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Influence of nutritional status and body composition on postoperative events and outcome in patients treated for primary localized retroperitoneal sarcoma

Manuel Ramanovic
Manuel Ramanovic
, 
Marko Novak
Marko Novak
, 
Andraz Perhavec
Andraz Perhavec
, 
Taja Jordan
Taja Jordan
, 
Karteek Popuri
Karteek Popuri
 et 
Nada Rotovnik Kozjek
Nada Rotovnik Kozjek
   | 21 févr. 2024
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Article Category: Research Article
Publié en ligne: 21 févr. 2024
Pages: 110 - 123
Reçu: 26 juil. 2023
Accepté: 03 nov. 2023
DOI: https://doi.org/10.2478/raon-2024-0013
Mots clés
© 2024 Manuel Ramanovic et al., published by Sciendo
This work is licensed under the Creative Commons Attribution 4.0 International License.

FIGURE 1.

Patients' flow diagram. Out of 123 patients, 58 (47.1%) with primary localized retrperitoneal sarcomas (RPS) were included in the study and 65 were excluded. 34 (27.6%) were excluded as they presented as primary metastatic cases (6), locally recurrent cases (14) or cases with residual disease after operation elsewhere (14), and 31 patients (25.2%) were excluded as they had CT performed > 30 days from initial assessment or CT image was not technically adequate for analysis
Patients' flow diagram. Out of 123 patients, 58 (47.1%) with primary localized retrperitoneal sarcomas (RPS) were included in the study and 65 were excluded. 34 (27.6%) were excluded as they presented as primary metastatic cases (6), locally recurrent cases (14) or cases with residual disease after operation elsewhere (14), and 31 patients (25.2%) were excluded as they had CT performed > 30 days from initial assessment or CT image was not technically adequate for analysis

FIGURE 2.

Kaplan-Meier curves for OS (A–D) and forest plots of multivariate Cox regression analysis of factors associated with OS (E) and LRFS (F). Kaplan-Meier curves for OS according to presence of: (A) myopenia based on EWGSOP2 criteria (red = myopenic, blue = non-myopenic), (B) cancer cachexia (red = cachectic, blue = non-cachectic), (C) high SATI (red = SATI above estimated cohort cut-off, blue = SATI below estimated cohort cut-off) and (D) high VSR (red = VSR > 0.26, blue = VSR < 0.26);EWGSOP2 = The European Working Group on Sarcopenia in Older People revised criteria from 2018; SATI = Subcutaneous Adipose Tissue Index, cm2/m2; SMI = Skeletal Muscle Index; VSR = Visceral-to-subcutaneous adipose tissue area ratio; OS = Overall survival; LRFS = Local recurrence-free survival; HR = Hazard ratio; AIC = Akaike Information Criterion
Kaplan-Meier curves for OS (A–D) and forest plots of multivariate Cox regression analysis of factors associated with OS (E) and LRFS (F). Kaplan-Meier curves for OS according to presence of: (A) myopenia based on EWGSOP2 criteria (red = myopenic, blue = non-myopenic), (B) cancer cachexia (red = cachectic, blue = non-cachectic), (C) high SATI (red = SATI above estimated cohort cut-off, blue = SATI below estimated cohort cut-off) and (D) high VSR (red = VSR > 0.26, blue = VSR < 0.26);EWGSOP2 = The European Working Group on Sarcopenia in Older People revised criteria from 2018; SATI = Subcutaneous Adipose Tissue Index, cm2/m2; SMI = Skeletal Muscle Index; VSR = Visceral-to-subcutaneous adipose tissue area ratio; OS = Overall survival; LRFS = Local recurrence-free survival; HR = Hazard ratio; AIC = Akaike Information Criterion

FIGURE 3.

