Table 2.
Characteristics of all included studies.
| Reference (author, year) | Country | Study period | Type of study | Indication to surgery | Comparator | Parameter | Pre-operative imaging | N° patients | Male Sex, n (%) | Age, median (range) or mean (SD) | BMI (kg/mq), median (range) or mean (SD) |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Peng (2011) | USA | 2000-2009 | Retrospective | CRLM | Sarcopenia, Sarcopenic obesity | TPA, BMI | CT | 259. S/NS: 41/218 | 155 (60). S: 8 (19.5); NS: 147 (67.4); (p<0.001) | 58 (12). S: 59 (1.4); NS: 58 (1.2); (p=0.68) | <30 (74); >30 (26) |
| Van Vledder (2012) | Netherlands | 2001-2009 | Retrospective | CRLM | Sarcopenia, central obesity | SMM, intra-abdominal fat | CT (perioperative) | 196. S/NS: 38/158 | 120. S/NS: 11/109 (p<0.001) | 64.5 (31–86). S/NS: 65.5 (47–84)/65.0 (31–86); (p=0.229) | S: 23.7 (3.0); NS: 26.7 (3.5); (p<0.001) |
| Harimoto (2013) | Japan | 2004-2009 | Retrospective | HCC | Sarcopenia | SMM | CT | 186. S/NS: 75/111 | S/NS: 50/95; (p=0.004) | S: 67 (11); NS: 66 (10); (p=0.55) | S: 20.5(2.4); NS: 24.0 (2.8); (p<0.001) |
| Lodewick (2014) | Netherlands, Germany, UK | 2005-2012 | Retrospective | CRLM | Sarcopenia, obesity, sarcopenic obesity | L3 MI, BMI | CT (within 3 months before surgery) | 171. S/NS: 80/91. O/NO: 69/102. SO/NSO: 49/102 | NA | 64 (24–86). S/NS: 65 (39–86)/64 (24–83); (ns). O/NO: 66 (41–86)/64 (24–83); (ns). SO/NSO: 67 (41–86)/64 (24–83); (ns) | 25.7 (18.4-42.8) |
| Itoh (2014) | Japan | 2004-2009 | Retrospective | HCC | visceral fat area | VFA | CT | 190. Low/High VFA: 84/106 | Low/High-VFA: 67 (80)/69 (65); (p=0.395) | Low/High-VFA: 68 (34–87)/69 (31–83); (p=0.918) | Low/High-VFA: 20.5 (14.2–26.1)/24.0 (18.7–32.1); (p<0.001) |
| Valero III (2014) | USA | 2000-2013 | Retrospective | Primary liver tumors (HCC, ICC) | Sarcopenia | TPA, TPV | CT (<60 days before surgery or <10 days after) | 96. S (TPA)/S (TPV): 44 (45.8)/47 (48.9); (p=0.12) | 59 (61.5) | 61.9 (12.3) | 27.4 (5.4) |
| Levolger (2015) | Netherlands | 2002-2013 | Retrospective | HCC | Sarcopenia | SMI | CT (<3 months prior to or >3 days after treatment) | 90; resected: 71 (67.8). SR/NSR: 36 (69.2)/25 (65.8) | S/NS: 39 (75.0)/24 (63.2); (p=0.226) | S/NS: 61 (22–86)/62 (25–77); (p=0.48) | S/NS: 24.7 (17.6–33.4)/26.0 (19.5–37.8); (p=0.003) |
| Otsuji (2015) | Japan | 2008-2014 | Retrospective | pCCA | Sarcopenia | TPA | preoperative abdominal/pelvic CT <30 days prior to surgery |
256. S/NS: 85/171 | 162 (63). S/NS: 461 (58)/66.1 (107); (p=0.954) | 67 (34–85). S/NS: 69 (9)/67 (10); (p=0.133) | 21.5 (15.1–30.8). S/NS: 20.5 (2.3)/22.0 (2.7); (p<0.001) |
