ORIGINAL ARTICLE

Differences in recognition of heartburn symptoms between Japanesepatients with gastroesophageal reflux, physicians, nurses, and healthylay subjects

NORIAKI MANABE1, KEN HARUMA2, JIRO HATA1, TOMOARI KAMADA2 &

HIROAKI KUSUNOKI1

1Division of Endoscopy and Ultrasonography, and 2Division of Gastroenterology, Department of Internal Medicine, Kawasaki

Medical School, Kurashiki, Japan

AbstractObjective. Patients who complain of ‘‘heartburn’’ to their general practitioner tend to use the word to indicate a variety ofsymptoms. The aim of this study was to investigate the differences in recognition of ‘‘heartburn’’ between normal healthy laysubjects (HS), patients with gastroesophageal reflux disease (GERD), nurses, and physicians. Material and methods. Ananonymous questionnaire survey concerning ‘‘heartburn’’ obtained responses from 583 persons including 198 GERDpatients (140 with non-erosive reflux disease (NERD) and 58 with reflux esophagitis (RE)) who were evaluated at KawasakiMedical School Hospital and affiliated facilities, as well as 170 HS, 111 nurses, and 104 physicians. Subjects were asked tochoose the option most closely describing a symptom that they would recognize as heartburn. Results. Recognition did notdiffer between RE patients and physicians, whereas NERD patients did not recognize ‘‘regurgitation’’ or ‘‘burning sensationin the chest’’ as heartburn as often as physicians, while confusing ‘‘stomach ache’’ with heartburn. Significantly more NERDpatients chose ‘‘stomach ache’’ than RE patients. Conclusions. Differences in recognition of heartburn were noticedbetween HS, GERD patients, nurses, and physicians. RE patients and physicians showed similar recognition patternsamong the descriptions of heartburn, whereas NERD patients differed from physicians and RE patients.

Key Words: Gastroesophageal reflux disease, non-erosive reflux disease, reflux esophagitis, symptom diagnosis

Introduction

‘‘Heartburn’’, defined as a burning sensation in the

retrosternal area [1], is the most common symptom

of gastroesophageal reflux disease (GERD). An

estimated 20�40% of the adult population experi-

ence heartburn, while 7% of adults exhibits this

symptom daily [2�4]. When present as the predo-

minant symptom, heartburn has a high, positive

predictive value for a diagnosis of GERD, but

sensitivity is low [5,6].

At present, GERD appears to be the most

common chronic disorder of the gastrointestinal

tract in Japan as well as in Western countries [7,8].

In up to half of cases, GERD is associated with

endoscopically demonstrable evidence of esophagitis

[9]. However, individuals with GERD can experi-

ence significant heartburn whether or not such

evidence is present, and impairment of quality of

life is not dependent on the endoscopic findings

[10,11]. Presently, patients with troublesome reflux-

associated symptoms but apparently intact mucosa

at endoscopy are diagnosed with non-erosive reflux

disease (NERD). Thus, a careful study of the

patient’s history is important for diagnosis of

GERD, especially the NERD form.

In a previous report [12] it was suggested that

Asian GERD patients seldom complained of heart-

burn, while many of them had a poor understanding

of the meaning of the term. In fact, in our experience

we have found general-practice patients referring to

a variety of symptoms as ‘‘heartburn’’. Previous

studies have not considered the differences in

recognition of heartburn between physicians and

Correspondence: Noriaki Manabe, MD, Divison of Endoscopy and Ultrasonography, Kawasaki Medical School, 577 Matsushima, Kurashiki, JP 701-0192,

Japan. Tel: �81 86 4621 111. Fax: �81 86 4621 199. E-mail: n_manabe@hkg.odn.ne.jp

Scandinavian Journal of Gastroenterology, 2008; 43: 398�402

(Received 24 September 2007; accepted 17 November 2007)

ISSN 0036-5521 print/ISSN 1502-7708 online # 2008 Taylor & Francis

DOI: 10.1080/00365520701815074

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GERD patients, or those between patients with

NERD and reflux esophagitis (RE) patients.

In this study we sought to investigate the differ-

ences in recognition of heartburn between healthy lay

subjects (HS), GERD patients, nurses, and physi-

cians, as well as between NERD and RE patients.

