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  • Research
  • Open Access
  • Open Peer Review

Preoperative malnutrition with mild hypoalbuminemia associated with postoperative mortality and morbidity of colorectal cancer: a propensity score matching study

  • 1, 2, 3,
  • 2,
  • 2 and
  • 2, 3Email author
Nutrition Journal201918:33

https://doi.org/10.1186/s12937-019-0458-y

  • Received: 5 October 2018
  • Accepted: 11 June 2019
  • Published:
Open Peer Review reports

Abstract

Background

Malnutrition with hypoalbuminemia (albumin < 35 g/L) is an important factor in predicting risks associated with colorectal cancer surgery. However, there is limited data about the effects of mild hypoalbuminemia with small decreases in albumin on postoperative complications.

Methods

This is a retrospective study using the multi-institutional, nationally validated database of the American College of Surgeons-National Surgical Quality Improvement Program (ACS-NSQIP) to investigate mild hypoalbuminemia and its association with postoperative mortality and morbidity by using a propensity score matching method.

Results

In a group of 30,676 colorectal cancer patients who received surgery, 5230 had mild hypoalbuminemia (< 35 and > =30 g/L) and 21,310 had normal albumin levels (> = 35 g/L). Significant differences were noted in 21 clinical characteristics between the two groups. After 1:2 propensity score matching postoperative mortality was significantly associated with mild hypoalbuminemia (OR = 1.74; p < 0.001). There were significant associations between mild hypoalbuminemia and 11 postoperative morbidities including deep vein thrombosis, pulmonary embolism, superficial and deep surgical site infection, pneumonia, septic shock, ventilator> 48 h, blood transfusion, return to operating room, stroke and re-intubation. Mild hypoalbuminemia was also associated with overall complication (B = 0.064, p < 0.001) and length of total hospital stay (B = 2.236, p < 0.001).

Conclusions

In colorectal cancer, this is the first propensity score matching study of malnutrition with mild hypoalbuminemia which demonstrates that a mild decrease in serum albumin contributes significantly to poor postoperative outcome.

Keywords

  • Mild hypoalbuminemia
  • Postoperative mortality and morbidity
  • Colorectal cancer
  • Propensity score matching

Background

Malnutrition is a significant risk factor in postoperative mortality, morbidities and length of hospital stay in hospitalized [1], surgical [2] and cancer patients [3]. Preoperative serum albumin serves as an excellent tool to assess malnutrition and to predict patient outcomes and survival [410]. Detection of hypoalbuminemia and appropriate intervention could decrease the complication rates [11] when associated with malnutrition.

In the United States, colorectal cancer is the third most common cancer [12] and it is the most common cancer in Taiwan [13]. Our previous study and other studies in the literature showed that malnutrition with hypoalbuminemia (< 35 g/L) is a predominant problem in colorectal cancer and is associated with poor postoperative outcomes [1416]. Serum albumin is a negative acute-phase protein with reduced expression and increased losses during inflammation processes [17] and in underweight people. Therefore hypoalbminemia is an indicator for malnutrition in acute and chronically ill patients. However, some studies concluded that hypoalbuminemia only becomes clinically significant at levels < 25 g/L [18, 19], and that albumin replacement is only covered by health insurance in Taiwan for patients with serum albumin levels < 30 g/L and who exhibit associated comorbidities. Subgroup analyses of the association between a mild decrease of serum albumin (< 35 and > =30 g/L) and postoperative complications is rare and generally focused on procedures [20]. We wanted to study the effect of mild hypoalbuminemia on the postoperative outcomes in colorectal cancer patients.

The American College of Surgeons-National Surgical Quality Improvement Program (ACS-NSQIP) database records the preoperative comorbidities and postoperative complications of many kinds of operations from more than five hundred medical hospitals in the United States and Canada [21]. Propensity score matching provides a method to minimize bias from observational treatment cohorts and seeks to approximate the characteristics of a randomized clinical trial [22]. The purpose of this study was to apply propensity score matching to this robust database to compare the postoperative outcomes in colorectal cancer patients with mild hypoalbuminemia to those with normal serum albumin.

