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بتجنب تناول او شرب الاغذية والمشروبات الحارة ونعتبرها عاملأ رئيسا مسببا لسرطان الفم والبلعوم والمريء
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High-temperature beverages and Foods and Esophageal Cancer Risk -- A Systematic Review
Abstract
Coffee,
tea, and maté may cause esophageal cancer (EC) by causing thermal
injury to the esophageal mucosa. If so, the risk of EC attributable to
thermal injury could be large in populations in which these beverages
are commonly consumed. In addition, these drinks may cause or prevent EC
via their chemical constituents. Therefore, a large number of
epidemiologic studies have investigated the association of an indicator
of amount or temperature of use of these drinks or other hot foods and
beverages with risk of EC.
We conducted a systematic
review of these studies, and report the results for amount and
temperature of use separately. By searching PubMed and the ISI, we found
59 eligible studies.
For coffee and tea, there was little
evidence for an association between amount of use and EC risk; however,
the majority of studies showed an increased risk of EC associated with
higher drinking temperature which was statistically significant in most
of them. For maté drinking, the number of studies was limited, but they
consistently showed that EC risk increased with both amount consumed and
temperature, and these two were independent risk factors. For other hot
foods and drinks, over half of the studies showed statistically
significant increased risks of EC associated with higher temperature of
intake.
Overall, the available results
strongly suggest that high-temperature beverage drinking increases the
risk of EC. Future studies will require standardized strategies that
allow for combining data, and results should be reported by histological
subtypes of EC.
Introduction
Recurrent
thermal injury to the esophageal mucosa due to consuming large amounts
of hot drinks has long been suspected to be a risk factor for esophageal
cancer (EC). In 1939, WL Watson, after reviewing clinical records from
771 EC cases, wrote: “thermal irritation is probably the most constant
factor predisposing to the cancer of the esophagus”.1
If hot drinks indeed cause EC, they can explain a large proportion of
all cases in populations in which drinking tea, coffee, or maté (an
herbal infusion of Ilex paraguariensis, commonly consumed in
several South American countries), or eating hot foods are common.
Nevertheless, the association of hot drinks with EC has been questioned
both based on biologic reasons and empirical evidence.
It
has been argued that the temperature of hot foods and drinks may fall
rapidly in the mouth and oropharynx so that it cannot cause thermal
injury to the esophageal mucosa.2
To test this hypothesis, De Jong and colleagues measured
intraesophageal temperature after consuming hot drinks. The results of
their study showed that drinking hot beverages could substantially
increase the intra-esophageal temperature and this increase was a
function of the initial drinking temperature and more importantly, the
size of the sip.3 For example, drinking 65 °C coffee increased the intra-esophageal temperature by 6–12 °C, depending on the sip size.3
Tea,
coffee, and maté may affect cancer risk not only through thermal
effects but also via their chemical constituents. Although some studies
have shown mutagenic effects for tea, coffee, and unprocessed maté herb (Ilex paraguariensis) extracts,4–10
a number of more recent experimental studies in animals have reported
cancer preventive activities for these beverages (reviewed in refs. 11–15).
A number of epidemiological studies have investigated a possible effect
of these beverages on cancer risk. With respect to gastrointestinal
cancers, recent meta-analyses did not find any significant association
between tea drinking and gastric and colorectal cancers,16–18 but coffee drinking was shown to be inversely associated with risk of liver cancer.19,20
In
1990, a Working Group of the International Agency for Research on
Cancer (IARC) concluded that there was not sufficient evidence to
recognize tea, coffee, or maté, in toto, as risk factors of human cancer, but they found that drinking hot maté was a probable risk factor in humans.21
The strongest evidence was for an association with EC. Since then, a
large number of additional studies have investigated the association of
the beverages and EC. We conducted a systematic review of the results of
epidemiologic studies on the association of tea, coffee, or maté
drinking or of high-temperature food consumption with EC.
