Prognostic nutrition index predicts short-term surgical complications in patients with rectal cancer after laparoscopic surgery

Introduction

In 2020, there were reportedly more than 730,000 new cases of rectal cancer, with more than 330,000 deaths worldwide (1). The past few years see a gradual growing in the incidence of rectal cancer in China, posing a great threat to people's lives and health (2). With the continuous development of surgical technology, continuous progress of neoadjuvant therapy, and increasing demand of patients for anal preservation, the proportion of laparoscopic sphincter-sparing surgery for low and even ultralow rectal cancer is gradually increasing. Moreover, it also poses great challenges to the management of surgical complications.

Surgical complications may not only negatively impact short-term outcomes but also affect oncological outcomes (3, 4). Law et al. found that sepsis complications and anastomotic leakage were important factors for recurrence and speculated that changes in immune response related to sepsis might adversely affect the prognosis of tumors (5). Therefore, it is necessary to identify patients with poor postoperative outcomes early, because assessment and adjustment of modifiable risk factors of patients can serve as a potential window of opportunity to optimize postoperative outcome. It may be an effective method to prevent postoperative complications and improve overall survival by evaluating patients' nutritional and immunological conditions. It has been proposed that, with the aid of the Prognostic Nutrition Index (PNI), the nutritional status and the risk of postoperative complications in patients with gastrointestinal malignancies can be evaluated, which was calculated by methods of serum albumin concentration and peripheral blood lymphocyte count (6). Previous studies have confirmed that PNI is a useful predictor of postoperative complications and prognosis in patients with colorectal cancer (7–10). However, only a few studies and subgroup analyses of the surgical complications of rectal cancer exist.

Postoperative complications differ between rectal and colon cancers in that surgical complications are more common in rectal cancer patients (11). In addition, there are differences in treatment, including neoadjuvant treatment of locally advanced rectal cancer (12), the application of transanal endoscopic resection of mid-low rectal cancer (13), and defunctioning ileostomy to protect the low anastomosis. However, current studies on PNI in rectal cancer are insufficient. PNI is associated with the permanent stoma rate after anterior resection and defunctioning stoma (14), postoperative complications of locally recurrent rectal cancer (15), and postoperative complications of early rectal cancer (16). However, regarding the connection between PNI and postoperative surgical complications after laparoscopic surgery for rectal cancer, seldom reports are published. Hence, aiming at exploring the relationship between PNI and postoperative surgical complications after laparoscopic surgery for rectal cancer, this study was developed.

Methods

Patient selection

A retrospective analysis was carried out on the prospectively collected data of 225 consecutive patients who suffered from rectal cancer and have received laparoscopic surgery at Beijing Friendship Hospital, Affiliated with Capital Medical University between January 2021 and April 2022 were analyzed. The inclusion criteria were as follows: (1) 18–80 years of age; (2) colonoscopic diagnosis of the lower edge of the tumor within 15cm of the anal verge; (3) preoperative pathologically confirmed rectal adenocarcinoma; and (4) laparoscopic sphincter-sparing surgery and abdominal-perineal resection (APR) following total mesorectal excision (TME) or partial mesorectal excision principles. Exclusion criteria were as follows: (1) open surgery; (2) previous history of rectal surgery; (3) presence of intestinal obstruction, perforation, bleeding, or other emergency operations; (4) treatment with local excision (i.e., endoscopic, anorectal, or transanal endoscopic microsurgery approach); (5) presence of other primary malignancies during the same period; (6) histology other than adenocarcinoma; (7) presence of blood or immune system diseases; (8) presence of infection and non-cancer inflammatory diseases; and (9) parenteral nutrition support before surgery. All patients underwent colonoscopy and tumor biopsy before surgery. Except for those with contraindications, all patients underwent thoracoabdominal computed tomography (CT) and pelvic magnetic resonance imaging (MRI) to evaluate clinical staging after the histological diagnosis of rectal adenocarcinoma. This study gained approval from the Institutional Research and Ethics Committee.

