Original Article
Familial Occurrence of Inflammatory Bowel Disease
Marianne Orholm, M.D., Pia Munkholm, M.D., Ebbe Langholz, M.D., Ole Haagen Nielsen, Thorkild I.A. S
rensen, and Vibeke Binder
N Engl J Med 1991; 324:84-88January 10, 1991
- Abstract
- Abstract
Background and Methods.
We assessed the familial occurrence of inflammatory bowel disease in Copenhagen County, where there has been a long-term interest in the epidemiology of such disorders. In 1987 we interviewed 662 patients in whom inflammatory bowel disease had been diagnosed before 1979, asking whether their first- and second-degree relatives had this disorder. Ninety-six percent of the patients (504 with ulcerative colitis and 133 with Crohn's disease) provided adequate information.
Results.
As compared with the general population, the first-degree relatives of the 637 patients with ulcerative colitis or Crohn's disease had a 10-fold increase in the risk of having the same disease as the patients, after standardization for age and sex. The risk of having the other of the two diseases was also increased, but less so, and the increase in the risk of having Crohn's disease was not significant in the relatives of patients with ulcerative colitis. The risk of ulcerative colitis in first-degree relatives of patients with ulcerative colitis appeared to be virtually independent of the generation to which the first-degree relative belonged and of the sex of the patient and the relative. The risk of ulcerative colitis in first-degree relatives tended to be higher if the disease had been diagnosed in the patient before the age of 50, but the risk seemed to be independent of the current age of the relatives. The prevalence of the same disease as that of the patient (either ulcerative colitis or Crohn's disease) among second-degree relatives was increased; the prevalence of the other disease was not increased.
Conclusions.
The 10-fold increase in the familial risk of ulcerative colitis and Crohn's disease strongly suggests that these disorders have a genetic cause. (N Engl J Med 1991;324:84–8.)
Media in This Article
Table 1
Sex- and Age-Specific Prevalence of Ulcerative Colitis and Crohn's Disease per 100,000 Inhabitants in the County of Copenhagen (January 1, 1988).Article Activity
- Article
THE origin and pathogenesis of inflammatory bowel disease remain an enigma. The reported increase in the incidence of Crohn's disease has been attributed to environmental factors, including bacterial or viral infection; however, no such factors have been proved to be of importance. Several immunologic abnormalities have been reported in relation to inflammatory bowel disease, but no consistent pattern has been found.1 A number of studies have demonstrated aggregation of cases of ulcerative colitis or Crohn's disease in families and of cases of both diseases in the same families,2 3 4 5 6 7 8 9 10 11 suggesting that patients share a genetic background. Perhaps because of differences in the selection of patients, study design, and diagnostic criteria, different patterns of occurrence of inflammatory bowel disease have been found among relatives of patients with these disorders.3 , 4
The goal of our study was to determine the prevalence and relative risk of inflammatory bowel disease in first- and second-degree relatives of patients with ulcerative colitis or Crohn's disease in a well-defined population, with sex and age taken into account.
Methods
Data Collection
The county of Copenhagen contains approximately 500,000 inhabitants, about 10 percent of the population of Denmark. The annual incidence of ulcerative colitis and Crohn's disease in this region was estimated for the years 1962 to 1978, and the prevalence rates were calculated as of December 31, 1978.12 Among the population of 1978, 662 patients with inflammatory bowel disease were alive on January 1, 1987. These patients served as probands in the present study. The majority were attending our outpatient clinic and department at Herlev Hospital. We obtained permission from other hospitals to contact the remaining patients with inflammatory bowel disease in connection with our investigation.
The diagnostic criteria for ulcerative colitis and Crohn's disease in the probands have been described previously.12 The diagnosis of ulcerative colitis was based on the presence of at least three of the following four criteria: a typical case history of diarrhea, stools containing blood and pus, or both, for more than one week or in repeated episodes; a typical sigmoidoscopic appearance, with granulated, friable mucosa, ulcerations, or both; histologic or cytologic signs of inflammation; and radiologic or colonoscopic signs of ulcerations with or without spiculation or granulation of the inner surface of the colon proximal to the rectum. The diagnosis of Crohn's disease was based on the presence of at least two of the following four criteria: a history of diarrhea lasting more than three months; radiologic findings, with typical stenoses and prestenotic dilatation in the small bowel or segments with a cobblestone appearance in the large bowel; histologic findings of transmural lymphocytic infiltration, occurrence of epithelial granulomas with giant cells of Langhans' type, or both; and the occurrence of fistulas or abscesses, or both, in a region of intestinal involvement. Before a diagnosis of either ulcerative colitis or Crohn's disease could be made, infectious and neoplastic diseases had to be ruled out.
