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Mobley HLT, Mendz GL, Hazell SL, editors. Helicobacter pylori: Physiology and Genetics. Washington (DC): ASM Press; 2001.

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Helicobacter pylori: Physiology and Genetics.

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Chapter 2Epidemiology of Infection


School of Microbiology and Immunology, The University of New South Wales, Sydney, 2052, Australia

In 1982 when Barry Marshall and Robyn Warren first isolated the gastric pathogen Campylobacter pyloridis, few if any gastroenterologists would have predicted that almost 20 years later, this bacterium would have been shown to be one of the most common bacterial infections in humans and the etiologic agent of the majority of upper gastroduodenal disease. Today, Helicobacter pylori, as it is now known, is firmly established as the etiologic agent of acute or chronic gastritis and a predisposing factor in peptic ulcer disease, gastric carcinoma, and B-cell mucosa-associated lymphoid tissue (MALT) lymphoma (47, 59, 87, 111).

Although over the past 18 years many important questions relating to the epidemiology of H. pylori have been defined, a number of issues, including the route of transmission of H. pylori, remain controversial. This chapter aims not only to provide the reader with the most recent data in regard to the epidemiology of H. pylori but also to review current areas of controversy.

Prevalence of Infection

H. pylori infection is ubiquitous and infects both males and females (42, 78, 90, 99, 150). Although infection occurs worldwide, there are significant differences in the prevalence of infection both within and between countries (42, 78, 90, 99, 150). In general, the overall prevalence of H. pylori infection in developed countries is lower than that in developing countries (9, 45, 99, 114). This difference in prevalence of infection has been attributed to the rate of acquisition of H. pylori in childhood (99). For example, in a study conducted in southern China, the overall prevalence of H. pylori infection in Chinese subjects was shown to be significantly higher than that in Australians (44.2 versus 21%). Examination of the data for age-related prevalence showed that this difference related to the rate of acquisition of H. pylori under the age of 10 years; the prevalence of infection in Australian children is 4% in comparison with 27% in Chinese children. Over the age of 10 years, however, the rate of acquisition of infection in both countries was similar (approximately 1% per annum) (99). Epidemiological data from other developed and developing countries support this finding, with the prevalence of H. pylori infection in children under 10 years resident in developed countries being approximately 0 to 5% compared with 13 to 60% in children resident in developing countries. Over this age an increase in prevalence in the order of 0.5 to 2% per annum is commonly observed (2, 45, 60, 90, 114). It has been proposed that the increasing prevalence of H. pylori from younger to older subjects reflects the passage through the population of distinct cohorts. That is, all persons are infected in childhood and the decreased levels of H. pylori infection associated with younger age groups, particularly in developed countries, are due to gradual improvements in medical care, sanitation, and/or living conditions (8, 23, 121, 133). In contrast to this view, a number of studies have argued that there is a continuous risk of acquisition of H. pylori of approximately 1% per year in adulthood (24, 143). Clarification of this issue will require large cohort studies that monitor the H. pylori status of approximately 1,000 subjects over a 5-year period. Given an acquisition rate of 0.5 to 2% per annum, at the end of this period it would be expected that 25 to 100 subjects would have seroconverted (92).

Natural History of Infection

Natural acquisition of H. pylori infection occurs, for the most part, in childhood. Once established within the gastric mucosa, the bacterium persists for life. Studies in children suggest, however, that in the early years of life prior to the establishment of infection, transient infection with H. pylori may be common. This is evidenced both by prevalence studies and a number of follow-up studies that have monitored H. pylori prevalence in the same children over a number of years (18, 49, 64, 82, 120, 137). One of the first studies to suggest that loss of infection may occur in children was by Klein et al., who showed that 6-month-old Peruvian children monitored for their H. pylori status at 6-month intervals over a 2-year period had an overall probability of acquiring H. pylori of between 0.28 and 0.38, and a probability of clearing the infection of between 0.22 and 0.45 in a given 6-month period (64). Similar findings have been reported by Granstrom et al., who monitored the prevalence of H. pylori infection in 294 Swedish children at the ages of 6, 8, 10, and 18 months and 2, 4, and 11 years. This study showed that while at 2 years 10% of children were H. pylori positive, by 11 years of age only 3% of children remained seropositive (49). Although the above studies clearly demonstrate loss of H. pylori infection in children, unfortunately neither study controlled for antibiotic usage, a factor that clearly may affect H. pylori status. Consumption of antibiotics was, however, taken into consideration in a 2-year follow-up study of 48 H. pylori-positive Italian children in whom H. pylori status was monitored by the [13C]urea breath test at 6-month intervals over a 2-year period. In this study, 40 of the children were shown to remain persistently positive for H. pylori despite the fact that 10 had been treated for concomitant infections with a short course of antibiotics. The remaining eight children were found to be negative for H. pylori after 2 years and, of these, two had been given antibiotics for concomitant infections (116).

Further indirect evidence for spontaneous clearance of infection in children has come from a recent seroprevalence study of 365 primary school children aged 4 to 7 years from a low-income United States–Mexico border community. This study showed a sequential falloff in H. pylori prevalence from 36% in 4-year-olds to 24% in 5-year-olds, to 20% in 6-year-olds to 14% in 7-year-olds (120). The authors of the study concluded that the downward trend in prevalence observed in these children suggests that transient infection might be common in young children.

Interestingly, in a recent study by Malaty et al. (82), acquisition and loss of infection were shown to differ in children who, although matched for socio-economic class, were from different racial backgrounds. In this large 12-year serological follow-up study, Malaty et al. found the rate of acquisition of infection among African American children to be four times higher than that among Caucasian children. Loss of infection over the 12-year period was shown to be significantly higher (50%) among Caucasian children as compared with African American (4%), with the latter group either remaining infected or becoming reinfected (82).

Thus, based on current evidence, it appears that in the early years of life spontaneous clearance of infection might occur. Further studies are required to determine factors that may lead to natural clearance of infection in children.

Source of Infection

A number of studies have proposed that acquisition of H. pylori occurs via a common environmental source. In particular, animals and water have been implicated as potential sources of infection.

Animals as a potential source of H. pylori

The possibility that H. pylori may be a zoonosis first arose following the publication of two seroepidemiological studies that showed that the prevalence of H. pylori infection in abattoir and meat workers was significantly increased as compared with that in subjects not involved in handling animals or animal products (102, 141). These findings have subsequently been questioned, and it is now suggested that the increased prevalence in these workers may have resulted from cross-reactivity between H. pylori and antibodies to other gastrointestinal organisms such as Campylobacter jejuni (39, 93). Although it has been shown that both germ-free and specific pathogen-free pigs can be experimentally colonized with H. pylori, attempts to identify H. pylori in abattoir pigs with both serological and cultural techniques have failed (33, 34, 50, 123). Dore et al. have reported a positive association between the prevalence of H. pylori in Sardinian shepherds and contact with sheep and sheepdogs (26). In this study, 98% of shepherds were shown to be infected with H. pylori, a prevalence significantly higher than that in their family members who did not have regular contact with sheep (73%) and blood donors (43%). These authors concluded that "the cycle of H. pylori infection might, in certain circumstances, include phases in the environment, animals (sheep or dogs) and human beings" (26). The subsequent recovery of H. pylori from sheep's milk led Dore et al. to suggest that sheep may be the ancestral host of H. pylori (27).

Although a number of groups have reported the isolation of H. pylori from rhesus monkeys, given the rare association between humans and monkeys, it is doubtful whether this represents an important reservoir of H. pylori infection (30, 39, 54, 105).

Seroepidemiological studies examining the relationship between pet ownership and the prevalence of H. pylori have in general failed to support such a relationship (3, 14, 130, 148). The isolation of H. pylori from the stomachs of an entire colony of pathogen-free cats led Handt et al. to suggest that cats might represent an important reservoir of H. pylori (53). The validity of this conclusion, however, is questionable given that these cats were commercially reared and had been maintained in isolation.

Although two studies have claimed that the domestic housefly may provide a vector for the transmission of H. pylori (51, 52), the finding that H. pylori could not be recovered from houseflies fed human feces either naturally infected or artificially infected with H. pylori suggests that the domestic housefly is neither a vector for transmission nor a reservoir for H. pylori (110).

