Volume 3, August 2016, Pages 1–7
Open Access
Review article
Coffee and metabolic impairment: An updated review of epidemiological studies
- Under a Creative Commons license
Abstract
Background
Coffee
is one of the most consumed beverages worldwide. In the last years,
coffee consumption has been associated with a number of beneficial
effects against metabolic impairment. The aim of this narrative review
was to report the most updated and comprehensive evidence from
epidemiological and experimental studies as well as mechanisms of action
of coffee on metabolic impairment.
Methods
A
search in electronic databases (PUBMED and EMBASE) was performed to
retrieve systematic and pooled analyses on coffee and diabetes,
hypertension, and dyslipidemia. Furthermore, the most accredited
hypotheses and mechanisms of action of coffee have been described.
Results
Coffee
consumption has been associated with reduced risk of diabetes in
observational studies. However, the effect seems not to be mediated by
caffeine. Contrasting results have been found in pooled analyses of
observational studies on hypertension, despite short- and long-term
follow-ups that have been demonstrated to influence the outcome. Poor or
little effect on plasma lipids has been reported in studies on acute
administration of coffee, yet depending on the type of coffee
preparation. The main beneficial effects of coffee consumption seem to
rely on the content of antioxidant and anti-inflammatory compounds
(i.e., polyphenols). Among the most important, chlorogenic acids have
demonstrated direct anti-hypertensive action through beneficial effect
on endothelial function, and significant improvement in glucose and
insulin metabolism. Also, diterpenes and melanoidins are major
candidates as antioxidant compounds showing the capacity to inhibit the
production of inflammatory mediators. However, caffeine and diterpenes
may also exert negative effects, such as acute rise in blood pressure
and serum lipids.
Conclusion
In
light of the most recent evidence, coffee consumption seems to be
favorably related with health and to protect by metabolic impairment.
Keywords
- Coffee;
- Caffeine;
- Metabolic disorders;
- Diabetes
1. Introduction
Metabolic
disorders, such as obesity, dysregulated glucose homeostasis,
dyslipidemia, and abnormal elevation of systolic and diastolic blood
pressure are important risk factors for cardiovascular disease (CVD) and
are among the major contributors for overall mortality [1].
Overweight and obese population have rapidly increased worldwide
leading to a concomitant rise of type 2 diabetes incidence, especially
in the highest income regions [2].
Hypertension and dyslipidemia affect 20%–40% of the population, showing
a significant association with elevated BMI, waist circumference, and
fasting blood glucose [3].
Altogether, these conditions represent a major public health issue that
could potentially be reduced by the adoption of a healthier lifestyle.
Besides well-known risk factors, such as sedentary and smoking habits,
dietary habits show a crucial impact toward metabolic disorders. Several
investigations pointed out the important role of certain dietary
patterns, such as the Mediterranean diet or the Dietary Approach to Stop
Hypertension (DASH), as significant protective factors against
metabolic disorders and CVD risk factors [4], [5], [6] and [7]. Cohort studies demonstrated positive effects of these dietary patterns in both Mediterranean and non-Mediterranean countries [8] and [9].
However, their application in non-Mediterranean areas is somehow
limited and some important foods have not been taken into account when
considering such dietary patterns. In the last ten years, research on
coffee drinking has increased dramatically suggesting that coffee
consumption is not as negative as it was hypothesized in earlier studies
[10].
In a recent State-of-the-Art review, a moderate coffee consumption (2
to 3 cups per day) has shown potential benefits on cardiometabolic
disease, cardiovascular health, and all-cause mortality [11]; although in other studies, high coffee consumption (> 4 cups per day) could have adverse effects [12].
The findings recently published pointed out convincing hypotheses on
its beneficial effects in preventing metabolic impairment and laboratory
research on its components provided biological plausibility for its
action [13].
In this narrative review, we report the most important epidemiological
evidence on coffee consumption and metabolic impairment, showing the
inconsistency between epidemiological and experimental studies as a
result of the biological differences between short- versus long-time
consumption. Furthermore, the most accredited hypotheses and mechanisms
of action have been described.
