Original Article
Gastrointestinal Damage Associated with the Use of Nonsteroidal Antiinflammatory Drugs
N Engl J Med 1992; 327:749-754September 10, 1992
- Abstract
- Abstract
Background
Long-term use of nonsteroidal antiinflammatory drugs (NSAIDs) may lead to inflammation of the small intestine associated with occult blood and protein loss. The aim of this study was to investigate the prevalence and structural correlates of this enteropathy.
Methods
We examined the stomach, duodenum, and small intestine of 713 patients post mortem. Of these patients, 249 had had NSAIDs prescribed during the six months before death and 464 patients had not. All visible small intestinal lesions were removed for histologic examination, and specific etiologic factors were sought. The prevalence of nonspecific small-intestinal ulcers and ulcers of the stomach and duodenum was compared in the two groups of patients.
Results
Nonspecific small-intestinal ulceration was found in 21 (8.4 percent) of the users of NSAIDs and 3 (0.6 percent) of the nonusers (difference, 7.8 percent; 95 percent confidence interval, 5.0 to 10.6 percent; P<0.001). Three patients who were long-term users of NSAIDs were found to have died of perforated nonspecific small-intestinal ulcers. Ulcers of the stomach or duodenum were found in 54 (21.7 percent) of the patients who used these drugs and 57 (12.3 percent) of those who had not (difference, 9.4 percent; 95 percent confidence interval, 3.9 to 15.1 percent; P<0.001).
Conclusions
Patients who take NSAIDs have an increased risk of nonspecific ulceration of the small-intestinal mucosa. These ulcers are less common than ulcers of the stomach or duodenum, but can lead to life-threatening complications. (N Engl J Med 1992;327:749–54.)
Media in This Article
Figure 1
Pathologic Findings at Autopsy of Three Patients Who Used NSAIDs.Table 1
Reasons for Exclusions from the Study.Article Activity
- Article
PATIENTS who take nonsteroidal antiinflammatory drugs (NSAIDs) have an increased risk of mucosal damage in the upper gastrointestinal tract.1 The development of new lesions weeks after the initiation of treatment with NSAIDs has been confirmed in a prospective study,2 and the risk of gastric and duodenal ulcers increases with the dose of NSAID.3 Other epidemiologic studies have shown a link between the use of NSAIDs and serious complications of peptic ulcer disease.4 5 6 7 Evidence that NSAIDs may cause perforation and hemorrhage of the small intestine comes from a case–control study8 and several case reports.9 10 11 12 These drugs also have been implicated in the development of intestinal strictures13 14 15 and narrow-based ileal stenoses.16 , 17
Several indirect approaches have been used to investigate the frequency and nature of NSAID-associated damage to the small intestine. Drug-induced increases in mucosal permeability have been demonstrated in normal subjects and in patients with rheumatic diseases.18 19 20 Bjarnason et al. identified inflammation of the small intestine by showing the accumulation of intravenously administered Radio-labeled leukocytes in the ileum and their subsequent excretion in feces by two thirds of patients receiving long-term NSAID therapy.21 They proposed that NSAID enteropathy is a common and underdiagnosed cause of weight loss and occult gastrointestinal bleeding in patients with rheumatic diseases.22 Fiberoptic enteroscopy has been used to identify mucosal lesions in selected hospitalized patients with iron deficiency anemia who are receiving NSAIDs,23 but there is little information on the structural correlates and clinical importance of NSAID-associated damage to the small intestine in the wider population.
This study was done to determine the prevalence and morphology of jejunal and ileal mucosal lesions at autopsy in consecutive patients with and without a history of having had an NSAID prescribed for them. In addition, we studied the prevalence of gastric and duodenal ulcers in these groups of patients and investigated whether the presence of ulcers in these two regions was a predictive marker for the occurrence of lesions of the jejunum and ileum in the patients receiving NSAIDs.
Methods
Patients Who Died in the Hospital
All patients who died at the hospitals involved in the study and were autopsied between January 1990 and October 1991 were eligible for inclusion in the study. The main investigator was told about imminent autopsies on patients thought to have been taking NSAIDs. Consecutive patients were studied unless the main investigator was absent or there were exclusion criteria (Table 1Table 1
Reasons for Exclusions from the Study.). Control patients were chosen consecutively in a similar manner from two large hospitals. The recruitment policy was designed to include the maximal available number of autopsy results for patients with a history of NSAID use before death. It is important to emphasize, however, that decisions to request autopsies were made on clinical grounds by attending medical staff who were unaware of the purpose of this investigation. No autopsies were done specifically for this study, and small-bowel diseases had not been suspected clinically in any of the patients.Patients Who Died outside the Hospital
We also studied a consecutive group of patients for whom NSAIDs had been prescribed and who had died outside the hospital, in order to reduce potential bias arising from studying only patients who died in the hospital. All these autopsies were conducted at the Glasgow City Mortuary at the instigation of the local Procurator Fiscal's office. This legal body orders autopsy examinations in cases in which the patient's family physician is uncertain about the cause of death or, rarely, if suicide or foul play cannot be ruled out. Medications in possession of the deceased are routinely recorded in the police report. The Procurator Fiscal's office informed us whenever NSAIDs were included in this report.
