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Avtanski, D.; Reddy, V.; Stojchevski, R.; Hadzi-Petrushev, N.; Mladenov, M. The Microbiome in the Obesity-Breast Cancer Axis. Encyclopedia. Available online: https://encyclopedia.pub/entry/52269 (accessed on 29 July 2024).
Avtanski D, Reddy V, Stojchevski R, Hadzi-Petrushev N, Mladenov M. The Microbiome in the Obesity-Breast Cancer Axis. Encyclopedia. Available at: https://encyclopedia.pub/entry/52269. Accessed July 29, 2024.
Avtanski, Dimiter, Varun Reddy, Radoslav Stojchevski, Nikola Hadzi-Petrushev, Mitko Mladenov. "The Microbiome in the Obesity-Breast Cancer Axis" Encyclopedia, https://encyclopedia.pub/entry/52269 (accessed July 29, 2024).
Avtanski, D., Reddy, V., Stojchevski, R., Hadzi-Petrushev, N., & Mladenov, M. (2023, December 01). The Microbiome in the Obesity-Breast Cancer Axis. In Encyclopedia. https://encyclopedia.pub/entry/52269
Avtanski, Dimiter, et al. "The Microbiome in the Obesity-Breast Cancer Axis." Encyclopedia. Web. 01 December, 2023.
The Microbiome in the Obesity-Breast Cancer Axis
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This entry is adapted from the peer-reviewed paper 10.3390/pathogens12121402

A large body of evidence has demonstrated a significant link between obesity and cancer risk. Adipose tissue, conventionally viewed as a passive reservoir for energy storage, is now recognized as a highly secretory endocrine organ that produces various pro- and anti-inflammatory cytokines, estrogens, and other bioactive molecules. Obesity, characterized by adipose tissue hypertrophy (increase in adipocyte size) and hyperplasia (increase in adipocyte number), causes the dysregulation of adipose tissue hormonal production, leading to chronic low-grade inflammation that can contribute to the initiation and progression of breast cancer, particularly among postmenopausal women. Furthermore, obesity-related metabolic changes can influence the composition of the gut microbiome, leading to dysbiosis, which may further affect breast cancer risk and outcomes. Over the past two decades, following advancements in DNA sequencing technologies, the microbiome has been recognized as a major factor in maintaining health. The interaction between the microbiome and the host organism is a dynamic bidirectional relationship, where disruptions in the microbiome reflect the host’s health and vice versa: modifications to the health status of the host lead to corresponding microbiome changes.

Microbiome Obesity Breast Cancer Dysbiosis Biomarker Diagnostic Therapeutic Diet

1. Role of the Microbiome in Obesity-Induced Inflammation

The consistent energy overload mainly affects visceral white adipose tissue. Adipose tissue hypertrophy impairs normal adipocyte differentiation and secretion and stimulates tissue infiltration of immune cells, resulting in elevated proinflammatory cytokine secretion and chronic low-grade inflammation [1], leading to the development of metabolic conditions such as metabolic syndrome, dyslipidemia, insulin resistance, and type 2 diabetes [2][3][4]. The level of adiposity also strongly correlates with an increased incidence and worse outcomes in many different types of cancer [5]. Obesity is thought to be related to a 30% increase in breast cancer risk [6][7], and various studies have found intriguing associations between microbiota and obesity [8]. Although obesity plays a protective role in the development of breast cancer in premenopausal (particularly European) women, it shows a strong positive correlation with breast cancer risk in postmenopausal settings [9]. Among the multiple factors involved in this association, cytokines released by the white adipocytes per se, or activated macrophages, may directly promote the invasive potential and aggressiveness of breast cancer cells [10][11].

The gut microbiome composition is tightly modulated by metabolic signals and plays a significant role in the development of obesity. The level of adiposity is positively associated with changes in the microbiome composition (referred to as dysbiosis), characterized by generally reduced diversity and a shift in the abundance of dominant species [12][13][14][15]. For example, a cohort study involving primary school students in China revealed that obese children had lower species diversity and a relative abundance of typically dominant bacterial strands but a higher abundance of other genera [16]. Obese leptin-deficient (ob/ob) mice have a higher Firmicutes/Bacteroidetes (F/B) bacterial ratio than their wild-type counterparts [17]. Similar changes in the F/B ratio were observed in obese and lean humans [12][17][18]. Differences in abundance between lean and obese individuals have also been detected in other bacterial groups, such as those from the Oscillospira genus or the Christensenellaceae family [19][20]. Lv et al. [15] demonstrated a linear relationship between the body mass index (BMI) and several bacterial families (Porphyromonadaceae, Acidaminococcaceae, Rikenellaceae, and Desulfovibrionaceae). White et al. [21] suggested that gut microbiota is a modifiable factor linked to early rapid weight gain during infancy, and early weight gain has been identified as a risk factor for obesity during adulthood. The connection between the gut microbiome and adiposity extends to preterm infants, where the microbial composition was found to correlate with weight gain and subsequent growth, showing the influence of the microbiota from the earliest stages of life [22]. Similar to the gut microbiome, the breast tissue microbiome shows disparities between lean and obese individuals, with obese individuals exhibiting reduced bacterial diversity [23][24].