Water as a potential source of H. pylori

One of the first reports to suggest that drinking water may be a source of H. pylori infection was published by Klein et al., who showed that Peruvian children whose homes had an external water supply were three times more likely to be infected with H. pylori than children whose homes had an internal water source (65). Although at that time attempts to culture H. pylori from water samples were unsuccessful, in a subsequent study Hulten et al. detected H. pylori DNA in drinking water samples collected from the same areas (58). In Colombia, acquisition of H. pylori infection in children has been associated with swimming more than one time per year in rivers, streams, and pools and drinking stream water (44). Also in South America, Hopkins et al. found Chilean children who consumed uncooked vegetables contaminated with water containing raw sewage to have an increased prevalence of H. pylori infection. This association, however, was only shown in children over 5 years old, which led the authors to conclude that unknown confounding factors may need to be considered (56). Interestingly, in their Colombian study, Goodman et al. found children who frequently ate raw vegetables to be more likely to be infected, although this was at the limit of significance (44).

In contrast to these studies in South America, seroepidemiological studies in southern China have failed to support the belief that water is important in the dissemination of H. pylori; no association was found between water source and the prevalence of H. pylori infection. Indeed, in this community, despite the fact that the majority of subjects boil their water prior to consumption, the prevalence of H. pylori infection is high (45%) (99). Studies in Korea and Bangladesh have also found no association between H. pylori infection and a particular water source (22, 83).

The presence of H. pylori-specific DNA in environmental water sources has been reported by a number of studies (57, 58, 129). For example, in a recent study that used primers based on the conserved region of ureH, Sasaki et al. reported H. pylori-specific DNA to be present in wells, springs, rivers, and ponds but not tap water of a region of Japan (129). In a second environmental study of water supplies conducted in Sweden, Hulten et al., using two different primers for their PCR assays (adhesin and 16S rRNA), showed 9 of 24 private wells, 3 of 25 municipal tap water sources, and 3 of 25 wastewater samples to be positive by PCR for H. pylori DNA (57). Although such studies may in some way support the presence of H. pylori in water, there are two important factors that must be considered; first, that the detection of H. pylori DNA does not indicate viable cells and, second, that the specificity of PCR in environments where as yet undiscovered Helicobacter spp. may be present is unknown.

Attempts to culture H. pylori from water samples have proven unsuccessful. It has been suggested that this failure may relate to the fact that when H. pylori is exposed to adverse environmental conditions, the organism takes on a viable but nonculturable coccoid form (13). Controversy exists, however, as to whether these coccoid forms of H. pylori exist in a viable form and hence are important in transmission (32, 35, 36, 67, 146). Although early studies reported nonculturable coccoid forms of H. pylori to be metabolically active, more recent studies suggest that coccoid forms are not viable dormant forms but represent early stages of bacterial death (67).

In conclusion, therefore, despite an extensive search for an environmental source of H. pylori, no significant reservoirs have been shown to exist outside the human stomach. This finding is perhaps not surprising given that analysis of the genome sequence of H. pylori shows that this bacterium does not possess the full complement of enzymes required for an exclusive aerobic or anaerobic metabolism (139) and hence its ability to survive in the natural environment seems less likely.

Transmission of H. pylori

Failure to consistently isolate H. pylori from reservoirs other than humans suggests that direct person-to-person contact is the most likely mode of transmission. The finding of an increased prevalence of H. pylori infection in institutionalized subjects supports this view and suggests that close personal contact is important for the spread of H. pylori (11, 63, 68, 147). The importance of close contact is further emphasized by the finding that the prevalence of H. pylori infection is significantly increased in family members of children infected with H. pylori as compared with that in family members of children not infected with H. pylori (29, 94, 101, 125). Such findings have led to the view that transmission of H. pylori occurs mainly within the family setting. The relative risk of a child becoming infected with H. pylori has been reported to be approximately eight times greater if the mother is infected and approximately four times greater if the father is infected (125).

The key role of infected mothers in the transmission of H. pylori within families has recently been confirmed by Malaty et al., who monitored longitudinal changes in H. pylori status in 46 Japanese families with children and 48 Japanese couples without children. This study showed that the relative risk of children with H. pylori-positive mothers acquiring infection was 5.3 times that of children whose mothers were H. pylori negative. Confirming the importance of adult-child transmission, seroconversion only occurred among children living with H. pylori-positive mothers over the period of the study (84). The finding in a number of studies of identical strains of H. pylori within family members further supports intrafamilial transmission (6, 20, 95).

Although the majority of studies support interfamilial transmission, a case-control study conducted in Bangladeshi families has reported the prevalence of infection in parents of H. pylori-positive children to be the same as that in H. pylori-negative children. This finding may indicate that in some countries the source of H. pylori infection may lie outside the family (128).

Family composition has also been shown to influence the transmission of H. pylori, the relative risk of infection being shown to increase according to the number of siblings within the household, the odds ratios for one, two, three, and four to five siblings being reported by Goodman et al. to be 1.4, 2.3, 2.6, and 4.3, respectively (43). This study also showed that transmission of infection occurred most readily among siblings who were close in age, transmission being most frequently from older to younger siblings (43). A similar finding has been reported by Rothenbacher et al. (126).

Whether transmission occurs between spouses remains controversial. Although a number of early seroprevalence studies found no evidence to support such transmission (115, 117), a recent study of 110 employees of a health insurance company and their partners showed a strong association between partners' infection status and infection (adjusted odds ratio, 7.0), the risk of infection increasing with the number of years that the spouses had lived together (15). Further evidence that could support transmission between spouses is the finding that a significant number of couples are infected with the same strain of H. pylori (41, 131). For example, Georgopoulos et al., using ribotyping to compare strains, found 8 of 18 couples to carry an identical strain of H. pylori, the remaining 10 couples in the study being colonized with different strains (41). In contrast, Suzuki et al., who used PCR-restriction fragment length polymorphism electrophoretic patterns of amplified ureB to compare strains of H. pylori from 21 asymptomatic couples infected with H. pylori, found only 1 couple to harbor identical strains (135).

Although such studies may suggest that in some cases transmission may occur between spouses, one cannot rule out the possibility that carriage of the same strain by spouses may have occurred due to a child infected by one parent subsequently infecting the second parent. Indeed, evidence that children may facilitate the spread of H. pylori has come from several studies, some showing that the number of children in a family is associated with an increased risk of infection in adult family members (16, 91, 136, 148).

Factors Influencing the Transmission of H. pylori

Socioeconomic status

Numerous studies conducted throughout the world have shown low socioeconomic status to be associated with an increased prevalence of H. pylori infection. In particular, the socioeconomic status of a subject during childhood is considered to be an important determinant of the development of H. pylori infection (80, 81, 103, 127, 142).

The role of socioeconomic status per se is particularly clear if one examines the prevalence of H. pylori infection in poorer racial groups living in developed countries. For example, in a study examining the relationship between socioeconomic status in childhood and the prevalence of H. pylori in African-American and Hispanic populations resident in the United States, Malaty et al. found the prevalence of H. pylori infection to be inversely related to social class during childhood, the prevalence of infection in the lowest social class (85%) being significantly higher than that in the highest social class (11%) (80). The importance of socioeconomic status in childhood has been further demonstrated in an elegant study of monozygotic twins reared apart and discordant for their H. pylori status (81). In this study, Malaty and colleagues showed that the twins infected with H. pylori had been raised in homes under poorer socioeconomic conditions than those of their unaffected co-twins (81).

Socioeconomic status is, however, a broad criterion and encompasses factors such as level of hygiene, sanitation, density of living, and educational opportunities, some or all of which have been reported to influence the level of infection within a population.

Low levels of sanitation have been associated with an increased prevalence of H. pylori infection (2, 91, 114). In particular, the absence of running water in the childhood home has been shown to be a significant risk factor for H. pylori infection (91). Interestingly, Irish soldiers exposed to poor living conditions and sanitation for 6 months showed no significant change in prevalence of H. pylori infection, a finding that further supports the view that acquisition of infection primarily occurs in childhood (10).

In both developed and developing countries high density of living has been consistently related to an increased prevalence of H. pylori infection (69, 81, 88, 91, 99). The importance of overcrowding in the acquisition of H. pylori is further accentuated by the finding that sharing a bed in childhood is associated with an increased prevalence of H. pylori infection (88).

