evaluation. Quantitative data are presented as mean ± SD or median (range), qualitative data are presented as number (percentage). Significance defined by p < 0.05.

Table 3 shows the characteristics of the studied groups according to their management. The age of the patients who underwent emergency surgery were less than 65 years old (96.3%) in comparison to those who underwent elective surgery (85.8%) with a significant difference (P = 0.012). Regarding sex predilection, the number of male patients who underwent emergency intervention was higher (58.8%) in contrast to females who underwent surgery in an elective setting (50.8%) without significance.

According to the clinical presentation in both groups, patients who underwent an elective surgery were presented with a higher significant abdominal pain (P < 0.001), constipation (P < 0.001), and vomiting (P = 0.044) than who underwent emergency intervention. On the other hand, intestinal obstruction was the commonest significant complication that needed emergency surgery (P < 0.001).

Table 3

Comparison between clinicopathological characteristics of the studied colorectal cancers according to their management
Clinic-pathological characteristics	Elective (n = 240)		Emergency (n = 80)		P value
Age (years)					0.325
• Mean ± SD	46.52 ± 15.04		44.83 ± 11.46
• Median (range)	45 (18–96)		45 (19–85)
• < 65 years	206	(85.8)	77	(96.3)	0.012
• ≥ 65 years	34	(14.2)	3	(3.8)
Sex					0.137
• Male	118	(49.2)	47	(58.8)
• Female	122	(50.8)	33	(41.3)
Clinical presentation
• Abdominal pain	118	(49.2)	16	(20.0)	< 0.001
• Constipation	92	(38.3)	3	(3.8)	< 0.001
• Bleeding per rectum	71	(29.6)	24	(30.0)	0.944
• Intestinal obstruction	18	(7.5)	22	(27.5)	< 0.001
• Changing bowel habit	10	(4.2)	0	(0.0)	0.072
• Diarrhea	8	(3.3)	2	(2.5)	1
• Vomiting	13	(5.4)	0	(0.0)	0.044
Tumor grade					0.036
• Well to moderate differentiated	197	(82.8)	74	(92.5)
• Poorly differentiated and undifferentiated	41	(17.2)	6	(7.5)
Tumor site					0.821
• Right colon	52	(21.7)	18	(22.5)
• Left colon	53	(22.1)	20	(25.0)
• Rectum	135	(56.3)	42	(52.5)
T stage					0.927
• Early (T2)	35	(14.6)	12	(15.0)
• Advanced (T3 + T4 + Tx)	205	(85.4)	68	(85.0)
N stage					0.520
• Negative (N0)	66	(27.5)	25	(31.3)
• Positive (N1, N2, N3, Nx)	174	(72.5)	55	(68.8)
M stage					< 0.001
• M0	138	(57.5)	70	(87.5)
• M1	102	(42.5)	10	(12.5)
Lymphovascular invasion (LVI)	100	(51.0)	24	(31.2)	0.003
Perineural invasion (PNI)	92	(46.9)	19	(24.7)	0.001
K-Ras*					0.194
• Wild	54	(30.5)	2	(8.7)
• Mutant	13	(7.3)	2	(8.7)

Regarding the pathological characteristics, 74 (92.5%) patients who underwent emergency surgery were grade I-II while unfavorable grades were detected only in 41 (17.2%) and 6 (7.5%) patients respectively with a significant difference (P = 0.036). meanwhile, there was no difference between both groups regarding the site of the tumor, K-RAS type, tumor (T), and node (N) stage. On the other hand, more than half of the patients (57.5%) who underwent an elective surgery were not metastatic while 10 (12.5%) patients who underwent an emergency intervention were presented with metastases with a higher significant difference (P = < 0.001). Lymph vascular and PNI were significantly higher in patients who underwent an elective operation (P = 0.003) and (P = 0.001) respectively as shown in Table 3.

