Consumption of processed red meat and its impact on human health: A review

Abstract

Meat is an important component of the human diet, and the consumption of processed meat is high, despite the increasing popularity of the vegetarian model of nutrition. Both meat and meat product consumption contribute to delivering many vitamins and minerals, such as iron, zinc, selenium and vitamin B12; moreover, meat products are a significant source of high biological value protein, providing essential amino acids. Processed meat should be eaten in moderation. Excessive consumption of processed red meat (cured and smoked) carries the risk of developing new diseases or intensifying existing ones. This review aims to present scientific reports on the role and safety of the consumption of processed red meat in the diet of healthy individuals. The impact of meat consumption on the risk of cancer, cardiovascular diseases, diabetes, obesity, inflammatory bowel diseases, non-alcoholic fatty liver and infertility was described.

Graphical Abstract

Carcinogenicity, epidemiological studies, health, processed red meat, red meat

Introduction

In human evolutionary history, meat was one of the main means of ensuring nutritional requirements. The start of meat and marrow consumption from large animals occurred at least 2.6 million years ago (Andrews et al., 1991). Nowadays, meat is a chief part of the human diet in many cultures, and the consumption of meat products has increased considerably in most parts of the world. The production of meat has doubled in the 30 years from 1988 to 2018 and has increased fourfold since the mid-1960s. According to the predictions, global meat consumption will reach 388 million tons in 2030 and between 460 and 570 million tons in 2050, which would mean meat consumption is twice as high as in 2008. Generally, as incomes rise, more meat is consumed (Alexandratos & Bruinsma, 2012; OECD Data, 2021).

In European legislation, meat definition is given in Regulation (EC) No 853/2004 of the European Parliament and the Council of 29 Apr. 2004 laying down specific hygiene rules for food of animal origin. The term ‘meat’ is considered as skeletal muscle deriving from specified animal species (domestic ungulates including bovine, porcine, ovine and caprine animals as well as domestic solipeds, poultry, lagomorphs, wild game, farmed game, small and large wild game), which may include edible offal and blood. The term meat does not include fish and seafood (EUR-Lex-3, 2004R0853, 2021).

In the same regulation, meat products are defined as ‘processed products resulting from the processing of meat or the further processing of such processed products so that the cut surface of the original product shows that the product no longer has the characteristics of fresh meat’ (EUR-Lex-3, 2004R0853, 2021). In turn, The American Institute for Cancer Research (IARC) defines processed meat as ‘meat preserved by smoking, curing or salting, or addition of chemical preservatives’ (IARC, 2015). The World Health Organization has a slightly broader definition: ‘meat that has been transformed through salting, curing, fermentation, smoking, or other processes to enhance flavour or improve preservation’ (WHO, 2021a).

Meat consumption contributes to delivering many vitamins and minerals, such as iron, zinc, selenium and vitamin B₁₂. Offal meats like the liver are also crucial sources of folic acid and vitamin A. Moreover, meat products are a significant source of high biological value protein, providing essential amino acids. High protein assortment includes chicken breast (32 g/100 g), pork chop (31.6 g/100 g), beefsteak (31 g/100 g) or lamb chop (29.2 g/100 g) (USDA, 2021). It is also important to note that this protein has high digestibility scores and distinguishes itself because of its richness in all the essential amino acids with no limiting amino acids (Górska-Warsewicz et al., 2018). On the other hand, there are types of meat that are low in protein, such as duck meat or processed meats. To sum up, the role of meat, especially red meat (e.g. pork, beef and their products), as a protein source is not unequivocal.

Meat is also an essential source of fat (Table 1). Fat content differs significantly among meat products such as offal and specialties like sausages, ham or retail beef cuts, poultry and others (Valsta et al., 2005). The USDA reports values from 5.4 to 7.9 g/100 g fat in retail beef cuts (USD, 2021). Pork fat ranges from 8 to 10.7 g/100 g in the USDA tables. The fat content in the main retail cuts from chicken and turkey range from 1 to 15 g/100 g, but the skin is probably the primary source of fat in poultry meat, where cuts including skin had higher values (Pereira 2013). Total fat concentrations are distinctly higher in many types of processed meat, with extreme values of up to 90 g/100 g total fat in fatty bacon (USDA, 2021). Meat products play an important role in daily nutrition in many populations. Therefore, making calculating the contribution of meat to the total daily caloric intake is one of the cornerstones of menu planning.