Data collection

The followings are included in the collected data: baseline characteristics, laboratory tests, and intraoperative indices. Baseline characteristics included age, sex, smoking, body mass index (BMI), comorbidities (hypertension, diabetes mellitus, and other diseases: respiratory diseases, cardiovascular, and cerebrovascular diseases), American Association of Anesthesiologists (ASA) score, preoperative tumor staging, tumor location [conditional on the distance between the lower edge of the tumor and the anal verge; they were classified as mid–low (0–10 cm), or high (10.1–15 cm)], neoadjuvant therapy, and previous abdominal and pelvic surgeries. Laboratory tests included preoperative serum albumin, lymphocyte count, C-reactive protein (CRP), hemoglobin, and serum albumin concentration and total lymphocyte count on postoperative day (POD) 1 (serum samples were collected before postoperative nutritional support). Intraoperative indices included operation time and method [anterior resection (AR) or low anterior resection (LAR), transanal TME (taTME), and APR], anastomosis, stoma form (permanent colostomy and defunctioning ileostomy), and intraoperative bleeding. Tumor stage and pathological tumor response grade was assessed according to the 8th American Joint Committee on Cancer Classification. All patients underwent high inferior mesenteric artery ligation, and anastomosis of patients undergoing anastomotic reconstruction was tension-free. The Enhanced Recovery After Surgery program was applied in all patients underwent laparoscopic surgery for rectal cancer.

Data regarding blood tests before the operation and on POD 1 were collected, including the serum albumin level and peripheral blood lymphocyte count. PNI calculation formula was: 10 × serum albumin value (g/dl) + 0.005 × peripheral blood lymphocyte count (per mm³).

Definition of surgical complications

According to previous studies, short-term surgical complications were defined and recorded as surgical related complications that occurred within 30 days after surgery, including anastomotic leakage, surgical site infection, intestinal obstruction, abdominal and pelvic abscess, hemorrhage (intra-abdominal bleeding and anastomotic bleeding), urinary retention, urinary tract infection, and stoma related complications (stoma infection, stoma prolapse, stoma outlet obstruction, and high stoma output) (17–20). Surgical complications were categorized as per the Clavien–Dindo classification (21)—grades I + II: minor surgical complications, grades III + IV: major surgical complications. In this study, no mortality was found within 30 days after surgery (grade V). Diagnosed from the definition proposed by the international rectal cancer research group, anastomotic leakage was confirmed (22). All diagnoses of anastomotic leakage were supported by CT scan.

Statistical analyses

All statistical analyses were performed using the R language package (version 3.6.3) and SPSS (version 26.0; IBM, Armonk, NY, USA). Categorical data were expressed as counts and percentages and the variables analyzed were by Fisher's exact or χ² test. Likewise, continuous data were expressed as mean ± standard deviation and the variables analyzed by two-tailed t-test. With the aid of a receiver operating characteristic (ROC) curve, the specificity and sensitivity of PNI can be evaluated in predicting postoperative surgical complications. The optimal cut-off value was determined according to the maximum Youden index (sensitivity + specificity − 1). The DeLong test was used to compare the area under the ROC curve (AUC) of the preoperative and postoperative PNI. By means of univariate analysis the risk factors for surgical complications were analyzed. The statistically significant variables in the univariate analysis (P < 0.05), analyzed as covariates, were incorporated in the multivariate analysis model to determine the independent risk factors for surgical complications after laparoscopic rectal cancer surgery. A two-tailed P-value <0.05 was considered statistically significant.