| Voron (2015) | France | 2006-2012 | Retrospective | HCC | Sarcopenia | SMI | CT (<2 months before surgery or <7 days after surgery) |
109. S/NS: 59/50 | 92 (84.4); S/NS: 53 (90)/39 (78); (p=0.09) | 61.6 (13.3). S/NS: 64.55 (12.92)/58.25 (13.08); (p=0.013) | 25.64 (4.49). S/NS: 24.62 (4.67)/26.85 (3.98); (p=0.009) |
| Coelen (2015) | Netherlands | 1998-2013 | Retrospective | pCCA | Total skeletal muscle mass at L3 |
low skeletal muscle mass | CT | 100 (normal/low SMM: 58/42) | normal/low SMM: 36/28; (p=0.636) | normal/low SMM: 62 (9)/61 (11); (p=0.520) | normal/low SMM: 26 (3)/24 (3); (p=0.001) |
| Hamaguchi (2015) | Japan | 2005-2014 | Retrospective | HCC | Sarcopenia (skeletal muscle quality) | IMAC | CT | 477. High/normal-IMAC: 209/268 | 389 (82). High/normal-IMAC: 171 (82)/218 (81); (p=0.8944) | 67 (10). High/normal-IMAC: 71 (7)/64 (10); (p<0.0001) | 23.1 (3.4). High/normal-IMAC: 23.9 (3.6)/22.6 (3.1); (p=0.0002) |
| Harimoto (2016) | Japan | 2004-2013 | Retrospective | HCC | Sarcopenia | L3-SMA | CT | 296. S/NS: 57/82 | S/NS: 40/58; (p=0.943) | S/NS: 76.5 (3.9)/75.9 (4.0); (p= 0.345) | S/NS: 23.3 (3.2)/23.0 (3.5); (p=0.6445) |
| Kamachi (2016) | Japan | 2005-2013 | Retrospective | HCC | Sarcopenia | L3-SMI | CT | 92. S/NS: 61/31. LR: 35 (57)/11 (35); (p=0.05). RFA 26 (43)/20 (65) |
S/NS: 51 (84)/14 (45); (p<0.01) | S/NS: 73 (49–84)/70 (47–80); (p=0.14) | S/NS: 21.2 (14.6–29.7)/24.6 (19.4–33.6); (p<0.01) |
| Takagi (2016) | Japan | 2007 - 2013 | Retrospective | HCC | Sarcopenia, ASA score | SMI | CT <3 months prior to surgery | 254. S/NS: 118/136 | 207. S/NS: 93/114; (p=0.31) | 65.7 (10.5). S/NS: 68.6 (10.0)/63.1 (10.3); (p<0.001) | 23.7 (3.5). S/NS: 22.0 (3.0)/25.2 (3.3); (p<0.001) |
| Higashi (2016) | Japan | 2007 - 2013 | Retrospective | Any malignancy requiring liver resection | Sarcopenia, Visceral fat amount | L3-SMI, L3-VFA | CT | 144. S/NS: 72/72. Low/High VFA: 75/69 | 108. S/NS: 54/54 (ns). Low/High VFA: 55/53 (ns) | 65.1 (10.1). S/NS: 64.9 (11.6)/65.4 (8.4); (p=0.95). Low/High VFA: 65 (10.4)/65 (9.7); (p=0.99) | 22.9 (4.2). S/NS: 21.6 (4.7)/24.2 (3.2); (p=0.0012). Low/High VFA: 21.3 (4.4)/24.7 (3.2); (p<0.001) |
| Hamaguchi (2016) | Japan | 2005 - 2014 | Retrospective | HCC | Sarcopenia, quality of skeletal muscle | PMI, IMAC | CT | 492. High/normal-IMAC: 219/273 | 403 (82). High/normal-IMAC: 180 (82)/223 (82); (p=0.885) | 68 years (31–89). High/normal-IMAC: 71 (8)/64 (10); (p<0.001) | 23.2 (3.4). High/normal-IMAC: 23.9 (3.6)/22.6 (3.1); (p<0.001) |
