Association of meat consumption with the risk of gastrointestinal cancers: a systematic review and meta-analysis

Di, Yan; Ding, Lei; Gao, Luying; Huang, Hongyan

doi:10.1186/s12885-023-11218-1

BMC Cancer

Table 2 Subgroup analyses for the association between meat consumption and the risk of gastrointestinal cancer

From: Association of meat consumption with the risk of gastrointestinal cancers: a systematic review and meta-analysis

Outcomes	Exposure	Factors	Subgroups	RR and 95%CI	P value	Heterogeneity (%)	RRR between subgroups
EC	Red meat	Country	Western	1.10 (0.87–1.40)	0.428	33.4	0.82 (0.53–1.27)^a
		Country	Eastern	1.34 (0.93–1.93)	0.116	-	0.82 (0.53–1.27)^a
		Sex	Male	1.35 (0.57–3.20)	0.496	75.7	1.23 (0.50–3.03)^b
		Sex	Female	1.10 (0.84–1.45)	0.496	0.0	1.23 (0.50–3.03)^b
		Follow-up	≥ 10.0	1.10 (0.72–1.68)	0.662	45.8	0.96 (0.59–1.55)^c
		Follow-up	< 10.0	1.15 (0.91–1.45)	0.252	25.6	0.96 (0.59–1.55)^c
		Adjusted level	High	1.10 (0.87–1.40)	0.428	33.4	0.82 (0.53–1.27)^d
		Adjusted level	Moderate	1.34 (0.93–1.93)	0.116	-	0.82 (0.53–1.27)^d
	Processed meat	Country	Western	1.17 (0.89–1.55)	0.262	56.7	1.34 (0.84–2.17)^a
		Country	Eastern	0.87 (0.59–1.28)	0.476	-	1.34 (0.84–2.17)^a
		Sex	Male	1.44 (0.81–2.58)	0.218	51.3	1.62 (0.80–3.26)^b
		Sex	Female	0.89 (0.60–1.32)	0.563	26.3	1.62 (0.80–3.26)^b
		Follow-up	≥ 10.0	0.94 (0.60–1.49)	0.798	49.3	0.75 (0.44–1.29)^c
		Follow-up	< 10.0	1.25 (0.94–1.67)	0.127	60.3	0.75 (0.44–1.29)^c
		Adjusted level	High	1.17 (0.89–1.55)	0.262	56.7	1.34 (0.84–2.17)^d
		Adjusted level	Moderate	0.87 (0.59–1.28)	0.476	-	1.34 (0.84–2.17)^d
	Total red and processed meat	Country	Western	1.33 (0.79–2.23)	0.286	63.5	1.28 (0.68–2.40)^a
		Country	Eastern	1.04 (0.73–1.49)	0.829	-	1.28 (0.68–2.40)^a
		Sex	Male	-	-	-	-
		Sex	Female	-	-	-	-
		Follow-up	≥ 10.0	1.04 (0.73–1.49)	0.829	-	0.78 (0.42–1.47)^c
		Follow-up	< 10.0	1.33 (0.79–2.23)	0.286	63.5	0.78 (0.42–1.47)^c
		Adjusted level	High	1.33 (0.79–2.23)	0.286	63.5	1.28 (0.68–2.40)^d
		Adjusted level	Moderate	1.04 (0.73–1.49)	0.829	-	1.28 (0.68–2.40)^d
GC	Red meat	Country	Western	1.02 (0.86–1.21)	0.805	24.7	1.00 (0.80–1.25)^a
		Country	Eastern	1.02 (0.88–1.17)	0.818	31.1	1.00 (0.80–1.25)^a
		Sex	Male	1.01 (0.87–1.17)	0.885	0.0	1.12 (0.88–1.43)^b
		Sex	Female	0.90 (0.74–1.09)	0.268	0.0	1.12 (0.88–1.43)^b
		Follow-up	≥ 10.0	1.01 (0.91–1.12)	0.869	0.0	0.97 (0.72–1.32)^c