Material and methods

Subjects

We conducted an anonymous questionnaire survey

on heartburn, and received responses from 583

persons including 198 GERD patients (140

NERD, 68 M, 72 F, mean age 58.891.9 years; 58

RE, 38 M, 20 F, mean age, 68.591.3 years) who

consulted either the Kawasaki Medical School

Hospital or three general practice offices; 170

healthy lay subjects (HS; 113 M, 57 F, mean age,

30.691.0 years); 111 nurses (all women; mean age,

32.991.0 years); and 104 physicians (59 specialists

in gastroenterology and 45 non-specialists; 98 M, 6

F; mean age, 49.491.3 years) between 1 August

2006 and 31 March 2007.

GERD patients entering this study were uninves-

tigated adult outpatients of over 20 years of age and

with a clinical diagnosis of GERD and the main

symptom identified as ‘‘heartburn’’ ascending from

the epigastrium or lower chest toward the neck.

Clinical diagnosis of GERD was made using the

Frequency Scale for Symptoms of GERD (FSSG)

developed by Kusano et al. [13]. A total FSSG score

exceeding 8 points was considered to indicate

GERD. Each patient then underwent upper gastro-

intestinal endoscopy in order to grade the severity of

GERD and to exclude organic disease of the

esophagus, stomach, or duodenum. Endoscopic

severity of GERD was determined according to the

Los Angeles (LA) classification [14]. If no mucosal

break was evident in the esophagus, the endoscopic

severity of GERD was considered normal (LA

classification grade N). Patients were excluded if

they had been treated with a proton-pump inhibitor

(PPI) and/or H2-receptor antagonists within 1

month prior to enrollment or had a past history of

gastrointestinal tract resection. The hospital ethics

committee approved this study, and verbal informed

consent was obtained from all patients.

Administration of the questionnaire

For this study we devised a new questionnaire

concerning recognition of heartburn (Table I). Sub-

jects were asked to choose the option that most clo-

sely described a symptom that they would recognize

as heartburn. If no option matched a symptom,

the subjects were asked to describe the symptom

themselves.

Statistical analysis

Data are expressed as the mean9standard error of

the mean (SEM). Statistical significance was eval-

uated at the 0.05 level, using the x2 test. A p-value of

less than 0.05 was considered to indicate significant

difference.

Results

Subject characteristics

Characteristics of subjects are presented in Table II.

As for endoscopic severity of GERD, the numbers of

patients with LA grades N, A, B, C, and D were 140,

34, 20, 4, and 0, respectively. Nearly all RE patients

(54/58) represented mild cases. GERD patients were

significantly older than the subjects in the other

groups. The NERD subgroup subjects were younger

than those in the RE subgroup, and lacked the male

preponderance evident in the RE subgroup. Symp-

tom frequency (FSSG score) showed no significant

difference between NERD and RE patients.

Table I. Questionnaire concerning recognition of heartburn.

Please choose the option closest to the symptom that you would

recognize as ‘‘heartburn’’. If these options do not match a

symptom that you find relevant, please choose ‘‘others’’ and

describe the symptom(s) in the box provided at the foot of the

page.

( ) Heavy feeling in the stomach

( ) Stomach ache

( ) No appetite (anorexia)

( ) Feeling of sour contents coming up from the stomach

( ) Burning sensation in the chest

( ) Chest pain

( ) Heavy feeling in the chest

( ) Queasy feeling

( ) Dysphagia

( ) Fit of coughing

( ) As I have not experienced ‘‘heartburn’’, I have no idea about

the term.

( ) Others (Please describe your sense of ‘‘heartburn’’

symptoms).

Symptoms signifying heartburn 399

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Comparison of recognition of heartburn between

non-patient groups

There was no significant difference in recognition of

heartburn between specialists in gastroenterology and

general practitioners (data not shown). However,

recognition of heartburn differed between physicians,

nurses, and HS (Figure 1). Significantly more physi-

cians recognized the ‘‘feeling of sour contents coming

up from the stomach’’ as heartburn than in the other

two non-patient groups (80 (76.9%) versus 57 HS

(33.5%) and 42 nurses (37.8%)). This was also true

for ‘‘burning sensation in the chest’’ (72 (69.2%)

versus 48 HS (28.2%) and 24 nurses (21.6%)). Thus,

neither HS nor nurses understood the term ‘‘heart-

burn’’ as well as physicians. In this study, we

considered only the choice of either ‘‘feeling sour

contents coming up from the stomach’’ or ‘‘burning

sensation in the chest’’ to represent a correct under-

standing of heartburn. More precisely, the fraction of

subjects who understood the term ‘‘heartburn’’ cor-

rectly was 86/104 (82.7%) among physicians, 79/170

(46.5%) among HS, and 50/111 (45.0%) among

nurses. Interestingly, HS was the group that most

frequently misrecognized ‘‘no appetite’’ as heartburn

(43 (25.3%)), while nurses formed the group that

most frequently misrecognized ‘‘queasy feeling’’ as

heartburn (71 (64.0%)).