The differential diagnosis was difficult in a few cases. In 10 patients in whom the criteria for ulcerative colitis had been met in 1978, the diagnosis was later changed to Crohn's disease, and in 3 patients originally considered to have Crohn's disease, the diagnosis was changed to ulcerative colitis. The diagnoses presented in this study were those made in 1987 — i.e., the conclusions reached after at least nine years of observation.
We did not obtain data on the families of patients with inflammatory bowel disease who died between 1978 and 1987. We have previously reported that the mortality rate of patients with inflammatory bowel disease does not differ from that expected in the background population.13 , 14 The majority of patients died of common, age-related diseases rather than inflammatory bowel disease. Furthermore, other studies15 have not found any correlation between familial occurrence and severity of the disease in probands.
A letter explaining the study and a questionnaire were mailed to each patient. The questionnaire requested a complete family history, including the number, year of birth (and death), and sex of first-degree relatives and the number, sex, and relationship of second-degree relatives. The patients were also asked to identify family members with inflammatory bowel disease. If there were any problems in the interpretation of the replies, follow-up telephone calls were made (to about 80 percent of all patients) to ensure that the family tree was accurate. All patients who stated that actual or possible inflammatory bowel disease was present in one or more family members were called. The names and dates of birth of the affected family members were obtained, and the diagnosis was confirmed or excluded by applying the criteria mentioned above to medical records from hospitals or private physicians.
Patients who refused to participate, who did not answer the letters or telephone calls, or who were mentally incompetent were excluded from subsequent analyses.
Statistical Analysis
The prevalence of ulcerative colitis and Crohn's disease among first- and second-degree relatives was estimated by dividing the number of relatives with either disease by the number of first- and second-degree relatives, respectively. The 95 percent confidence limits of the prevalence ratios were estimated according to the assumption that the number of cases followed a Poisson distribution.
The risk of familial occurrence was assessed by estimating the population relative risk of the disease in specified groups of relatives.16 This risk is calculated according to the following equation:
Since the prevalence of the diseases depends on sex and age (Table 1Table 1
Sex- and Age-Specific Prevalence of Ulcerative Colitis and Crohn's Disease per 100,000 Inhabitants in the County of Copenhagen (January 1, 1988).), the value of the denominator was adjusted according to the distribution of sex and age in the group of relatives studied (first-degree relatives only, because the ages of the second-degree relatives were unknown). Hence, this standardized population relative risk was estimated by dividing the observed number of affected first-degree relatives by the number expected according to the prevalence rates in the population. The expected number was calculated by adding the products of the current sex- and age-specific rates and the number of relatives within each corresponding sex—age category. The 95 percent confidence limits of the population relative risk were estimated according to the assumption that the number of cases among the relatives followed a Poisson distribution.The adjusted population relative risk of ulcerative colitis and that of Crohn's disease were estimated separately for the relatives of probands with ulcerative colitis and those of probands with Crohn's disease. In the analysis of probands with ulcerative colitis, the number of first-degree relatives with ulcerative colitis was great enough to allow estimation of the population relative risk for the relatives of each generation (parents, siblings, and children), for the four sex categories among probands and relatives, for specific age intervals at diagnosis of the disease among the probands, for specific age intervals of ascertainment among the relatives, and for the additional first-degree relatives of probands with at least one affected relative.
Since some of the relatives were dead at the time of the study, the standardized population relative risk was estimated according to the assumption that there had been no major secular trends in the prevalence of the diseases. To evaluate this assumption, the population relative risk was also estimated after all dead relatives were excluded.
Probands who appeared to be relatives of other probands were retained in the study because they had been identified through screening of the total population rather than through their relationship to another proband.