| Yabusaki (2016) | Japan | 2003-2014 | Retrospective | HCC | Sarcopenia | SMI, VFA | CT | 195. Low/high-SMI: 89/106 | 157 (80). Low/high-SMI: 57(64)/100(94); (p<0.001) | 66 (22-80). Low/high-SMI: 66.2 (10.1)/63.8 (10.1); (p=0.100) | 23.2 (14.3-37.3); Low/high-SMI: 21.8 (2.6)/24.3 (3.5); (p<0.001) |
| Kobayashi (2016) | Japan | 2007-2012 | Retrospective | HCC | Quality and quantity of skeletal muscle | IMAC, PMI (ΔIMAC, ΔPMI) | CT | 241. Preoperative normal IMAC: 112 (High/Low ΔIMAC 6 M: 32/43. High/Low ΔPMI 6 M: 24/51) | NA | NA | NA |
| Kobayashi (2017) | Japan | 2005-2015 | Retrospective | HCC | Sarcopenia, obesity, sarcopenic obesity | SMI, BMI | CT | 465. NN/NO/SN/SO: 184 (39.5)/ 219 (47.1)/31 (6.7)/31 (6.7) |
367 (78.9). NN/NO/SN/SO: 124 (67.4)/188 (85.8)/24 (77.4)/31 (100); (p<0.001) | 67.6 (9.60). NN/NO/SN/SO: 66.0 (10.1)/67.9 (9.2)/69.5 (9.0)/73.6 (7.8); (p<0.001) | 23.4 (3.6). NN/NO/SN/SO: 21.7 (2.4)/25.6 (3.3)/18.7 (2.1)/22.5 (2.9); (p<0.001) |
| Okumura (2017) | Japan | 2004-2015 | Retrospective | iCCA | Skeletal muscle mass, skeletal muscle quality, visceral adiposity | SMI, MA, VSR | CT (<2 months before operation) | 109. Low/High SMI: 69/40. Low/High MA: 53/56. Low/High VSR: 23/86 | 67 (61). Low/High SMI: 45/22 (p=0.291). Low/High MA: 35/32 (p=0.340). Low/High VSR: 11/56 (p=0.130) | 68 (61–73). Low/High SMI: 69 (63–74)/64.5 (55–71); (p=0.027). Low/High MA: 69 (65–77)/64 (54–71); (p<0.001). Low/High VSR: 63 (48-75)/68 (63–73); (p=0.137) | 21.9 (19.9–24.4). Low/High SMI: 21.4 (19.6–23.9)/22.7 (20.4–25.8); (p=0.042). Low/High MA: 23.3 (20.9–25.2)/21.1 (19.2–22.4) (p<0.001). Low/High VSR: 21.2(19.2–23.3)/22.1 (20.3–24.4); (p=0.333) |
| Eriksson (2017) | Sweden | 2010-2014 | Retrospective | CRLM | Muscle mass | SMI (if NAC muscle mass loss/no loss). | CT | 225. S/NS: 147/78. NAC: 97 (43). NAC muscle loss/no loss: 50/47 | S/NS: 94 (64)/39 (50); (p=0.043). NAC muscle loss/no loss: 34/27 (ns). | S/NS: 69.0 (63–76)/67.5 (62–72); (p=0.107). NAC muscle loss/no loss: 66.5 (63–75)/68.0 (62–71); (ns) | S/NS: 24.2 (21.5–26.1)/27.6 (25.4–29.9); (p<0.001). NAC muscle loss/no loss: 24.6 (21.4–27.0)/24.3 (22.9–27.1); (ns) |
| Okuno (2018) | USA | 2009-2013 | Retrospective | CRLM | sarcopenia, muscle mass, before and after NAC | SMI, muscle loss, body weight | CT (<30 days before preoperative chemotherapy and during the period between preoperative chemotherapy and surgery) | 169. Low/High SMI before NAC: 58/111. Low/High SMI after NAC: 61/108 | 97 (57.4). Minor/major muscle loss: 86 (58.5)/11 (50.0); (p=0.49) | 56.2 (11.7) | NA |