Table 1

Comparison of the nutritional value and the fat content of different meats (Kunachowicz et al., 2018)

Type of meat		Energy value (kcal/kJ in 100 g)	Fat content (g in 100 g)
Beef	fillet	112/471	3.5
	loin	152/636	7.3
	ribs	219/909	15.7
Chicken	raw meat	158/660	9.3
	breast without skin	98/414	1.3
Duck	raw meat	311/1288	28.6
Goose	raw meat	343/1416	31.8
Hen	raw meat	203/844	14.3
Horse	raw meat	109/458	2.5
Mutton	shoulder	287/1190	25.0
Pork	blade bone	160/668	8.6
	spare rib	205/852	14.4
	loin	129/545	4.2
	raw ham	128/538	4.7
Turkey	raw meat	129/541	6.8
	breast without skin	83/352	0.7
Veal	shoulder	105/442	2.8

Processed meat refers to any meat that has been transformed through one or several of the processes mentioned in the third paragraph of this section. Most processed red meats are not only made from pork or beef but may also include different assortment, for example meat by-products such as blood or offal. The most popular processed red meat products included as follows: cured meat pieces (bacon, cooked ham and corned beef), fresh industrial processed meat products (sausage and kebab), pre-cooked ready-to-eat products (frankfurter and mortadella), fermented sausages (salami, chorizo and pepperoni) and dried meat includes strips or flat pieces (Heinz & Hautzinger, 2007).

Salting, that is adding NaCl to meat, assists in reducing and preventing microbial growth, decreases the water content of meat, increases the ability of the meat to bind during cooking, aids in extracting salt‑soluble meat proteins for emulsion stability and enhances basic meat taste and flavour (Bae et al., 2018). Cured meats such as bacon, processed meats and sausages for hot dogs contain nitrites added to meat products as a preservative, colour fixative and antimicrobial agent (Govari & Pexara, 2018). Smoking is one of the oldest food preservation methods and is still widely used in fish and meat processing. Smoking inactivates microorganisms and enzymes and influences its taste. As a disadvantage, however, wood smoke contains a large number of polycyclic aromatic hydrocarbons (PAH) and their alkylated derivatives, which are formed by pyrolytic processes at high smoking temperatures (400–1000 °C) (Stumpe-Vīksna et al., 2008). It is believed that PAHs may contribute to some of the adverse health effects of processed meat. Fermentation is a biological acidulation (by wild or cultured microorganisms) and preservation method that results in a distinctive flavour, colour and tenderness, as well as enhanced microbiological safety (Ockerman & Basu, 2014).

The association between processed red meat consumption and cancer incidence, cardiovascular disease (CVD) or type-2 diabetes was extensively studied (Boada et al., 2016; Rohrmann & Linseisen, 2016). However, many other common disorders positively correlate with the high consumption of red meat. This article summarises the current information on the health effects of processed red meat consumption in adults, focusing on less described commonly described diseases (e.g. obesity, non-alcoholic fatty liver, infertility and inflammatory bowel diseases) related to processed red meat. Given the importance of this topic, this review was aimed at revising the current state-of-the-art on the impact of processed red meat on the health status in adults. A systematic search of the relevant literature published in PubMed, ScienceDirect and Cochrane Central Register of Controlled Trials Database was conducted.

