Wu ZJ, Lan B, Luo J, Ameti A, Wang H, Hu QY. Impact of preoperative inflammatory and nutritional markers on the prognosis of patients with peritoneal metastasis of colorectal cancer. World J Gastrointest Oncol 2024; 16(9): 3865-3874 [DOI: 10.4251/wjgo.v16.i9.3865]
Corresponding Author of This Article
Qiong-Yu Hu, MD, Department of Anesthesiology, The Sixth Affiliated Hospital, Sun Yat-sen University, No. 26 Yuancun Road, Tianhe District, Guangzhou 510000, Guangdong Province, China. huqy@mail.sysu.edu.cn
Research Domain of This Article
Gastroenterology & Hepatology
Article-Type of This Article
Retrospective Study
Open-Access Policy of This Article
This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Zhi-Jie Wu, Bing Lan, Jian Luo, Hui Wang, Qiong-Yu Hu, Department of General Surgery (Colorectal Surgery), The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou 510655, Guangdong Province, China
Zhi-Jie Wu, Bing Lan, Jian Luo, Hui Wang, Qiong-Yu Hu, Guangdong Provincial Key Laboratory of Colorectal and Pelvic Floor Diseases, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou 510655, Guangdong Province, China
Zhi-Jie Wu, Bing Lan, Jian Luo, Hui Wang, Qiong-Yu Hu, Biomedical Innovation Center, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou 510655, Guangdong Province, China
Ayniyazi Ameti, Department of Anesthesiology, Kashgar First People’s Hospital, Kashgar 844000, Xinjiang Uygur Autonomous Region, China
Qiong-Yu Hu, Department of Anesthesiology, The Sixth Affiliated Hospital, Sun Yat-sen University, Guangzhou 510000, Guangdong Province, China
Co-corresponding authors: Hui Wang and Qiong-Yu Hu.
Author contributions: Wu ZJ and Wang H contributed to the study concept and design; Wu ZJ, Lan B, Luo J, and Ameti A participated in the analysis and interpretation of data; Wu ZJ and Lan B drafted the manuscript; Wang H and Hu QY contributed to the revision of the manuscript; and all authors approved the manuscript. Wu ZJ and Lan B are co-first authors of the manuscript. They contribute equally to data analysis and article writing. Wang H and Hu QY are co-corresponding authors of the manuscript. They contribute equally to the revision of the manuscript.
Institutional review board statement: All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later. The study was approved by the Sixth Affiliated Hospital, Sun Yat-sen University, No. 2020ZSLYEC-109.
Informed consent statement: All patients provided written informed consent to participate.
Conflict-of-interest statement: All the authors report no relevant conflicts of interest for this article.
Data sharing statement: All the data are available without resection. Researchers can obtain data by contacting the corresponding.
Open-Access: This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: https://creativecommons.org/Licenses/by-nc/4.0/
Corresponding author: Qiong-Yu Hu, MD, Department of Anesthesiology, The Sixth Affiliated Hospital, Sun Yat-sen University, No. 26 Yuancun Road, Tianhe District, Guangzhou 510000, Guangdong Province, China. huqy@mail.sysu.edu.cn
Received: January 31, 2024 Revised: June 10, 2024 Accepted: July 16, 2024 Published online: September 15, 2024 Processing time: 222 Days and 7.7 Hours
Abstract
BACKGROUND
Identifying patients with peritoneal metastasis (PMs) of colorectal cancer (CRC) who will benefit from cytoreductive surgery and hyperthermic intraperitoneal chemotherapy is crucial before surgery. Inflammatory and nutritional indicators play essential roles in cancer development and metastasis.
AIM
To investigate the association of preoperative inflammatory and nutritional markers with prognosis in patients with CRC-PM.
METHODS
We included 133 patients diagnosed with CRC-PM between July 2012 and July 2018. Patients’ demographics, overall survival (OS), and preoperative inflammatory and nutritional markers were evaluated. The Kaplan-Meier method and log-rank test were used to estimate differences.