Methods

Patient selection

Data of the ACS-NSQIP from 2009 to 2013 was utilized to identify colorectal cancer patients using ICD-9 (International Classification of Disease, Ninth Revision) diagnosis codes (Additional file 1). Colorectal cancer patients undergoing related operations were selected by the Current Procedural Terminology (CPT) codes (Additional file 1) in: principle operative procedure; other procedure; or concurrent procedure records.

Postoperative outcomes

The primary outcomes studied were 30-day mortality, all morbidities, overall complication and length of total hospital stay. The postoperative morbidities included: surgical site infection (superficial, deep and organic); wound disruption; urinary tract infection; pneumonia; re-intubation; ventilator> 48 h; pulmonary embolism; deep vein thrombosis; progressive renal insufficiency; acute renal failure; stroke; myocardial infarction; cardiopulmonary resuscitation; blood transfusion; sepsis; septic shock; and return to operating room. Mortality and morbidities were graded and weighted using the Accordion Severity Grading System [23, 24]. The overall complication score was calculated as the sum of the weighted scores in each patient.

Statistical analysis

For our analyses, “control” was defined by a normal serum albumin levels (> = 35 g/L), and “case” was defined by mild hypoalbuminemia (< 35 and > =30 g/L) as measured by laboratory data collected within 2 weeks before surgery. Individual propensity scores were calculated by logistic regression method based on 21 clinical associated factors including age, gender, body mass index, smoking, emergent operation and other comorbidities. A 1:2 ratio propensity score matching study group was created using the Greedy method with a 0.2 caliper width using NCSS 10 software (NCSS Statistical Software, Kaysville, UT, USA) [25]. A chi-square test was used for univariate association. Binary logistic regression method was used to analyze the association between mild hypoalbuminemia and postoperative mortality and morbidity. The association among length of total hospital stay, overall morbidity and mild hypoalbuminemia was analyzed with regression analysis. Tests were two-tailed and statistical significance was defined at p < 0.05. All statistical analyses were performed on SPSS for Windows version 22.

Results

From the database of the ACS-NSQIP during the years 2009 to 2013, a total of 30,676 colorectal cancer patients who received associated surgery were identified. We selected 5230 (17%) with mild hypoalbuminemia (< 35 and > =30 g/L) and 21,310 (70%) with normal serum albumin levels (> = 35 g/L) for further study. Significant differences with respect to 21 clinical characteristics were demonstrated between the two groups (Table 1). The patients with mild hypoalbuminemia were older, more likely to be thin, female, used tobacco and steroids more frequently, had more comorbidities, and higher grades of American Society of Anesthesiologists and wound classification. After 1:2 ratio propensity score matching, 4305 patients with mild hypoalbuminemia and 8610 normal patients were retained for comparison. No significant differences in previously associated covariates were noted between the two groups (Table 1).
Table 1

Selected Cohort Characteristics Before and After Propensity Score-Matching

Variables

Full Cohort

Matched Cohort (1:2)

Albumin (g/dl)

P value

Albumin (g/dl)

P value

< 3.5 and > =3.0 (n = 5230)

> = 3.5 (n = 21,310)

< 3.5 and > =3.0 (n = 4305)

> = 3.5 (n = 8610)

Age, mean (SD), y

70.2(13.7)

65.2(13.6)

< 0.001

68.9(13.8)

69.3(13.1)

0.075

BMI, mean (SD)

27.6(7.2)

28.2(6.5)

< 0.001

28(7.2)

27.9(6.3)

0.441

Gender, male, n(%)

2527(48.3)

11,370(53.4)

< 0.001

2140 (49.7)

4290(49.8)

0.901

Smoking, n(%)

834(15.9)

3125(14.7)

0.02

677(15.7)

1327(15.4)

0.643

Ventilator, n(%)

6(0.1)

12(0.05)

0.146

4(0.09)

3(0.03)

0.181

COPD, n(%)

469(9)

1061(5)

< 0.001

325(7.5)

607(7)

0.301

Ascites, n(%)

108(2.1)

128(0.6)

< 0.001

43(1)

60(0.7)

0.069

CHF, n(%)

137(2.6)

161(0.8)

< 0.001

42(1)

74(0.9)

0.51

Hypertension, n(%)