Educational level, also a surrogate marker of socioeconomic status, has been shown in both developed and developing countries to be an important determinant of H. pylori prevalence (38, 48, 61, 109, 113, 124, 140). For example, in a large seroepidemiological study that examined the prevalence of H. pylori infection in 3,194 asymptomatic subjects living in 17 different populations, Forman et al. showed an inverse relationship to exist between the prevalence of H. pylori infection and educational level, 34% of subjects with a tertiary education being found to be infected compared with 47% of those with a secondary education and 63% of those with only a primary school education (38).

The influence of living conditions on the prevalence of H. pylori infection is clearly illustrated in countries where socioeconomic conditions have significantly improved over the last few decades. For example, in Japan the fall in prevalence of H. pylori infection in subjects less than 40 years of age has been related to the significant improvement of the Japanese economy, and hence living conditions, following the Second World War (4). A similar trend has been noted in Korea, another country that has recently undergone substantial improvements in its standard of living (83).

Genetic predisposition

To date, there have been few studies that have examined the role of genetic predisposition in relation to H. pylori infection. In an attempt to examine the importance of genetic factors on the acquisition of H. pylori infection, Malaty et al. compared the seroprevalence of H. pylori infection in 100 monozygotic and 169 dizygotic twins reared together and reared apart. The results of this study showed the correlation coefficient for the relative importance of genetic predisposition on acquisition of H. pylori infection to be approximately 0.66, with the remaining variance being accounted for by shared rearing environmental factors (20%) and non-shared environmental factors (23%) (77). As a result of this study, Malaty et al. concluded that genetic effects influenced the acquisition of H. pylori infection due to greater similarities within monozygotic twin pairs and that sharing of the same rearing environment also contributed to the familial tendency for acquiring H. pylori infection (77).

Route of Transmission

It is probably true to say that the most studied and certainly the most controversial area of H. pylori epidemiological research today is the route of transmission of H. pylori. Given the location of H. pylori infection and the basic need of this bacterium for gastric-type mucosa for in vivo proliferation, ingestion appears to be the most likely means of acquiring H. pylori. However, whether H. pylori reaches the oral cavity via the gastro-oral, oral-oral, or fecal-oral route remains open for conjecture. One of the major difficulties in attempting to culture H. pylori from feces or the oral cavity is the presence in these sites of the autochthonous microbiota. These bacteria tend to grow much more rapidly than H. pylori and hence, even if H. pylori is present, they will often mask its presence (58).

Evidence for gastro-oral transmission

The presence of H. pylori in the gastric juice of up to 58% of patients infected with H. pylori raises the possibility that refluxed gastric juice may represent a vehicle of transmission for this organism (145). Indeed, direct contact with gastric secretions has been implicated in the higher prevalence of H. pylori infection reported in gastroenterologists (74, 97) and in the reported epidemics of Helicobacter gastritis following gastric intubation experiments (46, 119).

The possibility that the gastro-oral route may be an important route of transmission of H. pylori in childhood has been postulated by a number of researchers (5, 96, 100). For example, an early report postulated that the most likely route of transmission of H. pylori was via stomach secretions or vomitus (96). Although at that time there was no evidence to support this view, vomiting and regurgitation of gastric material into the mouth are fairly common in childhood and may represent an important route of transmission (96).

Evidence to support the view that gastro-oral transmission via contaminated vomitus may represent an important mode of transmitting H. pylori, especially in children, has recently been published by Leung et al. (70). In this study, four children presenting with gastroenteritis-associated vomiting were shown serologically to be infected with H. pylori. In one of these children H. pylori was isolated from the vomitus and from two others H. pylori DNA was detected in vomitus by PCR. Interestingly, an 18-month-old girl, negative by serology for H. pylori but in whom H. pylori DNA was detected in vomitus 6 months later, showed seroconversion for H. pylori (70). Support for the view that vomitus may be an important vehicle in the spread of H. pylori has come from a recent study by Parsonnet et al. (112). In this study, H. pylori was cultured from the vomitus of 100% of adult subjects who had been given an emetic to induce vomiting (112). Interestingly, air sampled in an area 0.3 meter away from these subjects during vomiting grew H. pylori in 6 of 16 (37.5%) instances, but air samples collected 1.2 meters away from subjects failed to yield H. pylori (112).

Indirect evidence of the importance of vomiting in the transmission of H. pylori has also recently been shown by Luzza et al. (76). In this study, vomiting siblings and siblings of 100 vomiting index children were screened by means of the [13C]urea breath test for H. pylori. A high rate of active H. pylori infection was shown to be present in both vomiting siblings (60%) and siblings (67%) of H. pylori-infected vomiting index children, with a history of vomiting in siblings being shown to be positively associated with active H. pylori infection in index children (multivariate odds ratio 2.4) (76).

Evidence for and against oral-oral transmission of H. pylori

Attempts to culture H. pylori from the oral cavity have proved in many cases to be fruitless. There have, however, been a limited number of studies where H. pylori has been isolated from dental plaque and saliva (19, 37, 66). In an early study Krajden et al. isolated H. pylori from the dental plaque of 1 of 29 patients whose stomach biopsies were shown to be positive for H. pylori (66). Comparison of the strains isolated from the stomach and dental plaque of this patient with restriction endonuclease analysis subsequently showed one of three strains isolated from dental plaque to be indistinguishable from that isolated from the stomach (132). Cellini et al. also reported the isolation of H. pylori from the dental plaque of 1 of 20 H. pylori-positive endoscopy patients. In this case, comparison of the protein patterns as well as the restriction endonuclease pattern of H. pylori isolated from the stomach biopsy and from dental plaque again showed these to be identical (19). The isolation of low numbers of H. pylori from the saliva of one of nine H. pylori-positive subjects has been reported by Ferguson et al. (37). Again this group showed, using restriction fragment length polymorphism, that the H. pylori strain isolated from saliva was identical to that in gastric tissue (37). In contrast to the low detection rate in the above studies, Desai et al. found H. pylori to be present in the dental plaque of 98% of Indian dyspeptic patients; however, in this study, identification of H. pylori was based solely on the urease test. Given the presence of other urease-positive organisms in the mouth, it is possible that the identification of isolates as H. pylori in this study may have been false (25). The possibility of falsely identifying normal flora from the oral cavity as H. pylori has been reported by Namavar et al., who showed that organisms isolated from the tongue and palate of one patient and considered to be phenotypically identical to H. pylori were in fact negative by an H. pylori-specific PCR (104). In an important study recently published by Parsonnet et al., H. pylori was successfully cultured from the saliva of three subjects (19%). Following the induction of vomiting in these subjects with an emetic, Parsonnet and colleagues were able to culture H. pylori from nine (56%) subjects (112).

The ability to detect H. pylori-specific DNA from the oral cavity has varied significantly (7, 12, 17, 86, 107). Although a number of studies have failed to detect H. pylori DNA in the dental plaque of any H. pylori-positive patients (12, 17), Banatvala et al., using an H. pylori species-specific ureA (urease) gene internal sequence, showed 72% of dental plaque samples taken from 54 patients attending for endoscopy to be positive for H. pylori DNA (7). In a smaller study, Mapstone et al., using a 16S rRNA probe, detected H. pylori DNA in 38% of dental plaque samples obtained from 13 H. pylori-positive patients (86). Using nested PCR, Dowsett et al. detected H. pylori DNA in periodontal pockets as well as the dorsum of the tongue in 87% of subjects examined (28). No association was shown, however, between periodontal pocket depth and the detection of H. pylori (28). The presence of H. pylori DNA in the subgingival plaque of patients with adult periodontitis has also been reported (122).

It has been suggested that the differences in detection rate of H. pylori in the oral cavity with PCR may relate to the specificity of the primers used (89). This point may be particularly relevant to a recent study by Song et al., who using "a highly sensitive and specific PCR" detected H. pylori DNA in the saliva of 55% (23/42) of patients and the dental plaque of 97% of patients. Given that only 11 of these patients were positive for the presence of gastric H. pylori, Song et al. suggested that H. pylori might belong to the normal oral microflora (134). Although it is possible that these findings are correct, given that there may be as yet undiscovered Helicobacter species present in the oral cavity, some caution may be required in the interpretation of these data.