Dietary patterns may cause gut dysbiosis, which can lead to chronic inflammation [25]. A growing body of evidence has revealed that obesity-induced inflammation is associated with changes in microbiome composition. For example, using a high-fat diet (HFD)-induced obesity C57Bl/6 mouse model, Albornoz et al. [26] showed that obesity increases the susceptibility, pulmonary inflammation, and interferon-gamma (INF-γ) levels, following an infection with Mycobacterium tuberculosis. Gut bacteria metabolize dietary fiber into short-chain fatty acids (SCFAs), primarily butyrate, acetate, and propionate [27]. Butyrate has beneficial effects against obesity, including the promotion of lipolysis and an increase in energy expenditure. It also possesses anti-inflammatory properties by inhibiting proinflammatory cytokine production and reducing the translocation of lipopolysaccharides (LPSs) from the gut lumen to the bloodstream [28][29]. Butyrate also inhibits the expression of nitric oxide synthase (NOS) in intestinal cells by activating peroxisome proliferator-activated receptor gamma (PPARγ) signaling, thus limiting the growth of certain bacteria (such as those of the Enterobacteriaceae family) [30].

2. Microbiota and Breast Cancer

The microbiome profile has been linked to many types of cancers (stomach, colon, liver, lung, and skin, among others). The most robust connections are observed in cancers of the gastrointestinal tract, which are primarily associated with Helicobacter pylori and Fusobacterium bacteria [24][31][32][33][34][35][36].

Breast cancer patients are characterized by decreased microbial diversity, as reported in several studies [37][38][39][40]. Early observational studies detected impaired intestinal microbiota in breast cancer patients, represented by a higher proportion of fecal Enterobacteriaceae, aerobic Streptococci, Lactobacilli, and anaerobic species such as Clostridia, Lactobacilli, and Bacteroides [41]. A comparative analysis by Xuan et al. [37] showed the enrichment of Methylobacterium radiotolerans in breast tumor tissues and Sphingomonas yanoikuyae in paired normal breast tissues (Figure 1). Using 16S rRNA gene amplicon sequencing, Chan et al. [42] investigated microbiota from nipple aspirates from healthy women and those with breast cancer and reported a higher incidence of Sphingomonadaceae family in the healthy subject group and a higher proportion of the genus Alistipes in breast cancer patients (Figure 1). The microbiota of breast tissue adjacent to the tumor showed higher presence of the phylum Bacteroidetes and the genera Bacillus and Staphylococcus than those in healthy tissues [43]. Similarly, Meng et al. [44] analyzed breast tissue samples using needle biopsies from patients with breast cancer and benign tumors and observed an increase in the genus Propionicimonas and the families Micrococcaceae, Caulobacteraceae, Rhodobacteraceae, Nocardioidaceae, and Methylobacteriaceae (Figure 1). The microbial characterization of samples from 25 breast cancer patients showed lower abundance of Firmicutes and Bacteroidetes and higher abundance of Proteobacteria, Actinobacteria, and Verrucomicrobia bacteria, accompanied by a reduction in Faecalibacterium prausnitzii [45]. Another comparative study between patients with breast cancer and healthy individuals [46] demonstrated greater proportion of Enterobacteriaceae and Pseudomonadaceae families (such as the genera Pseudomonas, Proteus, Azomonas, and Porphyromonas) in breast tumors and predominance of the genera Staphylococcus and Propionibacterium in healthy controls (Figure 1). A comparison of the breast tissues adjacent to the tumor showed a higher abundance of Bacteroidetes (Bacillus and Staphylococcus). Additionally, the F/B ratio was found to be significantly higher in patients with breast cancer than in controls [45].

Furthermore, microbial profiles vary during the progression of breast cancer. A comparison of the microbiome profiles of malignant tissues of different histological grades revealed that the development of breast cancer was associated with a decreased proportion of bacteria from the Bacteroidaceae family and an increased proportion of bacteria from the Agrococcus genus [44]. Stage I breast cancers exhibit an abundance of Proteobacteria, Ruminococcaceae, and Hyphomicrobium; stage II breast cancers show higher presence of Euryarchaeota, Firmicutes, Spirochaetes, and Sporosarcina, whereas stages III and IV breast cancers are more abundant on Thermi, Gemmatimonadetes, Tenericutes, and Bosea [47].

Evidence suggests that shifts in microbial assemblages in the breast are related to breast cancer development, aggressiveness, and progression [24]. Using next-generation sequencing techniques and quantitative PCR analysis, Xuan et al. [37] demonstrated that breast tumor tissue has a reduced expression of antibacterial response genes, compared with adjacent healthy breast tissue. The observed dysbiosis in breast cancer suggests that bacteria may play a role in maintaining the normal cellular processes in the breast. Thus, it is speculated that the microbial components present in the breast may influence the local microenvironment. It is hypothesized that chronic exposure to low-residue antimicrobial drugs ingested from the diet could disrupt the gut microbiota equilibrium, which can contribute to corresponding physiological changes [48]. Dysbiosis caused by antibiotic use may increase the risk of breast cancer; however, more extensive studies are needed to confirm this hypothesis [49][50].