3104(59.3)

11,492(53.9)

< 0.001

2517(58.5)

5072(58.9)

0.631

Renal failure, n(%)

13(0.2)

27(0.1)

0.042

4(0.1)

15(0.2)

0.256

Dialysis, n(%)

47(0.9)

80(0.4)

< 0.001

21(0.5)

48(0.6)

0.609

DC, n(%)

770(14.7)

1977(9.3)

< 0.001

539(12.5)

1048(12.2)

0.57

Steroid, n(%)

185(3.5)

541(2.5)

< 0.001

140(3.3)

259(3)

0.45

Emergency, n(%)

503(9.6)

834(3.9)

< 0.001

242(5.6)

429(5)

0.123

BWL, n(%)

606(11.6)

1007(4.7)

< 0.001

315(7.3)

574(6.7)

0.169

Diabetes mellitus, n(%)

  

< 0.001

  

0.679

 No

4083(78.1)

17,604(82.6)

 

3415(79.3)

6816(79.1)

 

 Oral

723(13.8)

2702(12.7)

 

607(14.1)

1194(13.9)

 

 Insulin

424(8.1)

1004(4.7)

 

283(6.6)

600(7)

 

Dyspnea

  

< 0.001

  

0.590

 No

4443(85)

19,340(90.8)

 

3753(87.2)

7546(87.7)

 

 Exertion

696(13.3)

1858(8.7)

 

515(12)

1002(11.6)

 

 Rest

91(1.7)

112(0.5)

 

37(0.8)

62(0.7)

 

Systemic sepsis

  

< 0.001

  

0.156

 No

4798(91.7)

20,775(97.5)

 

4148(96.4)

8355(97)

 

 SIRS

303(5.8)

386(1.8)

 

114(2.6)

188(2.2)

 

 Sepsis

118(2.3)

128(0.6)

 

39(0.9)

57(0.7)

 

 Septic shock

11(0.2)

21(0.1)

 

4(0.1)

10(0.1)

 

Functional statusa, n(%)

  

< 0.001

  

0.883

 Independent

4781(91.4)

20,749(97.4)

 

4154(96.5)

8322(96.6)

 

 Partially Dependent

381(7.3)

504(2.4)

 

140(3.2)

266(3.1)

 

 Totally Dependent

68(1.3)

57(0.3)

 

11(0.3)

22(0.3)

 

ASA

  

< 0.001

  

0.169

 I

42(0.8)

519(2.4)

 

42(1)

95(1.1)

 

 II

1256(24)

8779(41.2)

 

1213(28.2)

2273(26.4)

 

 III

3307(63.2)

11,009(51.7)

 

2753(63.9)

5634(65.44)

 

 IV

620(11.9)

996(4.67)

 

295(6.85)

607(7.05)

 

 V

5(0.1)

7(0.03)

 

2(0.05)

1(0.01)

 

Wound

  

< 0.001

  

0.343

 II

4526(86.5)

19,604(92)

 

3885(90.24)

7805(90.6)

 

 III

375(7.2)

1252(5.9)

 

285(6.62)

574(6.7)

 

 IV

329(6.3)

454(2.1)

 

135(3.14)

231(2.7)

 

BMI body mass index, COPD chronic obstructive pulmonary disease, CHF Congestive heart failure, DC Disseminated cancer, BWL body weight loss, ASA American Society of Anesthesiologists, Wound II clean/contamination, Wound III contamination, Wound IV dirty

a assistance from another person for any activities of daily living

Table 2 shows the difference of rates of postoperative outcomes between normal and mild hypoalbuminemia patients before matching. Mortality and all morbidities, except organic surgical site infection, were significantly associated with mild hypoalbuminemia. After matching, the patients with mild hypoalbuminemia still had significantly higher in-hospital mortality rates compared with those with normal albumin levels (2.3% vs. 1.3%; OR = 1.74; p < 0.001) (Table 3). Low serum albumin had significant association with deep vein thrombosis (OR = 1.99; p < 0.001) and pulmonary embolism (OR = 1.55; p = 0.011). Problems related with infection including superficial surgical site infection, deep surgical site infection, pneumonia and septic shock occurred in patients with mild hypoalbuminemia. The other significant postoperative outcomes included ventilator dependence more than 48 h, blood transfusion, return to operating room, stroke and re-intubation. Higher incidence of other postoperative complications, like wound disruption, were noted in the mild hypoalbuminemia patients.
Table 2