		Follow-up	< 10.0	1.04 (0.78–1.38)	0.792	55.7	0.97 (0.72–1.32)^c
		Adjusted level	High	0.98 (0.88–1.10)	0.758	12.2	0.84 (0.64–1.12)^d
		Adjusted level	Moderate	1.16 (0.90–1.50)	0.250	31.6	0.84 (0.64–1.12)^d
	Processed meat	Country	Western	1.11 (0.94–1.33)	0.221	42.4	1.12 (0.90–1.40)^a
		Country	Eastern	0.99 (0.86–1.13)	0.871	14.0	1.12 (0.90–1.40)^a
		Sex	Male	1.02 (0.88–1.18)	0.774	0.0	0.89 (0.62–1.27)^b
		Sex	Female	1.15 (0.83–1.59)	0.404	62.1	0.89 (0.62–1.27)^b
		Follow-up	≥ 10.0	1.08 (0.94–1.25)	0.276	35.3	1.03 (0.74–1.42)^c
		Follow-up	< 10.0	1.05 (0.78–1.40)	0.759	61.0	1.03 (0.74–1.42)^c
		Adjusted level	High	1.07 (0.92–1.24)	0.382	50.4	0.97 (0.72–1.31)^d
		Adjusted level	Moderate	1.10 (0.85–1.42)	0.479	20.9	0.97 (0.72–1.31)^d
	Total red and processed meat	Country	Western	0.97 (0.76–1.24)	0.804	8.6	0.98 (0.72–1.34)^a
		Country	Eastern	0.99 (0.81–1.20)	0.896	45.6	0.98 (0.72–1.34)^a
		Sex	Male	0.96 (0.82–1.13)	0.618	-	1.17 (0.88–1.55)^b
		Sex	Female	0.82 (0.65–1.03)	0.091	-	1.17 (0.88–1.55)^b
		Follow-up	≥ 10.0	0.98 (0.78–1.23)	0.873	61.9	0.99 (0.72–1.35)^c
		Follow-up	< 10.0	0.99 (0.80–1.23)	0.927	0.0	0.99 (0.72–1.35)^c
		Adjusted level	High	0.93 (0.83–1.04)	0.221	0.0	0.68 (0.46-1.00) ^d
		Adjusted level	Moderate	1.37 (0.94–1.99)	0.100	-	0.68 (0.46-1.00) ^d
CRC	Red meat	Country	Western	1.12 (1.04–1.19)	0.001	20.4	1.11 (0.98–1.26)^a
		Country	Eastern	1.01 (0.91–1.13)	0.830	0.0	1.11 (0.98–1.26)^a
		Sex	Male	0.97 (0.80–1.18)	0.789	0.0	0.92 (0.75–1.14)^b
		Sex	Female	1.05 (0.96–1.15)	0.298	0.0	0.92 (0.75–1.14)^b
		Follow-up	≥ 10.0	1.06 (0.98–1.15)	0.131	0.0	0.96 (0.84–1.11)^c
		Follow-up	< 10.0	1.10 (0.98–1.23)	0.092	54.4	0.96 (0.84–1.11)^c
		Adjusted level	High	1.08 (1.01–1.15)	0.020	28.0	0.86 (0.68–1.10)^d
		Adjusted level	Moderate	1.25 (0.99–1.59)	0.058	0.0	0.86 (0.68–1.10)^d
	Processed meat	Country	Western	1.20 (1.13–1.29)	< 0.001	19.6	1.02 (0.89–1.16)^a
		Country	Eastern	1.18 (1.06–1.32)	0.003	0.0	1.02 (0.89–1.16)^a
		Sex	Male	1.27 (1.08–1.50)	0.005	23.8	1.11 (0.91–1.36)^b
		Sex	Female	1.14 (1.02–1.28)	0.023	0.0	1.11 (0.91–1.36)^b
		Follow-up	≥ 10.0	1.21 (1.12–1.32)	< 0.001	0.0	1.03 (0.91–1.05)^c
		Follow-up	< 10.0	1.18 (1.09–1.29)	< 0.001	25.7	1.03 (0.91–1.05)^c
		Adjusted level	High	1.18 (1.12–1.24)	< 0.001	0.0	0.91 (0.71–1.16)^d