Epidemiological data suggest that a number of cultural habits may enhance the oral transmission of H. pylori. For example, premastication of food by African mothers prior to feeding their children has been shown to be a risk factor for H. pylori infection (1). The use of chopsticks and communal eating have also been associated with transmission of H. pylori within Chinese communities outside of China (21). However, in a more recent study in Chinese subjects resident in Hong Kong, H. pylori was rarely detected in chopsticks after eating (71).

The finding that the prevalence of H. pylori infection in dentists or dental workers is not increased has been used to argue against the oral-oral transmission of H. pylori (73, 79, 106).

Evidence for and against fecal-oral transmission of H. pylori

Although there is some supportive evidence for the passage of H. pylori through the intestine (31), this bacterium is not well adapted for such passage. Indeed, several groups have shown that H. pylori is sensitive to the lethal effects of bile (98, 118); hence, survival of H. pylori after transit through the intestinal tract seems unlikely.

In an attempt to examine the role of the fecal-oral route in the transmission of infection, a number of studies have investigated the association between the prevalence of H. pylori infection and hepatitis A virus, an organism known to be transmitted by the fecal-oral route. In a study using paired sera from the same individuals, the prevalence pattern of hepatitis A was compared with that of H. pylori in an urban and rural southern Chinese population. Although initial examination of the seroprevalence data from rural areas supported a correlation between H. pylori and hepatitis A, when the prevalence data from the urban area were examined, it became evident that no such correlation existed. Although in this urban area the prevalence of H. pylori infection in subjects <10 years was high (approximately 32%), not one of these subjects was shown to be infected with hepatitis A. As a result of this study, it was concluded that community-wide fecal-oral spread of H. pylori might be of limited importance (55). This lack of association between the prevalence of H. pylori and hepatitis A has been reported by a number of other studies conducted in both developed and developing countries (40, 75, 130, 149).

Attempts to culture H. pylori from feces have by and large been unsuccessful. In 1994, however, the first report of the isolation of H. pylori from human feces appeared in the literature. In this study Thomas et al. isolated H. pylori from the feces of 1 infected adult and 9 of 23 randomly selected children living in a Gambian village (138). In the same year, Kelly and colleagues using the same isolation technique as Thomas's group also claimed to have isolated H. pylori from the feces of 12 of 25 H. pylori-positive subjects with dyspepsia (62). Definitive proof that the organisms cultured in this study were H. pylori was, however, unsubstantiated. Attempts by other groups to isolate H. pylori from patient populations using these methods have failed, and it has been suggested that the ability of Thomas et al. to culture H. pylori from Gambian children may relate to the fact that these children were malnourished and had an extremely short fecal transit time (89). This view is supported by a recent study by Parsonnet et al. that showed that although H. pylori could not be cultured from the stools of 16 H. pylori-positive adult subjects, if patients were given a cathartic to induce diarrhea and the stools were then tested, the bacterium could be cultured from the stools of 7 of 14 (50%) patients (112).

Attempts to detect H. pylori DNA in feces by PCR have resulted in variable outcomes. Whereas some studies have reported the detection of H. pylori DNA in the feces of 25 to 90% of subjects known to be infected with H. pylori (72, 85, 108), others have reported less than 10% of H. pylori-positive subjects to have H. pylori DNA in their feces (104, 144). Although detection of H. pylori DNA in feces may add to the evidence supporting the fecal-oral route of transmission, it is again essential to remember that the finding of H. pylori DNA does not necessarily mean that viable H. pylori is present in the feces.


Given the association between H. pylori and peptic ulcer disease, gastric cancer, and B-cell MALT lymphoma, there is an urgent need for the development of intervention strategies to prevent the spread of this bacterium. Although development of a vaccine against H. pylori is progressing well, it is highly likely that it will be 5 to 10 years before such a vaccine becomes available. Given the increasing levels of resistance to current antimicrobial therapies used against H. pylori and the high cost of such an approach, mass programs to treat H. pylori-infected individuals is clearly out of the question.

In many other diseases with an infectious etiology, public health measures based on epidemiological data have been extremely successful in preventing the spread of pathogenic agents. Before such measures can be implemented, clarification of the route of transmission of H. pylori will be essential.


