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Title: Coffee consumption rapidly reduces background DNA strand breaks in healthy humans: Results of a short term repeated uptake intervention study

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Molecular Nutrition & Food Research

Coffee consumption rapidly reduces background DNA strand breaks in healthy humans:
results of a short term repeated uptake intervention study

Tamara Bakuradze1, Roman Lang2, Thomas Hofmann2, Dorothea Schipp3, Jens Galan4,
Gerhard Eisenbrand1 and Elke Richling1*

1

Department of Chemistry, Division of Food Chemistry and Toxicology, Molecular Nutrition,

University of Kaiserslautern, Kaiserslautern, Germany
2

Chair of Food Chemistry and Molecular Sensory Science, Technische Universität München,

Freising, Germany
3

www.ds-statistik.de, Rosenthal-Bielatal, Germany

4

Gruenstadt, Germany

*Corresponding author: Dr. Elke Richling, Department of Chemistry, Division of Food
Chemistry and Toxicology, University of Kaiserslautern, Erwin-Schroedinger-Str. 52,

Received: 25-08-2015; Revised: 11-11-2015; Accepted: 16-11-2015

This article has been accepted for publication and undergone full peer review but has not been
through the copyediting, typesetting, pagination and proofreading process, which may lead to
differences between this version and the Version of Record. Please cite this article as doi:
10.1002/mnfr.201500668.

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67663 Kaiserslautern, Germany.
Phone: +49 631 205 4061. Fax: +49 631 205 3085. E-mail: richling@chemie.uni-kl.de

Keywords: coffee, defense, DNA, background damage, comet assay, short-term,
intervention study, strand breaks
Abbreviations:
ARE, antioxidant response element; BMI, body mass index; TI, tail intensity; Nrf2, nuclear
factor-erythroid-2-related factor 2.
Abstract
Scope: Intervention studies provide evidence that long-term coffee consumption correlates
with reduced DNA background damage in healthy volunteers. We here report on short–term
kinetics of this effect, showing a rapid onset after normal coffee intake.
Methods and results: In a short-term human intervention study, we determined the effects
of coffee intake on DNA integrity during 8 hours. Healthy male subjects ingested coffee in
200 ml aliquots every second hour up to a total volume of 800 ml. Blood samples were taken
at baseline, immediately before the first coffee intake and subsequently every two hours,
prior to the respective coffee intake. DNA integrity was assayed by the comet assay. The
results show a significant (p<0.05) reduction of background DNA strand breaks already 2 h
after the first coffee intake. Continued coffee intake was associated with further decrements
in background DNA damage within the 8h intervention (p<0.01 and p<0.001, respectively).
Mean tail intensities (TI%) decreased from 0.33 TI% (baseline, 0 h) to 0.22 TI% (within 8 h
coffee consumption).

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Molecular Nutrition & Food Research

Conclusion: Repeated coffee consumption was associated with reduced background DNA
strand breakage, clearly measurable as early as two hours after first intake resulting in a
cumulative overall reduction by about one third of the baseline value.

Graphical abstract:
The long-term consumption of coffee is associated with improved DNA integrity in healthy
volunteers. To test whether these effects could be shown after acute and repeated coffee
consumption

within

a

day,

a

short-term

study

was

performed.

The results demonstrate that the intake of coffee within hours significantly reduced background
DNA strand breaks, measured by comet assay.

1. Introduction

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Numerous epidemiological studies indicate potential health effects associated with coffee
consumption and with reduced risk of certain chronic and degenerative diseases, such as
diabetes, Parkinson’s disease, cardiovascular disorders and some types of cancer [1].
Coffee contains a multitude of compounds such as chlorogenic acids (e.g. caffeoylquinic
acids, CQAs) as well as constituents generated during the roasting, including Maillard
reaction products such as N-methylpyridinium or melanoidins. The latter have been reported
to account for about 25% of dry matter [2]. Such constituents have been discussed to act as
radical scavengers and / or to induce expression of antioxidant/electrophile response
element (ARE/ERE) dependent enzymes by activation of Nrf2-signaling pathways [3-7].
Several intervention studies indicate that consumption of coffee protects against DNAdamage in humans [8-12]. We have recently reported that four weeks consumption of coffee
rich in chlorogenic acid and roast products markedly reduced DNA strand breaks
(background and total) in white blood cells (WBC) and increased glutathione level in plasma
of healthy subjects [8]. Other research groups likewise observed in humans a decrease of
total DNA strand breaks in isolated lymphocytes after coffee intake [10, 12]. In a randomized
controlled study with healthy subjects, we reported a significant reduction of background
DNA strand breaks in white blood cells after four weeks coffee consumption [9]. All these
effects were observed after continuous coffee uptake during several days or weeks.
However, acute, short-term (one day) effects of coffee on DNA integrity have not been
reported yet. Such information is expected to produce new insights into potential mechanism
of protection against DNA damage; rapid onset would speak for direct radical scavenging by
coffee constituents whereas longer term responses may rather be attributed to other
mechanism, such as those mediated by activation of Nrf2 signaling.