RESULTS
Of the 133 patients, 94 (70.6%) had normal hemoglobin (Hb) and 54 (40.6%) had a high neutrophil-to-lymphocyte ratio (NLR). The median OS (mOS) was significantly lower for patients with high NLR (7.9 months) than for those with low NLR (25.4 months; P = 0.002). Similarly, patients with normal Hb had a longer mOS (18.5 months) than those with low Hb (6.3 months; P < 0.001). Multivariate analysis identified age, carbohydrate antigen 199 levels, NLR, Hb, and peritoneal cancer index as independent predictors of OS. Based on these findings, a nomogram was constructed, which demonstrated a good capacity for prediction, with a C-index of 0.715 (95% confidence interval: 0.684-0.740). Furthermore, the 1- and 2-year survival calibration plots showed good agreement between predicted and actual OS rates. The areas under the curve for the 1- and 2-year survival predictions of the nomogram were 0.6238 and 0.6234, respectively.
CONCLUSION
High NLR and low Hb were identified as independent predictive risk factors for poor prognosis in patients with CRC-PM. The established nomogram demonstrated high accuracy in predicting OS for patients with CRC-PM, indicating its potential as a valuable prognostic tool for this patient population.
Core Tip: The clinical data of single-center patients in our hospital were analyzed retrospectively. High neutrophil-to-lymphocyte ratio and low hemoglobin are independent predictive risk factors for poor prognosis in patients with peritoneal metastasis of colorectal cancer. The established nomogram predicted the overall survival of patients with colorectal cancer having peritoneal metastasis with high accuracy, indicating its usefulness as a valuable prognostic tool for the designated patient cohort.
Citation: Wu ZJ, Lan B, Luo J, Ameti A, Wang H, Hu QY. Impact of preoperative inflammatory and nutritional markers on the prognosis of patients with peritoneal metastasis of colorectal cancer. World J Gastrointest Oncol 2024; 16(9): 3865-3874
Recurrence and metastasis are the primary factors contributing to mortality in patients with colorectal cancer (CRC), with the peritoneum being the third most common site of metastasis, following liver and lung metastases[1,2]. Previously, palliative treatment was the only available strategy for managing peritoneal metastasis (PM), as it was considered an advanced stage of the disease with a poor prognosis[3]. However, research since the 1990s has indicated that combining cytoreductive surgery (CRS) and hyperthermic intraperitoneal chemotherapy (HIPEC) is the most effective treatment for CRC-PM and significantly increases disease-free survival and prolongs overall survival (OS)[4]. The median OS (mOS) of patients with CRC-PM treated with CRS/HIPEC was 41.7 months compared with only 13 months for those treated with palliative chemotherapy[5,6].
However, CRS/HIPEC carries a risk of complications: Mortality rates range from 0% to 8%, and complication rates can be as high as 64%[7]. Moreover, French multicenter registries report a 34% incidence of grade 3 or 4 complications[8]. Postoperative and severe complications are also considered independent risk factors for poor survival outcomes[9]. Therefore, identifying patients who will benefit from CRS/HIPEC is crucial before surgery.
Both inflammatory and nutritional indicators are known to influence cancer development and metastasis. In solid tumors, inflammatory markers such as the lymphocyte-monocyte ratio, neutrophil-to-lymphocyte ratio (NLR), and platelet-to-lymphocyte ratio have been extensively utilized. NLR is considered a more accurate prognostic indicator[10-12]. Patients with cancer frequently have anemia due to inflammation from prolonged immunological activation[13]. Furthermore, nutritional markers such as albumin and hemoglobin (Hb) are associated with cancer prognosis[14,15]. This study aimed to investigate the association between nutritional markers (Hb) and inflammatory markers (NLR) and the prognosis of patients with CRC-PM.
MATERIALS AND METHODS
Patient selection
This retrospective cohort study included 653 patients diagnosed with pathologically confirmed CRC-PM, excluding those with liver and lung metastases, at the Sixth Affiliated Hospital of Sun Yat-sen University (Guangzhou, China) between July 2012 and July 2018. We excluded patients with: (1) Incomplete medical records or follow-up data; (2) A history of immune or blood system disorders; and (3) Preoperative bleeding, infection, or obstruction. The study was approved by the Sixth Affiliated Hospital of Sun Yat-sen University’s Ethics Committee.
