Original Article
Intrafamilial Clustering of Helicobacter pylori Infection
N Engl J Med 1990; 322:359-363February 8, 1990
- Abstract
- Abstract
Colonization of the gastric antrum by Helicobacter pylori (formerly Campylobacter pylori) has been associated with primary gastritis. We determined the frequency of colonization by H. pylori in gastric-antrum biopsy specimens from 93 children undergoing gastroscopy for the evaluation of upper gastrointestinal symptoms. We also determined H. pylori IgG antibody levels by enzyme-linked immunosorbent assay in coded serum samples from these children, family members, and control subjects of comparable ages.
Among 27 children with primary, or unexplained, gastritis, H. pylori was identified by silver staining in 24 biopsy specimens and by culture in 22; specific antibodies were present in 23 children (96 percent). Three children with unexplained gastritis had no evidence of H. pylori in the antrum, nor did any of 13 children with secondary gastritis or any of 53 children with normal antral histologic features; specific antibodies were present in only 1 of these 69 children. H. pylori antibody was detected in 25 of 34 parents of colonized children, but in only 8 of 33 parents of noncolonized children (P<0.001). Of 22 siblings of children colonized by H. pylori, 18 had specific antibodies, as compared with only 5 of 37 controls (P<0.001).
We conclude that H. pylori—specific IgG antibodies are associated with bacterial colonization of the gastric antrum by this organism. The intrafamilial clustering of H. pylori infection suggests that there may be person-to-person spread of these bacteria. (N Engl J Med 1990; 322:359–63.)
Media in This Article
Table 1
Findings in 93 Children Who Underwent Upper Gastrointestinal Endoscopy and Mucosal Biopsy.*Table 2
Presence of Positive H. pylori—Specific IgG Antibody and Mean Specific IgG Levels in Parents of Children Who Underwent Upper Endoscopy.*Article Activity
- Article
IN the past five years numerous studies have reported an association between the presence of spiral-shaped, gram-negative bacteria, now referred to as Helicobacter pylori and previously as Campylobacter pylori,1 on the surface of the gastric mucosa and histologic evidence of antral inflammation.2 The presence of these organisms is associated with primary gastritis; H. pylori is not found in association with either secondary causes of gastritis or normal antral mucosa.3 Currently, there is little information available on the epidemiology of infection with H. pylori. Two groups have reported opposite conclusions about whether the organisms may be spread by close personal contact within families.4 , 5
Several studies have demonstrated the presence of specific H. pylori antibodies in human serum. These antibodies are uncommon in children, but their prevalence appears to increase with advancing age.6 , 7 Approximately 50 percent of persons over 60 years of age are seropositive. In adults, a strong correlation is found between the presence of H. pylori gastritis and a positive serologic response to the organism.7 , 8 As H. pylori—associated gastritis is uncommon among children in Toronto,3 we decided that studies of the serologic response to H. pylori among children and their immediate family members would provide information about the potential for the intrafamilial spread of these bacteria. We therefore examined specific H. pylori IgG antibody titers by enzyme-linked immunosorbent assay (ELISA) on coded serum samples that were obtained prospectively from children undergoing upper gastrointestinal endoscopy. Serum samples were also obtained from the parents of children with gastritis and from the siblings over the age of six of subjects with H. pylori—associated gastritis.
Methods
Two antral biopsies were performed in all children undergoing diagnostic upper endoscopy for the evaluation of symptoms referable to the upper gastrointestinal tract, irrespective of the endoscopic findings. Endoscopies were performed with Olympus GIF Q-10 or XP-10 gastroscopes (Carsen Medical and Scientific, Markham, Ont.) either under general anesthesia or after sedation with intravenous meperidine and diazepam. Informed parental consent was obtained for all endoscopies and mucosal biopsies.