		Adjusted level	Moderate	1.30 (1.03–1.66)	0.030	43.0	0.91 (0.71–1.16)^d
	Total red and processed meat	Country	Western	1.15 (1.07–1.23)	< 0.001	1.5	1.11 (0.95–1.28)^a
		Country	Eastern	1.04 (0.91–1.18)	0.574	0.0	1.11 (0.95–1.28)^a
		Sex	Male	1.21 (0.98–1.49)	0.070	0.0	1.09 (0.85–1.40)^b
		Sex	Female	1.11 (0.97–1.26)	0.128	15.4	1.09 (0.85–1.40)^b
		Follow-up	≥ 10.0	1.20 (1.05–1.37)	0.007	0.0	1.08 (0.92–1.27)^c
		Follow-up	< 10.0	1.11 (1.02–1.22)	0.016	23.3	1.08 (0.92–1.27)^c
		Adjusted level	High	1.13 (1.05–1.21)	0.001	10.9	0.97 (0.76–1.23)^d
		Adjusted level	Moderate	1.17 (0.92–1.47)	0.195	0.0	0.97 (0.76–1.23)^d
CC	Red meat	Country	Western	1.18 (1.03–1.35)	0.015	7.2	1.10 (0.91–1.34)^a
		Country	Eastern	1.07 (0.93–1.24)	0.346	0.0	1.10 (0.91–1.34)^a
		Sex	Male	1.05 (0.78–1.41)	0.747	-	1.02 (0.73–1.42)^b
		Sex	Female	1.03 (0.89–1.19)	0.675	0.0	1.02 (0.73–1.42)^b
		Follow-up	≥ 10.0	1.05 (0.92–1.20)	0.443	0.0	0.85 (0.71–1.03)^c
		Follow-up	< 10.0	1.23 (1.08–1.42)	0.003	0.0	0.85 (0.71–1.03)^c
		Adjusted level	High	1.14 (1.02–1.27)	0.021	13.0	1.07 (0.75–1.52)^d
		Adjusted level	Moderate	1.07 (0.76–1.50)	0.708	0.0	1.07 (0.75–1.52)^d
	Processed meat	Country	Western	1.24 (1.12–1.38)	< 0.001	0.0	0.99 (0.80–1.23)^a
		Country	Eastern	1.25 (1.03–1.50)	0.022	0.0	0.99 (0.80–1.23)^a
		Sex	Male	1.24 (1.04–1.49)	0.018	0.0	0.99 (0.78–1.26)^b
		Sex	Female	1.25 (1.06–1.47)	0.007	0.0	0.99 (0.78–1.26)^b
		Follow-up	≥ 10.0	1.25 (1.09–1.44)	0.002	0.0	1.01 (0.84–1.22)^c
		Follow-up	< 10.0	1.24 (1.09–1.40)	0.001	0.0	1.01 (0.84–1.22)^c
		Adjusted level	High	1.22 (1.11–1.35)	< 0.001	0.0	0.87 (0.64–1.17)^d
		Adjusted level	Moderate	1.41 (1.06–1.88)	0.019	0.0	0.87 (0.64–1.17)^d
	Total red and processed meat	Country	Western	1.24 (1.10–1.41)	0.001	0.0	1.06 (0.79–1.42)^a
		Country	Eastern	1.17 (0.90–1.52)	0.239	62.3	1.06 (0.79–1.42)^a
		Sex	Male	1.28 (1.02–1.61)	0.032	0.0	1.12 (0.84–1.51)^b
		Sex	Female	1.14 (0.95–1.38)	0.158	4.1	1.12 (0.84–1.51)^b
		Follow-up	≥ 10.0	1.26 (1.05–1.51)	0.014	0.0	1.10 (0.85–1.40)^c
		Follow-up	< 10.0	1.15 (0.97–1.36)	0.115	50.1	1.10 (0.85–1.40)^c
		Adjusted level	High	1.19 (1.04–1.35)	0.012	40.0	1.07 (0.67–1.71)^d
		Adjusted level	Moderate	1.11 (0.71–1.74)	0.635	0.0	1.07 (0.67–1.71)^d
RC	Red meat	Country	Western	1.33 (1.03–1.72)	0.029	44.5	1.41 (0.95–2.11)^a
		Country	Eastern	0.94 (0.69–1.27)	0.678	22.4	1.41 (0.95–2.11)^a
