Racial differences in the frequency of symptoms and complications of gastro-oesophageal reflux disease

Authors


Correspondence to: Dr S. J. Spechler, Chief, Division of Gastroenterology (111B), Dallas VA Medical Center, 4500 South Lancaster Road, Dallas, TX 75216, USA. E-mail: sjspechler@aol.com

Summary

Background : A number of reports have suggested that there are substantial racial differences in the frequency of gastro-oesophageal reflux disease and its complications, but few studies have compared directly the frequency of this disorder amongst different racial groups.

Aim : To explore the racial differences in the frequency of gastro-oesophageal reflux disease and its complications.

Methods : We reviewed endoscopy reports and medical records for data on race and complications of gastro-oesophageal reflux disease in 2477 consecutive patients who had endoscopic examinations at the general endoscopy unit of an academic hospital. In addition, we prospectively interviewed 129 out-patients attending general medical clinics in the hospital and in an Asian community health centre in Boston to obtain data on race and gastro-oesophageal reflux disease symptoms.

Results : One or more gastro-oesophageal reflux disease complications (peptic oesophageal ulcer, stricture or Barrett's oesophagus) were observed in 267 of 2174 white patients (12.3%), seven of 249 black patients (2.8%), one of 21 West Asian patients (4.8%) and none of 33 East Asian patients seen at the general endoscopy unit (P < 0.001); 34.6% of whites, 46.1% of blacks and 2.6% of East Asian patients interviewed claimed that they had heartburn (P < 0.01), but the term ‘heartburn’ was understood by only 34.6%, 53.8% and 13.2% of whites, blacks and East Asians, respectively (P < 0.01).

Conclusions : Asian patients in Boston infrequently complain of heartburn, whereas heartburn is commonly reported by both white and black patients. Many patients do not understand the meaning of the term heartburn, however, and so physicians should be cautious when using the term during patient interviews. Complicated gastro-oesophageal reflux disease appears to be predominantly a disorder of whites.

Introduction

Gastro-oesophageal reflux disease (GERD) appears to be the most common chronic disorder of the gastrointestinal tract in Western countries.1 Surveys suggest that approximately 20% of adults in the USA regularly experience heartburn, the cardinal symptom of GERD, and Americans may spend as much as $5 billion annually on anti-reflux medicines.2–4 GERD can be complicated by peptic ulcers of the oesophagus, and such ulcers may stimulate fibrous tissue deposition with oesophageal stricture formation.5 In some patients, the reflux-damaged squamous epithelium of the oesophagus is replaced by an abnormal intestinal-type epithelium, a condition called Barrett's oesophagus, that predisposes to adenocarcinoma.6 GERD and Barrett's oesophagus are the major recognized risk factors for oesophageal adenocarcinoma, a tumour whose frequency has risen dramatically in the USA and Western Europe over the past few decades.7, 8

Amongst different ethnic groups, there appear to be important differences in the frequency of GERD and its complications. One study has suggested that peptic oesophageal ulcers and stricture may be more common in whites than in African-Americans.9 Studies conducted in the Far East suggest that GERD is uncommon in Asians.10, 11 In a recent survey of 236 Chinese residents of Singapore, for example, only two (0.8%) reported frequent symptoms of GERD.10 Indeed, there is no word for ‘heartburn’ in Mandarin Chinese (K. Y. Ho 2001, personal communication). A number of studies have suggested that Barrett's oesophagus and its sequela, oesophageal adenocarcinoma, are predominantly disorders of whites.12–15 In mainland China, where squamous cell carcinoma of the oesophagus is the second most common malignancy in the general population, adenocarcinoma of the oesophagus is rare.16 Despite all of these suggestive data, however, few studies have compared directly the frequency of GERD and its complications amongst different racial groups. We have explored racial differences in the prevalence of heartburn and GERD complications amongst patients in a large hospital and in an Asian community health centre in Boston.

Methods

This study was approved by the Committee on Clinical Investigations, New Procedures, and New Forms of Therapy of the Beth Israel Deaconess Medical Center.