Comparison of recognition of the term ‘‘heartburn’’

between NERD and RE patients

Recognition of the term ‘‘heartburn’’ was compared

between NERD and RE patients in Figure 2. While

RE patients’ understanding of heartburn was no

different from that of physicians, NERD patients did

not recognize ‘‘regurgitation’’ or ‘‘burning sensation

in the chest’’ as heartburn as frequently as did

physicians (pB0.05), and confused ‘‘stomach

ache’’ with heartburn, unlike physicians (pB0.05).

The fraction of subjects who understood the term

‘‘heartburn’’ correctly was 36/140 (25.7%) among

NERD patients and 40/58 (69.0%) in RE patients.

Thus, RE patients were more likely to understand

the term than NERD patients (pB0.01).

Discussion

In this study we found certain differences in recogni-

tion of heartburn between HS, GERD patients,

nurses, and physicians. Physicians and RE pa-

tients had shared recognition of heartburn, while

Heavy feeling in the stomach

Stomach ache

No appetite (anorexia)Feeling of sour contentscoming up from the stomach

Burning sensation in the chest

Chest pain

Heavy feeling in the chest

Queasy feeling

Dysphagia

Fit of coughing

0 20 40 60 80 100(% of subject group)

***

* *

* *

* *

* *

* *

Figure 1. Recognition of various symptoms as indicating heartburn among healthy subjects (n�170, open bars), nurses (n�111, light

shading), and physicians (n�104, dense shading). *pB0.05.

Table II. Characteristics of subjects.

Number Gender (M/F) Mean age (years) FSSG score

NERD 140 68/72 58.891.9 10.291.6

RE 58 38/20 68.591.3 11.391.5

HS 170 113/57 30.691.0

Nurses 111 0/111 32.991.0

Physicians 104 98/6 49.491.3

Abbreviations: NERD�non-erosive reflux disease; RE�reflux esophagitis; HS�healthy lay subjects; FSSG�Frequency Scale for

Symptoms of GERD.

400 N. Manabe et al.

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differences in recognition of heartburn were no-

ticed between NERD patients and physicians, or RE

patients.

‘‘Heartburn’’ is firmly established as a descriptor of

the main symptom of GERD. Ismail-Beigi et al. [15]

defined heartburn as ‘‘substernal burning, radiating

into the neck, coming in waves, made worse by

recumbent position, and often accompanied by the

regurgitation of bitter or sour fluid into the mouth’’.

Bernstein & Baker [16] showed a direct relationship

between esophageal acidification and ‘‘heartburn’’.

However, ‘‘heartburn’’ is a term that translates poorly

into many languages, so various terms that are not

literal translations of ‘‘heartburn’’ are used by patients

as well as physicians in many countries. In this

Japanese study, we found that HS typically used

‘‘heartburn’’ as an essentially almost all-inclusive

description of upper abdominal symptoms. Spechler

et al. [12] reported that Asian GERD patients seldom

complained of heartburn, and many of them had a

poor understanding of the meaning of the term. In our

study, only 79 HS (46.5%) had a correct under-

standing of the term. This result is in agreement

with those of Spechler et al. [12]. We suspect that our

result was also influenced by the lack of personal

experience of heartburn among Japanese HS. Inter-

estingly, there have been some reports which indicate

how the term ‘‘heartburn’’ is interpreted in other

countries as well as in Japan [17�19].

As most patients with GERD do not have erosive

esophagitis, endoscopy is an insensitive test for

reflux disease, particularly in NERD patients. Symp-

tom evaluation has been proposed to be the most

effective way to identify occurrence of reflux, based

upon recognition of heartburn as the most typical

symptom [20]. However, we found that understand-

ing of ‘‘heartburn’’ differed between physicians and

many NERD patients. Caution is therefore needed

when using the term ‘‘heartburn’’ while taking a

history from a NERD patient.