Figure 1. Differences in microbial taxa between normal breast tissue (on the left) and breast cancer tissue (on the right) per various studies (Created with BioRender).

3. The Microbiome as a Biomarker and Treatment Target

Based on current knowledge, the microbiome has emerged as a promising biomarker for evaluating breast cancer risk and prognosis or predicting the surgical outcomes and survival of patients with breast cancer [39][51][52][53]. For example, the F/B ratio can be used as an indicator of breast cancer risk [43][54]. Evaluation of the microbiome profile could have broad implications for the diagnosis and staging of breast cancer [44]. Meng et al. [44] showed that glycerophospholipid levels and ribosome biogenesis are higher in grade III breast cancers than in grades I and II. Additionally, the microbiome involved in human estrogen metabolism (also known as the estrobolome) can be used as another target for breast cancer treatment [54]. Microbial communities can alter the response to breast cancer therapy [55]. Gut microbe dysbiosis undermines the outcome of both immune and non-immune chemotherapeutic cancer treatment modalities [56][57][58]. The microbiota may potentially be targeted to enhance the efficacy and reduce the toxicity of conventional anticancer therapies. Taken together, the complex scenario linking microbiome composition to oncogenesis and the response to anticancer treatments defines the frame of a new “oncobiotic” perspective.

Probiotics have been shown to improve gut microbiota composition and function, suggesting their potential implications in cancer prevention and treatment [59]. Lactobacillus bacteria can modulate dysregulated SCFA levels in obesity by influencing other gut microbiota, energy absorption, and chronic low-grade inflammation [60]. Lactic acid bacteria (LAB) have been reported to exert anti-obesity effects. Thus, targeting the microbiome could be considered a potential treatment option for obesity [61]. Animal and cell-based studies have shown that probiotics may have anticancer effects because they can modulate the immune system and reduce obesity-induced low-grade chronic inflammation, potentially inhibiting cancer cell growth [59][62]. A study investigating the effect of oral administration of probiotics for 12 weeks, involving 18 patients with breast cancer, demonstrated an improved microbiome profile and serum tests (ANC (absolute neutrophil count), fasting blood glucose (FBG), and low-density lipoprotein cholesterol (LDL-C) levels) [63]. The most prominent changes observed in this study were for Ruminococcus and Streptococcus spp. The effects of probiotics, prebiotics, and synbiotics on breast cancer have been reviewed in randomized controlled trials [59][64]. A systematic review and meta-analysis of randomized clinical trials of probiotic and prebiotic use in breast cancer patients and survivors by Thu et al. [65] demonstrated the beneficial effects of a combination of pro- and prebiotics on obesity and dyslipidemia, as well as the reduction of tumor-necrosis factor alpha (TNFα) levels, thus highlighting their potential against breast cancer. However, using probiotics to improve the gut microbiome as a treatment strategy for obesity is likely more complicated than anticipated and may require a long-term complex program [60].

Fecal microbiota transplantation (FMT) is another promising strategy for reducing obesity. Dietary interventions or FMT have emerged as promising strategies to help patients maintain a healthy weight [66]. FMT has been shown to reverse the effects of antibiotics and re-establish microbiota balance, resulting in the restoration of the normal functioning microbiome [67].

Furthermore, diet is known to influence the microbiota. The Mediterranean diet (characterized by a high content of plant-based foods and healthy fats) has been associated with a distinctive shift in the mammary gland microbiota, suggesting possible anti-breast cancer effects [68]. Long-term breast cancer risk is associated with diet-related plasma metabolic signatures involving exogenous steroid metabolites and microbiota-related compounds [69]. SCFAs are produced by two major groups of bacteria: Firmicutes bacteria produce butyrate, while Bacteroidetes bacteria – acetate and propionate. It has been shown that SCFAs, more specifically butyrate, inhibit tumor growth [70]. A typical Western diet decreases the generation of SCFAs, causing a leaky gut and leading to an increase in inflammatory marker levels in the bloodstream, which results in the progression of breast cancer. Conversely, healthy diets with a higher fiber content may decrease inflammation by increasing SCFA production [71].

Further studies should focus on elucidating the mechanisms underlying the impact of the microbiome on breast cancer and exploring its potential as a biomarker and treatment agent.

Abbreviations

ANC Absolute neutrophil count

F/B Firmicutes/Bacteroidetes bacterial ratio

FBG Fasting blood glucose

FMT Fecal microbiota transplantation

HFD High-fat diet

INF-γ Interferon-gamma

LAB Lactic acid bacteria

LDL-C Low-density lipoprotein cholesterol

LPS Lipopolysaccharide

NOS Nitric oxide synthase

ob/ob mice Leptin-deficient mice

PPARγ Peroxisome proliferator-activated receptor gamma

SCFA Short-chain fatty acid

TNFα Tumor necrosis factor-alpha

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Subjects: Oncology
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Dimiter Avtanski
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Varun Reddy
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Radoslav Stojchevski
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Nikola Hadzi-Petrushev
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Mitko Mladenov
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Update Date: 04 Dec 2023
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