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C-Reactive Protein as a Marker of Postoperative Complication of Emergency Colorectal Surgery

Abstract

Introduction

The literature converges regarding the use of C-reactive protein (CRP) tests between postoperative days (PODs) 3 and 5 of elective procedures. In this period, they have great sensitivity and negative predictive value (NPV) for severe and anastomotic complications about two days before the first clinical sign. The few studies on colorectal urgency suggest that, despite the different initial values according to the surgical indication, following POD 3, the level of CRP is similar to that of elective procedures. However, given the heterogeneity of the studies, there is no consensus on the cutoff values for this use.

Objective

To validate the use and propose a PO CRP cut-off value in urgent colorectal procedures as an exclusion criterion for complications of anastomosis or the abdominal cavity.

Method

Retrospective analysis of the medical records of 308 patients who underwent urgent colorectal surgical procedures between January 2017 andDecember 2019. The following data were considered: age, gender, surgical indication, type of procedure performed, complications, CRP levels preoperatively and from POD 1 to 4, and the severity of the complications. We compared the CRP levels and the percentage variations between the preoperative period and PODs 1 to 4 as markers of severe complications using the receiver operating characteristic (ROC) curve.

Results

The levels of CRP on POD4, and their percentage drops between PODs 2 to 4 and PODs 3 to 4, were better to predict severe complications. A cutoff of 7.45mg/dL on POD 4 had 91.7% of sensitivity and NPV. A 50% drop between PODs 3 and 4 had 100% of sensitivity and NPV.

Conclusion

Determining the level of CRP is useful to exclude severe complications, and it could be a criterion for hospital discharge in POD 4 of emergency colorectal surgery.

Keywords:
colorectal surgery; C-reactive protein; postoperative complications; acute surgery

Introduction

Colorectal surgical procedures have a high incidence of complications, reaching up to 65%.11 European Society of Coloproctology collaborating group (2017) Relationship between method of anastomosis and anastomotic failure after right hemicolectomy and ileo-caecal resection: an international snapshot audit. Colorectal Dis 2015;19:e296-e311. Doi: 10.1111/codi.13646
https://doi.org/10.1111/codi.13646...
Although these procedures are frequently performed, there are reports of up to 20% of anastomotic leaks when they are performed electively,22 Welsch T, Müller SA, Ulrich A, et al. C-reactive protein as early predictor for infectious postoperative complications in rectal surgery. Int J Colorectal Dis 2007;22(12):1499-1507. Doi: 10.1007/s00384-007-0354-3
https://doi.org/10.1007/s00384-007-0354-...
33 Straatman J, Cuesta MA, Gisbertz SS, Van der Peet DL. Value of a step-up diagnosis plan: CRP and CT-scan to diagnose and manage postoperative complications after major abdominal surgery. Rev Esp Enferm Dig 2014;106(08):515-521 with a mortality of ∼ 22% for this diagnosis.22 Welsch T, Müller SA, Ulrich A, et al. C-reactive protein as early predictor for infectious postoperative complications in rectal surgery. Int J Colorectal Dis 2007;22(12):1499-1507. Doi: 10.1007/s00384-007-0354-3
https://doi.org/10.1007/s00384-007-0354-...
44 Alberts JCJ, Parvaiz A, Moran BJ. Predicting risk and diminishing the consequences of anastomotic dehiscence following rectal resection. Colorectal Dis 2003;5(05):478-482. Doi: 10.1046/j.1463-1318.2003.00515.x
https://doi.org/10.1046/j.1463-1318.2003...
However, ∼ 30% of colorectal operations are performed as a matter of urgency,55 Lohsiriwat V, Jitmungngan R. Enhanced recovery after surgery in emergency colorectal surgery: Review of literature and current practices. World J Gastrointest Surg 2019;11(02):41-52. Doi: 10.4240/wjgs.v11.i2.41
https://doi.org/10.4240/wjgs.v11.i2.41...
and, in this condition, the overall mortality reaches around 25%.66 Biondo S, Kreisler E, Millan M, et al. Impact of surgical specialization on emergency colorectal surgery outcomes. Arch Surg 2010; 145(01):79-86. Doi: 10.1001/archsurg.2009.208
https://doi.org/10.1001/archsurg.2009.20...