Drug Histories
The drug history of each patient was corroborated by the hospital records, the patient's family physician, or both. Patients were classified in four categories: those for whom NSAIDs had not been prescribed during the six months before death (control group); those for whom aspirin had been prescribed for any length of time (aspirin group); those for whom NSAIDs other than aspirin had been prescribed daily for at least six months up to the month before death (long-term NSAID group); and those for whom NSAIDs other than aspirin had been prescribed during the six months before death but who did not fulfill the criteria for inclusion in the long-term NSAID group — that is, NSAIDs had been prescribed daily for less than six months or discontinuous courses of NSAIDs had been prescribed for six months or more (short-term NSAID group). We refer to the three NSAID subgroups as users of NSAIDs, although the extent of compliance with the drug regimen outside the hospital was not known.
Exclusion Criteria
Cadavers considered to present a serious risk of infection (e.g., carriers of the human immunodeficiency virus) were excluded. Other exclusion criteria were a premorbid diagnosis of inflammatory bowel disease, death more than 48 hours before arrival at the morgue, the administration of radiotherapy to the abdomen within the preceding year, and an inability to corroborate the drug history with hospital records or the family physician.
Examination of Viscera
The entire jejunum and ileum were opened along the antimesenteric border, and the mucosal surface was washed with tap water. All visibly abnormal areas were removed for histologic examination by a single study pathologist who was unaware of the individual clinical or drug history. Histologic sections were stained with hematoxylin and eosin, Sirrius red, and methyl scarlet blue.
The stomach and duodenum were opened, washed, and examined for ulcers. Only ulcers exceeding 3 mm in diameter were included in the analysis. Histologic examination of gastric and duodenal ulcers was not carried out routinely but instead at the discretion of the hospital or forensic pathologist. These sections were not analyzed as part of this study, but the results of the local pathologist's interpretation were collected subsequently. All ulcers subsequently found to be malignant were excluded from the analysis.
Definitions
The following definitions of terms were used to describe pathologic processes in the small intestine: abnormality, an abnormal finding on gross inspection that was confirmed histologically; erosion, a breach of epithelial surface not extending beyond the muscularis mucosae; ulcer, a breach of epithelial surface and lamina propria extending beyond the muscularis mucosae into the submucosa; inflammation, an abnormal area of mucosa with histologic evidence of acute or chronic inflammatory-cell infiltration but no mucosal breach; specific mucosal lesion, an abnormality for which a specific cause was identified by histologic or microbiologic investigation (ulcers overlying nodules or metastases were excluded); and nonspecific ulcer, an ulcer without an underlying cause identified by these methods.
Microbiologic Studies
Microbiologic studies were done whenever inflammation or ulceration of the small-bowel mucosa was seen. Cecal contents were cultured and examined for the presence of Clostridium difficile toxin. Serum samples were tested for the presence of agglutinating antibodies to Yersinia enterocolitica and Y. pseudotuberculosis at the public health reference laboratory.
Statistical Analysis
Most of the results are expressed as prevalences, both absolute values and percentages, together with differences in the prevalence between groups (and 95 percent confidence intervals). The differences in the proportions of patients with and those without lesions or complications were compared with chi-square tests. Yates' correction was incorporated whenever the number of patients in one cell of a fourfold table was less than 10.