2. Epidemiological versus experimental evidence
2.1. Diabetes mellitus, glucose tolerance, and insulin sensitivity
Two
recent systematic reviews and meta-analyses analyzing the specific
association between coffee (data from 28 studies with information on
1,109,272 participants) [14], and decaffeinated coffee (10 studies, 491,485 participants) [15]
on incidence of type 2 diabetes found a nonlinear dose–response
relationship between coffee intake and subsequent risk of type 2
diabetes, with a decrease of about 8% of risk for every 1 cup/day
increment in coffee intake after adjustment for potential confounding
factors (Table 1).
Since similar results were shown for decaffeinated coffee, it is likely
that the protective effect may exist aside from the influence of
caffeine intake. Another systematic review including 13 cohort studies
with 9473 type 2 diabetes cases and 47,387 participants, found a
reduction in type 2 diabetes incidence in those subjects who consumed 4
or more cups per day compared with less than 2 cups drinkers [16] (Table 1).
Advantage emerged comparing intake of filtered coffee over pot boiled
and decaffeinated coffee over caffeinated coffee. However, by analyzing
single studies reporting inconclusive results, a relation with factors
that could explain such results (i.e., type of coffee or country) could
not be found. In addition to the previous systematic reviews, more
recent observational studies are in line with the hypothesis that coffee
intake may be linked to a lower risk of diabetes [17], [18], [19], [20] and [21], reduced risk of deterioration of glucose metabolism [22] and [23], and insulin resistance [24], [25], [26] and [27].
- Table 1. Characteristics of meta-analysis and systematic review included in this review.
Author Year Number and design of the studies Participants Cases Outcome Exposure Main results and RR (95% CI) Diabetes mellitus, glucose tolerance, and insulin sensitivity Ding et al. [14] 2014 28 PCS 1,109,272 43,335 T2DM incidence 0 coffee cup/d 1 1 coffee cups/d 0.92 (0.90, 0.94) 2 coffee cups/d 0.85 (0.82, 0.88) 3 coffee cups/d 0.79 (0.75, 0.83) 4 coffee cups/d 0.75 (0.71, 0.80) 5 coffee cups/d 0.71 (0.65, 0.79) 6 coffee cups/d 0.67 (0.61, 0.74) Jiang et al. [15] 2014 26 PCS 1,096,647 50,595 T2DM incidence Coffee lowest vs highest 0.71 (0.67, 0.76) 10 PCS 491,485 29,165 T2DM incidence Decaffeinated coffee lowest vs highest 0.79 (0.69, 0.91) 6 PCS 321,960 9302 T2DM incidence Caffeine, lowest Vs highest 0.70 (0.65, 0.75) Whitehead et al. [28] 2013 2 RCTs 53 T1DM individuals N/A Hypoglycemic episodes Caffeine 400–500 mg Increased awareness and decreased duration of hypoglycemic episodes 6 RCTs 73 T2DM individuals N/A Blood glucose and insulin sensitivity Caffeine 200–500 mg Increased blood glucose (16%–28%) and insulin levels (19%–48%). Decreased insulin sensitivity by 14%–37%. 1 RCT 8 GDM individuals N/A Blood glucose and insulin sensitivity Caffeine 200 mg Increased blood glucose (19%) and insulin level (29%) and reduced insulin sensitivity by 18%. Muley et al. [16] 2012 13 PCS 12,47,387 9473 T2DM incidence Coffee T2DM incidence was reduced in subjects who drank 4–6 cups/d and 6–7 cups/d compared with < 2 cups/d drinkers Hypertension Mesas et al. [41] 2011 5 RCTs 85 hypertensive individuals N/A Acute effect on BP Caffeine 200–300 mg) SBP 8.14 mmHg (5.68, 10.61) DBP 5.7 mmHg (4.1, 7.4) 6 RCTs 364 hypertensive individuals N/A Long-term effect on BP Coffee or caffeine No change in BP Zhang et al. [39] 2011 6 PCS 172,567 37,135 Hypertension incidence < 1 coffee cup/d 1 1–3 coffee cups/d 1.09 (1.01, 1.18) 3–5 coffee cups/d 1.07 (0.96, 1.20) > 5 coffee cups/d 1.08 (0.96 ,1.21) Noordzija et al. [42] 2005 16 RTCs 110 N/A BP Coffee SBP 1.22 mmHg (0.52, 1.92) DBP 0.49 mmHg (− 0.06, 1.04) Caffeine SBP 4.16 mmHg (2.13, 6.20) DBP 2.41 mmHg (0.98, 3.84) Caffeine and coffee SBP 2.04 mmHg (1.10, 2.99) DBP 0.73 mmHg (0.14, 1.31) Dyslipidemia and lipid metabolism Cai et al. [54] 2012 12 RCT 1017 N/A Serum lipids Coffee 2.4 to 8.0 cups/day TC 8.05 mg/dl (4.48,11.62) LDL-C 5.44 mg/dl (1.38,9.51) HDL-C -0.12 mg/dl (− 0.62, 0.38) TG 12.55 mg/dl (3.47, 21.64) - CI, confidence interval; BP, blood pressure; DBP, diastolic blood pressure; GDM, gestational diabetes mellitus; HDL, high-density lipoprotein cholesterol; LDL-C, low-density lipoprotein cholesterol; N/A, not applicable; PCS, prospective cohort study; RTC, randomized controlled trial; SBP, systolic blood pressure; T1DM, type 1 diabetes mellitus; T2DM, type 2 diabetes mellitus; TC, total cholesterol; TG, triglyceride.
Generally,
results from randomized controlled trials (RCT) exploring the effect of
coffee consumption on glucose metabolism and biological risk factors
for type 2 diabetes widely contrasted those from observational studies. A
recent meta-analysis of RCT in people with type 2 diabetes reported
substantial negative effect of caffeine intake on blood glucose control [28] (Table 1).
As expected, a major limitation of the trials included in the pooled
analysis was the short period of study. Indeed, the beneficial effects
of caffeinated and decaffeinated instant coffee on glucose metabolism
were found in a recent study that lasted 16 weeks [29],
but studies exploring the acute effects following the meal reported
opposite or inconclusive results. An experimental study conducted on
healthy volunteers resulted in an increasing insulin response and
decreased insulin sensitivity index after a 75 g oral glucose tolerance
test, compared to water [30].
While in another RTC on healthy subjects, coffee consumption increased
glucose concentration and lowered insulin concentrations in the first
30 min after a standardized meal [31].
Caffeinated coffee, after either a high or low glycemic index meal,
significantly impaired acute blood glucose management and insulin
insensitivity compared with ingestion of decaffeinated coffee [32] and [33], despite these effects being stronger after a lipid-rich meal [34].
Moreover, coffee consumption during a carbohydrate meal seems to
decrease the insulin sensitivity of a second carbohydrate meal, even
without an additional coffee intake [35].
Some other experimental studies reported poorly significant results of
caffeinated coffee on postprandial glycemic tolerance and insulin
sensitivity [36] and [37]
or increase of coffee-derived compounds but no changes of markers of
glucose metabolism at an oral glucose tolerance test were found [38].
2.2. Hypertension
Epidemiological
studies exploring the role of coffee consumption on the development of
hypertension showed inconclusive results. Among the several pooled
analysis that have been conducted during last 10 years, the most recent
meta-analysis of epidemiological studies, including 6 prospective
cohorts with a total of 172,567 participants and 37,135 incident cases
of hypertension, concluded that the summary relative risks (RRs) for
hypertension was 1.09 (95% confidence interval (CI): 1.01, 1.18) for
consumption of 1–3 cups per day, whereas no significant risk was found
for higher categories (> 3 cups/day) [39] (Table 1).
A meta-analysis of experimental and observational epidemiological
studies on coffee consumption and hypertension reported low-quality
evidence, unable to show any statistically significant effect of coffee
consumption on blood pressure or the risk of hypertension [40] (Table 1).
Another meta-analysis investigating the role of coffee/caffeine intake
in hypertensive subjects results in an acute increment of BP for ≥ 3,
without any long-term association between coffee intake and BP [41] (Table 1).
These findings seem to confirm the results of a previous meta-analysis
of RCT conducted with regard to the intake of both coffee and caffeine [42] (Table 1).