In the last decade, there has been an increase in the number of studies aimed at reducing the impact of surgical complications. Measures for the optimization of interventions in the postoperative (PO) period and the detection of complications before the onset of clinical manifestations have helped reduce the severity of complications, the length of the hospital stay, and mortality.22 Welsch T, Müller SA, Ulrich A, et al. C-reactive protein as early predictor for infectious postoperative complications in rectal surgery. Int J Colorectal Dis 2007;22(12):1499-1507. Doi: 10.1007/s00384-007-0354-3
https://doi.org/10.1007/s00384-007-0354-...
For this purpose, the use of serum inflammatory markers is already well established.

The most commonly used inflammation marker is C-reactive protein (CRP). It is synthesized by hepatocytes as part of the acute phase response after stimulation by interleukin-6 (IL-6), tumor necrosis factor-α (TNF-α), and IL-1β originated from the site of inflammation. C-reactive protein is a valuable marker to detect disease activity, inflammatory response, and PO recovery due to its short half-life (19 hours).22 Welsch T, Müller SA, Ulrich A, et al. C-reactive protein as early predictor for infectious postoperative complications in rectal surgery. Int J Colorectal Dis 2007;22(12):1499-1507. Doi: 10.1007/s00384-007-0354-3
https://doi.org/10.1007/s00384-007-0354-...

The literature converges regarding the use of CRP tests between postoperative days (PODs) 3 and 5 of elective procedures. In this period, there is great sensitivity and negative predictive value (NPV) for severe and anastomotic complications about two days before the first clinical sign.77 Adamina M, Warschkow R, Näf F, et al. Monitoring c-reactive protein after laparoscopic colorectal surgery excludes infectious complications and allows for safe and early discharge. Surg Endosc 2014;28(10):2939-2948. Doi: 10.1007/s00464-014-3556-0
https://doi.org/10.1007/s00464-014-3556-...
The few studies on colorectal urgency suggest that despite the different initial values according to the surgical indication, following POD 3, the level of CRP is similar to that of elective procedures.88 Straatman J, deWeerdesteijn EW, Tuynman JB, CuestaMA, van der Peet DL. C-Reactive Protein as a Marker for Postoperative Complications. Are There Differences in Emergency and Elective Colorectal Surgery? Dis Colon Rectum 2016;59(01):35-41. Doi: 10.1097/DCR.0000000000000506
https://doi.org/10.1097/DCR.000000000000...

A recent review99 Benoit O, Faron M, Margot N, Creavin B, Debove C, Tiret E, Parc Y, Lefevre JH. C-Reactive Protein Values After Colorectal Resection: Can We Discharge a Patient With a C-Reactive Protein Value >100? A Retrospective Cohort Study. Dis Colon Rectum 2019 Jan;62(1):88-96. doi: 10.1097/DCR.0000000000001216. PMID: 30451748
https://doi.org/10.1097/DCR.000000000000...
validated the value of 10 mg/dL as a safe level for hospital discharge in POD 4 free of any complications of the surgical act, regardless of whether it is urgent or elective. However, given the heterogeneity of published studies, there is no consensus on the cutoff values for this use. Similarly, we found a single study1010 Lee S-H, Kim KH, Choi CW, et al. Reduction rate of C-reactive protein as an early predictor of postoperative complications and a reliable discharge indicator after gastrectomy for gastric cancer. Ann Surg Treat Res 2019;97(02):65-73. Doi: 10.4174/astr.2019.97.2.65
https://doi.org/10.4174/astr.2019.97.2.6...
using the variation in CRP levels as a prognostic factor in the PO period, but the procedure evaluated was gastrectomy, and, as far as we know, there is no publication with this assessment in colorectal emergency surgery. Thus, the present study aimed to validate the use and propose a PO CRP cut-off value in urgent colorectal procedures as an exclusion criterion for complications of anastomosis or the abdominal cavity.

Methods

A retrospective analysis of the medical records of patients older than 18 years of age submitted to urgent colorectal surgical between January 2017 and December 2019 by the General and Oncologic Surgery Service of Hospital do Servidor Publico Estadual – Francisco Morato de Oliveira, in São Paulo, Brazil.

The procedures considered were performed with broad access to the abdominal cavity by both laparotomy and laparoscopy, followed by decompressive ostomies or colorectal resections, excluding appendectomy for the persent analysis.