Cancer, CVD, type-2 diabetes and total mortality

In October 2015, the International Agency for Research on Cancer (the World Health Organization's cancer agency) classified processed meat as a Class 1 carcinogen and red meat as a Class 2A carcinogen to humans (IARC, 2015). IARC evaluated more than 800 epidemiological investigations that examined cancer associations using red meat and processed meat in many countries with diverse diets and ethnicities/races. Using the search term 'processed red meat and cancer' in PubMed, it is clear that there has been a systematically increasing annual number of publications focused on this topic, especially after 2015: only one in 1990, near to 50 each year 2010-2015 and about 80 each year 2016-2020. Most of them agree to a greater or lesser extent – that the consumption of red and processed meat is associated with an increased risk of cancer, especially colorectal cancer (Abu-Ghazaleh et al., 2021; Aykan, 2015; Behrens et al., 2018; Czaderny, 2019; Ganjavi & Faraji, 2019; Knuppel et al., 2020; Mafiana et al., 2018; Pouchieu et al., 2014; WCRF/AICR, 2018; Saliba et al., 2019). In contrast, only a few studies have not reached the same conclusion (Pramual et al., 2018). Among the potential mechanisms of carcinogenicity of red meat, the most frequently mentioned is adverse effects exerted by the haem iron contained in red meat, which would promote the formation of mutagenic and carcinogenic agents (Kruger & Zhou, 2018), certain chemical substances such as heterocyclic aromatic amines and polycyclic aromatic hydrocarbons, formed during the heating process of meats, and that of N-nitroso compounds, formed during the curing of meats, and the potential role played by environmental factors and gut microbiota (Domingo, 2019; Song & Chan, 2019).

The association between processed meat and the risk of type-2 diabetes has been investigated in several cohort studies and summarised in a few meta-analyses (Micha et al., 2010, 2012; Kaluza et al., 2012). Scientific evidence showed a higher relative risk of type-2 diabetes, which was in the range of 1.19 to 1.82, for the consumption of processed meat (Ekmekcioglu et al., 2018). Haem iron, provided mainly by red meat consumption, was proposed as a potential mechanism through which red meat exerts its adverse effect in diseases related to oxidative stress and inflammation, that is type-2 diabetes (Bendinelli et al., 2013). Furthermore, the observed significant association between processed meat and diabetes led to the hypothesis that protein and other ‘unhealthy’ nutrients included in processed products are responsible for abnormal glycaemic status (Ericson et al., 2013).

Many studies have examined the association between red and processed meat consumption and the risk of CVD, particularly myocardial infarction, or more broadly CHD, and stroke. Mainly processed red meat appears to be an important factor, which showed a significantly positive association of the above diseases' risk (Medeiros et al., 2019; Rohrmann & Linseisen, 2016). Some other potential mechanisms apply clearly to processed meat and red meat in general. Firstly, haem iron in red meat may lead to oxidative stress, similar to diabetes and cancer (Rohrmann & Linseisen, 2016). Moreover, processed meat is a source of saturated fatty acids and cholesterol. For many years, a positive association between saturated fatty acids (SFAs), blood cholesterol and CVD risk is suggested (Ekmekcioglu et al., 2018).

Taking into account the arguments mentioned above, this is estimated that a higher intake of processed meat (relative risk – RR: 1.23; 95% CI – Confidence Intervals) was associated with an increased risk of all-cause mortality (Schwingshackl et al., 2017). Also, several other prospective studies proved the association between processed red meat intake and mortality (Abete et al., 2014; Larsson & Orsini, 2014; Wang et al., 2016).

Obesity

According to World Health Organization (WHO), 650 million adults were obese in 2016, and more than 1.9 billion were overweight, also accounting for over 60% of deaths related to high body mass index (WHO, 2021b). It means that nowadays, more than one-third of the world's population is classified as obese or overweight (GBD, 2015). If the upward trend continues at the current level, researchers estimate that by 2030, this number will surpass 50% (Chooi et al., 2019). An excessive body weight adversely affects nearly all the body's physiological functions and comprises a significant public health threat. It increases the risk for developing multiple disease conditions, such as several types of cancers (Lauby-Secretan et al., 2016), cardiovascular disease (Czernichow et al., 2011; Singh et al., 2013), diabetes mellitus (Singh et al., 2013), infertility (González-Rodríguez et al., 2018), poor mental health (Anstey et al., 2011) and all of which have adverse effects on the quality of life, healthcare cost and work productivity (Hruby et al., 2016).