Results
Adequate information was obtained from 637 of the 662 patients in the study group (96 percent). Of the 504 patients with ulcerative colitis, 285 (57 percent) were women 18 to 90 years old (mean, 48) and 219 were men 19 to 89 years old (mean, 52); their median duration of disease was 16 years (range, 9 to 49). Of the 133 patients with Crohn's disease, 86 (65 percent) were women 20 to 80 years old (mean, 47) and 47 were men 18 to 84 years old (mean, 47); the median duration of disease was 14 years (range, 9 to 44).
Table 2Table 2
Family History of Inflammatory Bowel Disease among 637 Patients. shows the total number of first- and second-degree relatives, the number of probands who had first-degree relatives with ulcerative colitis or Crohn's disease, the number of probands with second-degree relatives with either disease, and the number of affected relatives. A total of 60 probands had relatives with inflammatory bowel disease.Some of the probands had more than one relative with inflammatory bowel disease. Fourteen of the probands with ulcerative colitis and two of those with Crohn's disease each had two relatives with inflammatory bowel disease. Two of the probands with ulcerative colitis and one of those with Crohn's disease had three relatives who were affected. One proband with ulcerative colitis had four relatives with ulcerative colitis. Six of the probands with ulcerative colitis and two of those with Crohn's disease had both first- and second-degree relatives who were affected.
Some of the affected relatives were also probands. Three probands — one with Crohn's disease and two with ulcerative colitis — belonged to one family, in which there was another relative with ulcerative colitis. Three probands with ulcerative colitis made up one family, and 12 others with this disease belonged to six families. Hence, the 60 probands belonged to 50 different families.
Fifteen of the 504 probands with ulcerative colitis and 2 of the 133 with Crohn's disease were twins. None of the pairs of twins, two of which were monozygotic, were concordant for inflammatory bowel disease.
The prevalence of ulcerative colitis and Crohn's disease among the relatives is shown in Table 3Table 3
Prevalence of Ulcerative Colitis and Crohn's Disease per 100,000 Persons among First- and Second-Degree Relatives.*. As compared with the prevalence rates in the background population, the rates of ulcerative colitis and Crohn's disease among first-degree relatives of the probands with ulcerative colitis were increased by factors of 9.5 and 1.8, respectively, and the rates of Crohn's disease and ulcerative colitis among first-degree relatives of the probands with Crohn's disease were increased by factors of 10.3 and 4.4, respectively. The prevalence rates of ulcerative colitis and Crohn's disease among second-degree relatives of probands with the same disease as these relatives were also increased, whereas the prevalence rates of disease among second-degree relatives with disease different from that of the probands were lower than in the background population. However, the 95 percent confidence limits of the prevalence rates overlapped the rates in the population (Table 3).Since the prevalence of the diseases depends on sex and age (Table 1), a sex- and age-standardized population relative risk was estimated for first-degree relatives (Table 4Table 4
Sex- and Age-Standardized Risk of Inflammatory Bowel Disease among First-Degree Relatives of Probands with Inflammatory Bowel Disease, Relative to the Population Risk.). The population relative risk for concordant disease was about 10, whereas that for discordant disease was elevated only slightly, and not significantly so with regard to Crohn's disease among relatives of probands with ulcerative colitis.A total of 883 first-degree relatives (24 percent) died before the survey; 84 percent had died within the preceding 40 years. When the dead relatives were excluded from analysis, there were no appreciable differences in the estimated population relative risks (Table 4).
Table 5Table 5
Effect of Selected Variables on the Population Relative Risk of Ulcerative Colitis among First-Degree Relatives of Probands with Ulcerative Colitis. shows that the population relative risk of ulcerative colitis among first-degree relatives of probands with ulcerative colitis was similar in the three generations. The sex of the probands and relatives did not influence the risk. The relative risk of disease in a proband's relatives varied with the proband's age at diagnosis, but not with the relatives' age. There was a tendency for the risk to be higher among relatives of probands in whom the disease was diagnosed before 50 years of age, whereas there was no consistent pattern in the variation of the risk among relatives of different ages at the time of the survey.When the population relative risk of ulcerative colitis was assessed among additional first-degree relatives of probands with at least one affected relative, 6 of 179 other first-degree relatives were found to have the disease. The expected number in this group after adjustment for sex and age was 0.33, giving a population relative risk of 18.1 (95 percent confidence limits, 6.7 and 39.5).
Discussion
The main findings of this study were that first-degree relatives of patients with ulcerative colitis or Crohn's disease, as compared with the general population, have a 10-fold increase in the risk of having the same disease as the patient. The risk of having the other of the two diseases was also increased, but less so and not significantly so for Crohn's disease among relatives of patients with ulcerative colitis.