We assessed the following data: gender, age, surgical indication, type of procedure, PO complication, preoperative, and PO CRP levels from PODs 1 to 4. We stratified the severity of PO complications based on the Clavien-Dindo classification,1111 Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240(02): 205-213 and considered Clavien-Dindo I and II mild complications, and III and IV, severe complications. Surgical-site infections (SSIs) were defined according to the guideline of the Centers for Disease Control and Prevention (CDC).1212 Berríos-Torres SI, Umscheid CA, Bratzler DW, et al; Healthcare Infection Control Practices Advisory Committee. Centers for disease control and prevention guideline for the prevention of surgical site infection, 2017. JAMA Surg 2017;152(08):784-791. Doi: 10.1001/jamasurg.2017.0904
https://doi.org/10.1001/jamasurg.2017.09...

We compared the median CRP level between PODs 1 to 4, as well as the percentage of variation between these days when infection and anastomotic complications were present.

Statistics

The continuous variables were expressed as means ± standard deviations or medians with interquartile ranges. The means were compared by the Student t-test or the Mann-Whitney, test according to the distribution. The qualitative variables were expressed as percentages and compared with the Chi-Squared or Fisher exact tests, when the expected value was lower than 5. We used the receiver operating characteristic (ROC) curve for CRP dosages and the percentage variation between subsequent PODs, setting the best areas under the curve (AUCs) to predict severe complications and deaths, and for intra-abdominal infections characterized as intracavitary abscesses, anastomotic leaks, or stoma collapses. For the best AUC, we then used the ROC individually to calculate the cutoff values for better sensitivity and NPV.

The threshold for statistical significance was established as p < 0.05 for all analyses. The data were analyzed using the Statistical Package for the Social Sciences (IBM SPSS Statistics for Windows, IBM Corp., Armonk, NY, US) software, version 23.0.

Results

We assessed the medical records of 308 patients (Table 1), with a mean age of 70.3 ± 12.65 years, 45.1% of whom were male. A total of 176 patients (57.1%) underwent surgery for neoplastic urgencies, with no difference between genders (p = 0.716).

Table 1
Characteristics of the study sample

The main surgical indication was colon obstruction (53.9%), followed by inflammation (21.4%) and perforation (17.5%). All indications had different frequencies between the groups (p < 0,001): the neoplastic group had more cases of obstruction (70.5%), but fewer cases of inflammation, ischemia, and perforation. An equal percentage for all groups was only observed in the Bonferroni post-hoc test for colorectal bleeding (Table 1). Among the procedures, regardless of the etiological group (p = 0.850), the most performed were right colectomy (42.9%) and anterior resection (33.4%). Anastomosis was performed in 110 patients (35.7%).

We observed a total of 51.3% of absent or mild complications, with the Bonferroni test showing that patients operated due to neoplastic disease had a greater number of Clavien-II complications (45.4% versus 26.5%) and lower mortality (19.3% versus 37.9%). There was a greater severity of PO complications among patients operated due to diseases of benign etiology (p = 0.006). The overall mortality was of 27.3%, with 10% of cases of colonic ischemia (Table 2).

Table 2
Postoperative complications of the study sample

The analysis of the CRP values for anastomotic/abdominal complications (Figs. 1 and 2) showed a better AUC (0.744) for the variation between PODs 2 to 4. For this period, an 83.5% drop had 100% of sensitivity and NPV. The variation between PODs 3 to 4 (AUC = 0.695) had, for a 50% drop, 96.9% of sensitivity and an NPV of 94.7%.

Fig. 1
Median CRP (C-reactive protein( levels (mg/dL), with standard error, in patients that had severe intra-abdominal postoperative complication and patients with mild or no complications between the preoperative period and the fourth postoperative day (POD 4).

Fig. 2
Receiver operating characteristic curve for the accuracy of C-reactive protein (CRP) between admission and the fourth postoperative day (POD 4), and the percentage variation between these dosages in the diagnosis of complications of anastomosis/ostomy and the abdominal cavity. Abbreviation: AUC, area under the curve.

The CRP values that provided the highest accuracy to exclude severe complications (Figs. 3 and 4) were those obtained for POD4 (AUC = 0.691) and the percentage variation between PODs 3to 4 (AUC = 0.702). Between PODs 3 to 4, a 50% drop in CRP levels had a sensitivity of 94%, with a specificity of 15.3%, and an NPV of 73.7%.