Materials and Methods
We
conducted a comprehensive search of the PubMed and ISI-Web of Knowledge
databases for all case-control or cohort studies published in English
language on the association of tea, coffee, maté, or other hot drinks or
high temperature foods and risk of EC. All results were updated on
January 23, 2009. The following terms were used in the PubMed Database
search: “(esophag* OR oesophag*) AND (cancer OR carcinoma OR
adenocarcinoma OR neoplasm OR neoplasia OR neoplastic) AND (tea OR mate
OR coffee OR beverage)”; the search was repeated by replacing the last
phrase with “(liquid OR drinks OR alcohol OR food) AND (hot OR cold OR
warm OR temperature)”. The same terms were used to search text words in
the ISI Database. In addition, references cited in the identified
articles were searched manually. Two of the authors (FI and FK) reviewed
the search results to reduce the possibility of missing the published
papers.
Using the above-mentioned approach, a total of 536 articles were retrieved. Figure 1
shows a summary of the article selection process. After reading the
abstracts of the retrieved articles, we excluded 417 articles because
they were not case-control or cohort studies of hot drinks and EC; the
excluded articles were reviews, animal studies, in vitro
studies, case-series, studies of cancers other than EC, or studies of
treatment and complications of EC. In case of any doubt, we also
reviewed the full texts of those articles. After reviewing the full
texts of the remaining 119 articles, we excluded another 57 because they
did not present data on the variables of interest, but we found an
additional 14 articles by searching the references of the articles. We
also included a study which was in press at the time of our review.22 Therefore, a total of 77 relevant articles were found. Of these, 7 articles 23–29 were excluded because they reported data on EC in combination with other cancers and an additional 10 publications 30–39
were excluded because their results were reported in other publications
or in combined analyses. One more study that referred to drinking of
hot Calvados,40
a strong spirit which is a well established cause of EC, was excluded
because separating the effect of temperature from that of the spirit per
se would be difficult. Finally, a total of 59 full-text articles were
included in this systematic review.22,41–98
Tea,
coffee, and maté constitute the three major types of hot drinks
consumed around the world. Therefore, we present data for each one of
these, as well as for the mixed group of other hot foods and drinks, in
separate tables. The two main variables of interest were: 1) an
indicator of amount consumed (frequency per day, amount per day,
duration of use, or a composite variable indicating cumulative use); and
2) temperature.
The etiological factors responsible for
the two main histological of EC, esophageal squamous cell carcinoma
(ESCC) and esophageal adenocarcinoma (EAC), may be different, and any
role of hot drinks and foods might be more relevant for ESCC etiology.99 Therefore, where data are available, we present the results for ESCC and EAC separately.
Where
both crude and adjusted odds ratios (ORs) and 95% confidence intervals
(95% CIs) were reported in the paper, we only present the adjusted
results. A small number of studies showed crude numbers but not ORs and
95% CIs, in which case we calculated these statistics using simple
logistic regression models and present them. Throughout the article, P values < 0.05 were considered as statistically significant.
Results
Tea
After
excluding duplicate publications, we found 38 papers, published between
1974 and 2008, that reported on the association of tea drinking with EC
(Table 1).
These included 33 individual case-control studies, a pooled analysis of
5 case-control studies, a pooled analysis of 2 case-control studies,
and 3 prospective studies. The studies were conducted in United States,
South America, Europe, South-Africa, Middle-East, and South and East
Asia, and included both high-risk and low-risk regions. Two of the
prospective studies were from Japan and one was from China. There were
large differences in study size, but the majority of the studies had
between 100 and 400 EC cases. Whereas some studies described the type of
tea consumed (e.g., green tea or black tea), the large majority did not
report on tea type; however, black tea represents the predominant type
of tea traditionally drunk in most regions outside East Asia.21
Amount consumed
Most
studies (n = 33) provided results for one of the indicators of amount
consumed, e.g., amount per day, frequency per day, duration of use, or
an indicator of cumulative use. However, not all studies reported ORs
(95% CIs) or crude numbers. There was no clear pattern of association
between amount of tea consumed and EC risk; 7 studies showed an increase
in risk (4 were statistically significant), and this was
counterbalanced by 15 individual studies and a pooled analysis of 5
case-control studies that showed an inverse association between tea
drinking and EC risk, either in the main analyses or in subgroup
analyses (the association in 8 studies was statistically significant).