Association between overall morbidity following surgery for primary RPS and body composition (A–F) and linear correlation analysis between VSR and VATI (G) and VSR and fat mass (H). VSR (F) and intraoperative blood loss (E) independently predicted worse postoperative outcome. In multivariate analysis skeletal muscle index (SMA), lean body mass (LBM), subcutaneous adipose tissue area (SAT) and visceral adipose tissue area (VAT) were not associated with statistically higher overall postoperative morbidity (A–D).VATI = Visceral Adipose Tissue Index; VSR = Visceral-to-subcutaneous adipose tissue area ratio. ȓPearson = Pearson Correlation Coefficient; tStudent = result of t-test for correlation
Association between overall morbidity following surgery for primary RPS and body composition (A–F) and linear correlation analysis between VSR and VATI (G) and VSR and fat mass (H). VSR (F) and intraoperative blood loss (E) independently predicted worse postoperative outcome. In multivariate analysis skeletal muscle index (SMA), lean body mass (LBM), subcutaneous adipose tissue area (SAT) and visceral adipose tissue area (VAT) were not associated with statistically higher overall postoperative morbidity (A–D).VATI = Visceral Adipose Tissue Index; VSR = Visceral-to-subcutaneous adipose tissue area ratio. ȓPearson = Pearson Correlation Coefficient; tStudent = result of t-test for correlation

Results of optimal stratification analysis for body composition parameters

BMI, kg/m2 Skeletal Muscle Indexa, cm2/m2 Visceral Adipose Tissue Indexb, cm2/m2 Subcutaneous Adipose Tissue Indexb, cm2/m2 Visceral to subcutaneous ratioc Muscle Radiation Attenuationd, HU
Male Female Male Female Male Female Male Female Male Male
< 25 49.21 49.21 61.38 25.55 49.23 86.89 0.26 47.41
≥ 25 49.90 50.64 35.88

Summary of univariate and multivariate analysis of association between body composition and outcome following surgery for primary RPS

Clinicopathological factor Length of hospital stay (> 10 days) Clavien-Dindo > IIIa Any complication (overall morbidity)
Uni-variable Multi-variable Uni-variable Multi-variable Uni-variable Multi-variable
OR (95% CI) p OR (95% CI) p OR (95% CI) p OR (95% CI) p OR (95% CI) p OR (95% CI) p
Myopenia, yes vs. noa 1.34 (0.38–5.54) 0.664 - - 0.32 (0.07–1.18) 0.112 - - 3.11 (0.85–15.08) 0.112 - -
Visceral obesity, yes vs. no 2.54 (0.68–12.40) 0.196 - - 0.65 (0.18–2.13) 0.49 - - 3.61 (1.09–14.44) 0.047 - -
Myopenic obesity, yes vs. no 0.01 (0.00–0.001) 0.993 - - 20090605.83 (0.00–NA) 0.993 - - 279.10 (0.00–NA) 0.993 - -
Myosteatosis, yes vs. no 1.39 (0.39–5.76) 0.626 - - 2.17 (0.58–10.58) 0.282 - - 5.05 (1.39–24.41) 0.023 4.63 (1.03–28.42) 0.063
Cancer cachexia, yes vs. no 0.68 (0.18–2.94) 0.585 - - 2.83 (0.76–10.59) 0.117 - - 0.95 (0.27–3.60) 0.935 - -
Body mass index, kg/m2 1.00 (0.89–1.14) 0.992 - - 0.94 (0.81–1.06) 0.351 - - 0.95 (0.27–3.60) 0.935 - -
Skeletal Muscle Area, HU 1.00 (0.99–1.02) 0.869 - - 1.00 (0.98–1.01) 0.679 - - 1.00 (0.99–1.02) 0.681 - -
Skeletal Muscle Index, cm2/m2 1.00 (0.95–1.07) 0.88 - - 1.00 (0.95–1.06) 0.909 - - 1.04 (0.98–1.10) 0.230 - -
Muscle Radiation Attenuation, HU 0.98 (0.92–1.04) 0.526 - - 0.99 (0.93–1.05) 0.775 - - 0.94 (0.88–1.00) 0.076 - -
SAT, cm2 1.00 (0.99–1.00) 0.336 - - 1.00 (0.99–1.00) 0.48 - - 1.00 (0.99–1.01) 0.866 - -
VAT, cm2 1.00 (1.00–1.01) 0.769 - - 1.00 (0.99–1.00) 0.622 - - 1.00 (1.00–1.01) 0.205 - -
VSR 1.55 (0.53–5.51) 0.456 - - 1.09 (0.39–2.861) 0.861 - - 1.72 (0.66–5.19) 0.292 - -
High VSRb, yes vs. no 2.50 (0.63–9.52) 0.179 - - 2.75 (0.63–19.26) 0.224 - - 6.19 (1.69–26.52) 0.008 5.05 (1.08–29.74) 0.05
Body fat, % 0.96 (0.87–1.05) 0.380 - - 1.00 (0.92–1.09) 0.962 - - 1.00 (0.93–1.09) 0.912 - -
Lean Body Mass, kg 1.01 (0.96–1.07) 0.765 - - 1.02 (0.97–1.08) 0.381 - - 1.02 (0.97–1.08) 0.381 - -
SATI, cm2/m2 0.99 (0.97–1.01) 0.279 - - 0.99 (0.97–1.01) 0.344 - - 1.00 (0.99–1.02) 0.794 - -
VATI, cm2/m2 1.00 (0.99–1.02) 0.625 - - 1.00 (0.98–1.01) 0.706 - - 1.01 (1.00–1.04) 0.122 - -
High SATIc, yes vs. no 1.80 (0.52–6.25) 0.346 - - 0.90 (0.26–2.93) 0.863 - - 1.50 (0.49–4.81) 0.481 - -
High VATId, yes vs. no 0.49 (0.10–1.87) 0.327 - - 0.38 (0.08–1.44) 0.184 - - 2.83 (0.84–11.45) 0.111 - -

