Is rowing involved in the induction of esophageal adenocarcinoma: a
literature review and questionnaire in active rowers
Romy E. Verbeek*1, Willemijn C.E.M. Kremer*1, Jantine W.P.M. van Baal1, Berend
Glazenburg2, Martijn G.H. van Oijen1, Peter D. Siersema1
*Both authors contributed equally
1
Department of Gastroenterology, University Medical Center Utrecht, Utrecht, the
Netherlands, 2Department of Ear, Nose and Throat Surgery, Aventino Medical Group, Rome,
Italy
Abbreviations:
BE=Barrett's
esophagus,
BMI=body mass
index,
EAC=esophageal
adenocarcinoma, IQR=interquartile range, MHR=maximum heart rate, SD=standard
deviation, VO2 max=maximal oxygen uptake
Correspondence:
Drs. Romy E. Verbeek
Department of Gastroenterology (F02.618)
University Medical Center Utrecht
P.O. Box 85500, 3508 GA Utrecht
R.E.Verbeek@umcutrecht.nl
Telephone number: +31 88 7559338
Fax number: +31 88 7555533
1
ABSTRACT
Introduction: Recently, three rowers of a Dutch rowing society were within a period of one
year diagnosed with esophageal adenocarcinoma (EAC). This resulted in the hypothesis that
rowing may induce gastro-esophageal reflux and thereby increases the risk of EAC
development. In this study, we evaluated the association between rowing and gastroesophageal reflux.
Methods: A literature review was performed to investigate the prevalence of gastroesophageal reflux related to type and intensity of sport (part I). In addition, a questionnaire
was sent to all rowers (n=380) of the particular rowing society to estimate the prevalence of
reflux symptoms during rowing (part II).
Results: The literature search revealed seven studies reporting on the prevalence of gastroesophageal reflux in a total of 439 athletes during exercise based on both pH monitoring and
questionnaires (part I). Only one study partially focused on rowers. All investigations
demonstrated that reflux symptoms are induced by any type of exercise. Moreover, frequency
and duration of reflux prevalence was associated with the type of sport and its intensity. pH
monitoring showed a higher number of reflux episodes per hour during weightlifting
compared to running and cycling. Additionally, rowing was identified to induce reflux. Of the
196 responders (response rate 52%) in the questionnaire study (part II), 100 rowers (51%)
experienced reflux symptoms, of which 52% less than once a month, 20% monthly, 22%
weekly and 6% daily. However, additional reflux symptoms were encountered during rowing
compared to daily life experience in this population. Marathon (67%) and tour (40%) rowers
indicated that they had more frequently reflux symptoms than recreational (23%) and
competition (19%) rowers (p=0.02).
Conclusion: Rowers experience more gastro-esophageal reflux symptoms during rowing than
in daily life and the frequency was found to be related to the intensity of rowing. This is
2
supported by previous studies demonstrating exercise-induced reflux associated with the type
of sport and its intensity. Nonetheless, the relatively low frequency of reflux symptoms in the
present rowing cohort when compared to the general prevalence, makes a direct association
between rowing-induced gastro-esophageal reflux and EAC development highly unlikely.
3
INTRODUCTION
Recently, three members of the same rowing society in the Netherlands were within a period
of one year diagnosed with esophageal adenocarcinoma (EAC). In the accompanying textbox
a representative case is described. In the Western world, EAC has been demonstrated to have
the fastest rising incidence of all malignancies.1, 2 The peak in EAC incidence in this specific
rowing population motivated us to further explore this epidemiologic and possibly causative
phenomenon.
Case
Patient R, a 60-year-old man, with no medical history and a rowing experience of 20 years,
including competition rowing, became suddenly unwell and developed with hematemesis. Because
of the suspicion of gastro-intestinal ulcer disease upper endoscopy was performed, which showed a
lesion in the distal esophagus suspect for malignancy. Biopsies confirmed a diagnosis of EAC.
Additional staging procedure showed no distant metastases. Prior to the diagnosis patient did not
experience any reflux symptoms. The patient was successfully treated with a combination of
chemoradiation and transthoracic esophagus-cardia resection with gastric tube reconstruction.