Albenque M., Tall F., Dabis F., Mégraud F. Epidemiological study of Helicobacter pylori transmission from mother to child in Africa. Enferm. Digest. 1990;78:48.
Al-Moagel M. A., Evans D. G., Abdulghani M. E., Adam E., Evans D. J. J., Malaty H. M., Graham D. Y. Prevalence of Helicobacter (formerly Campylobacter) pylori infection in Saudi Arabia, and comparison of those with and without upper gastrointestinal symptoms. Am. J. Gastroenterol. 1990;85:944–948. [PubMed: 2375321]
Ansorg R., Vonheinegg E. H., Vonrecklinghausen G. Cat owner's risk of acquiring a Helicobacter pylori infection. Zentralbl. Bakteriol. Int. J. Med. Microbiol. Vir. Parasitol. Infect. Dis. 1995;283:122–126. [PubMed: 9810653]
Asaka M., Kimura T., Kudo M. Relationship of Helicobacter pylori to serum pepsinogens in an asymptomatic Japanese population. Gastroenterology. 1992;102:760–766. [PubMed: 1537513]
Axon A. T. R. Is Helicobacter pylori transmitted by the gastro-oral route? Aliment. Pharmacol. Ther. 1995;9:585–588. [PubMed: 8824644]
Bamford K. B., Bickley J., Collins J. S. A., Johnston B. T., Potts S., Boston V., Owen R. J., Sloan J. M. Helicobacter pylori—comparison of DNA fingerprints provides evidence for intrafamilial infection. Gut. 1993;34:1348–1350. [PMC free article: PMC1374539] [PubMed: 8244100]
Banatvala N., Lopez C. R., Owen R. J., Hurtado A., Abdi Y., Davies G. R., Hardie J. M., Feldman R. A. Use of the polymerase chain reaction to detect Helicobacter pylori in the dental plaque of healthy and symptomatic individuals. Microb. Ecol. Health Dis. 1994;7:1–8.
Banatvala N., Mayo K., Megraud F., Jennings R., Deeks J. J., Feldman R. A. The cohort effect and Helicobacter pylori. J. Infect. Dis. 1993;168:219–221. [PubMed: 8515114]
Bardhan P. K. Epidemiological features of Helicobacter pylori infection in developing countries. Clin. Infect. Dis. 1997;25:973–978. [PubMed: 9402340]
Basso L., Beattie S., Lawlor S., Clune J., O'Morain C. A descriptive follow-up study on Helicobacter pylori infection before and after exposition to a war area. Eur. J. Epidemiol. 1994;10:109–111. [PubMed: 7957781]
Berkowicz J., Lee A. Person-to-person transmission of Campylobacter pylori. Lancet. 1987;ii:680–681. [PubMed: 2887955]
Bickley J., Owen R. J., Fraser A. G., Pounder R. E. Evaluation of the polymerase chain reaction for detecting the urease c gene of Helicobacter pylori in gastric biopsy samples and dental plaque. J. Med. Microbiol. 1993;39:338–344. [PubMed: 8246250]
Bode G., Mauch F., Malfertheiner P. The coccoid forms of Helicobacter pylori—criteria for their viability. Epidemiol. Infect. 1993;111:483–490. [PMC free article: PMC2271265] [PubMed: 8270008]
Bode G., Rothenbacher D., Brenner H., Adler G. Pets are not a risk factor for Helicobacter pylori infection in young children—results of a population-based study in southern Germany. Pediatr. Infect. Dis. J. 1998;17:909–912. [PubMed: 9802634]
Brenner H., Rothenbacher D., Bode G., Dieudonne P., Adler G. Active infection with Helicobacter pylori in healthy couples. Epidemiol. Infect. 1999;122:91–95. [PMC free article: PMC2809592] [PubMed: 10098790]
Breuer T., Sudhop T., Hoch J., Sauerbruch T., Malfertheiner P. Prevalence of and risk factors for Helicobacter pylori infection in the western part of Germany. Eur. J. Gastroenterol. Hepatol. 1996;8:47–52. [PubMed: 8900908]
Cammarota G., Tursi A., Montalto M., Papa A., Veneto G., Bernardi S., Boari A., Colizzi V., Fedeli G., Gasbarrini G. Role of dental plaque in the transmission of Helicobacter pylori infection. J. Clin. Gastroenterol. 1996;22:174–177. [PubMed: 8724252]
Casswall T. H., Sarker S. A., Albert M. J., Fuchs G. J., Bergstrom M., Bjorck L., Hammarstrom L. Treatment of Helicobacter pylori infection in infants in rural Bangladesh with oral immunoglobulins from hyperimmune bovine colostrum. Aliment. Pharmacol. Ther. 1998;12:563–568. [PubMed: 9678817]
Cellini L., Allocati N., Piattelli A., Petrelli I., Fanci P., Dainelli B. Microbiological evidence of Helicobacter pylori from dental plaque in dyspeptic patients. Microbiologica. 1995;18:187–192. [PubMed: 7603346]
Cho M. J., Lee W. K., Jeon Y. S., Kim K. H., Kim S. H., Baik S. C., Rhee K. H., Kim Y. O., Yoon H. S., Kim N. S. Intrafamilial transmission of Helicobacter pylori detected by random amplified polymorphic DNA fingerprinting. Molecules Cells. 1995;5:508–513.
Chow T., Lambert J. R., Wahlqvist M. L., Hsuhage B. Helicobacter pylori in Melbourne Chinese immigrants—evidence for oral-oral transmission via chopsticks. J. Gastroenterol. Hepatol. 1995;10:562–569. [PubMed: 8963032]
Clemens J., Albert M. J., Rao M., Huda S., Qadri F., Vanloon F. P. L., Pradhan B., Naficy A., Banik A. Sociodemographic, hygienic and nutritional correlates of Helicobacter pylori infection of young Bangladeshi children. Pediatr. Infect. Dis. J. 1996;15:1113–1118. [PubMed: 8970222]
Cullen D. J. E., Collins B. J., Christiansen K. J., Epis J., Warren J. R., Surveyor I., Cullen K. J. When is Helicobacter pylori infection acquired? Gut. 1993;34:1681–1682. [PMC free article: PMC1374462] [PubMed: 8282255]
de Oliveira A. M. R., Rocha G. A., Queiroz D., de Moura S. B., Rabello A. L. T. Seroconversion for Helicobacter pylori in adults from Brazil. Trans. R. Soc. Trop. Med. Hyg. 1999;93:261–263. [PubMed: 10492754]
Desai H. G., Gill H. H., Shankaran K., Mehta P. R., Prabhu S. R. Dental plaque: a permanent reservoir of Helicobacter pylori? Scand. J. Gastroenterol. 1991;26:1205–1208. [PubMed: 1754858]
Dore M. P., Bilotta M., Vaira D., Manca A., Massarelli G., Leandro G., Atzei A., Pisanu G., Graham D. Y., Realdi G. High prevalence of Helicobacter pylori infection in shepherds. Dig. Dis. Sci. 1999;44:1161–1164. [PubMed: 10389689]
Dore M. P., Sepulveda A. R., Osato M. S., Realdi G., Graham D. Y. Helicobacter pylori in sheep milk. Lancet. 1999;354:132. [PubMed: 10408497]
Dowsett S. A., Archila L., Segreto V. A., Gonzalez C. R., Silva A., Vastola K. A., Bartizek R. D., Kowolik M. J. Helicobacter pylori infection in indigenous families of Central America: serostatus and oral and fingernail carriage. J. Clin. Microbiol. 1999;37:2456–2460. [PMC free article: PMC85254] [PubMed: 10405384]
Drumm B., Perez P. G. I., Blaser M. J., Sherman P. M. Intrafamilial clustering of Helicobacter pylori infection. N. Engl. J. Med. 1990;322:359–363. [PubMed: 2300088]
Dubois A., Fiala N., Hemanackah L. M., Drazek E. S., Tarnawski A., Fishbein W. N., Perez Perez G. I., Blaser M. J. Natural gastric infection with Helicobacter pylori in monkeys: a model for spiral bacteria infection in humans. Gastroenterology. 1994;106:1405–1417. [PubMed: 8194685]
Dye K. R., Marshall B. J., Frierson, Jr H. F., Pambianco D. J., McCallum R. W. Campylobacter pylori colonizing heterotopic gastric tissue in the rectum. Am. J. Clin. Pathol. 1990;93:144–147. [PubMed: 2294694]
Eaton K. A., Catrenich C. E., Makin K. M., Krakowka S. Virulence of coccoid and bacillary forms of Helicobacter pylori in gnotobiotic piglets. J. Infect. Dis. 1995;171:459–462. [PubMed: 7844390]
Eaton K. A., Morgan D. R., Krakowka S. Persistence of Helicobacter pylori in conventionalized piglets. J. Infect. Dis. 1990;161:1299–1301. [PubMed: 2345307]
Engstrand L., Gustavsson S., Jorgensen A., Schwan A., Scheynius A. Inoculation of barrier-born pigs with Helicobacter pylori: a useful animal model for gastritis type B. Infect. Immun. 1990;58:1763–1768. [PMC free article: PMC258720] [PubMed: 2341177]
Enroth H., Wreiber K., Rigo R., Risberg D., Uribe A., Engstrand L. In vitro aging of Helicobacter pylori: changes in morphology, intracellular composition and surface properties. Helicobacter. 1999;4:7–16. [PubMed: 10352082]