Treatment
A multidisciplinary team evaluated each patient before surgery. CRS and HIPEC were performed, as described by Sugarbaker[16]. CRS involved complete removal of tumor deposits from the abdominal cavity, including primary and invasive peritoneal and visceral tumors. Multiorgan resection was performed when necessary to achieve complete cytoreduction. Remaining lesions were evaluated based on completeness of the cytoreduction (CC) score: CC-0 indicated no discernible peritoneal tumors following CRS; CC-1 indicated tumor nodules < 2.5 mm; CC-2 indicated residual tumors 2.5-25 mm; and CC-3 indicated tumor nodules > 25 mm or unresectable tumor nodules anywhere in the abdomen or pelvis.
Patients with CC 0 or 1 who were deemed suitable for HIPEC received postoperative HIPEC in a closed system to eliminate free tumor cells and prevent recurrence. The procedure, patients with CC 0/1 who might endure HIPEC were selected. Chemotherapeutic involved a mixture of chemotherapeutic drugs such as 5-fluorouracil, oxaliplatin, and platinum in normal saline. The initial perfusion rate was maintained at 100 mL/min, and the solution temperature was kept at 42 °C for 1 hour.
Study parameters and follow-up
NLR was calculated for all patients within 1 week before surgery. NLR is defined as total neutrophil count divided by total lymphocyte count. Clinicopathological data included age, sex, body mass index, NLR, carcinoma embryonic antigen, carbohydrate antigen 199 (CA199), CA125, preoperative Hb and albumin, T category, N category, peritoneal cancer index (PCI) score, CRS/HIPEC status, CC score, tumor location, and histology. Patients were followed by outpatient visits or phone calls to assess survival after surgery. The final follow-up was on June 20, 2021. OS was the primary endpoint, defined as the time from surgery to death or the last follow-up.
Statistical analysis
Statistical analyses were performed using R (version 4.0.3) and SPSS (Windows version 25.0). The R packages “survival”, “rms”, “foreign”, and “survivalROC” were used to generate the prognostic nomogram, C-index, calibration plots, and receiver operating characteristic curves, respectively. Categorical variables were compared using χ2 or Fisher’s exact tests. Log-rank tests and Kaplan-Meier curves were used to estimate differences in OS. A P value < 0.05 was considered statistically significant.
RESULTS
Patients’ characteristics
Based on the inclusion and exclusion criteria, 133 patients with pathologically confirmed CRC-PM were included in the study. Using the X-tile program (http://tissuearray.org; version 2.4.7), we determined an optimal NLR cutoff value of 3.1 for predicting OS. Patients with NLR ≥ 3.1 were categorized as the high NLR group, and those with NLR < 3.1 as the low NLR group. The average patient age was 57.4 years (SD = 15.1). There were 44 females (33.1%) and 89 males (66.9%). All patients underwent CRS. Among them, 76 (57.2%) had a CC score of 2, and 57 (42.8%) had a CC score of 0/1. Furthermore, 35 patients (26.4%) received HIPEC. Table 1 lists patient characteristics.
Table 1 Characteristics of patients with peritoneal metastases of colorectal cancer.
Variables
Number of patients
Age (years), n (%)
≥ 60
64 (48.2)
< 60
69 (51.8)
Sex, n (%)
Male
89 (66.9)
Female
66 (33.1)
T category, n (%)
T0-3
56 (42.2)
T4
77 (57.8)
N category, n (%)
N0-1
72 (55.6)
N2
59 (44.4)
Location of tumor, n (%)
Right side of the colon
56 (42.2)
Left side of the colon
77 (57.8)
BMI (kg/m2), n (%)
≥ 18.5
24 (18.1)
< 18.5
109 (81.9)
PCI, n (%)
≥ 20
51 (38.3)
< 20
82 (61.6)
Histology, n (%)
Adenocarcinoma
105 (78.9)
Mucinous adenocarcinoma and signet-ring cell carcinoma
28 (21.1)
CRS, n (%)
CC 0/1
57 (42.8)
CC 2
76 (57.2)
HIPEC, n (%)
Yes
35 (26.4)
No
98 (73.6)
NLR, n (%)
≥ 3.1
54 (40.6)
< 3.1
79 (59.4)
Hb, n (%)
Normal
94 (70.6)
Low
39 (29.4)
Albumin (g/L), n (%)
≥ 35
99 (74.5)
< 35
34 (25.5)
Prognostic value of NLR and Hb
NLR and Hb levels were evaluated in 133 patients. High NLR was observed in 54 patients (40.6%), and normal Hb in 94 (70.6%). NLR was significantly correlated with both CRS and albumin levels. Hb levels were significantly correlated with age, pN category, CRS, and albumin (Table 2). Univariate analysis and Kaplan-Meier survival curves with log-rank tests were used to assess the relationship between NLR, Hb, and OS. The mOS for patients with high NLR was 7.9 months compared with 25.4 months for those with low NLR (Figure 1A; P = 0.002). Similarly, patients with normal Hb had a significantly longer mOS (18.5 months) than those with low Hb (6.3 months; Figure 1B; P < 0.001).