		Sex	Male	1.21 (0.67–2.18)	0.527	-	1.07 (0.54–2.13)^b
		Sex	Female	1.13 (0.79–1.61)	0.518	59.8	1.07 (0.54–2.13)^b
		Follow-up	≥ 10.0	1.23 (0.94–1.60)	0.134	35.6	1.07 (0.68–1.69)^c
		Follow-up	< 10.0	1.15 (0.79–1.66)	0.467	58.8	1.07 (0.68–1.69)^c
		Adjusted level	High	1.10 (0.91–1.33)	0.332	32.4	0.50 (0.28–0.91) ^d
		Adjusted level	Moderate	2.18 (1.25–3.81)	0.006	0.0	0.50 (0.28–0.91) ^d
	Processed meat	Country	Western	1.29 (1.07–1.56)	0.007	19.9	1.13 (0.84–1.53)^a
		Country	Eastern	1.14 (0.90–1.44)	0.277	0.0	1.13 (0.84–1.53)^a
		Sex	Male	1.03 (0.79–1.36)	0.824	0.0	0.94 (0.65–1.38)^b
		Sex	Female	1.09 (0.84–1.43)	0.515	6.5	0.94 (0.65–1.38)^b
		Follow-up	≥ 10.0	1.09 (0.91–1.31)	0.345	0.0	0.77 (0.60-1.00) ^c
		Follow-up	< 10.0	1.41 (1.17–1.69)	< 0.001	0.0	0.77 (0.60-1.00) ^c
		Adjusted level	High	1.20 (1.05–1.37)	0.007	0.0	0.63 (0.38–1.06)^d
		Adjusted level	Moderate	1.90 (1.15–3.13)	0.012	0.0	0.63 (0.38–1.06)^d
	Total red and processed meat	Country	Western	1.32 (1.11–1.57)	0.002	0.0	1.26 (0.98–1.61)^a
		Country	Eastern	1.05 (0.88–1.26)	0.587	0.0	1.26 (0.98–1.61)^a
		Sex	Male	0.93 (0.58–1.49)	0.763	-	0.84 (0.48–1.46)^b
		Sex	Female	1.11 (0.83–1.49)	0.478	0.0	0.84 (0.48–1.46)^b
		Follow-up	≥ 10.0	1.09 (0.85–1.39)	0.507	0.0	0.85 (0.61–1.18)^c
		Follow-up	< 10.0	1.28 (1.03–1.60)	0.025	44.9	0.85 (0.61–1.18)^c
		Adjusted level	High	1.19 (1.03–1.37)	0.021	14.3	0.65 (0.21-2.00)^d
		Adjusted level	Moderate	1.82 (0.60–5.52)	0.290	-	0.65 (0.21-2.00)^d
PC	Red meat	Country	Western	1.03 (0.87–1.21)	0.764	55.0	1.91 (0.87–4.18)^a
		Country	Eastern	0.54 (0.25–1.16)	0.116	-	1.91 (0.87–4.18)^a
		Sex	Male	0.89 (0.70–1.14)	0.360	0.0	0.82 (0.58–1.15)^b
		Sex	Female	1.09 (0.86–1.38)	0.494	33.3	0.82 (0.58–1.15)^b
		Follow-up	≥ 10.0	0.94 (0.61–1.44)	0.777	63.6	0.91 (0.57–1.45)^c
		Follow-up	< 10.0	1.03 (0.86–1.23)	0.779	55.2	0.91 (0.57–1.45)^c
		Adjusted level	High	1.03 (0.86–1.22)	0.770	59.5	1.37 (0.73–2.58)^d
		Adjusted level	Moderate	0.75 (0.41–1.38)	0.357	27.4	1.37 (0.73–2.58)^d
	Processed meat	Country	Western	0.99 (0.83–1.18)	0.925	68.7	0.85 (0.43–1.68)^a
		Country	Eastern	1.16 (0.60–2.23)	0.657	-	0.85 (0.43–1.68)^a
		Sex	Male	0.99 (0.76–1.30)	0.953	59.2	1.09 (0.78–1.51)^b
		Sex	Female	0.91 (0.75–1.09)	0.293	28.5	1.09 (0.78–1.51)^b
		Follow-up	≥ 10.0	0.88 (0.71–1.10)	0.275	0.0	0.84 (0.62–1.13)^c
		Follow-up	< 10.0	1.05 (0.86–1.29)	0.639	74.1	0.84 (0.62–1.13)^c