They reported a significant rise of 2.04 mmHg (95% CI: 1.10, 2.99) in
systolic blood pressure and 0.73 mmHg (95% CI: 0.14, 1.31) in diastolic
blood pressure for pooled analysis of coffee and caffeine trials. When
coffee trials and caffeine trials were analyzed separately, blood
pressure elevations appeared to be significant only for caffeine but not
for coffee, suggesting that despite the biochemical mechanism of action
of caffeine supporting the biological plausibility that acute ingestion
of such compounds may increase blood pressure, when ingested through
coffee, the blood pressure effect of caffeine was somehow attenuated. It
is noteworthy that most recent investigations found a significantly
reduced risk of hypertension evaluated in both cross-sectional and
prospective design only when analysis was stratified by smoking status [43] and [44].
2.3. Dyslipidemia and lipid metabolism
The
early epidemiological studies published in the 1980s demonstrated a
significant association between coffee consumption and increased serum
cholesterol levels [45], [46], [47] and [48].
The hypercholesterolemic effect of coffee has been demonstrated to
depend on the diterpenes cafestol and kahweol, and by the method of
brewing [49].
Contrarily, filtered coffee consumption seems to have poor or no
association with serum lipid levels compared to boiled coffee, maybe due
to the retention of diterpenes by the paper filter [50].
Thus, results from epidemiological studies reported contrasting results
with strong country-specific characteristics due to the different
bioactive compounds contained in coffee in different countries and type
of preparation method used [51], [52] and [53].
Contrasting
with observational studies, a recent meta-analysis of RCT evaluated the
effects of coffee intake on serum lipids in 12 studies conducted on
1017 subjects [54] (Table 1).
On average, drinking coffee for 45 days was associated with an increase
of 8.1 mg/dl (95% CI: 4.5, 11.6) for total cholesterol, 5.4 mg/dl (95%
CI: 1.4, 9.5) for LDL-C, and 12.6 mg/dl (95% CI: 3.5, 12.6) for
triglycerides. Meta-regression analysis also revealed a positive
dose–response relation between coffee intake and total cholesterol,
LDL-C, and triglycerides. However, other more recent studies (thus not
included in the previous meta-analysis) reported poor or little
influence on plasma lipids following acute ingestion of coffee [55] or even a suppression of postprandial hyperlipidemia [56], significant decrease of triglycerides, and increase of HDL-cholesterol [55].
3. Potential beneficial mechanisms of action
3.1. Glucose and insulin metabolism regulation
Despite the acute ingestion of caffeine resulting in a reduction of insulin sensitivity due to decreased glucose storage [57] and [58],
this short-term effect cannot be observed after long-time consumption
of coffee because of an overall impairment of effects of caffeine after
continued intake [59].
Coffee has been reported to be the main contributor of a number of
antioxidant compounds, including some polyphenols such as chlorogenic
acids [60]. This family of polyphenols (mostly caffeic and ferulic acid) demonstrated the ability to affect some metabolic pathways [61] and [62]. In animal models, consumption of chlorogenic acids reduced fasting plasma glucose [63], [64] and [65], increased sensitivity to insulin [66], and slowed the appearance of glucose in circulation after glucose load [67] and [68].
This particular family of molecules showed a specific competitive
inhibition of the glucose-6-phosphate translocase in rat liver
microsomes [69]
an enzyme highly involved in the regulation of homeostasis and blood
glucose levels. At the cellular level, chlorogenic acids activate
adenosine monophosphate-activated protein kinase (AMPK), a sensor and
regulator of cellular energy balance, leading to beneficial metabolic
effects, such as the inhibition of fatty acid synthesis and hepatic
glucose production. Thus, chlorogenic acid by the activation of AMPK may
contribute to lipid and glucose metabolism regulation [70].
Further hypotheses on the mechanism through which chlorogenic acids may
prevent diabetes consist in their capacity to reduce sodium-dependent
glucose transport in brush border membrane vesicles isolated from rat
small intestine [71], and to inhibit α-amylase [72] and [73] and α-glucosidase activity [74] and [75],
two key enzymes responsible for digestion of dietary carbohydrates,
resulting in a reduction of intestinal absorption of glucose.