Fig. 3
Median CRP (C-reactive protein) levels (mg/dL), with standard error, in patients that had intra-abdominal postoperative complication and patients with no intra-abdominal complications between the preoperative and the fourth postoperative day (POD 4).

Fig. 4
Receiver operating characteristic curve for the accuracy of C-reactive protein (CRP) between admission and the fourth postoperative day (POD 4) and the percentage variation between these dosages in the diagnosis of severe complications. Abbreviation: AUC, area under the curve.

The cut-off value on POD 4 for 100% of sensitivity and NPV was of 2.83 mg/dL for both anastomotic/abdominal and severe complications. We determined a CRP of 7.48 mg/dL considering sensitivities of 91.7% for abdominal complications, and of 89.7% for severe complications, with NPVs of 91.7% and 73% respectively.

Discussion

In the present study, we were able to propose a useful cut-off value on POD 4, and associate a CRP drop compatible with its short half-life to the absence of severe and anastomotic/abdominal complications. When comparing all values in the ROC curve, the CRP on POD4 showed a higher AUC. When we individualized their cut-off values, however, the levels evidenced for maximum sensitivity and NPV were of 2.83 mg/dL, a very low and infrequent finding. Only four patients in the sample met this criterion, all with Clavien-Dindo II complications and no infection. However, following the rationale for the 19-hour half-life of CRP, we found that a 51% CRP drop between PODs 2 and 3 and a 46% drop between PODs 3 and 4 showed 100% of sensitivity and NPV for anastomotic leak and abdominal cavity abscess. We have not heard of another study so far using the percentage variation of CRP between PODs of colorectal operations, be them elective or urgent, to predict complications, or as a criterion for hospital discharge.

The use of inflammatory markers, especially CRP, has enabled safe early hospital discharge for patients undergoing elective colorectal procedures with a lower chance of readmission,1313 Pantel HJ, Jasak LJ, Ricciardi R, et al. Should they stay or should they go? the utility of C-reactive protein in predicting readmission and anastomotic leak after colorectal resection. Dis Colon Rectum 2019;62(02):241-247. Doi: 10.1097/DCR.0000000000001225
https://doi.org/10.1097/DCR.000000000000...
and the diagnosis of complications before their first clinical manifestation.22 Welsch T, Müller SA, Ulrich A, et al. C-reactive protein as early predictor for infectious postoperative complications in rectal surgery. Int J Colorectal Dis 2007;22(12):1499-1507. Doi: 10.1007/s00384-007-0354-3
https://doi.org/10.1007/s00384-007-0354-...
1414 Warschkow R, Beutner U, Steffen T, et al. Safe and early discharge after colorectal surgery due to C-reactive protein: a diagnostic meta-analysis of 1832 patients. Ann Surg 2012;256(02):245-250. Doi: 10.1097/SLA.0b013e31825b60f0
https://doi.org/10.1097/SLA.0b013e31825b...
Thus, reductions in the severity of complications, length of hospital stay, and mortality are expected.1515 Crockson RA, Payne CJ, Ratcliff AP, Soothill JF. Time sequence of acute phase reactive proteins following surgical trauma. Clin Chim Acta 1966;14(04):435-441. Doi: 10.1016/0009-8981(66)90030-1
https://doi.org/10.1016/0009-8981(66)900...

The serum values of CRP tend to be low in healthy individuals.1515 Crockson RA, Payne CJ, Ratcliff AP, Soothill JF. Time sequence of acute phase reactive proteins following surgical trauma. Clin Chim Acta 1966;14(04):435-441. Doi: 10.1016/0009-8981(66)90030-1
https://doi.org/10.1016/0009-8981(66)900...
1616 Straatman J, HarmsenAMKK, CuestaMA, Berkhof J, Jansma EP, van der Peet DL. Predictive Value of C-Reactive Protein for Major Complications after Major Abdominal Surgery: A Systematic Review and Pooled-Analysis. PLoS One 2015;10(07):e0132995. Doi: 10.1371/journal.pone.0132995
https://doi.org/10.1371/journal.pone.013...
Due to the metabolic response to surgical trauma, the release of inflammatory cytokines promotes the elevation of CRP levels up to POD The trend towards a complication-free course is a peak in serum CRP on POD 2 followed by a continuous drop on subsequent days. The higher levels of preoperative CRP in emergency surgery patients used to be a criterion to exclude this population from studies on inflammatory markers in the PO period. However, Straatman et al.88 Straatman J, deWeerdesteijn EW, Tuynman JB, CuestaMA, van der Peet DL. C-Reactive Protein as a Marker for Postoperative Complications. Are There Differences in Emergency and Elective Colorectal Surgery? Dis Colon Rectum 2016;59(01):35-41. Doi: 10.1097/DCR.0000000000000506
https://doi.org/10.1097/DCR.000000000000...
demonstrated that, despite that variation, the CRP levels stabilized starting on POD 3, as in elective cases.