Part I

We reviewed the endoscopy reports and computerized medical records of all patients who had undergone endoscopic examinations of the upper gastrointestinal tract in the general endoscopy unit of the Beth Israel Deaconess Medical Center between April 1, 1992 and December 31, 1994. Data on race and complications of GERD (Barrett's oesophagus, peptic oesophageal ulcer and peptic oesophageal stricture) were recorded for each subject. East Asian patients included those from China, Korea, Japan, Thailand and Vietnam. Patients from India, Pakistan and Iran were considered as West Asians. The diagnosis of oesophageal ulcer was made in patients who had mucosal breaks that exhibited depth and overlying exudate. An oesophageal stricture was recognized endoscopically as a persistent narrowing of the oesophageal lumen other than that caused by a ring or web. The demonstration of specialized intestinal metaplasia in biopsy specimens obtained from a columnar-lined oesophagus was required for inclusion in the Barrett's oesophagus group. Patients with a history of any condition other than GERD that might cause oesophageal injury (e.g. acquired immunodeficiency syndrome, oesophageal infections, caustic ingestions, radiation treatment to the chest) were excluded from the peptic oesophageal ulcer and peptic oesophageal stricture groups. The three GERD complication groups were not mutually exclusive.

Part II

We personally interviewed black, white and East Asian out-patients attending general medical clinics in our hospital and in a local Asian (predominantly Chinese), physician-operated community health centre about symptoms of GERD. The Asian health centre was included to increase the number of Asian study subjects. When we visited the medical clinics to conduct interviews, we invited all patients in the general waiting area to participate. Early in the interview, we asked patients if they experienced heartburn at least once each month. Those who said yes were included in the ‘Complained of Heartburn’ group. Later, we asked patients to describe the symptom of heartburn. Those who described at least a burning, warm or ‘acid’ sensation in the epigastrium, substernal area or both were included in the ‘Understood Heartburn’ group. Finally, without using the term ‘heartburn’, we asked patients specifically if they experienced symptoms that are components of heartburn. Those who experienced at least a burning, warm or ‘acid’ sensation in the epigastrium, substernal area or both were included in the ‘Had Heartburn’ group. The groups were not mutually exclusive.

Statistical methods

Data were analysed using standard extensions to Fisher's exact test to compare results across all four racial groups (Part I) or all three racial groups (Part II), followed by specific comparisons between races using Fisher's exact test. The binomial distribution was used to assess differences in the total number of GERD complications between racial groups. P < 0.05 (two-sided) indicated statistical significance. All analyses used SAS version 6.11 (SAS Institute, Cary, NC, USA).

Results

For Part I of the study, we reviewed the records of 2989 patients; racial data were not available for 512. Demographic data for the 2477 patients for whom racial data were available are shown in Table 1. Non-peptic oesophageal ulcers (i.e. ulcers in patients who had a history of acquired immunodeficiency syndrome, oesophageal infections, caustic ingestions or radiation treatment to the chest) were found in 26 (1.2%) of the 2174 white patients, five (2.0%) of the 249 black patients, none of the 21 West Asian patients and one (3.0%) of the 33 East Asian patients (N.S.). Non-peptic oesophageal strictures were found in 20 (0.9%) white patients, five (2.0%) black patients, none of the West Asian patients and one (3.0%) East Asian patient (N.S.). The distribution of racial groups for specific GERD complications, in all patients studied, is shown in Table 2. It should be noted that GERD complications were significantly less common in black and East Asian patients compared to white patients. Overall, one or more complications of GERD were observed in 267 of 2174 (12.3%) white patients, seven of 249 (2.8%) black patients, one of 21 (4.8%) West Asian patients and none of 33 East Asian patients (P < 0.001) (Figure 1).

Table 1.  Demographic data of patients who underwent endoscopic examination
 WhitesBlacksW. AsiansE. Asians
All patients studied21742492133
Males : females1053 : 1121112 : 13715 : 621 : 12
Mean age (years) (± s.d.)58 ± 1951 ± 1743 ± 1850 ± 19
Table 2.  Distribution of racial groups with regard to gastro-oesophageal reflux disease (GERD) complications
 Total no.WhitesBlacksW. AsiansE. Asians
  • *

      P  < 0.05 compared to whites. Note that the percentages pertain to the individual rows, not the columns.

