1School of Medicine, Nankai University, Tianjin, China
2Department of Hepatobiliary Surgery, Kailuan General Hospital, Tangshan, China
3Department of Radiation Oncology, North China University of Science and Technology Affiliated Hospital, Tangshan, China
4The Faculty of Hepatopancreatobiliary Surgery, The First Medical Center, Chinese People’s Liberation Army General Hospital, Beijing, China
Copyright © 2024 by the Korean Cancer Association
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Ethical Statement
The study was performed according to the guidelines of the Helsinki Declaration and was approved by the Ethics Committee of Kailuan General Hospital (approval number: 2006-05). All participants were agreed to take part in the study and provided informed written consent.
Author Contributions
Conceived and designed the analysis: Cui H.
Performed the analysis: Cui H, Tian F.
Wrote the paper: Cui H, Chen Y, Ma X.
Conflicts of Interest
Conflict of interest relevant to this article was not reported.
Values are presented as number (%), mean±SD, or median (P25-P75). ALT, alanine transaminase; BMI, body mass index; HDL-C, high density lipoprotein-cholesterol; Hs-CRP, high-sensitive C-reactive protein; MHNW, metabolic healthy normal-weight; MHO, metabolic healthy obesity; MUNW, metabolic unhealthy normal-weight; MUO, metabolic unhealthy obesity; SBP, systolic blood pressure; SD, standard deviation; TG, triglyceride; WC, waist circumference; WHR, waist-hip ratio; WHtR, waist-to-height ratio.
Multiple models adjusted for age, sex, educational level, drinking, smoking, physical exercise, family history of cancer, salt intake, highsensitive C-reactive protein, and alanine transaminase. BMI, body mass index; GI, gastrointestinal; MHNW, metabolic healthy normalweight; MHO, metabolic healthy obesity; MUNW, metabolic unhealthy normal-weight; MUO, metabolic unhealthy obesity; WC, waist circumference.
Multiple models adjusted for age/sex, educational level, drinking, smoking, physical exercise, family history of cancer, salt intake, highsensitive C-reactive protein, and alanine transaminase. The interaction effect was estimated by the Wald test. Interaction between metabolically healthy phenotypes by BMI and age (p for interaction < 0.001) and sex (p for interaction < 0.001). Interaction between metabolically healthy phenotypes by WC and age (p for interaction < 0.001). And no interaction between metabolically healthy phenotypes by WC and sex (p for interaction > 0.05). BMI, body mass index; GI, gastrointestinal; MHNW, metabolic healthy normal-weight; MHO, metabolic healthy obesity; MUNW, metabolic unhealthy normal-weight; MUO, metabolic unhealthy obesity; WC, waist circumference.
Multiple models adjusted for age, sex, educational level, drinking, smoking, physical exercise, family history of cancer, salt intake, high-sensitive C-reactive protein, and alanine transaminase. Model for colorectal cancer was additionally adjusted for high fat diet. Model for biliary tract cancer was additionally adjusted for gallstone. Model for liver cancer was additionally adjusted for hepatitis B virus surface antigen. Model for pancreatic cancer was additionally adjusted for history of chronic pancreatitis. BMI, body mass index; GI, gastrointestinal; MHNW, metabolic healthy normal-weight; MHO, metabolic healthy obesity; MUNW, metabolic unhealthy normal-weight; MUO, metabolic unhealthy obesity; WC, waist circumference.