		Adjusted level	High	0.99 (0.83–1.17)	0.870	68.2	0.98 (0.46–2.09)^d
		Adjusted level	Moderate	1.01 (0.48–2.10)	0.984	69.5	0.98 (0.46–2.09)^d
	Total red and processed meat	Country	Western	1.04 (0.87–1.24)	0.699	43.4	0.80 (0.62–1.03)^a
		Country	Eastern	1.30 (1.09–1.56)	0.004	-	0.80 (0.62–1.03)^a
		Sex	Male	0.86 (0.65–1.14)	0.287	0.0	0.96 (0.65–1.40)^b
		Sex	Female	0.90 (0.70–1.17)	0.439	0.0	0.96 (0.65–1.40)^b
		Follow-up	≥ 10.0	1.06 (0.72–1.56)	0.761	0.0	0.97 (0.64–1.49)^c
		Follow-up	< 10.0	1.09 (0.91–1.30)	0.363	59.3	0.97 (0.64–1.49)^c
		Adjusted level	High	1.08 (0.93–1.27)	0.305	48.3	-
		Adjusted level	Moderate	-	-	-	-
HCC	Red meat	Country	Western	1.04 (0.99–1.09)	0.103	0.0	0.90 (0.68–1.19)^a
		Country	Eastern	1.16 (0.88–1.53)	0.299	-	0.90 (0.68–1.19)^a
		Sex	Male	1.02 (0.97–1.08)	0.442	0.0	0.92 (0.81–1.04)^b
		Sex	Female	1.11 (1.00-1.24)	0.055	0.0	0.92 (0.81–1.04)^b
		Follow-up	≥ 10.0	1.13 (0.89–1.43)	0.315	0.0	1.09 (0.85–1.38)^c
		Follow-up	< 10.0	1.04 (0.99–1.09)	0.106	0.0	1.09 (0.85–1.38)^c
		Adjusted level	High	1.04 (1.00-1.09)	0.075	0.0	-
		Adjusted level	Moderate	-	-	-	-
	Processed meat	Country	Western	0.97 (0.85–1.10)	0.647	50.0	0.84 (0.63–1.13)^a
		Country	Eastern	1.15 (0.89–1.49)	0.288	-	0.84 (0.63–1.13)^a
		Sex	Male	1.37 (0.54–3.46)	0.502	86.1	1.32 (0.49–3.53)^b
		Sex	Female	1.04 (0.74–1.44)	0.837	37.7	1.32 (0.49–3.53)^b
		Follow-up	≥ 10.0	1.43 (0.96–2.13)	0.081	47.2	1.55 (1.04–2.32) ^c
		Follow-up	< 10.0	0.92 (0.87–0.97)	0.002	0.0	1.55 (1.04–2.32) ^c
		Adjusted level	High	1.00 (0.88–1.13)	0.979	52.3	-
		Adjusted level	Moderate	-	-	-	-
	Total red and processed meat	Country	Western	0.94 (0.67–1.32)	0.724	20.9	0.74 (0.48–1.15)^a
		Country	Eastern	1.27 (0.96–1.68)	0.094	-	0.74 (0.48–1.15)^a
		Sex	Male	1.69 (0.74–3.87)	0.214	-	1.71 (0.58–5.06)^b
		Sex	Female	0.99 (0.49-2.00)	0.978	-	1.71 (0.58–5.06)^b
		Follow-up	≥ 10.0	1.26 (0.99–1.62)	0.065	0.0	1.54 (0.96–2.45)^c
		Follow-up	< 10.0	0.82 (0.55–1.22)	0.324	23.2	1.54 (0.96–2.45)^c
		Adjusted level	High	1.05 (0.80–1.39)	0.709	34.1	-
		Adjusted level	Moderate	-	-	-	-

*^acompared Western countries with Eastern countries; ^bcompared male with female; ^ccompared follow-up ≥ 10.0 years with follow-up < 10.0 years; ^dcompared high adjusted level with moderate adjusted level

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