Figure 1 Kaplan-Meier curve for patients with high and low neutrophil-to-lymphocyte ratio, normal and low hemoglobin levels.
A: Kaplan-Meier curve for patients with high and low neutrophil-to-lymphocyte ratio; B: Kaplan-Meier curve for patients with normal and low hemoglobin levels. NLR: Neutrophil-to-lymphocyte ratio.
Table 2 Summary of demographics for patients treated with cytoreductive surgery according to the neutrophil-to-lymphocyte ratio/hemoglobin status.
variables
NLR ≥ 3.1, n = 54
NLR < 3.1, n = 79
P value
Hb (normal), n = 94
Hb (low), n = 39
P value
Age (years), n (%)
0.531
0.017
≥ 60
31 (57.4)
41 (51.8)
39 (41.5)
25 (64.1)
< 60
23 (42.6)
38 (48.2)
55 (58.5)
14 (35.9)
Sex, n (%)
0.423
0.097
Male
34 (62.9)
55 (69.6)
67 (71.2)
22 (56.4)
Female
20 (37.1)
24 (30.4)
27 (28.7)
17 (43.6)
T category, n (%)
0.177
0.187
T0-3
24 (44.4)
26 (32.9)
43 (45.7)
13 (33.3)
T4
30 (55.6)
53 (67.1)
51 (54.2)
26 (66.7)
N category, n (%)
0.710
0.029
N0-1
29 (53.7)
45 (56.9)
58 (61.7)
16 (41.1)
N2
25 (46.3)
34 (43.1)
36 (38.2)
23 (58.9)
CRS, n (%)
0.014
0.001
CC 0/1
30 (55.6)
27 (34.1)
49 (52.1)
8 (20.5)
CC 2
24 (44.4)
52 (65.9)
45 (47.9)
31 (79.5)
HIPEC, n (%)
0.473
0.065
Yes
16 (29.6)
19 (24.1)
29 (30.8)
6 (15.3)
No
38 (70.4)
60 (75.9)
65 (69.2)
33 (84.7)
Albumin (g/L), n (%)
0.019
< 0.001
≥ 35
46 (85.1)
53 (67.1)
78 (82.9)
21 (53.9)
< 35
8 (14.8)
26 (32.9)
16 (17.1)
18 (46.1)
BMI (kg/m2), n (%)
0.907
0.985
≥ 18.5
44 (81.5)
65 (82.3)
77 (82.0)
32 (82.1)
< 18.5
10 (18.5)
14 (17.7)
17 (18.0)
7 (17.9)
Location of tumor, n (%)
0.320
0.319
Right side of the colon
16 (29.6)
30 (37.9)
35 (37.2)
11 (28.2)
Left side of the colon
38 (70.4)
49 (62.1)
59 (62.8)
28 (71.8)
PCI, n (%)
0.535
0.708
≥ 20
19 (35.1)
32 (40.5)
37 (39.3)
14 (35.8)
< 20
35 (64.8)
47 (59.5)
57 (60.7)
25 (64.2)
Histology, n (%)
0.305
0.572
Adenocarcinoma
45 (83.3)
60 (75.9)
73 (77.6)
32 (82.1)
Mucinous adenocarcinoma and signet-ring cell carcinoma
9 (16.6)
19 (24.1)
21 (22.4)
7 (17.9)
Univariate and multivariate Cox analyses
Univariate Cox analysis identified several factors associated with better OS in patients with CRC-PM: Age ≤ 60 years (P = 0.006), CA199 < 37.0 U/mL (P = 0.014), NLR < 3.1 (P = 0.002), Hb (P < 0.001), albumin (P < 0.001), and PCI score < 20 (P < 0.001; Table 3). Hb and albumin levels were associated with better outcomes. Multivariate Cox analysis confirmed that age, CA199, NLR, Hb, and PCI were independent prognostic factors for OS (Table 3).