The ‘Western diet’ pattern includes high amounts of red and processed meat and is considered an 'obesity-inducing dietary pattern' (Esmaillzadeh & Azadbakht, 2008). While some clinical trials have suggested a correlation between obesity and red meat intake (Babio et al., 2012; Shay et al., 2012), more limited evidence exists regarding the relationship between processed red meat and obesity. There is only one comprehensive systematic review and meta-analysis to evaluate the relation between the consumption of red and processed meat and obesity to the best of our knowledge. Based on the available analysis, the authors proved that red, processed meat intake was directly associated with the risk of obesity. Moreover, the results illustrate that more red or processed meat intake was associated with higher abdominal obesity (defined by elevated waist circumference) and body mass index (Rouhani et al., 2014). This dependence may be due to the fact that processed red meats are rich sources of cholesterol and saturated fatty acids.

Moreover, processed red meat products are also high-calorie and tasty. For this reason, there are willingly choosing by consumers. Red, processed meat intake occurs in conjunction with other components of the Western dietary pattern (e.g. pre-packaged foods, butter, candy and sweets, fried foods, high-fat dairy products, eggs or refined grains) that also significantly impact the onset and promotion of obesity (Kopp, 2019; Rouhani et al., 2014). The count of some gut microbiota, such as Bacteroides enterotype, is positively related to animal protein consumption (Wu et al., 2011). Bacteroides are prominent among obese individuals, and their abundance is positively correlated with BMI. For this reason, gut microbiota might have a role in obesity (Tseng & Wu, 2019).

Non-alcoholic fatty liver

Non-alcoholic fatty liver disease (NAFLD) is defined as an increased accumulation of triglyceride in hepatocytes due to either de novo hepatic lipogenesis or increased inflow of free fatty acids, not caused by excessive alcohol consumption and other liver diseases (Chalasani et al., 2018). NAFLD incidence is growing rapidly, especially in Western countries. Approximately 25-30% of the adult population worldwide is affected (Bellentani, 2017). NAFLD has become distributed in parallel with metabolic syndrome; that is it is mainly associated with obesity, insulin resistance, glucose intolerance and dyslipidemia (Moosavian et al., 2020).

As shown above, processed red meat consumption has been linked to an increase in cancer incidence, type-2 diabetes and CVD. In parallel, NAFLD's prevalence is growing, and some components of the diseases, mentioned above, are also common to NAFLD. The few studies published on this topic demonstrated an independent positive correlation between high consumption of red and/or processed meat with NAFLD. Moreover, the consumption of red meat prepared by unhealthy methods (e.g. smoking and grilling) was independently associated with higher consumption of HCAs (heterocyclic amines), which are related to insulin resistance (IR), one of the leading risk factors for disease severity (Ryan et al., 2013; Zelber-Sagi et al., 2018). Some studies showed that grilled meat or fish intake more than once a week increased NAFLD odds by about twofold (Miele et al., 2014). The ‘western dietary pattern’ mainly consists of, for example a high intake of processed meat was significantly associated with the risk of NAFLD (Kalafati et al., 2019; Salehi-sahlabadi et al., 2021).

Furthermore, indirect support for the negative impact of red meat in NAFLD stems from the Mediterranean diet's protective effect NAFLD (Ryan et al., 2013), towards advocating low processed meat intake. The mechanisms by which meat intake is related to NAFLD are unknown. It can be claimed that the harmful association with meat may, at least partially, be related to a generally less healthy diet or lifestyle characterizing people who eat more processed meat rather than a causal effect of meat (Zelber-Sagi et al., 2018).

Infertility

The literature on the relationship between human fertility and eating choices has dramatically expanded over the last few years (González-Rodríguez et al., 2018; Silva et al., 2019). While there are only a few studies (Afeiche et al., 2014; Nassan et al., 2018; Xia et al., 2015) on the direct relationship between processed meat consumption and effects on fertility, specific eating patterns can be identified from them.