We also found that recognition of heartburn in

patients with NERD differed from that in patients

with RE. We suspect that this result reflected

differences in clinical features between NERD and

RE patients. Patients with NERD are more likely to

be younger or female, and less likely to be overweight

or have a hiatus hernia than patients with RE [21]. A

previous study by Martinez et al. [22] reports that

NERD patients were significantly less likely to have

an esophageal abnormal pH than those with RE or

Barrett’s esophagus. Some investigators indicated

that NERD might represent a process that is

separate from RE [23,24].

In this study, we also found that significantly more

NERD patients confused heartburn with stomach

ache. As for localizing the symptoms of ‘‘heartburn’’

in the retrosternal area, we suspected the localization

to reflect a significant overlap between NERD reflux

disease and functional dyspepsia (FD). Both entities

are extremely common, and both can cause chronic

or recurrent upper gastrointestinal symptoms. Epi-

demiologic, clinical, and pathophysiologic data in-

dicate a significant overlap between NERD and FD

[25,26]. Tack et al. [27] previously reported that

symptoms of epigastric pain were more prevalent in

dyspeptic patients with abnormal esophageal pH

according to monitoring, which is in accord with

our result.

The present study has a number of limitations that

should be taken into account in generalizing our

Heavy feeling in the stomach

Stomach ache

No appetite (anorexia) Feeling of sour contents comingup from the stomach

Burning sensation in the chest

Chest pain

Heavy feeling in the chest

Queasy feeling

Dysphagia

Fit of coughing

0 20 40 60 80 100

(% of subject group)

*

**

* *

* *

* *

*

*

Figure 2. Recognition of various symptoms as indicating heartburn in physicians (n�104, open bars), RE patients (n�58, light shading),

and NERD patients (n�140, dense shading). *pB0.05. RE�reflux esophagitis; NERD�non-erosive reflux disease.

Symptoms signifying heartburn 401

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findings. First, the setting of the study was a large

hospital involved in both primary and secondary care,

including a general gastroenterology clinic and care of

patients, referred by general practitioners. The find-

ings therefore might not directly apply to all NERD

patients seen in primary care. Second, mean age

differed significantly between NERD patients and

physicians. However, recognition of ‘‘heartburn’’ did

not differ significantly between younger (50 years)

and older (�50 years) HS. This suggests that heart-

burn recognition data were not skewed by age

differences. Third, in screening for GERD symptoms,

we used a simplified 9-item questionnaire, the FSSG

(cut-off total score �8.0) [13]. Recently, a number

of new GERD questionnaires have been developed

which may allow better recognition of reflux symp-

toms [19]. We do not know whether we would have

obtained the same results had we based the GERD

diagnosis on these newer questionnaires. However,

the FSSG has performed reasonably well, with a

sensitivity of 79.8%, a specificity of 53.6%, and an

accuracy of 63.4% for Japanese GERD patients [28].

We consider the FSSG to be useful for objective

evaluation of symptoms in that population. Fourth,

future studies are needed to investigate larger num-

bers of GERD patients including NERD, RE, and

patients with Barrett’s esophagus.

In conclusion, many non-patients and NERD

patients had a poor understanding of the meaning

of ‘‘heartburn’’, a term that should therefore be used

with caution during clinical interviewing.

References

[1] Vakil N, van Zanten SV, Kahrilas P, Dent J, Jones R. Global

Consensus Group. The Montreal definition and classifica-

tion of gastroesophageal reflux disease: a global evidence-

based consensus. Am J Gastroenterol 2006;101:1900�20.

[2] Wienbeck M, Barnert J. Epidemiology of oesophageal reflux

disease. Scand J Gastroenterol 1989;24 Suppl 168:33�7.

[3] Spechler S. Epidemiology and natural history of gastro-

oesophageal reflux disease. Digestion 1992;51 Suppl 1:24�9.

[4] Heading RC. Epidemiology of oesophageal reflux disease.

Scand J Gastroenterol 1987;22:714�8.

[5] Johnsson F, Joelsson B, Gudmundsson K, Greiff L. Symp-

toms and endoscopic findings in the diagnosis of gastro-

oesophageal reflux disease. Scand J Gastroenterol 1987;22:

714�8.

[6] Klauser AG, Schindlbeck NE, Muller-Lissner SA. Symp-

toms and endoscopic findings in the diagnosis of gastro-

oesophageal reflux disease. Lancet 1990;335:205�8.

[7] Manabe N, Haruma K, Mihara M, Miyoshi E, Hamada H,

Kido S, et al. The increasing incidence of reflux esophagitis

during the past 20 years in Japan. Gastroenterology

1999;166:A244.