Clinical characteristics of study population

Clinical characteristic (N = 58) Median (IQR); n (%)
Age, years 61.0 (46.0 – 67.0)
Gender
  Male 34 (58.6%)
  Female 24 (41.4%)
ASA grade
  1 9 (16%)
  2 30 (52%)
  3 16 (28%)
  4 3 (5.2%)
Baseline albumin, g/L 41.0 (34.2 – 45.0)
Baseline C-reactive protein, mg/L 13.5 (2.0 – 66.5)
Neutrophil-lymphocyte ratio 3.3 (2.1 – 4.7)
Body Mass Index, kg/m2 26.0 (24.7 – 29.7)
Nutrition and body composition characteristics
Nutritional team support before operation 28(48.3%)
Skeletal Muscle Area, cm2 45.5 (115.9 – 170.1)
Visceral Fat Area, cm2 104.5 (53.6 – 168.7)
Subcutaneous Adipose Tissue Area, cm2 167.9 (127.9 – 231.6)
Total Fat Area, cm2 23.6 (19.8 – 29.1)
Total Body Fat, % 30.6 (26.8 – 32.4)
Lean Body Mass, kg 52.7 (50.0 – 57.2)
Skeletal Muscle Index, cm2/m2 50.2 (44.0 – 55.6)
Appendicular Skeletal Muscle Index, cm2/m2 6.70 (6.00 – 7.3)
Myopenia based on estimated cut-off value for SMIa 18 (31.0%)
Myopenia based on EWGSOP2 criteria for SMI 19 (32.8%)
Cancer cachexia 13 (22.4%)
Visceral obesity 21 (36.2%)
Myopenic obesity 4 (6.9%)
Myosteatosisa 37 (63.7%)
Pathologic characteristics and postoperative outcome data
Postoperative (90 day) complication rate 37 (64%)
  Abdominal complication 24 (41%)
  Systemic complication 17 (29%)
  Abdominal and systemic complications 5 (9.0%)
Clavien-Dindo > IIIa
  Yes 17 (29%)
  No 41 (71%)
Comprehensive Complication Index 20.92 (0.0–32.55)
Histologic type
  Liposarcoma 35 (60%)
  Leiomyosarcoma 9 (16%)
  Pleomorphic sarcoma 1 (1.7%)
  Other 13 (22%)
Tumour size, cm 20 (11–30)
FNCLCC grade
  1 15 (26%)
  2 11 (19%)
  3 23 (40%)
  Unknown 9 (16%)
Stage AJCC (8th edition)
  1A 1 (1.7%)
  1B 23 (40%)
  3A 6 (10%)
  3B 28 (48%)
Completeness of surgical resection
  R0 47 (81%)
  R1/R2 11 (19%)

Comparison of clinical and body composition parameters between myopenic and non-myopenic patients (EGSWOP2 criteria)