Results
Postmortem results were available for 755 patients. Thirteen were excluded before autopsy, and 29 were excluded because examination of the small bowel would have been technically difficult or the results uninterpretable for the purposes of this study (Table 1). Thus, the results of autopsy examinations on 713 patients (including 49 who died outside the hospital) are included. Of these, 249 had had some form of NSAID prescribed during the six months before death and 464 had not (Table 2Table 2
Demographic Characteristics of the NSAID and Control Groups.*). There were 74 patients in the long-term NSAID group; these included 25 patients with osteoarthritis, 20 with rheumatoid arthritis, 8 with other forms of arthritis, and 2 with bone metastases; the reason for the regular prescription of NSAIDs was not clear in 19 patients. The aspirin group comprised 63 patients, for 61 of whom no more than 300 mg of aspirin daily had been prescribed for cardiovascular or cerebrovascular indications. The short-term NSAID group comprised 112 patients, of whom 34 were receiving analgesia for disseminated cancer, 18 for osteoarthritis, 11 for unclassified low back or sciatic-root pain, 7 for traumatic musculoskeletal injury, and 16 for a variety of other indications. We were unable to determine why NSAIDs had been prescribed for 26 of the patients in the short-term NSAID group. There were no significant differences in age or the length of time from death to postmortem examination between the four groups. The proportion of women in the long-term NSAID group was higher than in the other three groups. Men predominated in the short-term NSAID and aspirin groups (Table 2). The major causes of death in the NSAID and control groups did not differ significantly (Table 3Table 3
Causes of Death in the NSAID and Control Groups.*).Abnormalities of the Small Intestine
Specific mucosal lesions were identified in the small intestine in 4 of the 249 patients in the NSAID group (1.6 percent) and 7 of the 464 patients in the control group (1.5 percent) (Table 4Table 4
Small-Intestinal Abnormalities Identified at Autopsy in the NSAID and Control Groups.). Nonspecific erosions or areas of inflammation were found in four patients (1.6 percent) in the NSAID group. In the control group, two patients had acute jejunal erosions, both of whom had received slow-release oral potassium supplements. Two other control patients had areas of unexplained mucosal erosion or inflammation.Nonspecific ulcers were found in 21 patients (8.4 percent) in the NSAID group and 3 patients (0.6 percent) in the control group (Table 4). Possible confounding etiologic factors were identified in four patients with nonspecific ulceration in the NSAID group (recent anticancer chemotherapy or oral potassium supplementation). The difference between the two groups was also significant if these four patients were excluded from the calculation (difference, 6.2 percent; 95 percent confidence interval, 2.9 to 10.5 percent; P<0.001). The prevalence of nonspecific ulceration was slightly higher in the long-term NSAID group (10 patients, 13.5 percent) than in the short-term NSAID and aspirin groups combined (11 patients, 6.3 percent) (difference, 7.2 percent; 95 percent confidence interval, -1.3 to +15.5 percent; 0.05<P<0.1). The lesions in the patients in the long-term NSAID group were single or multiple and ranged from tiny punched-out ulcers on the tips of valvulae conniventes (Fig. 1Figure 1
Pathologic Findings at Autopsy of Three Patients Who Used NSAIDs.A) to confluent areas of deep ulceration and stricture formation (Fig. 1B). Three patients (4.1 percent) in the long-term NSAID group died as a direct consequence of peritonitis from perforated, nonspecific small intestinal ulcers; no patient in any other group had such lesions. All three of these patients had widespread ileal ulceration, and one also had a solitary jejunal perforation (Fig. 1C). Small-bowel disease had not been suspected clinically in these patients, and no specific or confounding etiologic factors could be identified. There were no other serious complications or deaths from small-intestinal disease in this series (those with bowel infarction had already been excluded).Gastric and Duodenal Ulcers
There were 54 patients with gastric or duodenal ulcers in the NSAID group (21.7 percent) as compared with 57 in the control group (12.3 percent) (Table 5Table 5
Gastric Ulcers, Duodenal Ulcers, and Their Complications at Autopsy in the NSAID and Control Groups.*). This difference was explained by a significantly greater number of patients with gastric ulcers in the NSAID group (35 as compared with 27 patients in the control group). Gastric ulcers were slightly more prevalent in short-term NSAID users (19 patients, 17.0 percent) than in long-term users (9 patients, 12.2 percent) or those in the aspirin group (7 patients, 11.1 percent). In contrast, duodenal ulcers were more equally distributed between patients with and those without a history of the use of NSAIDs. There were 34 control patients (7.3 percent) and 26 NSAID users (10.4 percent) with duodenal ulcers.More NSAID users had two or more ulcers of the stomach and duodenum than control patients (21 vs. 14 patients, 8.4 percent vs. 3.0 percent; difference, 5.4 percent; 95 percent confidence interval, 2.1 to 8.7 percent; P<0.001). Death from perforation or hemorrhage was more frequent in the NSAID group (14 patients, 5.6 percent) than in the control group (12 patients, 2.6 percent).
Relation between Small-Bowel and Upper Gastrointestinal Lesions in the NSAID Group
There was no demonstrable association between NSAID-associated gastric and duodenal ulcers and lesions of the small intestine. Five of the 54 patients (9.3 percent) who used NSAIDs and had ulcers of the stomach or duodenum had nonspecific ulcers of the small intestine. The latter were present in 16 of 195 patients (8.2 percent) without ulcers of the stomach or duodenum.