The association of postoperative mortality and morbidity in patients grouped by albumin level before propensity score matching

Postop outcomes

Albumin (g/dl)

OR (95% CI)

P value

< 3.5 and > =3.0 (n = 5230)

> = 3.5 (n = 21,310)

30-day mortality

196(3.7)

248(1.2)

3.31(2.74–4.00)

< 0.001

Stroke

40(0.8)

55(0.3)

2.98(1.98–4.48)

< 0.001

DVT

142(2.7)

239(1.1)

2.46(2.00–3.04)

< 0.001

Ventilator> 48 h

183(3.5)

319(1.5)

2.39(1.98–2.87)

< 0.001

Septic shock

159(3)

280(1.3)

2.36(1.93–2.87)

< 0.001

Transfusion

991(18.9)

2009(9.4)

2.25(2.07–2.44)

< 0.001

Re-intubation

177(3.4)

365(1.7)

2.01(1.68–2.41)

< 0.001

Pneumonia

211(4)

457(2.1)

1.92(1.63–2.27)

< 0.001

PRI

70(1.3)

163(0.8)

1.76(1.33–2.33)

< 0.001

Deep SSI

113(2.2)

302(1.4)

1.54(1.24–1.91)

< 0.001

Sepsis

245(4.7)

715(3.4)

1.42(1.22–1.64)

< 0.001

UTI

217(4.1)

646(3)

1.39(1.18–1.62)

< 0.001

Return to OR

353(6.7)

1068(5)

1.37(1.21–1.55)

< 0.001

Superficial SSI

430(8.2)

1411(6.6)

1.26(1.13–1.41)

< 0.001

ARF

49(0.9)

116(0.5)

1.73(1.24–2.42)

0.001

PE

71(1.4)

180(0.8)

1.62(1.23–2.13)

0.001

CPR

44(0.8)

103(0.5)

1.75(1.23–2.49)

0.002

MI

63(1.2)

163(0.8)

1.58(1.18–2.12)

0.002

Wound disruption

85(1.6)

259(1.2)

1.34(1.05–1.72)

0.019

Organ SSI

216(4.1)

869(4.1)

1.01(0.87–1.18)

0.865

Values in parentheses are percentage

DVT deep vein thrombosis, PRI progressive renal insufficiency, SSI surgical site infection, UTI urinary tract infection, OR operating room, ARF acute renal failure, PE pulmonary embolism, CPR cardiopulmonary resuscitation, MI myocardial infarction

Table 3

The association of postoperative mortality and morbidity in patients grouped by albumin level after propensity score matching

Postop outcomes

Albumin (g/dl)

OR (95% CI)

P value

< 3.5 and > =3.0 (n = 4305)

> = 3.5 (n = 8610)

30-day mortality

98(2.3)

114(1.3)

1.74(1.32–2.28)

< 0.001

DVT

109(2.5)

111(1.3)

1.99(1.52–2.60)

< 0.001

Ventilator> 48 h

113(2.6)

145(1.7)

1.57(1.23–2.02)

< 0.001

Transfusion

737(17.1)

991(11.5)

1.59(1.43–1.76)

< 0.001

Return to OR

291(6.8)

447(5.2)

1.32(1.14–1.54)

< 0.001

Superficial SSI

367(8.5)

599(7)

1.25(1.09–1.42)

0.001

Pneumonia

151(3.5)

214(2.5)

1.43(1.15–1.76)

0.001

Septic shock

100(2.3)

133(1.5)

1.52(1.17–1.97)

0.002

Deep SSI

98(2.3)

138(1.6)

1.43(1.10–1.86)

0.007

PE

60(1.4)

78(0.9)

1.55(1.10–2.17)

0.011

Stroke

27(0.6)

28(0.3)

1.93(1.14–3.29)

0.013

Re-intubation

124(2.9)

193(2.2)

1.29(1.03–1.63)