Table 3 Cox univariate and multivariate analyses of the 133 patients with peritoneal metastases of colorectal cancer.
Variables
Univariate analysis
Multivariate analysis
HR (95%CI)
P value
HR (95%CI)
P value
Sex (female)
0.89 (0.56-1.41)
0.621
Age (≤ 60)
0.55 (0.35-0.84)
0.006
0.63 (0.39-1.01)
0.050
CEA (≥ 5.0 ng/mL)
0.88 (0.73-1.75)
0.570
CA199 (≥ 37.0 U/mL)
1.71 (1.11-2.61)
0.014
1. 19 (0.74-1.91)
0.450
CA125 (≥ 35.0 U/mL)
1.07 (0.69-1.65)
0.769
BMI (< 18.5 kg/m2)
1.22 (0.88-1.62)
0.356
Location (right side)
0.94 (0.64-1.38)
0.756
NLR (≥ 3.1)
2.02 (1.28-3.19)
0.002
1.81 (1.13-2.89)
0.010
Hb (normal)
0.47 (0.31-0.72)
< 0.001
0.65 (0.39-1.07)
0.080
Albumin (< 35 g/L)
2.11 (1.37-3.51)
< 0.001
1.25 (0.72-2.17)
0.420
Category (T4)
1.04 (0.68-1.59)
0.854
Category (N2)
1.02 (0.79-1.21)
0.857
Histology (mucinous adenocarcinoma and signet-ring cell carcinoma)
1.46 (0.94-2.27)
0.090
PCI (≥ 20)
1.91 (1.24-2.93)
0.003
1.92 (1.21-3.07)
0.006
Development and validation of nomograms for predicting the prognosis of patients with CRC-PM
A nomogram was developed to estimate the 1- and 2-year postoperative survival probability for patients with CRC-PM (Figure 2). Points were assigned to each variable based on the scale at the top, and the total score was used to estimate survival probability. The C-index of the nomogram was 0.715 (95% confidence interval: 0.684-0.740), indicating good predictive power for 1- and 2-year OS. Additionally, the training cohort’s actual and predicted survival rates agreed well, as indicated in the 1- and 2-year calibration plots (Figure 3). The areas under the curve values for the 1- and 2-year survival predictions of the developed nomogram were 0.6238 and 0.6234, respectively (Figure 4).
Figure 2 Nomogram for predicting the 1- and 2-year postoperative survival probabilities of patients with peritoneal metastasis.
Hb: Hemoglobin; NLR: Neutrophil-to-lymphocyte ratio; PCI: Peritoneal cancer index; CA199: Carbohydrate antigen 199.
Figure 3 The 1-year and 2-year calibration plots of the nomogram.
A: 1-year; B: 2-year. While the vertical axes show the actual overall survival rates at 1 and 2 years, the horizontal axes show the nomogram-predicted probabilities of overall survival at those time points. The ideal forecast is indicated by the reference line that runs diagonally across the plot area, from the lower left to the top right corner.
Figure 4 Predictive accuracy of the model was assessed using an receiver operating characteristic curve.
A and B: The area under the receiver operating characteristic curve values for the 1-year (A) and 2-year (B) survival predictions of the nomogram. The larger the area under the receiver operating characteristic curve value, the better the prediction performance of the nomogram model. AUC: Area under the receiver operating characteristic curve.
DISCUSSION
This retrospective study of 133 patients with CRC-PM admitted to our hospital revealed that 40.6% (54/133) had a high NLR and 70.6% (94/133) had normal Hb. We found that high preoperative NLR and low Hb were associated with worse OS in patients with PM. In addition, OS was associated with age, PCI, Hb, NLR, CA19-9, and Hb as independent prognostic variables.
Treatment for PM is evolving with advancements in systemic medications and the growing importance of CRS/HIPEC. While CRS/HIPEC offers an mOS of 41.7 months for patients with PM[5], it is a complex procedure. A systematic review of large CRS/HIPEC studies found total postoperative morbidity rates ranging from 31% to 40%, with severe complications occurring in 23%-31% of patients[17,18]. Prior research also demonstrated that postoperative morbidity is an independent predictor of worse OS in patients receiving CRS and HIPEC[19]. Therefore, careful patient selection is crucial for this challenging treatment.