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We here describe the results of an eight-hour short-term intervention study with 13
healthy male volunteers.

2. Materials and Methods
This study was approved by the local ethic committee of Rhineland-Palatine, Mainz,
Germany, no. 837.218.12 (8319-F). Male volunteers (n = 14, ages 20-50, BMI 19-25), who
fulfilled the inclusion criteria (healthy non-smokers, no intake of pharmaceutical drugs or
food supplements during the study period) were recruited. After informed written consent,
volunteers were subjected to medical examination including standard clinical blood
biochemistry. They showed the following anthropometric characteristics: average age of
23 ± 2.4 years, BMI of 23.8 ± 1.6 kg/m2, body fat content of 14.4 ± 5.1 kg (Bioelectrical
impedance analysis, BIA 101, SMT medical GmbH, Wuerzburg, Germany). One individual
dropped out for private reasons. The remaining 13 volunteers completed the eight hour
intervention study. This was performed with four to five volunteers per three consecutive
study days, following a design as shown (see Figure 1). Volunteers were kept for the
intervention day in a clinical facility under tightly controlled environmental conditions. They
received identical quantities of the same food and beverage (water) throughout the
intervention day. Three days before (wash-out period) and during the study, volunteers were
instructed to avoid coffee (except study coffee) and caffeine-containing products as well as
dietary supplements and foods rich in polyphenols. The volunteers entered the facility in
fasted state and venous blood samples were taken. Thereafter the volunteers consumed the
first 200 mL aliquot of black coffee (with/without sugar, no milk), brewed in a commercially

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available standard coffee pad machine (2 x coffee pads á 7.5 g / 200 mL). The coffee blend
was prepared from a special roasted and blended Arabica (Coffea arabica) coffee, rich in
both, green and roast bean coffee constituents (see Table 1) and was packed into coffee
pads (Tchibo GmbH, Hamburg). Every brew was freshly prepared immediately before each
individual consumption. After 2, 4, 6, and 8 h this procedure was repeated (total coffee
consumption 800 mL/volunteer). Blood samples were drawn from the participants
immediately prior to the next coffee intake every two hours after each coffee intake. During
the study the volunteers consumed a light meal (bread roll with cheese) and a light dinner
(tortellini carbonara), respectively. Water consumption was allowed ad libitum.
The ground coffee was analytically characterized using HPLC-DAD and HPLC-MS/MS
methods as previously described [13]. In brief, caffeine and CQAs (sum of 5-O-, 4-O- and 3O-CQA) were quantified by HPLC-DAD (272 and 324 nm, respectively) with external
calibration. NMP and trigonelline were quantified by stable isotope dilution analysis with d3trigonelline and d3-N-methylpyridinium after sample clean-up via solid phase extraction
(SPE) on cationic exchange material [14].
Venous blood samples were collected in EDTA tubes and worked up as described for the
comet assay. DNA strand breaks were determined as reported before by the comet assay, a
well established method of alkaline single cell gel electrophoresis [8]. DNA migration was
calculated as mean tail intensity (TI%: DNA in the comet tail in percent of total DNA).
Results from 13 volunteers are reported as means and SD. The Shapiro-Wilk test was used
for analysis of normal distribution. Differences of parameters between baseline and each
coffee intake were analysed by analysis of variance (ANOVA). Differences without normal
distribution were analysed by ANOVA based on Blom- rank transformation [15].