| Chakedis (2018) | USA | 2007-2016 | Retrospective | BTC | Sarcopenia | PMI | CT (<90 days of the operation) | 117. NSR/SR/U: 48/30/39 | 52 (44). NSR/SR/U: 20 (42)/14 (47)/17 (44); (p=0.910) | 66 (50–82). NSR/SR/U: 68 (49–87)/67 (57–77)/64 (47–81); (p=0.929) | 28.1 (6.4). NSR/SR/U:29.1 (6.6)/27.7 (6.6)/27.4 (5.9); (p=0.410) |
| Kroh (2018) | German/Netherlands | 2010-2014 | Retrospective | HCC | Sarcopenia, obesity, sarcopenic obesity | L3 MI, BFA | CT (<3 months before resection) | 70. S/NS: 33/37. O/NO: 28/42. SO/NSO: 21/49 | 49 (70). S/NS: 21 (64)/28 (76); (p=0.3061). O/NO: 20 (71)/29 (69); (p=1.000). SO/NSO: 15 (71)/34 (69); (p=1.000) | 67.74 (12.95). S/NS: 66.97 (16.84)/68.43 (8.23); (p=0.6530). O/NO: 69.18 (12.14)/66.79 (13.53); (p=0.4432). SO/NSO: 69.67 (13.28)/66.92 (12.86); (p=0.4283) | 26.64 (4.62). S/NS: 25.29 (4.32)/27.85 (4.61); (p=0.0191). O/NO: 28.61 (4.82)/25.33 (4.04); (p=0.0045). SO/NSO: 26.73 (3.92)/26.61 (4.93); (p=0.9100) |
| Kobayashi (2018) | Japan | 2005-2014 | Retrospective | CRLM | Visceral adiposity and muscularity | SMI, IMAC, VSR | CT | 124; normal/L-SMI: 100/24. Normal/H-IMAC: 50/74. Normal/H-VSR: 78/46. | 78 (63). Normal/L-SMI: 60 (60)/18 (75). Normal/H-IMAC: 33 (66)/45 (61). Normal/H-VSR: 49 (63)/29 (63) | 65 (59–70). Normal/L-SMI: 64.5 (58–70)/66.5 (61–75); (p=0.126). Normal/H-IMAC: 60 (53–66)/69 (62–73); (p<0.001). Normal/H-VSR: 63 (55–70)/68 (61–72); (p=0.055) | 22.7 (20.3–24.7). Normal/L-SMI: 23.3 (20.5–24.9)/20.9 (18.1–23.5), (p=0.005). Normal/H-IMAC: 21.6 (18.8–23.5)/23.8 (21.0–25.2); (p<0.001). Normal/H-VSR: 22.7 (19.5–24.4)/22.8 (20.4–24.9); (p=0.492) |
| Miyachi (2019) | Japan | 2005-2015 | Retrospective | HCC | Bone Mineral Density | BMD at T11 | CT (<2months before surgery) | 465. Low/normal BMD: 206/161 | 367 | 69(62-75). Low/normal BMD: 70 (64–75)/66 (58–74); (p<0.001) | 23 (21-25). Low/normal BMD: 23 (21-26)/23 (21-25); (p=0.50) |
| Berardi (2020) | Italy | 2018-2019 | Prospective | Any malignancy requiring liver resection | sarcopenia, muscle strength | SMI, handgrip strength measured by a dynamometer | CT (<1 month before surgery) | 234. *Group A/B/C/D: 78/13/75/68 | 158. Group A/B/C/D: 56/10/61/31; (p<0.001) | 66.5(58.00-74.25). Group A/B/C/D: 68.00 (59.75-74.00)/66.00 (60.00-73.50)/66.00 (60.00-74.00)/68.00 (54.50-75.00); (p=0.90) |
27.12(23.28-29.55). Group A/B/C/D: 27.10 (22.26-30.32)/28.10 (22.7-31.75)/26.34 (25.62-29.70)/25.06 (23.40-31.18); (p=0.11) |
| Van Dijk (2020) | Canada | NA | Retrospective | CRLM | sarcopenia, myosteatosis, systemic inflammation | SM, SM-RA; VAT; SAT; CRP (z-scores) | CT | 97 | 67 (69). Low/high SM: 39 (65)/28 (76); (p=0.27) | 61.2 (10.7). Low/high SM: 63.0 (10.7)/58.3 (10.2); (p=0.035) |