The exact origin of EAC is unknown; however, a number of factors have been associated with
this malignancy. Patients with Barrett's esophagus (BE), caused by gastro-esophageal reflux
disease, are known to have an increased risk of developing EAC.3, 4 Athletes in general, and
possibly rowers in particular, are known to experience gastro-intestinal symptoms during
and/or (immediately) after exercise, including heartburn, regurgitation, belching, nausea and
vomiting, with reported rates of 30-67%.5-7 Reflux symptoms induced by exercise can be
explained by increased intra-abdominal pressure, delayed gastric emptying and transient
relaxation of the lower esophageal sphincter.8
4
The type and the intensity of exercise are suspected to affect the prevalence of reflux
symptoms. A comprehensive overview of the association between reflux symptoms and
diverse sport exercises and their intensity is not yet available.
As a result of these EAC diagnoses in three rowers, we became interested in the research
question whether reflux may be induced in rowing people . To this end, two studies were
conducted: 1) a literature review of published studies on gastro-esophageal reflux in athletes,
with particular attention to type and intensity of the exercise; and 2) a questionnaire study on
the prevalence of reflux symptoms and the association with the intensity of rowing in the
particular
rowing
society.
METHODS
Part I: Literature study
Using PubMed a systematic search was performed to identify the association between
exercise (type and intensity) and gastro-esophageal reflux in adults. Studies published from
1985 to March 2014 were included using the following search terms and synonyms: "Sports/
Athletes" AND "Gastro-esophageal reflux/ heartburn". Title and abstract of the papers that
resulted from the systematic search were evaluated for inclusion and exclusion criteria (Figure
1). Subsequently, the full text of the selected manuscripts was reviewed. Only Dutch and
English studies aiming to examine the induction of reflux during exercise were included.
Articles were excluded when they did not contain original data and if the study population
included less than 5 participating people performing sport. In included studies, the prevalence
of gastro-esophageal reflux during or immediately after exercise and related to the type and
intensity of exercise was evaluated by a questionnaire as well as esophageal pH monitoring.
In studies based on pH monitoring, reflux was defined as a drop in pH below 4 in more than
6% of the time.9 Information about the prevalence of gastro-esophageal reflux or associated
5
symptoms during exercise, the type and intensity of sport, and demographic data (such as age
and gender) were assembled. As a measure of exercise intensity, the percentage of maximal
oxygen uptake was used (VO2 max) or calculated if necessary.10
Part II: Questionnaire study
At the end of 2011, a total of 380 questionnaires, both digitally and on paper, were sent out to
all members of the particular rowing society of Southwest Netherlands. The questionnaire
comprised a general section with personal information, a section on current and history
rowing activities and a medical section, explicitly aiming at reflux symptoms. The returned
and completed questionnaires were anonymously processed. A distinction was made between
aspirant and recreational rowing, competitive rowing, tour rowing (a tour throughout the day)
and marathon rowing (a contest with a minimum distance of 50 kilometer).
The determined primary outcome was the prevalence of gastro-esophageal reflux, defined as
heartburn and/or (acidic or non-acidic) regurgitation during rowing and the association with
its intensity. A summary of the characteristics of the rowers was generated. Features of the
rowers, with or without encountering reflux symptoms during the most vigorous rowing
period were compared using a chi-square test, t-test and Mann-Whitney U test whenever
appropriate. Two-tailed p-values <0.05 were considered as statistically significant. The
statistical analyses were performed using SPSS version 20.0.
RESULTS
Part I: Literature study
The initial search strategy yielded 48 articles. Based on the inclusion and exclusion criteria
seven articles on the association between sport (type and intensity) and gastro-esophageal
reflux were ultimately included (Figure 1). The prevalence of reflux symptoms during
6
exercise was analyzed in a total of 439 athletes in the seven included studies. The age of the
athletes varied between 20 and 47 years and the majority was male (n=298, 68%) (Table 1).