All patients studied24772174 (87.8%)249 (10.1%)21 (0.8%)33 (1.3%)
No GERD complications22021907 (86.6%)242 (11.0%)20 (0.9%)33 (1.5%)
Any GERD complication275267 (97.1%)7 (2.5%)*1 (0.4%)0 (0%)*
Barrett's oesophagus201194 (96.5%)6 (3.0%)*1 (0.5%)0 (0%)
Peptic oesophageal ulcer6261 (98.3%)1 (1.6%)*0 (0%)0 (0%)
Peptic oesophageal stricture5050 (100%)0 (0%)*0 (0%)0 (0%)
Total GERD complications313305 (97.4%)7 (2.2%)*1 (0.3%)0 (0%)*
Figure 1.

Ethnic variations in the frequency of gastro-oesophageal reflux disease complications (Barrett's oesophagus, peptic oesophageal ulcer, peptic oesophageal stricture) amongst patients who underwent endoscopic examination of the upper gastrointestinal tract in a general endoscopy unit.

In Part II of the study, we interviewed 129 patients whose demographic features are shown in Table 3. Of these patients, 37 (28.7%) complained of heartburn, 44 (34.1%) understood heartburn and 47 (36.4%) had heartburn. Of the 37 patients who complained of heartburn, only 24 (65%) understood the meaning of the symptom, and only 26 (70%) actually experienced heartburn by our minimal criteria for the symptom. Conversely, of the 92 patients who denied heartburn, only 20 (22%) understood the symptom, and 21 (23%) had symptoms that a physician might consider as heartburn. Significant ethnic differences were observed in the prevalence, understanding and experience of heartburn, as summarized in Table 3 (all P < 0.01 overall).

Table 3.  Ethnicity and heartburn
 WhitesBlacksAsians
  • P  < 0.05 vs. other two groups.

Number of patients (males, females)52 (20, 32)39 (9, 30)38 (17, 21)
Mean age (years) (± s.d.)45 ± 1845 ± 1441 ± 15
Number who complained of heartburn18 (35%)18 (46%)1 (3%)*
Number who understood heartburn18 (35%)21 (54%)5 (13%)*
Number who had heartburn17 (33%)22 (56%)*8 (21%)*

Discussion

We have found significant differences in the prevalence of GERD complications amongst different racial groups. Complicated GERD appears to be predominantly a disorder of whites. GERD complications were found in 12.3% of all white patients who had endoscopic examinations in the general endoscopy unit of the Beth Israel Deaconess Medical Center. In contrast, only 2.8% and 4.8% of black and West Asian patients, respectively, had complicated GERD, and no GERD complication was seen in any East Asian patient.

A number of investigators have noted that patients with Barrett's oesophagus are predominantly white.12 Few data are available on the relative frequency of Barrett's oesophagus amongst different racial groups, however, and even fewer data are available on the frequency of peptic oesophageal ulcers and strictures. One study has suggested that the latter complications affect white patients more often than African-Americans.9 However, that study was based on a review of International Classification of Disease Clinical Modification codes compiled by the Health Care Financing Administration for Medicare beneficiaries. The accuracy with which these codes are recorded in general is questionable, and the codes for oesophageal ulcer and stricture do not distinguish between ulcers and strictures caused by GERD and those caused by other oesophageal disorders, such as infectious oesophagitis, radiation exposure and caustic ingestion. Our study on GERD complications was based on a review of endoscopic examinations performed in one endoscopy unit, and on a review of the patients' medical records. As a result, we were able to distinguish between peptic and non-peptic causes of oesophageal disease.

Reports from the Far East support the findings of our study that complicated GERD is rare in East Asian patients.10, 11, 17 In one study of 2044 patients in Taiwan, who had endoscopy as part of an annual health maintenance examination, only 102 (5%) had endoscopic evidence of oesophagitis, which was mild (grade 1) in the large majority of cases.11 Recent data suggest that endoscopic criteria for grade 1 oesophagitis are unreliable.18 Only two of the 2044 Chinese patients (0.1%) had complicated, grade 4 oesophagitis (defined as ulcer, fibrosis of the oesophageal wall, stricture, short oesophagus or columnar-lined oesophagus). In contrast, 12.3% of white adults in our endoscopy unit had grade 4 oesophagitis by the criteria used in the Chinese study. Another study from Taiwan found signs of oesophagitis in 66 of 455 patients (14.5%) who had endoscopic examinations because of upper gastrointestinal symptoms.17 Although the authors concluded that the frequency of oesophagitis in their Chinese patients was higher than expected, most patients had only mild oesophagitis of dubious importance. Grade 4 oesophagitis (defined as ulcer or stricture) was found in only four of the 455 patients (0.9%), and Barrett's oesophagus was observed in only nine subjects (2%).