Results

Patient characteristics

The clinical characteristics of the patients are detailed in Table 1. A total of 225 patients with rectal cancer who underwent laparoscopic surgery were included in this study: 148 (65.8%) men and 77 (34.2%) women. Their mean age and BMI were 62.7 ± 10.0 years and 23.9 ± 3.8 kg/m², respectively. There were 99 (44.0%) cases of hypertension, 52 (23.1%) cases of diabetes, and 38 (16.9%) cases of respiratory, cardiovascular, and cerebrovascular diseases. Middle and low rectal cancer accounted for most cases of rectal cancer (n = 173, 76.9%), and the mean distance from the lower edge of the tumor to the anal verge was 80.9 ± 34.0 mm. A total of 71 (31.6%) patients received neoadjuvant therapy. All patients underwent laparoscopic surgery, with a mean operation time of 205.3 ± 60.1 min. Conventional laparoscopic surgery included AR/LAR in 167 (74.2%) cases, APR in 16 (7.1%), and taTME in 42 (18.7%). Primary anastomosis was performed in 205 (91.1%) patients. The defunctioning ileostomy rate was 56.4% (127/205), and 20 (8.9%) patients underwent permanent colostomy. The overall incidence rate of short-term surgical complications was 36.0% (81/225). Based on the Clavien–Dindo classification, 71 (31.6%) patients suffer from minor complications (grade I + II), 10 (4.4%) had major complications (grade III + IV), and 16 (7.1%) were rehospitalized due to surgical complications.

TABLE 1

Table 1. Demographic and clinical features of patients.

Predictive value of preoperative and POD 1 PNI for surgical complications

A ROC curve was adopted to compare the predictive accuracy of the preoperative PNI and PNI on POD 1. As shown in Figure 1, the AUC of the preoperative PNI was 0.582, with a sensitivity of 0.272, specificity of 0.903, and Youden's index of 0.175; the AUC of the PNI on POD 1 was 0.601, with a sensitivity of 0.432, specificity of 0.785, and Youden's index of 0.217. The optimal cut-off value of the preoperative PNI for surgical complications was 40.15, while that of the PNI on POD 1 was 35.28. The results of the Delong test showed no statistical difference between the AUCs (P = 0.598). These data show that PNI is an important indicator for the early prediction of surgical complications and that PNI on POD 1 is more sensitive.

FIGURE 1

Figure 1. Receiver operating characteristic curve analysis of PNI preoperative and on POD 1 in predicting surgical complications. AUC, area under the curve; PNI, prognostic nutrition index; POD, postoperative day.

Univariate and multivariate analyses of risk factors for surgical complications

After the univariate analysis on various clinical factors, the results are suggested in Table 2: including age, sex, smoking, ASA score, comorbidities, tumor location, tumor T stage, previous abdominal surgery history, neoadjuvant treatment, preoperative hemoglobin and CRP levels, preoperative lymphocyte count, surgical approach, anastomosis, stoma, operation time, intraoperative bleeding, preoperative PNI, and PNI on POD 1. Among these, male sex [odds ratio (OR) = 1.191, 95% confidence interval (CI):0.791–2.447, P = 0.002], other complications (respiratory, cardiovascular, and cerebrovascular system diseases) (OR = 2.295, 95% CI: 1.132–4.651, P = 0.021), ASA ≥3 (OR = 2.105, 95% CI: 1.102–4.023, P = 0.024), anastomosis (OR = 0.338, 95% CI: 0.132–0.866, P = 0.024), colostomy/ileostomy (OR = 2.500, 95% CI: 1.345–4.646, P = 0.004), preoperative PNI ≤40.15 (OR = 3.462, 95% CI: 1.656–7.238, P = 0.001), and PNI on POD 1 ≤35.28 (OR = 2.773, 95% CI: 1.533–5.016, P = 0.001) were significantly associated with surgical complications. Variables with statistical differences in the univariate analysis (P < 0.05) were included as covariates in the multivariate analysis model to determine the independent risk factors for surgical complications after laparoscopic surgery for rectal cancer. The association of preoperative PNI and PNI on POD 1 with surgical complications was analyzed (Table 3). Preoperative PNI ≤40.15 (OR = 2.856, 95% CI: 1.287–6.341, P = 0.010) and PNI on POD 1 ≤35.28 (OR = 3.118, 95% CI: 1.586–6.130, P = 0.001) were independent risk factors for surgical complications.

TABLE 2

Table 2. Univariate analysis of risk factors associated with surgical complications.

TABLE 3

Table 3. The association between PNI and the occurrence of surgical complications.