Histologic Procedures
Biopsy specimens were evaluated as previously described.3 , 9 Briefly, one antral-biopsy specimen was fixed in formalin, sectioned, and stained with hematoxylin and eosin. The presence of gastritis was determined as previously described,3 , 9 with the use of established criteria.10 Gastritis was defined as secondary if a cause for the inflammation could be clearly identified (e.g., gastroduodenal Crohn's disease). Sections were subsequently stained with silver to identify campylobacter-like organisms.
Culture of H. pylori
A second antral biopsy specimen was placed in a sterile container without transport medium and immediately taken to the microbiology laboratory. The culture of biopsy tissue was performed as previously described.3 Briefly, the mucosal tissue was ground with a pestle and inoculated onto three agar plates that were then incubated at 37°C under reduced oxygen tension for up to seven days. Organisms were identified as H. pylori if they were gram-negative, showed a characteristic spiral shape on phase-contrast microscopy, had urease, oxidase, and catalase activity, but not hippurase and nitrate reductase activity, and were susceptible to cephalothin and resistant to nalidixic acid.11
Serologic Studies
We studied serum samples from a total of 219 people, including 93 children who underwent esophagogastroduodenoscopy and mucosal biopsy. A sample of 0.5 ml of whole blood was collected from these children when venipuncture was performed for routine blood work before the procedures. Ten patients, seven with H. pylori—associated antral gastritis and three with secondary gastritis, were discussed in a previous report.3 Venipuncture was also performed in 67 consenting parents, and blood was obtained from 22 siblings over the age of six of children who were colonized by H. pylori. The study was reviewed and approved by the Human Subjects Review Committee of the Hospital for Sick Children. The committee decided that serum samples should not be obtained from children under seven or from the siblings of children who were not colonized by H. pylori.
To evaluate serologic responses in a young control population, serum samples were collected on two separate days from 25 children, of comparable ages to the younger siblings, who underwent venipuncture for blood typing. The samples were collected sequentially, without other inclusion or exclusion criteria. Further clinical information about these 25 inpatients (14 boys and 11 girls) was obtained retrospectively. Eleven had preoperative blood work performed for nonintestinal illnesses. Underlying medical conditions in 10 others included hyperlipidemia (2 children), multiple trauma (2), chronic renal failure (2), and one case each of hepatitis, adult respiratory distress syndrome, thalassemia, and upper gastrointestinal tract hemorrhage. Four patients were receiving chemotherapeutic agents for the treatment of neoplasias. Twelve additional samples were obtained from healthy young adult volunteers (18 to 29 years old) of comparable ages to the older siblings (samples kindly provided by Dr. P. Durie, the Hospital for Sick Children). Serum samples were stored in cryovials at −70°C. Each sample was identified by a code number, and the code was not broken until all the H. pylori—specific antibody assays were completed.
The ELISA used to detect the presence of H. pylori—specific IgG antibodies in serum was performed as described previously.7 , 8 Five H. pylori strains originally isolated from U.S. patients were disrupted by sonication. After centrifugation, the supernatants were pooled and plated in 0.05 M carbonate buffer (pH 9.6) onto flat-bottomed microtiter wells (Immulon-2, Dynatech Laboratories, Alexandria, Va.) as test antigen.7 Serum samples obtained from 40 healthy U.S. children between six months and nine years of age had previously been used to establish normal values for optical-density readings in the ELISA.7 The samples included preimmune serum from 15 healthy children enrolled in the trial of a vaccine and 25 children with minor medical problems. Coded samples from Toronto were considered positive if the optical density of the serum (tested at a dilution of 1:800) showed the presence of H. pylori IgG antibodies at levels more than 3 standard deviations above the mean value obtained in the serum samples from U.S. children. Antibody levels are expressed here as a ratio of the 3-SD cutoff value, which was considered to be an antibody level of 1.0. All assays were performed in duplicate on at least two separate days with positive and negative internal controls. Correction for deviations in the results for reference serum samples was used to control for day-to-day variability.7
Statistical Analysis
Results are expressed as means ±SD. The two-tailed, unpaired Student t-test12 was used to compare differences in mean values between groups. A two-tailed Fisher exact test12 was performed to determine the significance of differences in the categories defined by the presence or absence of findings.