Fan X. G., Chua A., Li T. G., Zeng Q. S. Survival of Helicobacter pylori in milk and tap water. J. Gastroenterol. Hepatol. 1998;13:1096–1098. [PubMed: 9870794]
Ferguson D. A., Chuanfu L., Patel N. R., Mayberry W. R., Chi D. S., Thomas E. Isolation of Helicobacter pylori from saliva. J. Clin. Microbiol. 1993;31:2802–2804. [PMC free article: PMC266021] [PubMed: 8253990]
Forman D., Debacker G., Elder J., Moller H., Damotta L. C., Roy P., Abid L., Debacker G., Tjonneland A., Boeing H., Haubrich T., Wahrendorf J., Manousos O., Kafatos A., Tulinius H., Ogmundsdottir H., Palli D., Cipriani F., Fukao A., Tsugane S., Miyajima Y., Zatonski W., Tycznski J., Calheiros J., Zakelj M. P., Potocnik M., Webb P., Knight T., Wilson A., Kaye S., Potter J., Newell D. G., Hengels K. J., Kyrtopoulos S., Wild C., Moller H., Webb P., Newell D., Forman D., Palli D., Hengels K., Elder J., Debacker G., Coleman M. Epidemiology of, and risk factors for, Helicobacter pylori infection among 3194 asymptomatic subjects in 17 populations. Gut. 1993;34:1672–1676.
Fox J. G. Non-human reservoirs of Helicobacter pylori. Aliment. Pharmacol. Ther. 1995;9:93–103. [PubMed: 8547534]
Furuta T., Kamata T., Takashima M., Futami H., Arai H., Hanai H., Kaneko E. Study of transmission routes of Helicobacter pylori in relation to seroprevalence of hepatitis A virus. J. Clin. Microbiol. 1997;35:1891–1893. [PMC free article: PMC229866] [PubMed: 9196218]
Georgopoulos S. D., Mentis A. F., Spiliadis C. A., Tzouvelekis L. S., Tzelepi E., Moshopoulos A., Skandalis N. Helicobacter pylori infection in spouses of patients with duodenal ulcers and comparison of ribosomal RNA gene patterns. Gut. 1996;39:634–638. [PMC free article: PMC1383384] [PubMed: 9026475]
Goh K. L. Prevalence of and risk factors for Helicobacter pylori infection in a multi-racial dyspeptic Malaysian population undergoing endoscopy. J. Gastroenterol. Hepatol. 1997;12:S29–S35. [PubMed: 9195409]
Goodman K. J., Correa P. Transmission of Helicobacter pylori among siblings. Lancet. 2000;355:358–362. [PubMed: 10665555]
Goodman K. J., Correa P., Aux H. J. T., Ramirez H., Delany J. P., Pepinosa O. G., Quinones M. L., Parra T. C. Helicobacter pylori infection in the Colombian Andes—a population-based study of transmission pathways. Am. J. Epidemiol. 1996;144:290–299. [PubMed: 8686698]
Graham D. Y., Adam E., Reddy G. T., Agarwal J. P., Agarwal R., Evans D. J., Malaty H. M., Evans D. G. Seroepidemiology of Helicobacter pylori infection in India. Comparison of developing and developed countries. Dig. Dis. Sci. 1991;36:1084–1088. [PubMed: 1864201]
Graham D. Y., Alpert L. C., Smith J. L., Yoshimura H. H. Iatrogenic Campylobacter pylori infection is a cause of epidemic achlorhydria. Am. J. Gastroenterol. 1988;83:974–980. [PubMed: 3414650]
Graham D. Y., Lew G. M., Klein P. D., Evans D. G., Evans D. J., Saeed Z. A., Malaty H. M. Effect of treatment of Helicobacter pylori infection on the long-term recurrence of gastric or duodenal ulcer, a randomized, controlled study. Ann. Intern. Med. 1992;116:705–708. [PubMed: 1558340]
Graham D. Y., Malaty H. M., Evans D. G., Evans D. J. J., Klein P. D., Adam E. Epidemiology of Helicobacter pylori in an asymptomatic population in the United States. Effect of age, race, and socioeconomic status. Gastroenterology. 1991;100:1495–1501. [PubMed: 2019355]
Granstrom M., Tindberg Y., Blennow M. Seroepidemiology of Helicobacter pylori infection in a cohort of children monitored from 6 months to 11 years of age. J. Clin. Microbiol. 1997;35:468–470. [PMC free article: PMC229601] [PubMed: 9003617]
Grasso G. M., Ripabelli G., Sammarco M. L., Ruberto A., Iannitto G. Prevalence of Helicobacter-like organisms in porcine gastric mucosa—a study of swine slaughtered in Italy. Comp. Immunol. Microbiol. Infect. Dis. 1996;19:213–217. [PubMed: 8800547]
Grubel P., Hoffman J. S., Chong F. K., Burstein N. A., Mepani C., Cave D. R. Vector potential of houseflies (Musca domestica) for Helicobacter pylori. J. Clin. Microbiol. 1997;35:1300–1303. [PMC free article: PMC229738] [PubMed: 9163433]
Grubel P., Huang L. L., Masubuchi N., Stutzenberger F. J., Cave D. R. Detection of Helicobacter pylori DNA in houseflies (Musca domestica) on three continents. Lancet. 1998;352:788–789. [PubMed: 9737291]
Handt L. K., Fox J. G., Dewhirst F. E., Fraser G. J., Paster B. J., Yan L. L., Rozmiarek H., Rufo R., Stalis I. H. Helicobacter pylori isolated from the domestic cat: public health implications. Infect. Immun. 1994;62:2367–2374. [PMC free article: PMC186520] [PubMed: 8188360]
Handt L. K., Fox J. G., Yan L. L., Shen Z., Pouch W. J., Ngai D., Motzel S. L., Nolan T. E., Klein H. J. Diagnosis of Helicobacter pylori infection in a colony of rhesus monkeys (Macaca mulatta) J. Clin. Microbiol. 1997;35:165–168. [PMC free article: PMC229531] [PubMed: 8968900]
Hazell S. L., Mitchell H. M., Hedges M., Shi X., Hu P. J., Li Y. Y., Lee A., Reisslevy E. Hepatitis A and evidence against the community dissemination of Helicobacter pylori via feces. J. Infect. Dis. 1994;170:686–689. [PubMed: 8077729]
Hopkins R. J., Vial P. A., Ferreccio C., Ovalle J., Prado P., Sotomayor V., Russell R. G., Wasserman S. S., Morris J. G. Seroprevalence of Helicobacter pylori in Chile—vegetables may serve as one route of transmission. J. Infect. Dis. 1993;168:222–226. [PubMed: 8515115]
Hulten K., Enroth H., Nystrom T., Engstrand L. Presence of Helicobacter species DNA in Swedish water. J. Appl. Microbiol. 1998;85:282–286. [PubMed: 9750301]
Hulten K., Han S. W., Enroth H., Klein P. D., Opekun A. R., Gilman R. H., Evans D. G., Engstrand L., Graham D. Y., Elzaatari F. Helicobacter pylori in the drinking water in Peru. Gastroenterology. 1996;110:1031–1035. [PubMed: 8612990]
International Agency for Research on Cancer. 1994. IARC Monographs on the Evaluation of Carcinogenic Risks to Humans, vol. 61, p. 177–240. World Health Organization, Lyon, France.
Jones D. M., Eldridge J., Fox A. J., Sethi P., Whorwell P. J. Antibody to the gastric campylobacter-like organism ("Campylobacter pyloridis")—clinical correlations and distribution in the normal population. J. Med. Microbiol. 1986;22:57–62. [PubMed: 3735391]
Katelaris P., Tippett G., Zoli G., Lowe D., Norbu P., Farthing M. An evaluation of factors affecting Helicobacter pylori prevalence in Tibetans exiled in India. Trans. R. Soc. Trop. Med. Hyg. 1993;87:400–403. [PubMed: 8249063]
Kelly S. M., Pitcher M. C. L., Farmery S. M., Gibson G. R. Isolation of Helicobacter pylori from feces of patients with dyspepsia in the United Kingdom. Gastroenterology. 1994;107:1671–1674. [PubMed: 7958677]
Kimura A., Matsubasa T., Kinoshita H., Kuriya N., Yamashita Y., Fujisawa T., Terakura H., Shinohara M. Helicobacter pylori seropositivity in patients with severe neurologic impairment. Brain Dev. 1999;21:113–117. [PubMed: 10206529]
Klein P. D., Gilman R. H., Leonbarua R., Diaz F., Smith E. O., Graham D. Y. The epidemiology of Helicobacter pylori in Peruvian children between 6 and 30 months of age. Am. J. Gastroenterol. 1994;89:2196–2200. [PubMed: 7977241]
Klein P. D., Graham D. Y., Gaillour A., Opekun A. R., Smith E. O. Water source as risk factor for Helicobacter pylori infection in Peruvian children. Gastrointestinal Physiology Working Group. Lancet. 1991;337:1503–1506. [PubMed: 1675369]