Patients with poor outcomes are more likely to have high CRP levels even in the first 24 PO hours, and a drop in this indicator was associated with a lower complication rate.1515 Crockson RA, Payne CJ, Ratcliff AP, Soothill JF. Time sequence of acute phase reactive proteins following surgical trauma. Clin Chim Acta 1966;14(04):435-441. Doi: 10.1016/0009-8981(66)90030-1
https://doi.org/10.1016/0009-8981(66)900...
1717 Fischer CL, Gill C, Forrester MG, Nakamura R. Quantitation of "acute-phase proteins" postoperatively. Value in detection and monitoring of complications. Am J Clin Pathol 1976;66(05): 840-846. Doi: 10.1093/ajcp/66.5.840
https://doi.org/10.1093/ajcp/66.5.840...
1818 Mustard RA Jr, Bohnen JM, Haseeb S, Kasina R. C-reactive protein levels predict postoperative septic complications. Arch Surg 1987; 122(01):69-73. Doi: 10.1001/archsurg.1987.01400130075011
https://doi.org/10.1001/archsurg.1987.01...
This finding has been corroborated by most studies since the beginning of the use of CRP in the PO of surgical procedures in general,1919 Ortega-Deballon P, Radais F, Facy O, et al. C-reactive protein is an early predictor of septic complications after elective colorectal surgery. World J Surg 2010;34(04):808-814. Doi: 10.1007/s00268-009-0367-x
https://doi.org/10.1007/s00268-009-0367-...
2020 Warschkow R, Tarantino I, Torzewski M, Näf F, Lange J, Steffen T. Diagnostic accuracy of C-reactive protein and white blood cell counts in the early detection of inflammatory complications after open resection of colorectal cancer: a retrospective study of 1,187 patients. Int J Colorectal Dis 2011;26(11):1405-1413. Doi: 10.1007/s00384-011-1262-0
https://doi.org/10.1007/s00384-011-1262-...
and, more recently, specifically in the case of colorectal resections.88 Straatman J, deWeerdesteijn EW, Tuynman JB, CuestaMA, van der Peet DL. C-Reactive Protein as a Marker for Postoperative Complications. Are There Differences in Emergency and Elective Colorectal Surgery? Dis Colon Rectum 2016;59(01):35-41. Doi: 10.1097/DCR.0000000000000506
https://doi.org/10.1097/DCR.000000000000...
We observed the same high CRP levels in the preoperative period or on POD 1 (Fig. 5), but the values were not useful for closer follow-up, for lowering the threshold for intervention, or for making radiology-based tests mandatory in the initial PO for early diagnosis of severe or anastomotic complications.

Fig. 5
Evolution of the mean dosages of C-reactive protein according to the surgical indication between the preoperative period and the fourth postoperative day (POD 4).

The study groups were thus stratified considering the different characteristics of indication for urgent surgery of patients with neoplastic and non-neoplastic (“benign”) disease, as well as the greater possibility of prevention of cases of advanced tumors. Our service is in the only hospital of a health insurance company for ∼ 1.5 million public servants and their dependents in the state of São Paulo, most of them elderly. This survey of the total neoplastic emergencies composes a study recognizing our patterns for establishing prevention plans. Our sample had a higher frequency of obstruction for neoplasms (124 of 176; 70.5%), while non-neoplastic indications included mostly (86 of 132; 65,1%) etiologies with higher tissue and inflammation such as acute diverticulitis with peritonitis and acute colonic ischemia.