Three existing scoring systems for PM prognosis are Peritoneal Surface Disease Severity Score[20], Verwaal’s N score[21], and Gilly score[22], which all rely on intra- or postoperative data, limiting their use in preoperative patient selection for CRS and HIPEC. Moreover, established clinical parameters like PCI scores seem to lack sufficient discriminatory power for selecting patients for CRS and HIPEC. Studies show that enhanced computed tomography has only 11% sensitivity for detecting PM nodules < 0.5 cm in diameter but 94% sensitivity for nodules > 5 cm[23].
The link between systemic inflammation and cancer progression has recently gained attention as a potential prognostic indicator for various cancers[11,24]. NLR is a better predictive biomarker for CRC than other inflammatory biomarkers, probably because neutrophils are a significant part of leukocytes involved in cell matrix remodeling to encourage tumor growth. In consideration of this, we investigated NLR and its association with PM prognosis. The optimal NLR cutoff value for predicting prognosis remains debated. Different studies have employed various cutoff values and calculation methods[12,25]. There is currently no established threshold applicable to all patient groups. Using the X-tile application, we found a cutoff value of 3.1 for NLR. However, this value might not be generalizable to other patient cohorts, and further research is needed for validation.
Our findings suggest that a single inflammatory marker may have limited predictive power for PM. Studies have shown that C-reactive protein measured after CRS is a more accurate biomarker for assessing postoperative complications and long-term survival in patients with ovarian peritoneal carcinoma. C-reactive protein was excluded from this study because it relies on prior lab results[26]. Cancer and long-term immune system activation often lead to poor nutritional status in patients. Nutritional status is a significant prognostic factor for gastrointestinal tumors[27], and albumin levels are commonly used as an indicator[28,29]. We included albumin as a study factor, but while it showed significance in univariate Cox analysis, it was not an independent prognostic factor in the multivariate analysis. Patients with low Hb in our study typically had a poorer prognosis. This could be explained by the lower albumin levels observed in a larger proportion of the low Hb group (Table 2; P < 0.001). Our findings indicate that Hb is a better indicator of nutritional status and prognosis than albumin in this context.
There are some limitations to this study. Since this is a single-center retrospective study, the data are biased by nature and may contain missing information. Furthermore, PM being the advanced stage of CRC and the fact that patients often are not actively seeking treatment made it difficult to determine disease-free survival, potentially weakening the analysis. Furthermore, the lack of standardized NLR values could introduce bias in clinical practice. Prospective multicenter studies are needed to verify these findings. Finally, the established nomogram requires external validation from future studies.
CONCLUSION
High NLR and low Hb are independent prognostic risk factors for patients with CRC-PM. Our novel nomogram, developed and validated in this study to predict OS in patients with CRC-PM based on the NLR and Hb status, demonstrated strong discriminative power and accuracy in predicting the 1- and 2-year OS in this patient population.
Footnotes
Provenance and peer review: Unsolicited article; Externally peer reviewed.
Peer-review model: Single blind
Specialty type: Oncology
Country of origin: China
Peer-review report’s classification
Scientific Quality: Grade B
Novelty: Grade B
Creativity or Innovation: Grade A
Scientific Significance: Grade B
P-Reviewer: Fernández-Candela A S-Editor: Wang JJ L-Editor: A P-Editor: Zhao S
Verwaal VJ, van Ruth S, de Bree E, van Sloothen GW, van Tinteren H, Boot H, Zoetmulder FA. Randomized trial of cytoreduction and hyperthermic intraperitoneal chemotherapy versus systemic chemotherapy and palliative surgery in patients with peritoneal carcinomatosis of colorectal cancer.J Clin Oncol. 2003;21:3737-3743.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 1396][Cited by in F6Publishing: 1442][Article Influence: 68.7][Reference Citation Analysis (0)]