0.027

Sepsis

189(4.4)

320(3.7)

1.19(0.99–1.43)

0.064

UTI

173(4)

304(3.5)

1.14(0.95–1.38)

0.166

Wound disruption

69(1.6)

116(1.3)

1.19(0.88–1.61)

0.249

PRI

47(1.1)

76(0.9)

1.24(0.86–1.79)

0.249

ARF

31(0.7)

48(0.6)

1.29(0.82–2.04)

0.264

MI

50(1.2)

91(1.1)

1.10(0.78–1.56)

0.590

Organ SSI

176(4.1)

366(4.3)

0.96(0.80–1.15)

0.664

CPR

26(0.6)

51(0.6)

1.02(0.64–1.64)

0.936

Values in parentheses are percentage

DVT deep vein thrombosis, OR operating room, SSI surgical site infection, PE pulmonary embolism, PRI progressive renal insufficiency, ARF acute renal failure, UTI urinary tract infection, CPR cardiopulmonary resuscitation, MI myocardial infarction

Regression analyses revealed that overall complication and length of total hospital stay were associated with mild hypoalbuminemia. After matching, both overall complication (B = 0.064, p < 0.001) and length of total hospital stay (B = 2.236, p < 0.001) were still greater in the mild hypoalbuminemia group than in the group with normal serum albumin levels (Table 4).
Table 4

Regression analysis of overall complication and length of total hospital stay in patients grouped by albumin level before and after propensity score matching

Post-operative outcomes

Albumin (g/dl)

Mean

B (coefficient)

95% C.I.

P value

Overall Complicationb

< 3.5 and > =3.0

0.2821

0.121

0.107–0.135

< 0.001

> = 3.5

0.1612

0

0

 

Length of total hospital stayb

< 3.5 and > =3.0

11.0069

3.453

3.201–3.705

< 0.001

> = 3.5

7.5539

0

0

 

Overall Complicationa

< 3.5 and > =3.0

0.2468

0.064

0.047–0.082

< 0.001

> = 3.5

0.1826

0

0

 

Length of total hospital staya

< 3.5 and > =3.0

10.4407

2.236

1.902–2.57

< 0.001

> = 3.5

8.2045

0

0

 

b before; a after

Discussion

Using the nationally validated ACS-NSQIP database, our multi-institutional study demonstrates the effects of mild hypoalbuminemia on postoperative outcomes of colorectal cancer patients. We matched mild hypoalbuminemia patients and patients with normal serum albumin levels using a propensity score matching method to decrease the biases associated with the selecting of two groups with significant differences in other clinical characteristics. After matching, postoperative mortality, overall complication and length of hospital stay were still associated with mild hypoalbuminemia.

The association between hypoalbuminemia and comorbidities has been discussed in the literature. Hospitalized patients with mild hypoalbuminemia (albumin 25–35 g/L) were older, lower body mass index, and more hypertension, congestive heart failure and chronic renal failure than those with normal albumin levels [9]. Severe hypoalbuminemia was noted in 4% of chronic obstructive pulmonary disease patient and was a strong risk factor for developing acute renal failure [26]. The rates of hypoalbuminemia ranged from 20 to 25% in chronic heart failure patients to 90% in weak, elderly patients suffering from acute heart failure [27]. In our study, mild hypoalbuminemia was not rare and was significantly associated with many comorbidities in colorectal cancer patients. Because there is more postoperative risk associated with even mild hypoalbuminemia, early identification of malnutrition in patients with multiple comorbidities is recommended.

In our retrospective study, randomization was not possible. However, strong associations between mild hypoalbuminemia and the patients’ clinical characteristics were demonstrated. We used a propensity score matching method to reduce the bias in estimating the effect of mild hypoalbuminemia on postoperative outcomes, and the likelihood of confounding when analyzing the observational data [28]. After matching, a mild decrease in serum albumin level still had serious effects on postoperative outcomes including increased mortality, morbidities, overall complication and length of total hospital stay.