Four studies reported ORs close to one, on both sides of the null line,
which were not statistically significant. In addition, 6 other studies
only stated that the results were not statistically significant, without
reporting detailed results. We did not find a clear pattern of
association by geographic region. However, the majority of the inverse
associations were from East-Asian countries, especially China, where
mostly green tea is used.
Temperature
Results
for the association of tea drinking temperature and EC were reported in
14 publications. Of these, 7 individual case-control studies, a
combined analysis of 5 other case-control studies, and a prospective
study found an increased risk; of these, the association was
statistically significant in 8 studies. Two case-control studies
reported statistically non-significant inverse associations, and 3 other
studies only stated that the results were not statistically
significant, without reporting crude numbers or ORs.
Coffee
We found 22 independent papers, published between 1974 and 2008, that reported on the association between coffee intake and EC (Table 2).
These included 17 individual case-control studies, a pooled analysis of
5 case-control studies, a pooled analysis of 2 case-control studies,
and 3 cohort studies. Most reports (n = 14) were from the United States
or Europe. Most studies included between 100 and 400 EC cases.
Amount consumed
Most
studies (n = 20) reported one of the indicators of amount consumed and
EC. Four case-control studies showed statistically non-significant
positive associations. Seven studies reported an inverse association
between coffee drinking and EC risk, of which only 1 prospective study
from Japan and a combined analysis of 2 case-control studies from Italy
and Switzerland showed statistically significant results for drinking 3
or more cups per day. Four other studies, including 2 prospective
studies, showed non-significant results with ORs close to one, on both
sides of null line. The remaining 5 studies only reported that the
results were not statistically significant.
Temperature
Six
individual case-control studies and a pooled analysis of 5 other
case-control studies reported on temperature of coffee consumption in
relation to EC risk. Of these, 2 individual studies and the pooled
analysis showed an increased risk with drinking hot or very hot coffee,
either in the main analyses or in subgroup analyses; 2 studies suggested
statistically non-significant inverse associations, and 2 other studies
only reported that the results were not statistically significant.
Maté
We
found 4 independent papers, including 3 individual case-control studies
and a combined analysis of 5 other case-control studies. These reports
were published between 1985 and 2008 and all came from South American
countries (Table 3).
Amount consumed
All
reports showed significantly increased EC risk with amount consumed,
with approximately 3-fold higher risk in those in the highest category
of consumption compared to those who did not consume maté. The pooled
analysis of the case-control studies found that amount per day and
duration of drinking both increased risk.
Temperature
Three
of these publications reported on the association of temperature of
maté drinking and EC risk and all showed significant increased risk with
increasing temperature. Mutual adjustment for temperature and amount in
the pooled analysis suggested that amount and temperature of use were
independent risk factors for EC.
High temperature food or other drinks
We
found 19 publications (17 individual case-control studies, a combined
analysis of 5 other case-control studies, and 1 prospective study) that
presented results on the association of consumption of high temperature
food, other drinks, or all beverages combined with risk of EC (Table 4).
The reports were published between 1974 and 2008, and the studies were
conducted in South Americas, Europe, Africa, and South and East Asia.
For this category, we only present results on temperature.
