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RED MEAT AND PROCESSED MEAT volume 114 This publication represents the views and expert opinions of an IARC Working Group on the Evaluation of Carcinogenic Risks to Humans, which met in Lyon, 6–13 October 2015 LYON, FRANCE - 2018 iarc monographs on the evaluation of carcinogenic risks to humans 3. CANCER IN EXPERIMENTAL ANIMALS No long-term bioassays of full carcino- and colon/caecum. Mice fed the modified diet genicity with red meat or processed meat were containing beef had a greater number of tumours available to the Working Group; however, the in the small intestine compared with mice fed Working Group considered a variety of animal the control diet, with the difference being signif- bioassays. icant in the distal small intestine (P = 0.009) (Mutanen et al., 2000). [The Working Group 3.1 Mouse noted that the tumour data were confounded by the fact that the beef diet contained considerably See Table 3.1 more fat (274.8 g/kg diet) than the control diet (70.0 g/kg diet). The control diet contained 3.1.1 Red meat calcium at a concentration of 5.1 g/kg diet, and did not contain fibre; however, there was no Groups of seven to nine male C57Bl/6J- increase in the incidence of tumours of the small ApcMin mice (age, 6–8 weeks), a strain primarily intestine in a separate non-fibre, high-fat group.] susceptible to spontaneous adenomas of the Groups of six to eight male and six to eight small intestine, were fed American Institute female C57Bl/6J-ApcMin mice (age, 5 weeks) were of Nutrition (AIN-93G)–based diets, either a transferred from a standard rodent chow diet semisynthetic control diet or a modified diet in and fed AIN-93G–based diets, either a semi- which casein, the protein source, was replaced synthetic control diet or a modified diet in which with beef (24%), for 5–6 weeks. The beef was casein was replaced with beef. The control diet minced and freeze-dried before being added to contained 40% fat and a fatty acid profile similar the diet. [The authors did not specify whether to that of a “Western-type” (i.e. enriched in fat and the meat had been cooked before being minced cholesterol) diet. The carbohydrate and protein and freeze-dried.] The control diet contained sources were provided by dextrose and casein, calcium at a concentration of 5.1 g/kg diet, and respectively. The beef diet contained freeze- fat was obtained from sunflower and rapeseed dried, low-fat ground beef instead of casein as oil. In the modified diet, fat was provided by the protein source. The other ingredients were beef, butter, and sunflower and rapeseed oil. The adjusted to keep the proportions of energy from energy content was similar for both diets. The carbohydrate, protein, and fat similar to those extent of intestinal neoplasms was determined in the control diet. [The authors did not specify by light microscopy. Statistical analyses were whether the low-fat ground beef had been cooked conducted. Mean body weight (bw) was similar before being freeze-dried.] The number and size for mice given the control or modified diet. of intestinal adenomas, as determined by light Tumours were observed in the small intestine 389 390 IARC MONOGRAPHSIARC 114 – Table 3.1 Studies of carcinogenicity in mice fed diets containing red meat or processed meat Species, Dosing regimen Results Significance Comments strain (sex) Animals/group at start For each target organ: Age at start No. surviving animals incidence (%) and/or Duration multiplicity of tumours Reference Mouse, Full carcinogenicity study Small intestine Limitations: tumour data were C57Bl/6J- AIN-93G–based control diet or Total tumours, mean (SD): NS confounded by the fact that the beef ApcMin (M) modified AIN-93G diet in which 24% 35.3 (11.6), 52.8 (13.2) diet contained considerably more fat Age 6–8 wk beef replaced casein as the protein Colon and caecum (274.8 g/kg diet) than the control diet 5–6 wk source, fed ad libitum (70.0 g/kg diet); histopathological Tumour incidence: 88%, NS Mutanen 7–9 mice/group examination not conducted 89% et al. (2000) 7, 7 Total tumours, mean (SD): NS 1.8 (0.9), 3.2 (2.3) Distal small intestine Total tumours, mean (SD): *P = 0.009 (ANOVA with Tukey 19.6 (6.8), 36.6 (9.4)* post hoc test) Mouse, Full carcinogenicity study Small intestine Diets were balanced for carbohydrates, C57Bl/6J- Mice were fed a control diet (AIN-93G Adenoma multiplicity, Decrease; *P < 0.01 (multiple linear protein, and fat ApcMin (F) diet with 40% fat) or diet containing mean (SEM): 72.3 (15.27), regression) Age 5 wk low-fat ground beef (AIN-93G with 30.9 (4.90)* 15 wk 40% fat, 