Comparison of surgical complications associated with preoperative PNI and POD 1 PNI

On the grounds of the preoperative PNI cut-off value, the patients were divided into the low (preoperative PNI ≤40.15) and high (preoperative PNI >40.15) preoperative PNI groups. They were also divided into the low (PNI on POD 1 ≤35.28) and high (PNI on POD 1 >35.28) PNI on POD 1 groups according to the PNI on POD 1 cut-off value (Table 4). Patients with a low preoperative PNI were more vulnerable to of surgical complications compared with patients with a higher one (61.1% vs. 31.2%, P = 0.001). In the subgroup analysis, the incidence of mild complications (Clavien–Dindo I + II) was significantly different between the two preoperative PNI groups (52.8% vs. 27.5%, P = 0.003). Although the incidence of major surgical complications (Clavien–Dindo III + IV) was higher in the low preoperative PNI group, the difference was not statistically significant (8.3% vs. 3.7%, P = 0.218). In addition, patients with preoperative PNI ≤40.15 were observed to have prolonged postoperative stay (10.4 ± 8.2 vs. 7.8 ± 3.6, P = 0.002). Similar trends were observed in the PNI on POD 1 group.

TABLE 4

Table 4. Comparison of surgical complications in different PNI groups.

Discussion

The clinical significance of PNI was witnessed from the data of this study on 225 patients with rectal cancer receiving laparoscopic surgery. The results showed that low PNI values (preoperative PNI ≤40.15 and PNI on POD 1 ≤35.28) were independent risk factors for surgical complications and could lead to prolonged hospitalization. In addition, preoperative PNI and PNI on POD 1 were significantly associated with postoperative complications. However, PNI on POD 1 was more sensitive than preoperative PNI in predicting complications. Therefore, PNI is a potential and valuable predictor of surgical complications after laparoscopic surgery for rectal cancer.

PNI was originally designed to evaluate the immunonutritional status of patients undergoing surgery for gastrointestinal malignancy (6). Among the studied indicators of nutritional status, serum albumin is one of the most frequented, and lymphocyte count reflects the immune status of patients. Research on the relationship between PNI and colorectal cancer has mainly focused on the prognosis. In addition, most researches on the correlation between PNI and postoperative complications of colorectal cancer have shown that low PNI values are associated with the occurrence of severe complications; however, the relationship of PNI with minor complications has not been determined (8, 23). Rectal and colon cancers differ in the occurrence of postoperative complications, and the proportion of postoperative complications after rectal cancer surgery is higher (11). Therefore, it is of value to study the correlation between PNI and surgical complications after laparoscopic surgery for rectal cancer.

In a study on PNI in rectal cancer, Wang et al. (14) found that preoperative PNI was an independent predictive factor in predicting permanent stoma in patients who underwent AR and defunctioning stoma. Paku et al. (15) found that low preoperative PNI was a risk factor posing influence on postoperative major complications of locally recurrent rectal cancer. Xia et al. (16) found that it is rewarding to use PNI to predict postoperative complications in patients with T1–2 rectal cancer. However, these studies did not analyze overall complications after primary resection of rectal cancer and did not include postoperative PNI. Furthermore, hardly can we see studies on the correlation between PNI and surgical complications after laparoscopic surgery for rectal cancer. Evidence suggests that surgical complications of rectal cancer surgery are associated with adverse oncological outcomes (4). Therefore, early prediction and reduction of surgical complications may help to improve oncological outcomes. The correlation between PNI and surgical complications after laparoscopic surgery for rectal cancer was evaluated in this study.