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3. Results and discussion
To characterize the ground study coffee, concentrations of selected compounds are
presented in Table 1. The roast product N-methylpyridinium, NMP (1.1 mg/g), was present at
a level associated with dark roast, whereas the total amount of green bean coffee
constituents, as exemplified by CQAs (10.4 mg/g, sum of 3-, 4- and 5-caffeoylquinic acids)
was in the range expected for medium roasted coffee. Normally, dark roasts contain lower
concentrations of these compounds than light roasts [16, 17]. The caffeine level (16.7 mg/g)
was in the upper range of commercial ground coffee [14]. The trigonelline content (3.9 mg/g)
likewise was in the range of medium roast coffee. Trigonelline degrades during the roast
process into a spectrum of thermal degradation products, including NMP and further pyridine
derivatives and, nicotinic acid. More than 90% of the compounds mentioned are known to be
extracted into the coffee brew when brewing is performed at a water to coffee ratio (v/w)
>16, as used here [18]. During this eight hour intervention study volunteers consumed four
portions of 200 mL coffee brew every two hours (see Figure 1) resulting in a total uptake of
800 ml during the intervention day. As exemplified in Figure 2, a significant (p < 0. 05)
reduction of background DNA strand breaks became observable already two hours after the
first coffee (200 ml) intake, compared to the baseline. The mean tail intensities (TI%)
decreased from 0.33 TI% (baseline) to 0.28 TI% (after 200 ml coffee). Further consumption
of coffee brew every two hours up to a total of 800 mL revealed a significant further
incremental reduction of DNA damage (p < 0.01 and p < 0.001, respectively) in relation to
the baseline. The respective TI % values decreased from 0.33 TI% (baseline) to 0.25 TI%
(after 400 ml coffee), 0.23 TI% (after 600 ml coffee) and 0.22 TI% (after 800 ml coffee).

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These results indicate an additive protective effect on DNA integrity by repeated coffee
intake, summing up to about 30%.
Previously published intervention studies described longer term effects of coffee
consumption on DNA integrity. Although using slightly different experimental conditions, a
significant reduction of background and total DNA strand breaks in white blood cells was
invariably reported [8, 9, 12]. Background DNA strand breaks may be conceived to result
from endogenous exposure to DNA damaging agents from internal or external sources and/
or may reflect incomplete DNA repair. In addition to background DNA strand breaks, total
DNA damage includes DNA damage as provoked by reactive oxygen species (ROS) and
other electrophilic reactants, causing lesions detectable by processing with specific enzymes
of the (bacterial) DNA repair machinery, such as formamidopyrimidine glycosylase (FPG)
[19].
In the present study, we observed a decrease in background DNA damage already within
two hours after coffee consumption. Such an early onset of DNA protection most probably
reflects direct mitigating effects of certain coffee constituents. For instance, polyphenols like
chlorogenic acids (e.g. CQA and their metabolites) as well as compounds formed during
roasting (e.g. melanoidins) have been found to exert radical scavenging as well as metal
chelating activities in vitro and in vivo [20, 21]. Bioavailability studies of coffee constituents
have shown that chlorogenic acids after absorption in the small intestine rapidly appear in
the circulatory system. Within 60 min after ingestion of coffee, free chlorogenic, caffeic,
ferulic or isoferulic acids, as well as their sulfate and glucuronide conjugates have been
detected [22-25]. Furthermore, metabolites conceived to be generated primarily by the gut
microbiome, including dihydroferulic and dihydrocaffeic acids and corresponding conjugates
occur later in plasma (tmax = 6 - 10 hours) [23, 24]. The latter metabolites are more slowly

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excreted and are present in plasma samples up to 20 h after ingestion [24]. In contrast, the
caffeic acid derivatives (chlorogenic acids, caffeic and ferulic and isoferulic acids) were
found to reach baseline after 6 hours. Depending on the ingested dose, up to 25% of
chlorogenic acids were recovered in the urine [24, 26].
Based on these kinetic data, it can be concluded that plasma concentrations of chlorogenic
acids and their metabolites attained two hours after the first coffee intake will suffice to
contribute to the rapid onset of the observed protective effects on DNA background damage.
On the premise that residual plasma concentrations of relevant coffee constituents are still
present from the foregoing intake at time points of subsequent coffee intakes, incrementally
enhanced DNA protective effects may be expected. Indeed, stepwise decrements in DNA
background damage became apparent, in parallel with the cumulative coffee intake during
the eight hours intervention. It thus can be inferred that the fractionated coffee uptake results
in a steady built-up of plasma levels of chlorogenic acids and their metabolites, most
probably also of melanoidins and their potential metabolites [27, 28]. Plasma kinetics of
trigonelline and N-methylpyridinium (the latter generated from trigonelline during roasting)
are within a similar range. For example, maximal plasma concentrations were reached at
about ~ 1-3 h after coffee intake, and an elimination half-life of about 2-5 h was reported
[29]. Of note, because these well water soluble compounds are excreted primarily in the
urine (about 60-70 % within 8h) they have been utilized to verify compliance in coffee
intervention studies [29].
Taken together, a comprehensive spectrum of coffee constituents and their metabolites can
be inferred to be responsible for the observed rapid onset of mitigating effects on DNA
background damage.