NA |
| Van Dijk (2021) | Netherlands | 2008-2013 | Retrospective | CRLM | myosteatosis, NAFLD | VAT, SAT, TAT, liver steatosis (0-3). (z-scores) | CT <4 months before surgery | 218 | 142 (65.1) | 63.8 (10) | 26.3 (3.8) |
| Okubo (2021) | Japan | 2011-2017 | Retrospective | HCC | Visceral adiposity | VSR | CT | 181. High/low VSR: 60/121 | 123 (68). High/low VSR: 50 (83)/73 (60); (p=0.001) | 67 (34-87). High/low VSR: 68 (53–82)/66 (34–87); (p=0.534) | 23.1(13.8-40.4). High/low VSR: 23.2 (17.8-34.2)/22.9 (13.8-40.4); (p=0.573) |
| Yang (2021) | South Korea | 2002-2011 | Retrospective | HCC | sarcopenia, myosteatosis, visceral adiposity | PMI, PMA, VATI | CT (<3 months before surgery) | 160. S/NS: 28 (17.5)/132 (82.5) | 120 (75). S/NS: 17 (60.7)/103 (78.0); (p=0.055) | 55 (11). S/NS: 64.07 (8.32)/53.31 (11.22); (p<0.001) | 24.26 (2.80). S/NS: 23.57 (2.79)/24.42 (2.81); (p=0.079) |
| Meister (2022) | Germany | 2008-2019 | Retrospective | HCC | Sarcopenia, Myosteatosis | SMI, SM-RA | CT (<12 weeks before surgery) | 100. MYS/NMYS: 60/40; S/NS: 54/46 | 72 (72). MYS/NMYS: 42 (70)/30 (75); S/NS: 36 (67)/36 (78); (ns) | 67 (11). MYS/NMYS: 70 (8)/64 (14); S/NS: 68 (11)/66 (11); (ns) | 26 (22-30). MYS/NMYS 26 (5)/26 (3); (ns). S/NS: 24 (3)/29 (4); (ns) |
| Martin (2022) | Switzerland | 2014-2020 | Retrospective | Any liver disease | Sarcopenia | SMI, SMRA | CT (<1 month before surgery) | 355. S/NS: 212/143 | 210 (59.2). S/NS: 139 (65.6)/71 (49.9); (p<0.01) | 62 (13.0). S/NS: 64 (13.5)/59 (12.7); (p<0.01) | 25.5 (4.9). S/NS: 23.9(3.5)/27.7 (4.9); (p<0.01) |
HCC, hepatocellular carcinoma; iCCA, intrahepatic cholangiocarcinoma; pCCA, perihilar cholangiocarcinoma; CRLM, colorectal liver metastases; S, sarcopenia; NS, non-sarcopenia; SMM, skeletal muscle mass; SMI, skeletal muscle index; PMI, psoas muscle index; IMAC, intramuscular adipose content; PMA, psoas muscle attenuation; VATI, visceral adipose tissue index; MA, muscle attenuation; SR-MA, muscle attenuation; VAT, visceral adispose tissue; SAT, subcutaneous adipose tissue; TAT, total adipose tissue; VSR, visceral to subcutaneous adipose tissue area ratio; BTC, biliary tract cancers; NSR, non-sarcopenic resectable; SR, sarcopenic resectable; NA, not assessed.
*Skeletal muscle loss= decrease SMI >5%. *Patients divided in 4 groups: group A (normal muscle mass and strength), group B (reduced muscle strength), group C (reduced muscle mass), group D (reduced muscle mass and strength).