MHNW | MUNW | MHO | MUO | p-value | |
---|---|---|---|---|---|
No. | 25,067 | 68,889 | 2,079 | 18,960 | - |
Age (yr) | 45.35±12.90 | 52.82±12.21 | 45.53±12.70 | 51.62±11.96 | < 0.001 |
Male sex | 18,323 (73.1) | 56,843 (82.5) | 1,581 (76.1) | 15,641 (82.5) | < 0.001 |
BMI (kg/m2) | 22.89±2.52 | 24.20±2.37 | 29.94±1.92 | 30.22±2.03 | < 0.001 |
WC (cm) | 81.68±8.76 | 85.98±8.36 | 93.57±8.61 | 96.25±8.48 | < 0.001 |
WHR | 0.36±0.48 | 0.49±0.50 | 0.62±0.49 | 0.69±0.46 | < 0.001 |
WHtR | 0.40±0.49 | 0.61±0.49 | 0.91±0.29 | 0.94±0.24 | < 0.001 |
SBP (mmHg) | 112.68±9.55 | 135.08±20.40 | 115.68±8.38 | 140.81±20.24 | < 0.001 |
TG (mmol/L) | 0.92 (0.69-1.21) | 1.36 (0.94-2.08) | 1.13 (0.87-1.39) | 1.79 (1.23-2.61) | < 0.001 |
HDL-C (mmol/L) | 1.59±0.42 | 1.52±0.45 | 1.50±0.31 | 1.47±0.39 | < 0.001 |
Hs-CRP (mg/dL) | 0.66 (0.26-1.80) | 0.90 (0.35-2.40) | 1.20 (0.50-2.84) | 1.40 (0.60-3.20) | < 0.001 |
ALT (IU/L) | 16.40 (12.00-23.00) | 18.00 (13.00-25.00) | 20.00 (14.00-28.00) | 21.00 (15.00-30.00) | < 0.001 |
High school or above | 3,233 (12.9) | 3,964 (5.8) | 242 (11.6) | 1,158 (6.1) | < 0.001 |
Salt intake > 12 g/day | 2,538 (10.1) | 7,622 (11.1) | 251 (12.1) | 2,488 (13.1) | < 0.001 |
Current drinker | 3,733 (14.9) | 13,931 (20.2) | 252 (12.1) | 3,207 (16.9) | < 0.001 |
Current smoker | 7,908 (31.6) | 22,663 (32.9) | 650 (31.3) | 5,679 (30.0) | < 0.001 |
Physical exercise | 3,323 (13.3) | 11,755 (17.1) | 259 (12.5) | 3,228 (17.0) | < 0.001 |
Family history of cancer | 830 (3.3) | 2,045 (3.0) | 86 (4.1) | 644 (3.4) | < 0.001 |
No. | Event | Cumulative incidence (%) | Age- and sex- adjusted | Multiple-adjusted | |
---|---|---|---|---|---|
BMI category | |||||
MHNW | 25,067 | 333 | 1.45 | Ref | Ref |
MUNW | 68,889 | 1,515 | 2.42 | 1.31 (1.16-1.48) | 1.29 (1.15-1.46) |
MHO | 2,079 | 41 | 2.16 | 1.53 (1.11-2.12) | 1.54 (1.11-2.13) |
MUO | 18,960 | 418 | 2.43 | 1.39 (1.20-1.60) | 1.37 (1.18-1.58) |
WC category | |||||
MHNW | 20,355 | 253 | 1.37 | Ref | Ref |
MUNW | 46,911 | 978 | 2.28 | 1.34 (1.16-1.54) | 1.32 (1.15-1.52) |
MHO | 6,791 | 121 | 1.91 | 1.24 (1.00-1.54) | 1.23 (0.99-1.53) |
MUO | 40,938 | 959 | 2.59 | 1.39 (1.21-1.60) | 1.36 (1.18-1.57) |
Age (yr) |
Sex |
|||||
---|---|---|---|---|---|---|
≤ 60 | > 60 | p for interaction | Male | Female | p for interaction | |
BMI category | ||||||
MHNW | Ref | Ref | < 0.001 | Ref | Ref | < 0.001 |
MUNW | 1.31 (1.14-1.51) | 1.13 (0.90-1.41) | 1.22 (1.08-1.39) | 1.27 (1.09-1.46) | ||
MHO | 1.50 (1.02-2.20) | 1.70 (0.93-3.10) | 1.52 (1.05-2.13) | 1.26 (1.01-1.58) | ||
MUO | 1.23 (1.07-1.52) | 1.33 (1.02-1.72) | 1.30 (1.12-1.51) | 1.30 (1.12-1.51) | ||
WC category | ||||||
MHNW | Ref | Ref | < 0.001 | Ref | Ref | > 0.05 |
MUNW | 1.33 (1.13-1.56) | 1.15 (0.88-1.50) | 1.97 (1.28-3.02) | 1.77 (1.10-2.86) | ||
MHO | 1.20 (0.92-1.55) | 1.17 (0.78-1.74) | 1.72 (0.60-4.94) | 0.84 (0.37-1.90) | ||
MUO | 1.33 (1.12-1.57) | 1.19 (0.82-1.55) | 1.86 (1.13-3.08) | 1.71 (1.06-2.77) |
Esophageal cancer |
Gastric cancer |
Colorectal cancer |
Biliary tract cancer |
Liver cancer |
Pancreatic cancer |
|||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|
Case | Multiple-adjusted | Case | Multiple-adjusted | Case | Multiple-adjusted | Case | Multiple-adjusted | Case | Multiple-adjusted | Case | Multiple-adjusted | |
BMI category | ||||||||||||
MHNW | 24 | Ref | 66 | Ref | 107 | Ref | 14 | Ref | 100 | Ref | 22 | Ref |