Together
with phenolic compounds, trigonelline and sex hormone-binding globulin
(SHBG) also demonstrated a protective effect against diabetes [67] and [76]. The vitamin B3
precursor trigonelline has been shown to potentially improve insulin
sensitivity in animal studies by inhibiting dipeptidylpeptidase-4 and
α-glucosidase activities in both plasma and small intestine [77]
and ameliorating the oxidative stress in type 2 diabetic rats
downregulating the gene expressions involved with NADPH oxidase and
mitochondrial electron transfer system [78].
SHBG have been related with type 2 diabetes since membranes of a
variety of cells are able to specifically bind them with high affinity,
and SHBG mediates the steroid-signaling system at the cell membrane
through the SHBG receptors and exerting direct metabolic effects [79].
3.2. Lipid metabolism regulation
It
has been reported that some components present in unfiltered coffee
(i.e., cafestol and kahweol) raise serum lipids, but a clear involvement
in the deposition of LDL-C and/or an oxidation of this lipid fraction
has not been demonstrated. Accordingly, it is still debatable if coffee
consumption can affect lipid metabolism in order to significantly
increase cardiovascular risk [80].
On the contrary, it has been reported that coffee intake increase LDL-C
resistance to oxidative modifications probably as a result of the
incorporation of the phenolic acids in coffee into the cells [81].
An experimental study evaluating the effects of chlorogenic acids on
lipid metabolism in diabetic rats found a significant increase in the
concentrations of plasma and tissue (liver and kidney) lipids,
cholesterol, triglycerides, free fatty acids and phospholipids, and LDL
and very low-density lipoproteins, respectively, and a decrease in the
concentration of HDL [82].
It was demonstrated that their action depended on the capacity to
increase the activity of 3-hydroxy 3-methylglutaryl coenzyme A (HMG-CoA)
reductase in the liver and kidney and a decrease in the activities of
lipoprotein lipase (LPL) and lecithin cholesterol acyl transferase
(LCAT) in the plasma [82].
A
number of epidemiological studies reported a positive association
between coffee consumption and adiponectin levels, an insulin-sensitive
hormone playing a central role in glucose and lipid metabolism, both in
healthy individuals [83], [84], [85] and [86] and in those with metabolic syndrome-related disorders [87] and [88].
These studies remarked the inverse association between coffee
consumption and obesity or visceral fat area. Experimental studies
reported that coffee may play a role in the expression of adipo-R2 gene,
which activate its downstream signaling pathways mainly by activating
AMPK and peroxisome proliferator-activated receptors alpha (PPAR-a) [89].
Coffee polyphenols and melanoidins protected the liver from damage
caused by a hypercaloric diet in an animal model, and this protection
was partially mediated by a reduction in liver inflammation, through
increases of adipo-R2 gene and anti-inflammatory cytokines IL-4 and
IL-10 [90].
3.3. Effects on blood pressure
Despite
caffeine inhibiting phosphodiesterase non-selectively, thereby causing
an accumulation of cAMP, which can mediate a vasoconstrictive response [91], experimental studies reported that an acute increase in blood pressure due to coffee intake develops with rapid tolerance [92] and [93]
and that intravenous caffeine is responsible for the increase in muscle
sympathetic activity and blood pressure in both habitual and
non-habitual coffee drinkers, but coffee intake led to increased blood
pressure only in non-habitual coffee drinkers [94]. Several components of coffee demonstrate anti-hypertensive action [95].
Chlorogenic acids are hypothesized to exert anti-hypertensive effects
by increasing nitric oxide bioavailability and improving endothelial
function, which lead to a reduction of blood pressure [96].
Experimental studies also demonstrated that the depletion in roasted
coffee of hydroxyhydroquinone, a particular fraction of chlorogenic
acid, enhanced the anti-hypertensive effects of chlorogenic acids in a
marginally dose-dependent manner [97].
Moreover, coffee is also rich in blood pressure-lowering minerals
(i.e., potassium and magnesium) that may contribute to its effect on
blood pressure [98].
3.4. Antioxidant activity
Oxidative
stress is heavily involved in metabolism impairment pathways, as well
as in the development of chronic subclinical inflammation that
contribute to chronic disease incidence and progression. The
inflammatory response could be mediated by many factors, such as the
main phenolic compounds of coffee [99].