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Molecular Nutrition & Food Research

Beyond these immediate DNA protective responses also long term effects have been
observed in previous human intervention studies [8, 9, 12]. It has been found that
chlorogenic acids, but also roast-associated constituents such as NMP, as well as certain
Maillard reaction products ingested in coffee can up-regulate several physiological defense
systems. These constituents have been identified as activators of the Nrf2/ARE pathway,
activating nuclear Nrf2 translocation as well as gene- and protein expression of different
phase II enzymes, such as glutathione transferase and reductase, glucuronyl transferase,
heme oxygenase, superoxide dismutase , catalase and some others, in vitro and in vivo [4,
5]. Of note, roasted, but not green coffee extract has been reported to up-regulate nuclear
translocation of Nrf2 in macrophages [2]. Likewise, only a heated, but not an unheated
Maillard reaction mixture was found to exert a strong Nrf2 activating effect [2]. Thus, longterm activation of Nrf2-mediated defense may be inferred to result from green bean and
roast-associated coffee constituents in combination. In addition to radical scavenging and
induction of detoxification systems, DNA repair may also be influenced by coffee
constituents. However, as yet there is only limited and inconclusive information concerning
effects of coffee on DNA repair modulation. No effects of instant coffee consumption was
reported on DNA damage and DNA repair in mouse liver [30]. At variance, in rats, Turkish
coffee and its diterpene components kahweol and cafestol were reported to increase the
expression of DNA repair protein O6-methylguanine-DNA methyltransferase (MGMT), in
parallel with some phase II enzymes [31].
.

4. Concluding remarks

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We conclude that regular daily consumption of coffee is associated with mitigating activity
against background DNA damage. This DNA protective activity has a very rapid onset,
observed already two hours after the first intake. It is further increasing with continuing
coffee intake throughout the here described one-day intervention. Former studies revealed
sustained DNA protective effects during longer term regular coffee consumption (4 weeks).
Thus, in line with these earlier findings, this study clearly shows a very early onset of DNA
protective efficacy, augmented during further coffee intake during the day and becoming
sustained during long-term coffee ingestion.

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We are grateful for the contribution of the participants in the study. The authors thank Sylvia
Schmidt for preparing blood samples and performing the comet measurements. We thank
Dirk Galan and Axel Stachon for their support during the study. The authors thank Tchibo
GmbH, especially G. Bytof, I. Lantz and H. Stiebitz for providing the study coffee, packed
into pads and the coffee pad machines.

Potential conflict of interest statement: G. Eisenbrand is scientific advisor with Tchibo GmbH
and with the Institute for Scientific Information on Coffee, La Tour de Peilz, Switzerland
(ISIC).
All other authors have no interests declared.

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5. References

[1] Ludwig, I. A., Clifford, M. N., Lean, M. E., Ashihara, H., Crozier, A., Coffee: biochemistry and
potential impact on health. Food Funct 2014, 5, 1695-1717.
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factor Nrf2 in macrophages, Caco-2 cells and intact human gut tissue by Maillard reaction products
and coffee. Amino Acids 2013, 44, 1427-1439.
[3] Bakuradze, T., Lang, R., Hofmann, T., Stiebitz, H., et al., Antioxidant effectiveness of coffee
extracts and selected constituents in cell-free systems and human colon cell lines. Mol Nutr Food Res
2010, 54, 1734-1743.

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[4] Boettler, U., Sommerfeld, K., Volz, N., Pahlke, G., et al., Coffee constituents as modulators of Nrf2
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[15] Blom, G., Statistical estimates and transformed beta-variables, Wiley, New York, 1958.

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[16] Moon, J. K., Yoo, H. S., Shibamoto, T., Role of roasting conditions in the level of chlorogenic acid
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bioactives upon coffee consumption. Anal Bioanal Chem 2013, 405, 8487-8503.
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isotope dilution analysis and pharmacokinetic studies on bioactive pyridines in human plasma and
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Legends to the figures:

Figure 1: Design of short-term intervention study.

: Blood sampling

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Figure 2: Background DNA strand breaks in WBC of 13 volunteers at start of study and two
hours after each coffee consumption (total 800 ml). Data are expressed as TI % showing
means and SD; significantly different DNA strand breaks: ***p<0.001, ** p<0.01, * p<0.05,
Variance analysis ANOVA, influences factor “time”. BS: blood sampling.

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Table

Table 1: Concentration [mg/g of selected constituents in the ground study coffee
compound

c (mg/g)

16.7 ± 0.7

Caffeine

10.4 ± 0.9

Caffeoylquinic acids

a

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1.1 ± 0.15

N-Methylpyridinium

3.9 ± 0.32

Trigonelline

a

Values are expressed as mean ± SD. Sum of 3-, 4- and 5-caffeoylquinic acid

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