In men's case, an adverse effect of high consumption of processed red meat has been demonstrated for low sperm parameters (fewer than 15 million sperm per millilitre or less than 39 million sperm total per ejaculate), fertilisation rates and sperm motility. Afeiche et al. (2014) showed that compared with men in the lowest quartile of processed red meat intake, men in the highest quartile had 23.2% fewer morphologically normal sperm. This dependence has not been confirmed for all kinds of meat because, according to the published results, the intake of poultry or unprocessed red meats was unrelated to semen quality indicators (Afeiche et al., 2014). The case–control study results demonstrate that an increased intake of processed meats was associated with a significantly higher risk of asthenozoospermia (low sperm motility). In this study, the authors also showed that being in the highest tertile of poultry intake was associated with a lower risk of this disease (Eslamian et al., 2012). Xia et al. (2015) published the convergent results, connected with a general fertilisation rate study. They demonstrated that processed meat intake was inversely related to fertilisation in conventional insemination cycles but not intracytoplasmic sperm injection cycles. Importantly, these relations were unchanged after adjustment for the female partner's overall dietary patterns, including processed meat intake (Xia et al., 2015). In general, epidemiological observations are concordant in the association of low-quality sperm parameters with a higher intake of red, processed meat (Benatta et al., 2020; Salas-Huetos et al., 2017).

According to Nassan et al. (2018), consuming fish instead of any other protein-rich food was consistently related to greater odds of live birth among women undergoing infertility treatment. The contrast was most significant when fish was consumed instead of processed meats. Among women from The Nurses' Health Study II (NHS-II cohort), one additional serving of different types of meat (including processed meats) per day, while holding calories constant, was associated with a 32% increase in the risk of ovulatory infertility (Chavarro et al., 2008).

Inflammatory bowel diseases

Inflammatory bowel diseases (IBD), which include ulcerative colitis (UC) and Crohn's disease (CD), are chronic relapsing and remitting inflammatory diseases of the gastrointestinal tract that are increasing in prevalence and incidence globally. Epidemiological evidence suggests that diet impacts the risk of developing IBD and modulates disease activity. Using diet as a therapeutic option is attractive to patients and clinicians alike due to its availability, low cost and few side effects. Diet may influence IBD risk and disease behaviour through several mechanisms (Wark et al., 2020). Research into the role of diet, especially anti-inflammatory, in treating IBD has emerged over the past three years, showing that the problem still exists (Gajendran et al., 2018; Keshteli et al., 2019; Mirmiran et al., 2019; Reddavide et al., 2018).

Meat consumption may increase the risk of inflammatory bowel disease. The results of scientific works have already been published that confirm this position. Ge et al. (2015) published a meta-analysis in which they collected data from nine thematic publications. The results suggest that high meat intake increases IBD risk, and this association varies by the type of meat consumed. Relative to those who did not or seldom eat meat, meat consumers had a significantly greater risk of inflammatory bowel disease.

On the other hand, Albenberg et al. (2019) performed a randomised controlled trial to determine whether reduced consumption of red and processed meats decreases the risk of symptomatic relapse of CD. In the study, individuals who were in remission with CD consumed a serving of red meat at least once weekly. The authors concluded that among patients with CD in remission, the level of red and processed meat consumption was not associated with time to symptomatic relapse.

Should we reduce the consumption of processed red meat?