Results
Patient Studies
During the period of this study, serum samples were collected prospectively from 93 children who underwent upper gastrointestinal endoscopy and mucosal biopsy. Fifty-three children (57 percent) had normal histologic features, and 40 (43 percent) had antral gastritis. Thirteen children had an identifiable (i.e., secondary) cause for the gastric inflammation. In 11 of the 13 a diagnosis of gastroduodenal Crohn's disease was established by the presence of a noncaseating granuloma in the gastroduodenal mucosa or by the presence of mucosal inflammation characteristic of Crohn's disease elsewhere in the intestinal tract.13 Two patients had eosinophilic infiltrates in the gastric mucosa consistent with eosinophilic gastroenteritis.14 In the other 27 children with gastritis there was no apparent underlying cause for the antral inflammation. They were therefore classified as having primary or unexplained gastritis. It is possible that in some of these subjects the gastritis had an identifiable (i.e., secondary) cause that was not apparent in the history or on endoscopic, histologic, and ancillary laboratory investigations. In 13 of these 27 children a duodenal ulcer was also identified on endoscopy. The mean ages of the children with primary gastritis, secondary gastritis, or normal antral histologic features were similar (Table 1Table 1
Findings in 93 Children Who Underwent Upper Gastrointestinal Endoscopy and Mucosal Biopsy.*). Twenty-one of the 27 children with primary gastritis (78 percent) were boys, whereas those with normal antral histologic features were equally divided between boys and girls.After silver staining, spiral-shaped organisms resembling H. pylori morphologically were identified in the samples from 24 of 27 children with primary gastritis (89 percent). H. pylori was cultured from antral-biopsy specimens in 22 of these 24 children. H. pylori was not demonstrated by either culture or silver staining in any of the 53 children with normal antral histologic features or in the biopsy specimens of the 13 children with secondary gastritis (Table 1).
The H. pylori—specific IgG antibody titer was positive (i.e., more than 3 SD above the mean for U.S. children) in 23 of 24 children with primary gastritis and H. pylori colonization of the antrum (96 percent). The mean antibody level in the 13 children with associated duodenal ulcers (ratio, 1.78) was not significantly different from that in children with H. pylori-associated gastritis but no ulcer (ratio, 2.04; P = 0.27). Tests for antibody to H. pylori were negative in the three children with primary gastritis in whom organisms were not identified by either silver staining or culture of the antral mucosa. All 13 children with secondary gastritis were negative for H. pylori IgG antibody. Only 1 of the 53 children with normal antral histologic features was positive for H. pylori IgG antibody on ELISA. As shown in Table 1, the mean H. pylori—specific IgG antibody levels were lower in both the children with secondary gastritis (P<0.001) and those with normal antral histologic features (P<0.001) than in the children with primary gastritis. The differences between the low specific IgG levels in children with secondary gastritis and those with normal antral mucosa were not significant (P = 0.30).
Family Studies
Sixty-seven parents of children who underwent endoscopy provided blood for this study (Table 2Table 2
Presence of Positive H. pylori—Specific IgG Antibody and Mean Specific IgG Levels in Parents of Children Who Underwent Upper Endoscopy.*). Serum was obtained from 34 parents of children who had H. pylori colonization of the antrum. They included 14 couples (i.e., both the mother and father provided blood) and 6 single parents (i.e., only the mother or father underwent venipuncture). Serum was also collected from 33 parents of children who did not have evidence of H. pylori infection (13 couples and 7 single parents). The ages of the 34 parents of children with H. pylori—associated gastritis (42.8±5.8 years) were similar to those of the 33 parents whose children were not colonized by this organism (40.2±5.3 years).Twenty-five of the 34 parents of children who were colonized by H. pylori (74 percent) had H. pylori IgG antibodies in serum, as compared with only 8 of the 33 parents of children who were not colonized by H. pylori (24 percent) (P<0.001). There was also a marked difference in H. pylori antibody levels between the two groups of parents (P<0.001) (Table 2).