Clinicopathological factor Levela Myopenicb Non Myopenicb p
Age, years Median (IQR) 66.0 (50.5–71.5) 61.0 (46.0–64.8) 0.236
Gender Male 11(57.9) 23 (60.5) 1
Female 8(42.1) 15 (39.5)
ASA Grade, 2–3 vs. 1 1 3 (15.8) 6 (15.8) 1
2–3 16 (84.2) 32 84.2)
FNCLCC Grade 1 5 (29.4) 10 (32.3) 0.547
2 5 (29.4) 5 (16.1)
3 7 (41.2) 16 (51.6)
(Missing) 7 (18.4) 2 (10.5)
Tumour size, cm Median (IQR) 26.0 (20.5–34.0) 17.5 (10.0–24.8) 0.005
Clavien-Dindo > IIIa Yes 3 (15.8) 14 (36.8) 0.183
No 16 (84.2) 24 (63.2)
Neutrophil-lymphocyte ratio Median (IQR) 3.9 (2.4–4.7) 3.0 (2.1–4.7) 0.504
Baseline albumin, g/L Median (IQR) 40.0 (32.0–42.5) 43.0 (35.0–45.8) 0.232
Baseline C-reactive protein, mg/L Median (IQR) 44.0 (7.5–99.5) 6.0 (2.0–45.0) 0.088
Haemoglobin level, g/L Median (IQR) 128.0 (101.5–136.5) 132.5 (115.2–145.8) 0.141
Preoperative radiotherapy No 19 (100.0) 37 (97.4) 1
Yes 0 (0.0) 1 (2.6)
Resection status R0 17 (89.5) 29 (76.3) 0.406
R1 2 (10.5) 9 (23.7)
Intraoperative blood loss, ml Median (IQR) 1300.0 (425.0–4100.0) 1350.0 (500.0–2075.0) 0.78
Stage AJCC, 8th edition 1A–1B 7 (36.8) 17 (44.7) 0.776
3A–3B 12 (63.2) 21 (55.3)
Histology subtype Pleomorphic 1 (5.3) 0 (0.0) 0.184
Liposarcoma 14 (73.7) 21 (55.3)
Leiomyosarcoma 2 (10.5) 6 (15.8)
Other 2 (10.5) 11 (28.9)
Nutrition team before surgery Yes 12 (63.2) 16 (42.1) 0.223
No 7 (36.8) 22 (57.9)
Length of hospital stay, days Median (IQR) 20.0 (11.0–28.8) 15.0 (11.5–27.0) 0.593
Visceral obesity Yes 4 (21.1) 16 (42.1) 0.202
No 15 (78.9) 22 (57.9)
Myosteatosis Yes 16 (84.2) 21 (56.8) 0.079
No 3 (15.8) 16 (43.2)
Cancer cachexia No 12 (63.2) 31 (83.8) 0.163
Yes 7 (36.8) 6 (16.2)
Body Mass Index, kg/m2 Median (IQR) 25.7 (23.3–27.2) 26.9 (24.8–30.9) 0.071
Skeletal Muscle Area, HU Median (IQR) 115.8 (106.5–153.3) 149.9 (130.6–177.1) 0.019
Skeletal Muscle Index, cm2/m2 Median (IQR) 41.0 (38.3–46.8) 53.5 (46.2–58.8) < 0.001
Muscle Radiation Attenuation, HU Median (IQR) 35.6 (31.8–43.2) 38.1 (29.9–42.2) 0.959
Subcutaneous Adipose Tissue Area, cm2 Median (IQR) 156.4 (103.2–194.4) 185.4 (131.4–254.1) 0.078
Visceral Adipose Tissue Area, cm2 Median (IQR) 64.6 (38.1–131.6) 125.5 (66.1–201.7) 0.07
Visceral-to-subcutaneous adipose tissue area ratio Median (IQR) 0.5 (0.2–0.9) 0.8 (0.3–1.1) 0.393
Body fat, % Median (IQR) 28.3 (21.3–31.6) 31.1 (28.1–33.3) 0.024
Lean Body Mass, kg Median (IQR) 52.5 (50.4–57.7) 52.8 (49.8–56.4) 0.684
Subcutaneous Adipose Tissue Index, cm2/m2 Median (IQR) 46.8 (30.6–67.2) 64.6(43.9–95.0) 0.048
Visceral Adipose Tissue Index, cm2/m2 Median (IQR) 20.6 (13.2–43.8) 42.3 (24.2–63.6) 0.025
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