In six studies the incidence of reflux was determined by pH monitoring in 76 athletes.9, 11-15
The remaining study evaluated reflux symptoms using a questionnaire (adapted from the
Gastro-intestinal Symptom Rating Scale).16
Four studies compared the prevalence of reflux for different types of sports.9, 12, 15, 16 For all
athletes esophageal acid exposure was normal prior to exercise. pH monitoring showed that
reflux occurred over a longer period of time in weightlifters compared to runners (p= 0.04)
and cyclists (p=0.03) (Figure 2A).12 Weightlifters experienced moderate symptoms of
heartburn whereas other athletes encountered mild symptoms; reflux symptoms were more
severe when exercise was performed immediately after meals. Reflux was significantly more
likely to occur in triathlon athletes during running than during cycling.9 In another study, pH
monitoring showed that reflux was induced by rowing in 70% of the rowers (p=0.03).15
However, based on quantitative determinations, no significant difference in the degree of
reflux before and during rowing and no considerable association between symptoms and the
prevalence of reflux were observed. The questionnaire survey showed a higher prevalence of
reflux symptoms during exercise in surfers (21%; 38/178) compared to other athletes (6%;
12/185) (p=0.001).16
Five included studies examined the association between the intensity of exercise and the
prevalence of reflux.11-14, 16 A higher intensity of exercise was found to be associated with a
significantly longer time of acid exposure to the esophagus in both cyclists and runners
(Figure 2B)11,
13, 14
, or with significantly more reflux symptoms among surfers and other
athletes.16 The association between reflux and intensity of exercise was confirmed in runners
in a study by Collings et al, but no association was found in studies in which cyclists and
weightlifters were included.12
7
Part II: Questionnaire study
Of the 380 questionnaires, 196 were returned (52%). Among the responders 51% was male
(n=96), the mean age ± standard deviation (SD) was 49±14 years and 84% of participants
obtained a high degree of education (Table 2). Of all participants, 45% had a history of
competitive rowing. In total 100 rowers (51%) encountered reflux symptoms. Of these, 81
athletes explicitly indicated the frequency of reflux symptoms; 6% (5/81) daily, 22% (18/81)
weekly, 20% (16/81) monthly and 52% (42/81) less than once a month, respectively.
During the most vigorous rowing period additional (mild, moderate or severe) symptoms of
reflux were experienced during rowing (24%, 25 of 103 rowers designating the prevalence of
reflux symptoms in this rowing period; p=0.04) than immediately after rowing (10%, 10/103;
p=0.009), or in daily life experience (18%, 18/103; p=0.03) (Figure 3). Significantly more
women experienced symptoms of reflux while rowing than men; age and body mass index
(BMI) were not associated with rowing (Table 3). Competition rowers experienced the lowest
frequency of reflux symptoms during the most vigorous rowing period in their life, followed
by aspirant or recreational and tour rowers. Marathon rowers indicated most frequently reflux
symptoms (p=0.02; Table 3). The prevalence of reflux symptoms was not associated with the
number of rowing hours per week.
DISCUSSION
The literature review (part I) demonstrated the induction of gastro-esophageal reflux during
exercise, in which type and intensity of sport were found to be determining. The most
frequent and severe reflux episodes were observed during weightlifting, which may be
explained by a high increase in intra-abdominal pressure during weightlifting.12 Furthermore,
reflux was significantly more frequent during running compared to cycling9, 12, which may be
8
the result of continuous total body movement.17 However, in cyclists upper gastro-intestinal
symptoms were also common and these were suggested to be caused by an increased intraabdominal pressure created by the stooped posture.5
Accordingly, pH monitoring previously demonstrated induction of gastro-esophageal reflux
during rowing15, which may be explained by the increased intra-abdominal pressure during
rowing.5-8 In our questionnaire study (part II), 28% of rowers encountered weekly or daily
reflux symptoms, which was more frequent compared to the reported prevalence of reflux
symptoms in athletes, including surfers and non-surfers (14%).16 Additionally, rowers
experienced more symptoms of reflux during rowing than in daily life. However, the
prevalence of reflux symptoms in rowers was lower compared to the general Western
population; reflux symptoms were encountered monthly in 8% vs. 25%, weekly in 9% vs.