Univariate analysis showed a significant difference between complicated and non-complicated cases about the tumor site (P = 0.009) with a higher rate of complications encountered in the right (27.2%) and left (26.5%) colon, nodal stage (P = 0.001), LVI and PNI (P = < 0.001). However, after statistical analysis with multivariate logistic regression, only the tumor site (right colon P = 0.010, left colon P = 0.022) as well as the LVI (P = 0.038) remained the most important predicting factors for complication as shown in Table 4.

Table 4

Multivariate logistic regression analysis for prediction of complicated CRC
Variables	B		Multivariate analysis
Variables	B	SE	OR	95% CI	P value
Tumor site
• Right colon	0.842	0.328	2.320	1.219–4.415	0.010
• Left colon	0.738	0.322	2.091	1.113–3.930	0.022
• Rectum			ref
N stage
• Negative			ref
• Positive	0.278	0.304	1.320	0.728–2.395	0.360
LVI
• No			ref
• Yes	0.909	0.437	2.481	1.053–5.844	0.038
PNI
• No			ref
• Yes	0.566	0.477	1.761	0.733–4.232	0.206

B: beta; SE: standard error; CI: Confidence interval; OR: Odds ratio.

The five-year overall survival (OS) according to the clinicopathological characteristics of the studied cases was calculated using the Kaplan–Meier curves with the log-rank test. There was a significantly higher rate of OS in patients with early stages T1 and T2 (P = 0.002), in patients with early grades I and II (P = 0.005), node-negative and non-metastatic disease with (P = < 0.001) and (P = < 0.001) respectively. Furthermore, patients who underwent an emergency intervention, those with a negative LVI and PNI, and who received radiotherapy have a higher rate of OS with a significant difference as shown in Fig. 1.

In the last decade, although many therapeutic interventions for CRC have been developed, the long-term survival of patients admitted with emergency complications remains unsatisfactory, due to local recurrences and metastases. In emergency surgeries, about half of the patients can benefit from resection with curative intent, however, the morbidity and the mortality are higher in comparison to the elective interventions. The 5-year survival of these patients rarely exceeds 30% even with curative surgery (13). Furthermore, about 20% of patients with CRC have metastases at the initial diagnosis, while up to half of patients with initially localized tumors will develop metastases. The methods of spread include lymphatic, hematogenous as well as peritoneal routes. The most frequent sites for metastases are regional lymph nodes, liver, lungs, and peritoneum. Although the prognosis of metastatic CRC patients has significantly improved in the past decade due to the effective surgery of liver and lung metastases as well as the novel anticancer drugs, most cases remain a non-curable disease (14).

Herein we evaluate the risk factors for complications and metastases as well as the prognosis according to these factors.

In our study, 47% of patients had presented with a type of complication related to CRC and this was in accordance with the study of Savu et al., (15) and this may be attributed to the lack of a screening program in our locality.

In our study we have a higher significant rate of complicated right and left colon cancer contrary to the higher rate of non-complicated rectal and rectosigmoid tumors, this view coincides with the recent epidemiological study which suggested that the anatomical distribution of CRC may be subjected to a shift from left to right (16).

The lymph node involvement is considered the prognostic factor which is related to the overall survival (OS) and the disease-free survival (DFS). So, patients with early stages have a 5-year survival rate of more than 75% while those with stage III or IV have a 30–60% (17). In our series, there was a higher prevalence of positive lymph nodes in the complicated than in the non -complicated group. This finding follows the results reported by previous studies (18, 19) in which they found that the complicated CRC cases had a greater rate of infiltrated LNs.

The lympho-vascular invasion and PNI are well established to be poor prognostic factors in many types of malignancies including CRC (20). There was a significantly higher rate of LVI and PNI in complicated cases in comparison to the non-complicated ones and this agreed with Wanis et al., (21) who stated that there was an association between complications of CRC and LVI as well as PNI.