The serologic responses among parents were also analyzed separately for fathers and mothers (Table 2). Among fathers of H. pylori—positive and H. pylori—negative children, the numbers with positive serologic results (10 of 16 vs. 6 of 16; P>0.05) and H. pylori—specific IgG levels (ratio, 1.29±0.98 vs. 0.95±1.20; P>0.05) were similar. In contrast, the number of mothers of colonized children with a positive serologic response to H. pylori (15 of 18, 83 percent) was significantly higher than the number of mothers of H. pylori—negative children (2 of 17, 12 percent; P<0.001). There was also a significant difference in H. pylori—specific IgG levels between the two groups of mothers (1.61 ±0.80 vs. 0.47±0.67; P<0.001), although they were of similar ages.
Of the 14 couples examined who were parents of children colonized by H. pylori, both parents were positive for H. pylori—specific IgG antibody in eight cases. In four cases, a single parent had positive serologic results. Neither parent had a positive serologic response in only two couples.
Serum was also obtained from 22 siblings of 20 patients with H. pylori—associated gastritis (Table 3Table 3
Presence of Positive H. pylori—Specific IgG Antibody and IgG Levels among the Siblings over Six Years Old of Children with Documented H. pylori—Associated Gastritis.*). This number included all the siblings who were over six years of age in 15 of the 20 families. Remarkably, 18 of the 22 siblings (82 percent) had positive serologic results for H. pylori. This contrasts with the virtual absence of a positive H. pylori serologic response among the children with normal antral histologic features (1 of 53, 2 percent) and the low prevalence of specific antibody among the Toronto children and young adults of similar ages (5 of 37, 14 percent). The mean H. pylori—specific IgG level was significantly higher for the siblings (1.3±0.63) than for either the children who did not have H. pylori colonization of the antrum (0.16±0.25; P<0.001) or the Toronto comparison group (0.43±0.67; P<0.001). The antibody levels detected in the siblings (1.38± 0.63) were similar to those in the children with documented H. pylori colonization of the gastric mucosa (1.71±0.76; P>0.05).Discussion
Numerous reports have confirmed an association between the presence of H. pylori on the gastric antrum and chronic antral gastritis.2 The organisms appear to cause gastritis because they are specifically found in association with primary, or unexplained, gastritis,3 , 9 because clearing of H. pylori results in the healing of associated gastric inflammation,15 , 16 and because challenge of both laboratory animals17 and humans18 , 19 results in gastritis. Research on the epidemiology of H. pylori infections has been greatly hampered by the fact that no serotyping system exists with which to characterize H. pylori isolates.11 Using an ELISA to document specific IgG systemic antibodies, we produced data showing an excellent correlation between serologic evidence of H. pylori infection and the demonstration of this infection by microbiologic and histopathological methods.
As defined in this study, a positive serologic response to H. pylori was both an extremely sensitive (96 percent) and a highly specific (99 percent) marker of H. pylori—associated antral gastritis. Both the positive predictive value (96 percent; 23 of 24) and the negative predictive value (99 percent; 68 of 69) we obtained using coded serum samples in this ELISA were high. Our findings therefore indicate that measuring H. pylori—specific IgG serologic responses can serve as a useful screening test in children and can be employed in both clinical and epidemiologic studies. In adults the presence of H. pylori IgG antibodies also correlates with bacterial colonization of the antrum.20 21 22 23
The absence of a serologic response to H. pylori among children with gastritis due to secondary causes supports our previous findings that gastric inflammation does not in itself predispose people to colonization by H. pylori.3 , 9 Although positive serologic results correlated well with histologic and microbiologic evidence of H. pylori—associated gastritis, the ELISA did not differentiate between the subjects with endoscopically proved duodenal ulcers and those without mucosal ulceration. The overlap in antibody levels as measured with the use of this ELISA indicates that diagnostic considerations and treatment in an individual patient cannot be determined with the ELISA alone. We16 and others24 have shown previously that medical therapy directed at clearing the H. pylori colonization and healing the associated antral inflammation is most effective for symptomatic improvement among subjects with associated duodenal ulcers. Among symptomatic persons of any age, the combination of upper endoscopy and mucosal biopsy therefore remains an important diagnostic tool.