Quénet F, Elias D, Roca L, Goéré D, Ghouti L, Pocard M, Facy O, Arvieux C, Lorimier G, Pezet D, Marchal F, Loi V, Meeus P, Juzyna B, de Forges H, Paineau J, Glehen O; UNICANCER-GI Group and BIG Renape Group. Cytoreductive surgery plus hyperthermic intraperitoneal chemotherapy versus cytoreductive surgery alone for colorectal peritoneal metastases (PRODIGE 7): a multicentre, randomised, open-label, phase 3 trial.Lancet Oncol. 2021;22:256-266.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 172][Cited by in F6Publishing: 403][Article Influence: 134.3][Reference Citation Analysis (0)]
Chua TC, Yan TD, Saxena A, Morris DL. Should the treatment of peritoneal carcinomatosis by cytoreductive surgery and hyperthermic intraperitoneal chemotherapy still be regarded as a highly morbid procedure?: a systematic review of morbidity and mortality.Ann Surg. 2009;249:900-907.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 387][Cited by in F6Publishing: 398][Article Influence: 26.5][Reference Citation Analysis (0)]
Chua TC, Moran BJ, Sugarbaker PH, Levine EA, Glehen O, Gilly FN, Baratti D, Deraco M, Elias D, Sardi A, Liauw W, Yan TD, Barrios P, Gómez Portilla A, de Hingh IH, Ceelen WP, Pelz JO, Piso P, González-Moreno S, Van Der Speeten K, Morris DL. Early- and long-term outcome data of patients with pseudomyxoma peritonei from appendiceal origin treated by a strategy of cytoreductive surgery and hyperthermic intraperitoneal chemotherapy.J Clin Oncol. 2012;30:2449-2456.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 658][Cited by in F6Publishing: 719][Article Influence: 59.9][Reference Citation Analysis (0)]
Yang Y, Gao P, Chen X, Song Y, Shi J, Zhao J, Sun J, Xu Y, Wang Z. Prognostic significance of preoperative prognostic nutritional index in colorectal cancer: results from a retrospective cohort study and a meta-analysis.Oncotarget. 2016;7:58543-58552.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 54][Cited by in F6Publishing: 58][Article Influence: 9.7][Reference Citation Analysis (0)]
Verwaal VJ, van Tinteren H, van Ruth S, Zoetmulder FA. Predicting the survival of patients with peritoneal carcinomatosis of colorectal origin treated by aggressive cytoreduction and hyperthermic intraperitoneal chemotherapy.Br J Surg. 2004;91:739-746.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 168][Cited by in F6Publishing: 176][Article Influence: 8.8][Reference Citation Analysis (0)]
Nakamura N, Kinami S, Fujii Y, Miura S, Fujita J, Kaida D, Tomita Y, Miyata T, Fujita H, Ueda N, Iida Y, Kosaka T. The neutrophil/lymphocyte ratio as a predictor of peritoneal metastasis during staging laparoscopy for advanced gastric cancer: a retrospective cohort analysis.World J Surg Oncol. 2019;17:108.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 13][Cited by in F6Publishing: 15][Article Influence: 3.0][Reference Citation Analysis (0)]
Zager Y, Hoffman A, Dreznik Y, Jacoby H, Cordoba M, Horesh N, Nevler A, Gutman M, Berger Y. Cytoreductive surgery plus hyperthermic intraperitoneal chemotherapy in patients with peritoneal carcinomatosis from colorectal cancer: The prognostic impact of baseline neutrophil-lymphocyte, platelet-lymphocyte and lymphocyte-monocyte ratios.Surg Oncol. 2020;35:321-327.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 2][Cited by in F6Publishing: 4][Article Influence: 1.0][Reference Citation Analysis (0)]
Medina Fernández FJ, Muñoz-Casares FC, Arjona-Sánchez A, Casado-Adam A, Gómez-Luque I, Garcilazo Arismendi DJ, Thoelecke H, Rufián Peña S, Briceño Delgado J. Postoperative time course and utility of inflammatory markers in patients with ovarian peritoneal carcinomatosis treated with neoadjuvant chemotherapy, cytoreductive surgery, and HIPEC.Ann Surg Oncol. 2015;22:1332-1340.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 27][Cited by in F6Publishing: 32][Article Influence: 3.6][Reference Citation Analysis (0)]
Luvián-Morales J, González-Trejo S, Carrillo JF, Herrera-Goepfert R, Aiello-Crocifoglio V, Gallardo-Rincón D, Ochoa-Carrillo FJ, Oñate-Ocaña LF. Association of the prognostic nutritional index and overall survival in patients with colorectal cancer: A STROBE compliant retrospective cohort study.Cancer Med. 2019;8:3379-3388.
[PubMed] [DOI][Cited in This Article: ][Cited by in Crossref: 17][Cited by in F6Publishing: 29][Article Influence: 5.8][Reference Citation Analysis (0)]