MUNW | 183 | 2.78 (1.81-4.27) | 318 | 1.69 (1.29-2.22) | 554 | 1.82 (1.48-2.25) | 52 | 1.17 (0.64-2.13) | 307 | 1.17 (0.93-1.47) | 105 | 1.64 (1.03-2.61) |
MHO | 3 | 1.54 (0.46-5.11) | 12 | 2.16 (1.17-4.00) | 14 | 1.59 (0.91-2.77) | 0 | - | 10 | 1.15 (0.60-2.21) | 2 | 1.09 (0.26-4.63) |
MUO | 28 | 1.62 (0.93-2.82) | 96 | 1.86 (1.36-2.56) | 156 | 1.89 (1.47-2.43) | 9 | 0.76 (0.32-1.77) | 94 | 1.26 (0.95-1.67) | 35 | 1.97 (1.15-3.39) |
WC category | ||||||||||||
MHNW | 20 | Ref | 54 | Ref | 78 | Ref | 13 | Ref | 68 | Ref | 20 | Ref |
MUNW | 121 | 2.54 (1.58-4.10) | 219 | 1.67 (1.24-2.26) | 337 | 1.80 (1.41-2.32) | 30 | 0.85 (0.44-1.65) | 202 | 1.32 (0.99-1.74) | 69 | 1.39 (0.84-2.29) |
MHO | 7 | 1.17 (0.49-2.77) | 24 | 1.33 (0.82-2.15) | 43 | 1.67 (1.15-2.42) | 1 | 0.23 (0.03-1.67) | 42 | 1.82 (1.24-2.66) | 4 | 0.58 (0.20-1.70) |
MUO | 90 | 2.54 (1.55-4.16) | 195 | 1.78 (1.31-2.43) | 373 | 2.39 (1.86-3.07) | 31 | 1.03 (0.53-2.01) | 199 | 1.60 (1.21-2.12) | 71 | 1.68 (1.02-2.80) |
Values are presented as number (%), mean±SD, or median (P25-P75). ALT, alanine transaminase; BMI, body mass index; HDL-C, high density lipoprotein-cholesterol; Hs-CRP, high-sensitive C-reactive protein; MHNW, metabolic healthy normal-weight; MHO, metabolic healthy obesity; MUNW, metabolic unhealthy normal-weight; MUO, metabolic unhealthy obesity; SBP, systolic blood pressure; SD, standard deviation; TG, triglyceride; WC, waist circumference; WHR, waist-hip ratio; WHtR, waist-to-height ratio.
Multiple models adjusted for age, sex, educational level, drinking, smoking, physical exercise, family history of cancer, salt intake, highsensitive C-reactive protein, and alanine transaminase. BMI, body mass index; GI, gastrointestinal; MHNW, metabolic healthy normalweight; MHO, metabolic healthy obesity; MUNW, metabolic unhealthy normal-weight; MUO, metabolic unhealthy obesity; WC, waist circumference.
Multiple models adjusted for age/sex, educational level, drinking, smoking, physical exercise, family history of cancer, salt intake, highsensitive C-reactive protein, and alanine transaminase. The interaction effect was estimated by the Wald test. Interaction between metabolically healthy phenotypes by BMI and age (p for interaction < 0.001) and sex (p for interaction < 0.001). Interaction between metabolically healthy phenotypes by WC and age (p for interaction < 0.001). And no interaction between metabolically healthy phenotypes by WC and sex (p for interaction > 0.05). BMI, body mass index; GI, gastrointestinal; MHNW, metabolic healthy normal-weight; MHO, metabolic healthy obesity; MUNW, metabolic unhealthy normal-weight; MUO, metabolic unhealthy obesity; WC, waist circumference.
Multiple models adjusted for age, sex, educational level, drinking, smoking, physical exercise, family history of cancer, salt intake, high-sensitive C-reactive protein, and alanine transaminase. Model for colorectal cancer was additionally adjusted for high fat diet. Model for biliary tract cancer was additionally adjusted for gallstone. Model for liver cancer was additionally adjusted for hepatitis B virus surface antigen. Model for pancreatic cancer was additionally adjusted for history of chronic pancreatitis. BMI, body mass index; GI, gastrointestinal; MHNW, metabolic healthy normal-weight; MHO, metabolic healthy obesity; MUNW, metabolic unhealthy normal-weight; MUO, metabolic unhealthy obesity; WC, waist circumference.