Discussion
We studied the prevalence of gastrointestinal ulcers and their complications in a large number of patients at autopsy. The main limitation of the study was the inability to obtain information from the patients themselves about compliance and the use of drugs obtained without prescription (aspirin and ibuprofen can be purchased without a prescription in the United Kingdom). It could be argued, however, that the influences of the use of nonprescription drugs and noncompliance led to an underestimation of the risks of ulceration of the stomach and small intestine in patients taking NSAIDs. This argument is based on the belief that more patients in the NSAID population would have had ulcers if all had adhered to their prescribed drug regimens and that nonprescription NSAIDs might have caused some of the lesions in the control group.
Numerous epidemiologic and endoscopic studies have documented the risks of gastric and duodenal ulcers in patients taking NSAIDs.1 Gastric ulcers are more common than duodenal ulcers in such patients.2 , 24 We found that there was also an association between NSAID use and gastric ulcers in older patients with terminal illnesses. Although the prevalence of duodenal ulcers in the NSAID and control groups did not differ, the higher death rate from gastric and duodenal ulcers combined in the NSAID group was accounted for by a higher rate of complications due to duodenal ulcers. These findings, which are in agreement with those from a large case–control study,25 lend support to the view that NSAIDs increase the risk of complications from preexisting duodenal ulcers.
The main finding in this study was the higher prevalence of nonspecific ulcers of the small intestine in the NSAID group than in the control group. By convention the term "nonspecific ulcer" does not apply to patients with identifiable etiologic factors such as Crohn's disease, vasculitis, or infection.26 Focal ischemia27 and the use of slow-release potassium chloride tablets28 have been implicated in the development of nonspecific ulcers, but one large retrospective study failed to identify any predisposing factors in the great majority of cases.26 The higher prevalence of ulceration and perforation of the small intestine in our long-term NSAID group contrasted with the more frequent gastric ulceration in the short-term NSAID group. This finding may suggest that different pathophysiologic mechanisms underlie the development of gastric ulcers and ulcers of the small intestine in patients taking NSAIDs.
Techniques involving radionuclides and sugar permeability probes have been used to examine the integrity of the small-intestinal mucosa in patients taking NSAIDs.18 19 20 21 22 Bjarnason interpreted the results of his work and that of others as indicating that NSAID enteropathy occurs in approximately two thirds of patients taking NSAIDs regularly for at least six months.29 This enteropathy is thought to be characterized by intestinal inflammation, occult blood loss, and protein-losing enteropathy. Iron-deficiency anemia and occult blood loss in the feces are common clinical problems in patients with rheumatic diseases taking NSAIDs, and upper gastrointestinal endoscopy identifies a possible cause in only half these patients.30 , 31 The results of a recent enteroscopic study suggested that 66 percent of such patients have "red spots" or ulcers of the small intestine.23 Thus, the small intestine is a likely site of occult inflammation and blood loss in long-term users of NSAIDs. Our results support the view that long-term users of NSAIDs are at greater risk of damaging the small intestine than short-term users.29 The 14 percent prevalence of nonspecific ulcers in long-term users contrasts with the reported 70 percent prevalence of NSAID enteropathy in previous studies.20 , 21 , 29 This difference could be explained by the wider selection criteria used in this study. Alternatively, technical factors, such as mucosal autolysis, could have limited our ability to detect minor erosions in the small intestine.
In conclusion, we found an association between the use of NSAIDs and nonspecific ulceration of the small intestine. The majority of the lesions were subclinical, but some patients had serious complications due to their ulcers. Our findings, taken together with those of the case–control study of Langman et al.8 and the numerous reports of small-bowel complications in patients taking NSAIDs,9 10 11 12 13 14 15 lead us to propose that these drugs may be responsible for a large proportion of hitherto unexplained ulcers of the small intestine.
Supported by grants from Searle UK and the Greater Glasgow Health Board.
We are indebted to the medical and technical staff of the Departments of Pathology at the Western Infirmary and Gartnavel General Hospital, Glasgow, especially Professor R.N.M. MacSween, Dr. A. Mowat, and Dr. B. Michie; to Ms. E. Munro, Glasgow Procurator Fiscal Depute, and her staff; and to the Department of Forensic Medicine, University of Glasgow.
Source Information
From the Gastroenterology Unit (M.C.A., C.J.T., R.I.R.) and the Department of Pathology (A.G.H., F.D.L.), Royal Infirmary, Glasgow, Scotland. Address reprint requests to Dr. Allison at Royal Gwent Hospital, Newport, Gwent, NP9 2UB, United Kingdom.
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