The higher incidence of death among patients without neoplasia might be due to the inclusion in this group of diseases of vascular and perforative etiology, with mortality rates of 61.5% and 40.7% respectively. Despite its rate, mortality in the present study was equivalent to the mortality reported in the literature: 26 to 81% for acute mesenteric ischemia,2121 Ehlert BA. Acute Gut Ischemia. Surg Clin North Am 2018;98(05): 995-1004. Doi: 10.1016/j.suc.2018.06.002
https://doi.org/10.1016/j.suc.2018.06.00...
and 30 to 70% for perforations.2222 Shin R, Lee SM, Sohn B, et al. Predictors ofMorbidity andMortality After Surgery for Intestinal Perforation. Ann Coloproctol 2016;32 (06):221-227. Doi: 10.3393/ac.2016.32.6.221
https://doi.org/10.3393/ac.2016.32.6.221...

Preoperative CRP values may vary even in elective patients, as well as the inflammatory PO response of each individual due to differences in immune response associated with age, gender, race, and nutrition status.1010 Lee S-H, Kim KH, Choi CW, et al. Reduction rate of C-reactive protein as an early predictor of postoperative complications and a reliable discharge indicator after gastrectomy for gastric cancer. Ann Surg Treat Res 2019;97(02):65-73. Doi: 10.4174/astr.2019.97.2.65
https://doi.org/10.4174/astr.2019.97.2.6...
It seems more reliable to use the variation than an isolated value. Since CRP has a 19-hour half-life, when there is no stimulus for its production, there is a significant drop in levels from one day to the next.2323 Ridker PM. Clinical application of C-reactive protein for cardiovascular disease detection and prevention. Circulation 2003;107(03):363-369. Doi: 10.1161/01.CIR.0000053730.47739.3C
https://doi.org/10.1161/01.CIR.000005373...

The present study is limited by its retrospective design. Moreover, we did not consider the comorbidities of patients and preoperative clinical conditions or demographic data, as in most publications.

We suggest daily CRP tests from POD 2 onwards for the use of its gradient as a criterion for hospital discharge on PODs 3 or 4 of colorectal surgical procedures as a matter of urgency.

Conclusion

The levels of CRP can be used for the exclusion of severe complications and as a criterion for hospital discharge on POD 4 of emergency colorectal surgery.

Acknowledgments

The authors would like to thank Helena Passarelli Giroud Joaquim and Sidney Roberto Nadal, for their critical review of the manuscript.