Krajden S., Fuksa M., Anderson J., Kempston J., Boccia A., Petrea C., Babida C., Karmali M., Penner J. L. Examination of human stomach biopsies, saliva, and dental plaque for Campylobacter pylori. J. Clin. Microbiol. 1989;27:1397–1398. [PMC free article: PMC267568] [PubMed: 2754008]
Kusters J. G., Gerrits M. M., Vanstrijp J., Vanden-brouckegrauls C. Coccoid forms of Helicobacter pylori are the morphologic manifestation of cell death. Infect. Immun. 1997;65:3672–3679. [PMC free article: PMC175523] [PubMed: 9284136]
Lambert J. R., Lin S. K., Sievert W., Nicholson L., Schembri M., Guest C. High prevalence of Helicobacter pylori antibodies in an institutionalized population—evidence for person-to-person transmission. Am. J. Gastroenterol. 1995;90:2167–2171. [PubMed: 8540509]
Lee A. The microbiology and epidemiology of Helicobacter pylori infection. Scand. J. Gastroenterol. 1994;29:2–6. [PubMed: 8047819]
Leung W. K., Siu K. L. K., Kwok C. K. L., Chan S. Y., Sung R., Sung J. J. Y. Isolation of Helicobacter pylori from vomitus in children and its implication in gastro-oral transmission. Am. J. Gastroenterol. 1999;94:2881–2884. [PubMed: 10520837]
Leung W. K., Sung J. J. Y., Ling T. K. W., Siu K. L. K., Cheng A. F. B. Use of chopsticks for eating and Helicobacter pylori infection. Dig. Dis. Sci. 1999;44:1173–1176. [PubMed: 10389692]
Li C. F., Ha T. Z., Ferguson D. A., Chi D. S., Zhao R. G., Patel N. R., Krishnaswamy G., Thomas E. A newly developed PCR assay of H. pylori in gastric biopsy, saliva, and feces—evidence of high prevalence of H. pylori in saliva supports oral transmission. Dig. Dis. Sci. 1996;41:2142–2149. [PubMed: 8943965]
Lin S. K., Lambert J. R., Schembri M. A., Nicholson L., Johnson I. H. The prevalence of Helicobacter pylori in practising dental staff and dental students. Aust. Dent. J. 1998;43:35–39. [PubMed: 9583224]
Lin S. K., Lambert J. R., Schembri M. A., Nicholson L., Korman M. G. Helicobacter pylori prevalence in endoscopy and medical staff. J. Gastroenterol. Hepatol. 1994;9:319–324. [PubMed: 7948812]
Luzza F., Imeneo M., Maletta M., Paluccio G., Giancotti A., Perticone F., Foca A., Pallone F. Seroepidemiology of Helicobacter pylori infection and hepatitis A in a rural area—evidence against a common mode of transmission. Gut. 1997;41:164–168. [PMC free article: PMC1891453] [PubMed: 9301493]
Luzza F., Mancuso M., Imeneo M., Contaldo A., Giancotti L., Pensabene L., Doldo P., Liberto M. C., Strisciuglio P., Foca A., Guandalini S., Pallone F. Evidence favouring the gastro-oral route in the transmission of Helicobacter pylori infection in children. Eur. J. Gastroenterol. Hepatol. 2000;12:623–627. [PubMed: 10912479]
Malaty H. M., Engstrand L., Pedersen N. L., Graham D. Y. Helicobacter pylori infection: genetic and environmental influences. Ann. Intern. Med. 1994;120:982–986. [PubMed: 8185146]
Malaty H. M., Evans D. G., Evans D. J., Graham D. Y. Helicobacter pylori in Hispanics—comparison with blacks and whites of similar age and socioeconomic class. Gastroenterology. 1992;103:813–816. [PubMed: 1499931]
Malaty H. M., Evans D. J., Abramovitch K., Evans D. G., Graham D. Y. Helicobacter pylori infection in dental workers: a seroepidemiology syudy. Am. J. Gastroenterol. 1992;87:1728–1731. [PubMed: 1449133]
Malaty H. M., Graham D. Y. Importance of childhood socioeconomic status on the current prevalence of Helicobacter pylori infection. Gut. 1994;35:742–745. [PMC free article: PMC1374869] [PubMed: 8020796]
Malaty H. M., Graham D. Y., Isaksson I., Engstrand L., Pedersen N. L. Co-twin study of the effect of environment and dietary elements on acquisition of Helicobacter pylori infection. Am. J. Epidemiol. 1998;148:793–797. [PubMed: 9786234]
Malaty H. M., Graham D. Y., Wattigney W. A., Srinivasan S. R., Osato M., Berenson G. S. Natural history of Helicobacter pylori infection in childhood: 12-year follow-up cohort study in a biracial community. Clin. Infect. Dis. 1999;28:279–282. [PubMed: 10064244]
Malaty H. M., Kim J. G., Kim S. D., Graham D. Y. Prevalence of Helicobacter pylori infection in Korean children—inverse relation to socioeconomic status despite a uniformly high prevalence in adults. Am. J. Epidemiol. 1996;143:257–262. [PubMed: 8561159]
Malaty H. M., Kumagai T., Tanaka E., Ota H., Kiyosawa K., Graham D. Y., Katsuyama T. Evidence from a nine-year birth cohort study in Japan of transmission pathways of Helicobacter pylori infection. J. Clin. Microbiol. 2000;38:1971–1973. [PMC free article: PMC86638] [PubMed: 10790131]
Mapstone N. P., Lewis F. A., Tompkins D. S., Lynch D. A. F., Axon A. T. R., Dixon M. F., Quirke P. PCR identification of Helicobacter pylori in faeces from gastritis patients. Lancet. 1993;341:447. [PubMed: 8094221]
Mapstone N. P., Lynch D. A. F., Lewis F. A., Axon A. T. R., Tompkins D. S., Dixon M. F., Quirke P. Identification of Helicobacter pylori DNA in the mouths and stomachs of patients with gastritis using PCR. J. Clin. Pathol. 1993;46:540–543. [PMC free article: PMC501291] [PubMed: 8331177]
Marshall B. J., McGechie D. B., Rogers P. A., Glancy R. J. Pyloric Campylobacter infection and gastroduodenal disease. Med. J. Aust. 1985;142:439–444. [PubMed: 3982346]
McCallion W. A., Murray L. J., Bailie A. G., Dalzell A. M., Oreilly D., Bamford K. B. Helicobacter pylori infection in children—relation with current household living conditions. Gut. 1996;39:18–21. [PMC free article: PMC1383223] [PubMed: 8881801]
Megraud F. Transmission of Helicobacter pylori—faecal-oral versus oral-oral route. Aliment. Pharmacol. Ther. 1995;9:85–91. [PubMed: 8547533]
Megraud F., Brassens Rabbe M. P., Denis F., Belbouri A., Hoa D. Q. Seroepidemiology of Campylobacter pylori infection in various populations. J. Clin. Microbiol. 1989;27:1870–1873. [PMC free article: PMC267687] [PubMed: 2549098]
Mendall M. A., Goggin P. M., Molineaux N., Levy J., Toosy T., Strachan D., Northfield T. C. Childhood living conditions and Helicobacter pylori seropositivity in adult life. Lancet. 1992;339:896–897. [PubMed: 1348299]
Mitchell H. M. The epidemiology of Helicobacter pylori. Gastroduodenal Disease and Helicobacter pylori: Pathophysiology, Diagnosis and Treatment. 1999;241:11–30. [PubMed: 10087654]
Mitchell, H. M. 1993. The epidemiology of Helicobacter pylori infection and its relation to gastric cancer, p. 95–114. In C. S. Goodwin and B. W. Wormsley (ed.), Helicobacter pylori: Biology and Clinical Practice. CRC Press, Boca Raton, Fla.
Mitchell H. M., Bohane T., Hawkes R. A., Lee A. Helicobacter pylori infection within families. Zentralbl. Bakteriol. Int. J. Med. Microbiol. 1993;280:128–136. [PubMed: 8280934]
Mitchell H. M., Hazell S. L., Kolesnikow T., Mitchell J., Frommer D. Antigen recognition during progression from acute to chronic infection with a cagA-positive strain of Helicobacter pylori. Infect. Immun. 1996;64:1166–1172. [PMC free article: PMC173899] [PubMed: 8606074]
Mitchell, H. M., A. Lee, and T. D. Bohane. 1989. Evidence for person-to-person spread of Campylobacter pylori, p. 197–202. In B. J. Rathbone and R. V. Heatley (ed.), Campylobacter pylori and Gastroduodenal Disease. Blackwell Scientific Publications, Oxford, United Kingdom.
Mitchell H. M., Lee A., Carrick J. Increased incidence of Campylobacter pylori infection in gastroenterologists: further evidence to support person-to-person transmission of C. pylori. Scand. J. Gastroenterol. 1989;24:396–400. [PubMed: 2789427]
Mitchell H. M., Li Y., Hu P., Hazell S. L., Du G., Byrne D. J., Lee A. The susceptibility of Helicobacter pylori to bile may be an obstacle to faecal transmission. Eur. J. Gastroenterol. Hepatol. 1992;4:S79–S83.