After matching, venous thromboembolism (VTE), including deep vein thrombosis (OR = 1.99) and pulmonary embolism (OR = 1.55) was associated with mild hypoalbuminemia in our study. Aaron et al. [29] demonstrated low serum albumin was a modest marker of an increased risk of venous thromboembolism after adjusting for age, sex, race, use of hormone replacement therapy, estimated GFR, history of cancer, and diabetes. The adjusted hazard ratio for albumin below the fifth percentile was 1.28 and 1.8 in their two cohorts’ data. Hypoalbuminemia (serum albumin level < 35 mg/L) was reported to be associated with deep vein thrombosis (AOR 1.69) in colon and rectal surgery [30]. In cancer patients, a similar result was also noted [31]. The mechanism of association between hypoalbuminemia and VTE is poorly understood but may be due to hyperinflammatory or hypercoagulable states. Further studies of the mechanism are necessary, and closer monitoring for VTE in cancer patients with hypoalbuminemia is recommended.

A multi-institutional study showed preoperative hypoalbuminemia (serum albumin < 30 g/L) was an independent predictor for development of superficial and deep surgical site infection and prolonged hospital stay following gastrointestinal surgery [32]. The associations were also reported in other operative procedures [3335]. In our study, a mild decrease in serum albumin also had a significant effect on surgical site infection, pneumonia, septic shock and length of total hospital stay. Low serum albumin was an excellent assessment tool for malnutrition [14], which was associated with poor wound healing [36] and infection [37]. Albumin serves an immunomodulatory role [38], and impairment of macrophage activation and granuloma formation were noted in hypoalbuminemic mice [39]. Serum albumin is a negative acute-phase protein during inflammatory reaction by bacterial infection [40]. These factors may promote surgical site infection and pneumonia in hypoalbuminemia and in mild hypoalbuminemic colorectal cancer patients.

There are several limitations to our study. First, the database only records the events that happened during the 30-day postoperative period, so it may not correctly estimate the true rate of postoperative outcomes, some of which may have occurred after 30 days. Second, nutritional supplementation may have been given to mild hypoalbuminemia patients and the information was not recorded. This means that part of the patients with mild hypoalbuminemia might receive supplementation pre- and postoperatively and their outcome was supposedly improved. The data of patients being purely without nutrition supplementation would make the results, ie. the mild hypoalbuminemia associated with worse outcome more contrasting. In addition, some of the important postoperative complications associated with colorectal surgery, like anastomotic leakage and ileus were not included in the database. Finally, the database has no cancer-specific variables like stage and tumor size, which may interact with mild hypoalbuminemia in postoperative outcome evaluation. We excluded the patients who only received palliative surgery to minimize the effect of the advanced stage on postoperative complications.

Conclusions

In colorectal cancer patients, malnutrition with mild hypoalbuminemia is a common problem and associated with more comorbidities. After propensity score matching, a significant association with many postoperative complications was demonstrated. Randomized controlled trials are needed to evaluate if early identification and aggressive nutritional intervention in patients with even mild hypoalbuminemia would reduce the rate of postoperative complications and improve postoperative outcomes.

Abbreviations

ACS-NSQIP: 

American College of Surgeons-National Surgical Quality Improvement Program

CPT: 

Current Procedural Terminology

ICD-9: 

International Classification of Disease, Ninth Revision

Declarations

Acknowledgements

We thank Prof. Sheng-Nan Lu, Chih-Yun Lin, Shin-Yi Chien, and the Biostatistics Center, Kaohsiung Chang Gung Memorial Hospital for statistics work.

Funding

There is no any funding for the research.

Authors’ contributions

WHH was involved in interpretation of data, statistical analysis and drafting the manuscript. SE and LP participated in revising the manuscript for important intellectual content. SR was responsible for study design and final approval of the manuscript. All authors read and approved the final manuscript.

Ethics approval and consent to participate

The data is de-identified and contains no patient information. The data is considered exempt from human subjects review.

Consent for publication

Our manuscript doesn’t contain any individual person’s data.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Colorectal Surgery, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of Medicine, Kaohsiung, Taiwan
(2)
Department of Surgery, University of California, San Diego Health System, La Jolla, San Diego, CA, USA
(3)
Department of Surgery and Rebecca and John Moores Cancer Center, University of California San Diego, 3855 Health Sciences Drive, La Jolla, San Diego, CA 92093, USA

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