An optimal diet has been estimated to prevent 11 million deaths per year globally, or 255 million summed up years of life lost due to premature mortality and the years lived with a disability (GBD, 2017 Diet Collaborators, 2019). In turn, 'Western' dietary pattern with high intakes of red and processed meats, sugar-sweetened beverages, and low intakes of vegetables and high-fibre foods is associated with detrimental effects cardiometabolic health and increased risk of obesity (Drake et al., 2018; Naja et al., 2015). The current systematic reviews on processed meat proved that a reduction in 21 g per day is associated with a relative risk decrease of 8% for untimely deaths. On the other hand, each 50 g serving/day of processed meats was associated with a 20% higher risk of all-cause mortality (Fadnes et al., 2020). In contrast to the above pieces of evidence, in October 2019, a series of 5 review articles (journal Annals of Internal Medicine) focused on the possible effect of red and processed meat on human health, especially cancer cardiometabolic diseases. These publications are the part of Nutritional Recommendations and accessible Evidence summaries composed of systematic reviews (NutriRECs), the goal of which was to develop trustworthy guideline recommendations on human nutrition (Johnston et al., 2019). Three of these reviews were most focused on cancer. These articles' main conclusion was that certainty of evidence about red and processed meat consumption on cancer and mortality is low to very low, and the possible incidence is minimal. NutriRECs suggest that dietary patterns with less red and processed meat intake may result in very small reductions in adverse cardiometabolic and cancer outcomes, and diets restricted in red meat may have little or no effect on total mortality. In conclusion, the authors suggest that adults should continue their current processed meat consumption (Han et al., 2019; Vernooij et al., 2019; Zeraatkar et al., 2019). NutriRECs guidelines are not justified as they contradict the evidence generated from much strong evidence (Abete et al., 2014; Larsson & Orsini, 2014; Medeiros et al., 2019). These claims also were contributed to emerge a harsh response of the scientific and medical community, which demonstrated many methodological flaws in NutriRec's articles and said that the publication of these studies and the meat guidelines in a major medical journal is unfortunate because it may also harm the credibility of nutrition science and erode public trust in scientific research (Qian et al., 2020; Science Media Centre, 2019). The main conclusion is that current studies do not cast doubt on the importance of the current dietary recommendations to reduce the intake of red and processed meat. NutriRECs articles should not change current recommendations on healthy and balanced eating patterns to prevent chronic diseases (Fadnes et al., 2020).

Future investigates

Future research should investigate the relation between sub-types of red, processed meat and specific causes of mortality. It is not fully understood whether each type of processed red meat affects the human body in the same way. Due to the wide range of processed meat products, it is worth systematising this issue. There are still few scientific reports and no recommendations on the safety of consuming offal and products based on them. To avoid different dietary recommendations, better biomarkers of meat intake and co-disease occurrence and updated food composition databases are required for future studies. Moreover in the future, the development of electronic medical records and other systems for collecting and handling objective data should assist in the design and conduct of improved prospective observational studies, which will explain the relationship and mechanisms between processed red meat consumption and other diseases. Future research priorities should also focus on meat analogues, especially new products such as cultured meat. It seems that these studies must be related to their long-term health effects, the safety of immediate consumption and consumer acceptance.

Conclusions

Despite some of the health benefits of consuming red meat (a major source of high biological value protein, iron and vitamin B₁₂), current studies have found that high red and processed meat intake increases the risk of all-cause mortality, type-2 diabetes, colorectal cancer and cardiovascular disease. These conclusions are based on strong scientific evidence. More scientific reports link high intake of red, processed meat with less apparent diseases such as non-alcoholic fatty liver, infertility, obesity or inflammatory bowel diseases. Current studies do not doubt the importance of the current dietary recommendations to reduce the intake of red and processed meat to a proper health condition.

Conflict of interest

The authors declare no conflicts of interests.

Author Contributions

Justyna Libera: Conceptualization (lead); Formal analysis (equal); Supervision (lead); Visualization (lead); Writing-original draft (lead); Writing-review & editing (equal). Katarzyna Iłowiecka: Formal analysis (lead); Methodology (lead); Resources (lead); Software (supporting); Visualization (equal); Writing-original draft (supporting); Writing-review & editing (equal). Dariusz Mirosław Stasiak: Project administration (lead); Validation (lead).

Ethical approval

Ethics approval was not required for this research.

Peer Review

The peer review history for this article is available at https://publons.com/publon/10.1111/ijfs.15270.

DATA AVAILABILITY STATEMENT

Data sharing not applicable to this article as no datasets were generated or analysed during the current study