The endoscopic portion of our study was not conducted prospectively, and hence is subject to the limitations of retrospective analyses. Ethnic differences in symptom reporting and in physician referral for endoscopic examination could have resulted in selection bias that might have skewed the results. The findings may also have been influenced by the relatively small number of Asian patients included, and by the failure to control for the use of antisecretory medications. Nevertheless, it seems unlikely that the large differences observed in the frequency of GERD complications amongst different ethnic groups could have resulted solely from these potential sources of study error.

Our prospective interview of patients regarding the symptom of heartburn also revealed significant differences amongst racial groups in the reporting, understanding and experience of the symptom. The frequency with which heartburn was reported by our white and black patients (34.6% and 46.1%, respectively) was similar to that described in other reports of predominantly white individuals in the USA.2, 3 In contrast, only 2.6% of the East Asian patients interviewed complained of heartburn. Furthermore, most patients in our study (65.9%) did not understand the meaning of the term ‘heartburn’. Of all patients who claimed that they had heartburn, 29.7% did not describe symptoms that a knowledgeable physician would regard as heartburn. Conversely, 22.8% of patients who denied having heartburn in fact experienced symptoms that physicians might consider to be heartburn.

The factors underlying the significant ethnic differences observed in the experience of GERD symptoms and complications are unknown. One potential factor might be ethnic differences in the frequency of gastric infection with Helicobacter pylori, a bacterium that is especially prevalent in black and Asian populations.19 A number of recent reports have suggested that gastric infection with H. pylori may protect the oesophagus from reflux oesophagitis, Barrett's oesophagus and oesophageal adenocarcinoma, perhaps because the infection causes a chronic gastritis that can decrease gastric acid secretion.20–24 This hypothesis fits in with the observation that the frequency of oesophageal adenocarcinoma has increased in Western countries during a period in which the frequency of H. pylori infection in the general population has declined substantially.19 Evidence for H.pylori infection was not sought in our study, and the contribution of H. pylori to the observed differences in GERD complications remains speculative. Other potential factors that might contribute to ethnic differences in GERD frequency include disparities in parietal cell mass and gastric acid secretion,25 dietary differences, disparate rates of obesity and unspecified genetic factors that predispose to GERD and its sequelae. Finally, potential sources of study error include selection bias, language difficulties (English was not a first language for some of our East Asian patients) and the failure to control for the use of antisecretory medications.

Regardless of the reasons underlying the significant differences in the frequency of GERD and its complications amongst different ethnic groups, our findings have several important clinical implications. During patient interviews, first of all, physicians should be cautious in the way in which they use and interpret the term ‘heartburn’, because many patients do not understand the meaning of the term. Next, peptic oesophageal ulcers and strictures appear to be decidedly uncommon in black and Asian patients. For black and Asian patients found to have oesophageal ulcers and strictures, therefore, causes other than GERD should be considered strongly and pursued vigorously. Finally, endoscopic examination often is performed in patients with chronic GERD symptoms specifically to identify the complication of Barrett's oesophagus.26 The rationale for this practice is that patients with Barrett's oesophagus might benefit from regular endoscopic surveillance to detect curable oesophageal neoplasia. However, the efficacy of endoscopic screening and surveillance in decreasing cancer mortality has not been established, even for middle-aged white men, the group most at risk of Barrett's oesophagus and adenocarcinoma.27 Indeed, the very need for endoscopic surveillance in this group has been challenged.28, 29 Our finding that Barrett's oesophagus is so uncommon in black and Asian patients suggests that screening for this disorder may not be an appropriate rationale for endoscopy in black and Asian populations.

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