The incidence of malnutrition among patients undergoing gastrointestinal surgery in hospitals is approximately 50% (24, 25). Convincing evidence has been found that nutritional risk is associated with increased complications and mortality after elective surgery (26, 27). Preoperative hypoalbuminemia is a well-known indicator of malnutrition and is viewed as a high-risk factor for postoperative complications in patients with rectal cancer (28). In addition, lymphocytes play a vital role in the host cytotoxic immune response to tumors and can be used to evaluate the health status of patients. Preoperative systemic inflammatory response through host-tumor interaction may potentially predict postoperative complications in cancer patients (29, 30). The results of this study confirm that both preoperative PNI and PNI on POD 1 are independent predictors of postoperative surgical complications after laparoscopic rectal cancer surgery. Nonetheless, PNI on POD 1 was more sensitive. On POD 1, serum samples were obtained prior to postoperative nutritional support to avoid potential bias as much as possible. Therefore, the results of the study of PNI on POD 1 are valid. Decreased postoperative serum albumin levels is closely related to systemic inflammatory response syndrome, triggering increased fractional synthesis and pathological capillary leakage of serum albumin (31). Low serum albumin level in the early postoperative period is a primary risk factor for postoperative complications after gastrointestinal surgery (32, 33). In addition, because of surgical stress, lymphocytes can change both quantitatively and qualitatively, and the number of lymphocytes gradually decreases for several days after surgery (34). This may be the reason for the higher sensitivity of the PNI on POD 1.

In this study, the preoperative PNI and PNI on POD 1 were sorted into two groups according to the cut-off value, and surgical complications were analyzed in subgroups. The results showed significant differences in the overall surgical and minor complications between the low and high PNI groups. Higher rates of major surgical complications were seen in low PNI group than the high PNI group (8.3% vs. 3.7%; 7.6% vs. 3.1%), however, no significant difference was found in the major complication subgroup (P = 0.218 and P = 0.142, respectively). The incidence of major surgical complications in this study was only 4.4% (10/225). Therefore, this may be caused by the small sample size. The predictive value of PNI for short-term major surgical complications after laparoscopic surgery for rectal cancer requires further study.

Several limitations can be found in this study. First, it was a single-center, case-control study involving just 225 patients, thus only a small sample size is available. In this case, for example, prolonged operation time increases catabolism and may induce lower levels of POD1 PNI, but no significant relationship between operation time and postoperative complications was found in this study. Second, we did not evaluate other known predictors of short-term surgical complications. Third, long-term complications were not included in this study, and further follow-up is required to obtain long-term complication results for further verification. However, the results of this study provide new ideas and possibilities for predicting and managing short-term surgical complications after laparoscopic surgery for rectal cancer.

Conclusion

In conclusion, this study confirmed that preoperative PNI ≤40.15 and PNI on POD 1 ≤35.28 were independent risk factors for short-term surgical complications after laparoscopic rectal cancer surgery. PNI has a potential predictive value for the occurrence of short-term surgical complications after laparoscopic surgery for rectal cancer, and PNI on POD 1 was more sensitive. However, more multicenter, prospective, high-quality studies are needed to validate our results.

Data availability statement

The original contributions presented in the study are included in the article/Supplementary Material, further inquiries can be directed to the corresponding author/s.

Ethics statement

The studies involving human participants were reviewed and approved by the Institutional Research and Ethics Committee of Beijing Friendship Hospital, Capital Medical University. As this study was a retrospective observational study, written informed consent for participation was not required for this study in accordance with the national legislation and the institutional requirements.

Author contributions

Study concept and design: GW, HY, ZZ. Acquisition of data: FX, CM, HL, JG, LS, XZ, QW. Analysis and interpretation of data: FX, CM, ZY, HL, JG. Drafting of the manuscript: FX, CM. Critical revision of manuscript: ZY, GW, HY, ZZ. All authors contributed to the article and approved the submitted version.

Funding

This work was supported by the National Key Technologies R / D Program (No. 2015BAI13B09); National Key Research and Development Project (No. 2017YFC0110904); Beijing Key Clinical Discipline Fund (No. 2018-118); Capital Health Development and Research Key Project (No. 2018-1-1111); Clinical Center for Colorectal Cancer, Capital Medical University (No. 1192070313); and Clinical Research Launching Project of Beijing Friendship Hospital, Capital Medical University (No. YYQDKT2016-5).

Acknowledgments

Thanks to all authors for their contributions to this article.

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher's note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

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