Regarding the surgical intervention, 80 out of 320 patients underwent emergency surgery with a clinical presentation of pain, constipation, and vomiting in favor of the elective group which coincides with the previous studies (22, 23). On the other hand, patients who underwent emergency surgery were presented with a higher rate of intestinal obstruction as evidenced in the literature (24).

The most common site for CRC is the rectosigmoid junction followed by the left and the right colon. In our series, there were no differences regarding the location of the tumor in association with the mode of presentation and this may be due to the recent concept of increasing frequencies of the tumor in the proximal colon as reported by Rozen et al., (25).

Many studies (26, 27) examined the association between the tumor type and the mode of presentation. Pruitt et al., (26) found a reverse relation between emergency presentation and simple adenocarcinomas (83% vs 85%) but there was an association with the mucinous type (12% vs 11%) however it was unclear regarding the statistical significance. Our results were against these findings where we have a higher significant rate of emergency cases with well and moderately differentiated adenocarcinoma while elective intervention was found with poorly and undifferentiated carcinoma, this may be attributed to the small number of cases that underwent emergency surgery. Furthermore, Golder and his colleagues (28) in their systematic review and meta-analysis reported that there was an association between metastases, LVI, and PNI and the emergency presentation but this was contrary to our findings because the number of our elective cases equal to three times the number of emergent one.

The risk of emergency complications has an association with the site of the tumor. Colon obstruction frequently occurs with cancer of the left colon as reported by previous studies (15, 29). Our study confirmed this result. Meanwhile in our series, the right colon cancer was associated with complications either emergency presentation or metastases and this may be attributed to two main factors, the first is the great affinity of the right colon cancer to metastasize to the liver which is the prevalent site for CRC metastases and the second factor is the shifting paradigm of CRC from left to right as evidenced by Li & Gu (16). On the other hand, in our study the LVI was associated with complications as reported in the literature (15, 30).

Regarding survival, our study revealed that the 5 years OS was significantly better in patients with early stages, in patients with early grades, node-negative, and non-metastatic disease as evidenced by Constantin et al., (31). In addition to his reports about those with negative LVI and PNI and who received radiotherapy have a higher rate of OS that coincides with our results. On the other hand, multiple studies (32, 33) agree that emergency intervention is considered a negative prognostic factor for survival in complicated colorectal cancer but this was against our results in which we found that patients who underwent emergency surgery have a higher rate of OS and this may be due to the small number of cases which was candidate for emergency surgery in comparison to those underwent an elective intervention and was associated with metastases.

Our study included all CRC cases admitted and operated on in a colorectal surgery unit and their data from two medical oncology departments related to our university. We included all elective and emergency cases as well as metastatic and non-metastatic tumors over a period of 10 years. The limitations of our study were its retrospective nature, the small number of cases, the lack of operative data for the patients, and the incomplete information regarding microsatellite instability and other relevant biomarkers.

In conclusion, the right and left colon cancers as well as the positive LVI are considered risk factors for surgical complications and metastases with a poor prognosis in cases of advanced stages, unfavorable grades and node-positive tumors. The higher rate of complicated tumors in our study is an indication of a higher number of advanced cancers in our locality and this must make a changing paradigm for a screening program in our country. Further studies with a large sample size from different centers focusing on the genetic biomarkers are needed to detect other accused risk factors for complications

CRC colorectal cancer

LVI lympho-vascular invasion

PNI peri-neural invasion

FAP familial adenomatous polyposis

IBD inflammatory bowel disease

TNM tumor, node, metastases

LNs lymph nodes

OS overall survival

DFS disease free survival

Funding:

Not applicable

Ethics approval and consent to participate

The ethical approval for this study was obtained from research ethics committee board (IRB: 04-2024-300345)

Consent for publication

Not applicable

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No competing interests reported.

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Clinicopathological characteristics of complicated colorectal cancers: a retrospective analysis over 10 years in two tertiary centers in Egypt

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