12%, and daily in 3% vs. 5%.18
Long-distance rowers (marathon and tour) experienced the most frequent symptoms of reflux
compared to other types of rowing activities. As long-distance rowers are successively
exercising for hours, these rowers need to utilize sufficient carbohydrates, which may,
together with repetitive physical movements with consequently increased intra-abdominal
pressure, may induce gastro-esophageal reflux. In general, competition rowers are no longer
than one and a half hour consecutively exercising and therefore will not take large
consumptions such as complete meals immediately before or during rowing. Accordingly,
aspirant and recreational rowers are usually training for a shorter period and do not use
consumptions. Previously, more severe reflux was demonstrated when performing exercise
immediately after a meal or sports drink consumption in weightlifters and runners.9, 12
The long-term consequences of reflux in rowers are expected to be comparable to the general
population and include esophagitis, stricture formation, BE and EAC.19 In the study by Choi
et al, 16 runners with a high training intensity of ≥ 200 running kilometers per week, were
9
undergoing upperendoscopy.20 Six runners (38%) revealed endoscopic esophagitis, which
may have been caused by exercise-induced reflux. However, due to the high intensity of
exercise these results cannot be extrapolated to the regular sport population. No previous
studies have demonstrated an association between rowing and development of EAC. When
compared to the crude EAC incidence rate of 9.9 per 100,000,000 inhabitants at risk in 2009
in the Netherlands21, the detection of EAC in 3 rowers of a rowing society with not even 400
members is at least remarkable. Previous studies have suggested a protective effect of
physical activity on gastro-intestinal cancer risk. In a prospective European study including
420,449 participants, weekly exercise was associated with a reduced gastric cancer risk
(hazard ratio 0.69; 95% confidence interval 0.50-0.94).22 No association between physical
activity and esophageal cancer was found. Additionally, moderate physical activity was
demonstrated to reduce colorectal cancer risk with 20-25%.23 These results, in combination
with the relatively low frequency of reflux symptoms in rowers compared to the general
population, suggest that the peak in EAC incidence in this particular rowing cohort may be
most likely due to coincidence than to a causal relation between rowing-induced reflux and
EAC development.
A strength of this study is the combination of a literature review and a questionnaire survey in
a rowing cohort. The questionnaire investigation compared reflux symptoms during and
immediately after rowing and in daily life and the association with rowing intensity. A
limitation is the possible reporting bias in the questionnaire investigation. Not all active
rowing members returned the questionnaire and rowers with reflux symptoms may actually
have been more likely to respond. Because of the anonymous return of the questionnaires, it
was not possible to compare characteristics of responders and non-responders. Furthermore,
the prevalence of reflux in rowers was only analyzed by means of a symptom-questionnaire
and not combined with pH monitoring or upper endoscopy. Finally, the current study design
10
does not allow to conclude on a causal relation between rowing and EAC. Future studies are
required to examine the possible long-term consequences of exercise-induced reflux in a large
cohort of athletes, including rowers.
Based on these results, it is recommendable not to underestimate reflux symptoms in athletes.
When sportsmen, including rowers, experience reflux symptoms, first life style modifications
should be considered. The American College of Gastroenterology recommends elevation of
the head of the bed, to reduce dietary fat intake and discontinue smoking, and to avoid a
horizontal position shortly postprandial.24 Prior to demanding exercise solid food and drinks
with high carbohydrate content should possibly be avoided.25
In conclusion, exercise has been demonstrated to induce gastro-esophageal reflux, which is
related to the type of sport and intensity. Rowers experienced more symptoms of reflux while
rowing than in daily life. Given the relatively low prevalence of reflux symptoms in the
present rowing cohort compared to the general population, an association between rowing,
gastro-esophageal reflux and EAC seems unlikely.
ACKNOWLEDGEMENTS
The authors thank the board of the particular rowing, and all participating rowers for their
cooperation.
11
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