References

  • 1
    European Society of Coloproctology collaborating group (2017) Relationship between method of anastomosis and anastomotic failure after right hemicolectomy and ileo-caecal resection: an international snapshot audit. Colorectal Dis 2015;19:e296-e311. Doi: 10.1111/codi.13646
    » https://doi.org/10.1111/codi.13646
  • 2
    Welsch T, Müller SA, Ulrich A, et al. C-reactive protein as early predictor for infectious postoperative complications in rectal surgery. Int J Colorectal Dis 2007;22(12):1499-1507. Doi: 10.1007/s00384-007-0354-3
    » https://doi.org/10.1007/s00384-007-0354-3
  • 3
    Straatman J, Cuesta MA, Gisbertz SS, Van der Peet DL. Value of a step-up diagnosis plan: CRP and CT-scan to diagnose and manage postoperative complications after major abdominal surgery. Rev Esp Enferm Dig 2014;106(08):515-521
  • 4
    Alberts JCJ, Parvaiz A, Moran BJ. Predicting risk and diminishing the consequences of anastomotic dehiscence following rectal resection. Colorectal Dis 2003;5(05):478-482. Doi: 10.1046/j.1463-1318.2003.00515.x
    » https://doi.org/10.1046/j.1463-1318.2003.00515.x
  • 5
    Lohsiriwat V, Jitmungngan R. Enhanced recovery after surgery in emergency colorectal surgery: Review of literature and current practices. World J Gastrointest Surg 2019;11(02):41-52. Doi: 10.4240/wjgs.v11.i2.41
    » https://doi.org/10.4240/wjgs.v11.i2.41
  • 6
    Biondo S, Kreisler E, Millan M, et al. Impact of surgical specialization on emergency colorectal surgery outcomes. Arch Surg 2010; 145(01):79-86. Doi: 10.1001/archsurg.2009.208
    » https://doi.org/10.1001/archsurg.2009.208
  • 7
    Adamina M, Warschkow R, Näf F, et al. Monitoring c-reactive protein after laparoscopic colorectal surgery excludes infectious complications and allows for safe and early discharge. Surg Endosc 2014;28(10):2939-2948. Doi: 10.1007/s00464-014-3556-0
    » https://doi.org/10.1007/s00464-014-3556-0
  • 8
    Straatman J, deWeerdesteijn EW, Tuynman JB, CuestaMA, van der Peet DL. C-Reactive Protein as a Marker for Postoperative Complications. Are There Differences in Emergency and Elective Colorectal Surgery? Dis Colon Rectum 2016;59(01):35-41. Doi: 10.1097/DCR.0000000000000506
    » https://doi.org/10.1097/DCR.0000000000000506
  • 9
    Benoit O, Faron M, Margot N, Creavin B, Debove C, Tiret E, Parc Y, Lefevre JH. C-Reactive Protein Values After Colorectal Resection: Can We Discharge a Patient With a C-Reactive Protein Value >100? A Retrospective Cohort Study. Dis Colon Rectum 2019 Jan;62(1):88-96. doi: 10.1097/DCR.0000000000001216. PMID: 30451748
    » https://doi.org/10.1097/DCR.0000000000001216
  • 10
    Lee S-H, Kim KH, Choi CW, et al. Reduction rate of C-reactive protein as an early predictor of postoperative complications and a reliable discharge indicator after gastrectomy for gastric cancer. Ann Surg Treat Res 2019;97(02):65-73. Doi: 10.4174/astr.2019.97.2.65
    » https://doi.org/10.4174/astr.2019.97.2.65
  • 11
    Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg 2004;240(02): 205-213
  • 12
    Berríos-Torres SI, Umscheid CA, Bratzler DW, et al; Healthcare Infection Control Practices Advisory Committee. Centers for disease control and prevention guideline for the prevention of surgical site infection, 2017. JAMA Surg 2017;152(08):784-791. Doi: 10.1001/jamasurg.2017.0904
    » https://doi.org/10.1001/jamasurg.2017.0904
  • 13
    Pantel HJ, Jasak LJ, Ricciardi R, et al. Should they stay or should they go? the utility of C-reactive protein in predicting readmission and anastomotic leak after colorectal resection. Dis Colon Rectum 2019;62(02):241-247. Doi: 10.1097/DCR.0000000000001225
    » https://doi.org/10.1097/DCR.0000000000001225
  • 14
    Warschkow R, Beutner U, Steffen T, et al. Safe and early discharge after colorectal surgery due to C-reactive protein: a diagnostic meta-analysis of 1832 patients. Ann Surg 2012;256(02):245-250. Doi: 10.1097/SLA.0b013e31825b60f0
    » https://doi.org/10.1097/SLA.0b013e31825b60f0
  • 15
    Crockson RA, Payne CJ, Ratcliff AP, Soothill JF. Time sequence of acute phase reactive proteins following surgical trauma. Clin Chim Acta 1966;14(04):435-441. Doi: 10.1016/0009-8981(66)90030-1
    » https://doi.org/10.1016/0009-8981(66)90030-1
  • 16
    Straatman J, HarmsenAMKK, CuestaMA, Berkhof J, Jansma EP, van der Peet DL. Predictive Value of C-Reactive Protein for Major Complications after Major Abdominal Surgery: A Systematic Review and Pooled-Analysis. PLoS One 2015;10(07):e0132995. Doi: 10.1371/journal.pone.0132995
    » https://doi.org/10.1371/journal.pone.0132995
  • 17
    Fischer CL, Gill C, Forrester MG, Nakamura R. Quantitation of "acute-phase proteins" postoperatively. Value in detection and monitoring of complications. Am J Clin Pathol 1976;66(05): 840-846. Doi: 10.1093/ajcp/66.5.840
    » https://doi.org/10.1093/ajcp/66.5.840
  • 18
    Mustard RA Jr, Bohnen JM, Haseeb S, Kasina R. C-reactive protein levels predict postoperative septic complications. Arch Surg 1987; 122(01):69-73. Doi: 10.1001/archsurg.1987.01400130075011
    » https://doi.org/10.1001/archsurg.1987.01400130075011
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    Ortega-Deballon P, Radais F, Facy O, et al. C-reactive protein is an early predictor of septic complications after elective colorectal surgery. World J Surg 2010;34(04):808-814. Doi: 10.1007/s00268-009-0367-x
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Publication Dates

  • Publication in this collection
    24 Jan 2022
  • Date of issue
    Oct-Dec 2021

History

  • Received
    20 Jan 2021
  • Accepted
    15 June 2021
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