A
summary of studies on the association between high temperature foods or
drinks (other than tea, coffee and maté, unless the results have been
reported as a combination of them) and risk of esophageal cancer
Temperature
In
all, 11 individual case-control studies and the combined analysis
showed positive associations (11 were statistically significant),
whereas 2 case-control studies found statistically non-significant
inverse associations. Two case-control studies and the prospective study
reported ORs close to one, on both sides of null line, with no
statistically significant association. Two other studies only stated
that the results were not statistically significant, without reporting
crude numbers or ORs.
Summary of all hot foods and drinks
A
summary of the associations between amount or temperature of consumed
tea, coffee, or maté, or consumption of high temperature food or other
beverages, and risk of EC is presented in Table 5.
Discussion
In
this systematic review, we collected the published literature on the
association between consuming tea, coffee, maté, or other
high-temperature beverages or foods and risk of EC. We analyzed the
results for amount consumed and temperature of drinking separately. For
tea and coffee, there was little evidence that the amount consumed was
associated with EC risk, but the majority of the publications reported
statistically significant increased risks associated with higher
temperature of use. For maté, individual studies and the combined
analyses showed increased risk of EC associated with both amount
consumed and with temperature of drinking, and these two seemed to be
independent risk factors. For other hot foods and drinks, the majority
of studies showed higher risk of EC associated with higher temperature
of use.
There are several limitations to making
definitive conclusions about the association of amount or temperature of
these drinks with EC risk. Some of these limitations are due to the
design of the published studies (retrospective nature of the data,
subjective questions, incomplete questionnaires, and lack of information
on histologic type of EC) and others are due to incomplete analysis or
reporting of the data. The large majority of the reports were based on
retrospective case-controls studies, so the data might have been subject
to interviewer bias or recall bias. This is further complicated by
asking subjective questions, such as “how hot do you drink your tea?”,
which can be particularly prone to such biases. To our knowledge, very
few published studies have actually measured the actual temperature of
tea, coffee, or maté drinking (reviewed in ref 22).
Obtaining data on amount or frequency of drinking per day, total
duration of drinking, sip size (or an indicator of this), and
temperature of drinking are important. Unfortunately, many of the
published studies did not collect data on several of these factors or
did not report the results; studying the effect of hot temperature
drinks was not the main aim of most of these studies. Furthermore, few
studies adjusted the results of drinking temperature for amount consumed
and vice versa, and many studies failed to adjust the results for other
confounders. Also, many studies combined the results for several types
of beverages (e.g., tea and coffee), which made it difficult to look at
effects of these drinks separately; this problem was more prominent for
black and green tea use. A number of studies reported that the results
were not significant, but provided no counts or ORs (95% CIs). Such
incomplete reporting prohibits use of the results in future
meta-analyses. There is a large body of evidence suggesting that the
risk factors for ESCC and EAC may be different. For example, there is
strong evidence for a positive dose-response association between body
mass index and risk of EAC,100 whereas several studies have reported an inverse association between body mass index and risk of ESCC.99 Nevertheless, few studies reported the results for ESCC and EAC separately.
Because
of large heterogeneity in design and reporting, and also incomplete
reporting in several studies, we conducted a systematic review but
avoided formal combination of the results as a meta-analysis. However,
many of the limitations mentioned above can be addressed in future
studies. Using a standard questionnaire across studies would help in
collecting uniform data. Actual measurement of tea temperature is
already being conducted in a cohort study in Iran,22,101 where very high rates of ESCC are seen.102,103
In this study, two simultaneous cups of tea are poured; one is given to
the study subject and a thermometer is put in the second cup.101
At intervals of 5°C (75°C, 70°C, 65°C, …) the subject is asked to sip
the tea and tell the interviewer whether this is the usual temperature
at which he/she drinks tea. This method for measuring tea temperature
had shown a very good repeatability 101
and can be used in future studies, especially in areas with very high
risk of EC. Measurement of relevant metabolites in biological samples
might be helpful to validate the self-reported data on amount of
consumed beverages.