The results of surveys of the familial occurrence of inflammatory bowel disease may be influenced by limitations of data collection. In designing our study, we tried to avoid the most important sources of bias.3 , 10 , 17 The study was based on an unselected, regionally defined, relatively large group of thoroughly characterized patients12 , 18 followed over a period of at least nine years. Simultaneous epidemiologic studies conducted in the same area that involved about 10 percent of the total Danish population have yielded prevalence rates for this back-ground population,19 , 20 making it possible to calculate the sex- and age-standardized population relative risk among our probands' relatives.
We achieved a response rate of 96 percent. In studies with a lower response rate,11 , 17 , 21 it is conceivable that a lower rate of familial occurrence among persons not responding may have contributed to the higher rates of familial occurrence in those studied.
A more difficult problem would result from bias in the information provided by the probands, particularly bias due to a failure to report existing inflammatory bowel disease.17 Our procedures for interviewing and verification were intended to minimize these problems.
As expected, we found that the prevalence of inflammatory bowel disease, especially that of discordant disease, in second-degree relatives was lower than in the first-degree relatives (Table 3). Although we were unable to estimate the sex- and age-standardized population relative risk, we suspect that the number of affected second-degree relatives was somewhat under-reported.
The frequency of a family history of inflammatory bowel disease varies in the literature, from 6 to 33 percent.3 , 4 Comparing studies may require that the familial risk be expressed in terms of sex- and age-standardized population relative risk.16
It has been claimed by several authors3 , 5 , 21 22 23 that the prevalence of familial Crohn's disease tends to be greater than that of ulcerative colitis. However, we found almost the same relative risk for the two diseases, as did Monsén et al. for ulcerative colitis10 and Mayberry et al. for Crohn's disease.7
Many studies have reported that siblings have a higher incidence of inflammatory bowel disease than other first-degree relatives.3 , 7 , 9 , 10 , 22 In the present study, there was no significant difference in the relative risk among parents, siblings, and children. Such comparisons are particularly sensitive to standardization according to the age of the relative. One study,21 using another kind of correction for age, found that the risk of inflammatory bowel disease among children was higher than among their parents and equal to that among their siblings.
We did not find any relation between familial risk and the sex of the probands or their relatives. Previous studies15 , 16 have shown that a similar percentage of male and female probands had relatives with inflammatory bowel disease.
It has been reported that familial occurrence of inflammatory bowel disease is more frequent among patients with early onset of disease.10 , 17 We found that among patients with ulcerative colitis, being 50 years old or younger at diagnosis did not influence the familial risk. Being older at diagnosis was associated with a lower familial risk, but the numbers of subjects were small.
In families in which one first-degree relative was affected, the population relative risk among the remaining relatives in those families was somewhat higher than in the group of relatives taken together. This may suggest that an increased load of the etiologic factors is responsible for familial occurrence. However, the confidence limits of the relative risk over-lapped the estimates for the total group of relatives. It is also possible that the presence of two cases in a family increased the awareness of the disease.
Familial occurrence of inflammatory bowel disease might be due to genetic factors as well as to a shared environment. There have been only a few reports of affected, unrelated members of families and households, such as spouses and adopted children,24 but there have been no thorough studies using modern epidemiologic techniques. A study of twins23 has suggested that there is a strong genetic contribution to Crohn's disease but not to ulcerative colitis. However, the number of affected pairs of twins was too small to confirm this suggestion in relation to either disease. Theoretically, a shared environment will produce relative-risk ratios of the magnitude observed here only under rather unlikely, extreme conditions.25 However, proper assessment of this question requires either large studies of separated family members or identification of gene markers.
We are indebted to Dr. J
rgen Hilden (Institute of Human Genetics, University of Copenhagen) for helpful comments on the paper.Source Information
Dr.MeD.Sc.i.
Dr.MeD.Sc.i.
Dr.MeD.Sc.i.
From the Medical Gastroenterologic Department C, Herlev Hospital, University of Copenhagen, Herlev, Denmark. Address reprint requests to Dr. Orholm at the Department of Infectious Diseases 7721, Rigshospitalet, Tagensvej 20, DK-2200 Copenhagen N, Denmark.
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