27% beef), fed ad libitum Total adenomas, mean Decrease; *P < 0.01 (multiple linear Kettunen 6–8 mice/group (SEM): 55.8 (8.46), 28.7 regression) et al. (2003) 6, 6 (3.77)* Small intestine Medium adenoma, Decrease; *P < 0.05 (both sexes incidence, mean (SEM): combined, multiple linear 30.1% (3.8), 22.6% (3.3)* regression) Mouse, Full carcinogenicity study Small intestine Mice were fed a modified AIN-93G C57Bl/6J- Control diet or diet containing beef Medium adenoma Decrease; *P < 0.05 (both sexes containing 40% fat or low-fat ground ApcMin (M) (g/kg diet), fed ad libitum incidence, mean (SEM): combined, multiple linear beef instead of casein as the protein Age 5 wk 6–8 mice/group 44.3% (2.9), 36.3% (4.6)* regression) source. Diets were balanced for 15 wk 8, 8 carbohydrates, protein, and fat Kettunen et al. (2003) Table 3.1 (continued) Species, Dosing regimen Results Significance Comments strain (sex) Animals/group at start For each target organ: Age at start No. surviving animals incidence (%) and/or Duration multiplicity of tumours Reference Mouse, Initiation–promotion study Colon Limitations: tumour incidence in BALB/c (M) Diet containing low milk protein with Tumour incidence: 23/38 Decrease; *P ≤ 0.05 (test for the the control groups was not reported; Age 5 wk low fat or low beef protein with low fat, (60.5%), 4/23 (17.4%)* equality of two proportions) the duration of this experiment (54 54 wk fed ad libitum wk) was probably not sufficient to Nutter et al. 100 mice/group determine if the diets by themselves (1983) 38, 23 were tumorigenic; histopathological Diet containing low milk protein with Colon examination not conducted high fat or low beef protein with high Tumour incidence: 19/24 Decrease; *P ≤ 0.05 (test for the Mice were allocated to six isocaloric fat, fed ad libitum (79.2%), 6/28 (21.4%)* equality of two proportions) diet groups that differed in protein 100 mice/group source (milk or beef), protein level 24, 28 (11% or 33%), and fat level (5% or Diet containing high milk protein with Colon 30%), and injected with DMH (11 weekly injections of 20 mg/kg bw) low fat or high beef protein with low Tumour incidence: 19/29 Decrease; *P ≤ 0.05 (test for the fat, fed ad libitum (65.5%), 5/44 (11.4%)* equality of two proportions) 100 mice/group 29, 44 *, statistically significant; AIN, American Institute of Nutrition; ANOVA, analysis of variance; DMH, dimethylhydrazine; F, female; M, male; NR, not reported; NS, not significant; SD, standard deviation; SEM, standard error of the mean; wk, week Red meat and processed meat processed and meat Red 391 IARC MONOGRAPHS – 114 microscopy, were assessed when the mice were mice fed the corresponding diets containing placed on the control and beef diets, and then milk protein and fat. When assessed at 59 weeks assessed after they were fed the test diets for of age, DMH-injected mice fed the beef protein 3 weeks or 10 weeks. Statistical analyses were diets had a significantly lower incidence of colon conducted. Male mice fed the control diet gained tumours than DMH-injected mice fed the milk less weight than male mice fed the beef diet. This protein diets, irrespective of the percentage of difference in body weight was not observed in the protein or fat (P < 0.05) (Nutter et al., 1983). female mice. Female mice fed the beef diet had [Tumour incidence in the control groups was significantly fewer intestinal adenomas P( < 0.01) not reported. The duration of this experiment (54 and a significantly lower tumour burden (meas- weeks) was probably not sufficient to determine ured as mm2; P < 0.01) when assessed after 15 if the diets by themselves were tumorigenic.] weeks of feeding. Mice fed the beef diet also had significantly fewer medium-sized (1.0–1.5 mm) 3.2 Rat adenomas than did mice fed the control diet when both sexes were combined (P < 0.05) See Table 3.2 (Kettunen et al., 2003). 3.2.1 Red meat 3.1.2 Red meat with known carcinogens A study was conducted to investigate the Groups of 100 male BALB/c mice (age, 5 effects of a “complete human diet” prepared weeks) were allocated to one of six isocaloric diet under normal household conditions. Male and groups that differed in protein source (milk or female Wistar rats (age, 4 weeks) were placed on beef), protein level (11% or 33%), and fat level (5% one of five diets (50 males and 50 females per diet): or 30%). [The authors did not state whether the Diet A, a commercial semisynthetic rodent diet; meat had been cooked and/or freeze-dried before Diet B, a semisynthetic rodent diet supplemented being added to the diet.
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