Thermal injury may cause EC via both
direct and indirect pathways. Inflammatory processes associated with
chronic irritation of the esophageal mucosa by local hyperthermia might
stimulate the endogenous formation of reactive nitrogen species, and
subsequently, nitrosamines.104 This hypothesis is supported by high rates of somatic G > A transitions in CpG dinucleotides of the TP53 gene in ESCC tumor samples from areas in which drinking hot beverages is considered an important risk factor for ESCC;105–108 these mutations may indicate increased nitric oxide synthase activity in tumors.109
Thermal injury can also impair the barrier function of the esophageal
epithelium, which may increase the risk of damage from exposure to
intra-luminal carcinogens.110 An association between hot drinks and precancerous lesion of the esophagus has also been reported.111,112
Nevertheless, further prospective studies are indicated to investigate
the association between high-temperature beverage or food consumption
and risk of EC.
Chemical composition of tea, coffee, and maté has been reviewed in detail elsewhere.21
Some constituents of tea, coffee, and maté may have anti-carcinogenic
properties; for example, flavonoids and caffeine show antioxidant
activities.12,13,113
Composition of the beverages may change during production procedures;
for example, in production of black tea and coffee, fermentation of tea
leaves reduces a large percentage of some flavonoids,12,13 and severe roasting of coffee beans can considerably reduce their total cholorogenic acid content.21
Furthermore, black tea and maté may acquire some potentially
carcinogenic contaminants, such as polycyclic aromatic hydrocarbons
(PAH) and mycotoxins, when being processed;114,115 high levels of PAH exposure has been reported among black tea and maté drinkers.116,117 Both black and green tea drinking may increase plasma antioxidant activity in humans.118
On the other hand, in a clinical trial in Linxian and Huixian, China,
decaffeinated green tea was not shown to have beneficial effects in
alleviating esophageal precancerous lesions and abnormal cell
proliferation patterns after 11 years of follow-up.119 Other hot foods and drinks, such as foods containing processed meat and preserved fish,120
may potentially have carcinogenic chemical constituents. However, most
studies used in this review compared the intake of the same food in
higher versus lower temperatures. Therefore, unless higher temperature
results in further formation or release of carcinogens, the results
should not be confounded by chemical constituents, and any association
should be attributed to thermal injury.
Although the
number of studies that reported inverse associations between amount of
tea or coffee consumed is higher than the number of studies that showed
positive associations, the overall results are mixed. Despite cancer
preventive activity of tea in experimental studies, it is not clear why
epidemiological studies have not consistently shown an inverse
association between tea drinking and risk of EC. Furthermore, all of the
epidemiological studies that showed a statistically significant inverse
association between tea drinking and risk of EC were case-control
studies. In case-control studies, a possible reduction in tea intake by
EC cases following their symptoms might lead to under-reporting of past
tea consumption, and subsequently, resulting in spurious inverse
associations. Tea and coffee contain several compounds other than
flavonoids21
and may have some contaminants, which their interactions and their
complex metabolisms might alter the protective effect of the individual
compounds.17
It has also been suggested that flavonoids, or other anti-oxidants, in
high doses may act as pro-oxidant that can generate free radicals, which
may lead to DNA damage and finally irreversible pre-neoplastic lesions
(reviewed in refs. 8,121).
In
conclusion, there was little evidence for an association between EC
risk and amount of tea or coffee consumed but the results suggest an
increased risk of EC associated with higher drinking temperature.
Amount, duration, and temperature of maté intake were all associated
with higher EC risk, but number of the studies that investigated these
associations was limited. For other hot foods and drinks, there was some
evidence showing increased risk with higher temperature. Overall, the
available results strongly suggest that high-temperature beverage
drinking increases the risk of EC. Future studies will require
standardized strategies that allow for combining data, and results
should be reported by histological subtypes of EC.
Acknowledgements
This
study was supported in part by the Intramural Research Program of the
National Cancer Institute, National Institutes of Health.
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