[8] Mishima I, Adachi K, Arima N, Arima N, Amano K,

Takashima T, et al. Prevalence of endoscopically negative

and positive gastroesophageal reflux disease in the Japanese.

Scand J Gastroenterol 2005;40:1005�9.

[9] Sonnenberg A, El-Serag HB. Clinical epidemiology and

natural history of gastroesophageal reflux disease. Yale J

Biol Med 1999;72:81�92.

[10] Wiklund I, Talley NJ. Update on health-related quality of life

in patients with gastroesophageal reflux disease. Expert Rev

Pharmacoeconomics Outcomes Res 2003;3:341�50.

[11] Kulig M, Leodolter A, Vieth M, Schulte E, Jaspersen D,

Labenx J, et al. Quality of life in relation to symptoms in

patients with gastro-oesophageal reflux disease: an analysis

based on the ProGERD initiative. Aliment Pharmacol Ther

2003;18:767�76.

[12] Spechler SJ, Jain SK, Tendler DA, Parker RA. Racial

differences in the frequency of symptoms and complications

of gastro-oesophageal reflux disease. Aliment Pharmacol

Ther 2002;16:1795�800.

[13] Kusano M, Shimoyama Y, Sugimoto S, Kawamura O,

Maeda M, Minashi K, et al. Development and evaluation

of FSSG: frequency scale for the symptoms of GERD. J

Gastroenterol 2004;39:888�91.

[14] Armstrong D, Bennett JR, Blum AL, Dent J, de Dombal FT,

Galmiche JP, et al. The endoscopic assessment of esophagi-

tis: a progress report on observer agreement. Gastroenterol-

ogy 1996;111:85�92.

[15] Ismail-Beigi F, Horton PF, Pope CE II. Histological con-

sequences of gastroesophageal reflux in man. Gastroenter-

ology 1970;58:163�74.

[16] Bernstein LM, Baker LA. A clinical test for esophagitis.

Gastroenterology 1958;34:760�81.

[17] Carlsson R, Dent J, Bolling-Sternevald E, Johnsson F,

Junghard O, Lauritsen K, et al. The usefulness of a

structured questionnaire in the assessment of symptomatic

gastroesophageal reflux disease. Scand J Gastroenterol

1998;33:1023�9.

[18] Locke GR, Talley NJ, Weaver AL, Zinsmeister AR. A new

questionnaire for gastroesophageal reflux disease. Mayo

Clinic Proc 1994;69:539�47.

[19] Shaw M. Diagnostic utility of reflux disease symptoms. Gut

2004;53 Suppl IV:iv25�7.

[20] Dent J. Definitions of reflux disease and its separation from

dyspepsia. Gut 2002;50 Suppl 4: iv17�20.

[21] Fass R. Epidemiology and pathophysiology of symptomatic

gastroesophageal reflux disease. Am J Gastroenterol 2003;98

Suppl: S2-S7.

[22] Martinez SD, Malagon IB, Garewal HS, Cui H, Fass R.

Non-erosive reflux disease (NERD): acid reflux and symp-

tom patterns. Aliment Pharmacol Ther 2003;17:537�45.

[23] Fass R, Ofman JJ. Gastroesophageal reflux disease: should

we adopt a new conceptual framework? Am J Gastroenterol

2002;97:1901�9.

[24] Locke GR III. Natural history of nonerosive reflux disease. Is

all gastroesophageal reflux disease the same? What is the

evidence? Gastroenterol Clin North Am 2002;31 Suppl:

S59�66.

[25] Quigley EMM. Motility, heartburn and dyspepsia. Aliment

Pharmacol Ther 1997;II Suppl 2:41�50.

[26] Talley NJ, Dennis EH, Schettler-Duncan VA, Lacy BE,

Olden KW, Crowell MD. Overlapping upper and lower

gastrointestinal symptoms in irritable bowel syndrome pa-

tients with constipation or diarrhea. Am J Gastroenterol

2003;98:2452�9.

[27] Tack J, Caenepeel P, Arts J, Lee KJ, Sifrim D, Jassens J.

Prevalence of acid reflux in functional dyspepsia and its

association with symptom profile. Gut 2005;54:1370�6.

[28] Shimoyama Y, Kusano M, Sugimoto S, Kawamura O,

Maeda M, Minashi K, et al. Diagnosis of gastroesophageal

reflux disease using a new questionnaire. J Gastroenterol

Hepatol 2005;20:643�7.

402 N. Manabe et al.

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