In particular, chlorogenic acids demonstrated strong antioxidant effect
in a dose–response relationship as a results of the inhibition of the
production of inflammatory mediators [100], [101] and [102], by inhibiting protein tyrosine phosphatase 1B [103] and depressing the expression of pro-inflammatory cytokine genes [104] and [105]. These compounds also demonstrated decreased endothelial dysfunction [106]
by modulating inflammatory NF-κB activation via the redox-related
c-Src/ERK and NIK/IKK pathways via the reduction of oxidative stress [107]. Diterpenes are multitasking molecules that play a role in the regulation of angiogenesis and inflammation processes [108] and [109]. The most studied effects of cafestol regard its capacity to regulate pathological angiogenesis [108].
Kahweol has demonstrated antioxidant properties by inhibiting both
cyclo-oxigenase-2 (COX-2) expression and monocyte chemoattractant
protein-1 (MCP-1) secretion in endothelial cells, key proteins mediating
inflammatory processes [109].
It has been reported that cafestol and kahweol regulate Sp1 target
proteins, which are involved in various biological processes such as
differentiation, metabolism, cell growth, angiogenesis, and apoptosis [110].
Melanoidins, compounds formed during the roasting of coffee beans, have
demonstrated strong antioxidant activity and to significantly inhibit
lipid oxidation [111] and [112].
In an animal model of steatohepatitis, melanoidins protected liver from
damage caused by a high-fat diet by a reduction in hepatic fat
accumulation (through increased fatty acid β-oxidation), systemic and
liver oxidative stress (through the glutathione system), liver
inflammation (through modulation of genes), and expression and
concentrations of proteins and cytokines related to inflammation [90].
Finally, caffeine itself and its metabolites theobromine and xanthine,
have been reported to possess antioxidant properties, such as
DNA-protection through quenching of hydroxyl radical generating systems [113].
4. Controversial effects and future prospective
Besides
the potential beneficial effects of coffee consumption, great attention
should be paid in order to explain its negative effects on human
health. It has been often reported a U-shaped effect of coffee on
several health outcomes [42], [114] and [115],
suggesting that a detrimental effect may occur at higher quantities of
consumption. Moreover, results from epidemiological and experimental
studies are rarely univocal, but rather they are opposite and biased by
methodological limits. Epidemiological studies provide insight into the
long-term effects of coffee consumption but observational evidence
cannot demonstrate causal relationship. Moreover, cross-sectional
studies may have a lack of reliability due to the phenomenon of “reverse
causation”, namely, an adaptation of coffee consumption after
developing the disease. Prospective cohort studies should minimize such
phenomenon, but control over time of coffee consumption may results
difficult and the time distance between the exposure assessment (i.e.,
coffee intake at baseline) and the outcome evaluation may bias results.
Thus, evidence from epidemiological studies is only in part demonstrated
in the experimental setting, and potential confounders (i.e., cigarette
smoking) may affect findings. The randomization process of RCT should,
at least in part, attenuate the effects of confounders theoretically
equally distributed over both intervention and control groups. However,
compared to epidemiological studies, RCT are usually conducted over a
limited period of time. Moreover, the effects follow generally a fixed
dose of coffee (or caffeine) and controlled in a predetermined moment,
thus estimating mostly acute effects of coffee and often not
corresponding to “real-world” coffee drinking. Finally, regarding
experimental studies, most of the data existing is based on in vitro and animal studies, therefore the relevance of findings for the application in humans is still unclear.
5. Conclusion
In
conclusion, in light of the most recent epidemiological and
experimental evidence, coffee consumption seems to be favorably related
with health and to protect by metabolic impairment. Despite the
mechanisms of action being not completely understood, its content in
polyphenols and antioxidant compounds may be countering many of the
negative effects reported in the early researches. Moreover, components
with demonstrated harmful effects (i.e., caffeine and diterpenes) are
nowadays also being reconsidered due to novel discoveries of new
potential positive effects or new hypotheses on their interaction with
metabolism regulation.
Conflict of interest
The authors declare that they have no conflict of interest.
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