Concerns have been raised previously about the potential for cross-reactivity between the antigens of H. pylori and those of intestinal campylobacters.22 , 25 For example, Lee et al.26 showed that there is cross-reaction between the flagellin subunits of flagella extracted from H. pylori and flagellins derived from C. jejuni and C. coli. However, other surface antigens on H. pylori strains are distinct from those expressed by intestinal campylobacters.26 , 27 In addition, although the incidence of C. jejuni and C. coli infections is higher in children than adults,28 false positive results were not a complicating factor in the ELISA employed in both this and a previous study.7
Other noninvasive tests, such as the [13C]urea breath test, have also been reported to be specific and sensitive diagnostic methods.29 These noninvasive assays will probably serve as complementary diagnostic tools. For example, breath tests are well suited to follow the clearing of H. pylori colonization of the antrum in response to medical therapy. In contrast, less costly serologic assays, including the ELISA, appear better suited to epidemiologic surveys and the assessment of persons without access to centers with facilities for stable-radioisotope assays and endoscopy.
North American children represent an excellent group in which to study the epidemiology of H. pylori because, in contrast to adults, children are infrequently colonized by the organism.3 , 5 , 7 Therefore, the finding in the present study that most siblings of the children with H. pylori colonization also had positive serologic responses provides evidence in support of intrafamilial spread of the organism. The prevalence of a positive H. pylori serologic response (>80 percent) among the siblings of children with H. pylori infection was higher than observed previously in any Western population, irrespective of age.6 , 7 , 30 , 31 For further comparisons, serum from the siblings of children with normal antral histologic features and H. pylori—negative gastritis would have been optimal. Because of ethical considerations, we restricted our evaluation of the serologic response to H. pylori to children who required a venipuncture for clinical reasons. Our results in this comparison group from the same hospital that served the patients and their siblings parallel those of previous studies showing a low prevalence of a systemic immune response to H. pylori among young populations in North America7 and Europe.6 , 30 , 31
Further evidence for the intrafamilial clustering of H. pylori is provided by the finding that parents of H. pylori—positive children were more likely to have a positive serologic response than the comparably aged parents of noncolonized children. This difference in colonization between the two groups of parents was due to a marked difference in the number of mothers with a positive serologic response in the two groups. The reasons for the strong association between infection in the mothers and H. pylori colonization of the antrum in their children are not clear, although person-to-person transmission is possible.
In summary, this study has demonstrated that the detection of H. pylori—specific IgG systemic antibody serves as a sensitive and specific test in screening for H. pylori colonization in children. Using an ELISA, we showed that there is marked intrafamilial clustering of H. pylori infection. Further studies are needed to determine whether H. pylori isolates from members of a single family have identical characteristics.
Supported in part by the Medical Service of the Department of Veterans Affairs and by Procter & Gamble. Dr. Sherman is the recipient of a Career Scientist Award from the Ontario Ministry of Health.
Presented at the 1989 annual meeting of the American Gastroenterological Association, Washington, D.C, and published in abstract form (Gastroenterology 1989; 96:Suppl:A130).
In accordance with the Journal's policy, Drs. Blaser and Perez-Perez state that they have applied for a patent on the serologic technique described in this report.
We are indebted to Drs. M. Karmali and E. Cutz for their continuing support.
Source Information
From the Division of Gastroenterology, Departments of Pediatrics and Microbiology, Research Institute, the Hospital for Sick Children, University of Toronto, Toronto (B.D., P.M.S.), and the Infectious Diseases Section, Veterans Affairs Medical Center, Denver (G.I.P.-P., M.J.B.). Address reprint requests to Dr. Sherman at the Division of Gastroenterology (Rm. 1448), the Hospital for Sick Children, 555 University Ave., Toronto, ON M5G 1X8, Canada.
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