Mitchell H. M., Li Y. Y., Hu P. J., Liu Q., Chen M., Du G. G., Wang Z. J., Lee A., Hazell S. L. Epidemiology of Helicobacter pylori in Southern China—identification of early childhood as the critical period for acquisition. J. Infect. Dis. 1992;166:149–153. [PubMed: 1607687]
Mitchell J. D., Mitchell H. M., Tobias V. Acute Helicobacter pylori infection in an infant, associated with gastric ulceration and serological evidence of intra-familial transmission. Am. J. Gastroenterol. 1992;87:382–386. [PubMed: 1539579]
Miyaji H., Azuma T., Ito S., Abe Y., Gejyo F., Hashimoto N., Sugimoto H., Suto H., Ito Y., Yamazaki Y., Kohli Y., Kuriyama M. Helicobacter pylori infection occurs via close contact with infected individuals in early childhood. J. Gastroenterol. Hepatol. 2000;15:257–262. [PubMed: 10764025]
Morris A., Nicholson G., Lloyd G., Haines D., Rogers A., Taylor D. Seroepidemiology of Campylobacter pyloridis. N. Z. Med. J. 1986;99:657–659. [PubMed: 3463897]
Murray L. J., McCrum E. E., Evans A. E., Bamford K. B. Epidemiology of Helicobacter pylori infection among 4742 randomly selected subjects from northern Ireland. Int. J. Epidemiol. 1997;26:880–887. [PubMed: 9279623]
Namavar F., Roosendaal R., Kuipers E. J., Degroot P., Vanderbijl M. W., Pena A. S., Degraaff J. Presence of Helicobacter pylori in the oral cavity, oesophagus, stomach and faeces of patients with gastritis. Eur. J. Clin. Microbiol. Infect. Dis. 1995;14:234–237. [PubMed: 7614967]
Newell D., Hudson M. J., Baskerville A. Naturally occurring gastritis associated with Campylobacter pylori infection in the rhesus monkey. Lancet. 1987;ii:1338. [PubMed: 2890941]
Nguyen A., Elzaatari F., Graham D. Y. Helicobacter pylori in the oral cavity. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endodontics. 1995;79:705–709. [PubMed: 7621027]
Nguyen A. M. H., Engstrand L., Genta R. M., Graham D. Y., Elzaatari F. A. K. Detection of Helicobacter pylori in dental plaque by reverse transcription polymerase chain reaction. J. Clin. Microbiol. 1993;31:783–787. [PMC free article: PMC263562] [PubMed: 8463387]
Notarnicola M., Russo F., Cavallini A., Bianco M., Jirillo E., Pece S., Leoci C., Dimatteo G., Dileo A. PCR identification of Helicobacter pylori DNA in faeces from patients with gastroduodenal pathology. Med. Sci. Res. 1996;24:785–787.
Olmos J. A., Rios H., Higa R. Prevalence of Helicobacter pylori infection in Argentina—results of a nationwide epidemiologic study. J. Clin. Microbiol. 2000;31:33–37. [PubMed: 10914773]
Osato M. S., Ayub K., Le H. H., Reddy R., Graham D. Y. Houseflies are an unlikely reservoir or vector for Helicobacter pylori. J. Clin. Microbiol. 1998;36:2786–2788. [PMC free article: PMC105211] [PubMed: 9705441]
Parsonnet J., Hansen S., Rodriguez L., Gelb A. B., Warnke R. A., Jellum E., Orentreich N., Vogelman J. H., Friedman G. D. Helicobacter pylori infection and gastric lymphoma. N. Engl. J. Med. 1994;330:1267–1271. [PubMed: 8145781]
Parsonnet J., Shmuely H., Haggerty T. Fecal and oral shedding of Helicobacter pylori from healthy infected adults. JAMA. 1999;282:2240–2245. [PubMed: 10605976]
Peach H. G., Pearce D. C., Farish S. J. Helicobacter pylori infection in an Australian regional city—prevalence and risk factors. Med. J. Aust. 1997;167:310–313. [PubMed: 9322776]
Perez-Perez G. I., Taylor D. N., Bodhidatta L., Wongsri-chanalai J., Baze W. B., Dunn B. E., Echeverria P. D., Blaser M. J. Seroprevalence of Helicobacter pylori infections in Thailand. J. Infect. Dis. 1990;161:1237–1241. [PubMed: 2345304]
Perez-Perez G. I., Witkin S. S., Decker M. D., Blaser M. J. Seroprevalence of Helicobacter pylori infection in couples. J. Clin. Microbiol. 1991;29:642–644. [PMC free article: PMC269836] [PubMed: 2037687]
Perri F., Pastore M., Clemente R., Festa V., Quitadamo M., Niro G., Conoscitore P., Rutgeerts P., Andriulli A. Helicobacter pylori infection may undergo spontaneous eradication in children—a 2-year follow-up study. J. Pediatr. Gastroenterol. Nutr. 1998;27:181–183. [PubMed: 9702650]
Polish L. B., Douglas J. M. J., Davidson A. J., Perez Perez G. I., Blaser M. J. Characterisation of risk factors for Helicobacter pylori infection among men attending a sexually transmitted disease clinic: lack of evidence for sexual transmission. J. Clin. Microbiol. 1991;29:2139–2143. [PMC free article: PMC270287] [PubMed: 1939565]
Raedsch, R., S. Pohl, J. Plachky, A. Stiehl, and B. Kommerell. 1989. The growth of Campylobacter pylori is inhibited by intragastric bile acids, p. 409–412. In F. Megraud and H. Lamouliatte (ed.), Gastroduodenal Pathology and Campylobacter pylori. Elsevier, Amsterdam, The Netherlands.
Ramsey E. J., Carey K. V., Peterson W. L., Jackson J. J., Murphy F. K., Read N. W. T. Epidemic gastritis with hypochlorhydria. Gastroenterology. 1979;76:1449–1457. [PubMed: 437444]
Redlinger T., O'Rourke K., Goodman K. J. Age distribution of Helicobactor pylori seroprevalence among young children in a United States/Mexico border community: evidence for transitory infection. Am. J. Epidemiol. 1999;150:225–230. [PubMed: 10430225]
Replogle M. L., Kasumi W., Ishikawa K. B., Yang S. F., Juji T., Miki K., Kabat G. C., Parsonnet J. Increased risk of Helicobacter pylori associated with birth in wartime and post-war Japan. Int. J. Epidemiol. 1996;25:210–214. [PubMed: 8666492]
Riggio M. P., Lennon A. Identification by PCR of Helicobacter pylori in subgingival plaque of adult periodontitis patients. J. Med. Microbiol. 1999;48:317–322. [PubMed: 10334600]
Rocha G. A., Queiroz D. M. M., Mendes E. N., Oliveira A. M. R., Moura S. B., Silva R. J. A. Source of Helicobacter pylori infection: studies in abattoir workers and pigs. Am. J. Gastroenterol. 1992;87:1525. [PubMed: 1415120]
Rosenstock S. J., Andersen L. P., Rosenstock C. V., Bonnevie O., Jorgensen T. Socioeconomic factors in Helicobacter pylori infection among Danish adults. Am. J. Public Health. 1996;86:1539–1544. [PMC free article: PMC1380686] [PubMed: 8916517]
Rothenbacher D., Bode G., Berg G., Knayer U., Gonser T., Adler G., Brenner H. Helicobacter pylori among preschool children and their parents: evidence of parent-child transmission. J. Infect. Dis. 1999;179:398–402. [PubMed: 9878024]
Rothenbacher D., Bode G., Brenner H. Helicobacter pylori among siblings. Lancet. 2000;355:1998. [PubMed: 10859066]
Rothenbacher D., Bode G., Winz T., Berg G., Adler G., Brenner H. Helicobacter pylori in out-patients of a general practitioner—prevalence and determinants of current infection. Epidemiol. Infect. 1997;119:151–157. [PMC free article: PMC2808836] [PubMed: 9363013]
Sarker S. A., Rahman M. M., Mahalanabis D., Bardham P. K., Hildebrand P., Beglinger C., Gyr K. Prevalence of Helicobacter pylori infection in infants and family contacts in a poor Bangladesh community. Dig. Dis. Sci. 1995;40:2669–2672. [PubMed: 8536529]
Sasaki K., Tajiri Y., Sata M., Fujii Y., Matsubara F., Zhao M. G., Shimizu S., Toyonaga A., Tanikawa K. Helicobacter pylori in the natural environment. Scand. J. Infect. Dis. 1999;31:275–280. [PubMed: 10482057]
Sathar M. A., Gouws E., Simjee A. E., Mayat A. M. Seroepidemiological study of Helicobacter pylori infection in South African children. Trans. R. Soc. Trop. Med. Hyg. 1997;91:393–395. [PubMed: 9373630]
Schutze K., Hentschel E., Dragosics B., Hirschl A. M. Helicobacter pylori reinfection with identical organisms—transmission by the patients' spouses. Gut. 1995;36:831–833. [PMC free article: PMC1382617] [PubMed: 7615268]
Shames B., Krajden S., Fuksa M., Babida C., Penner J. L. Evidence for the occurrence of the same strain of Campylobacter pylori in the stomach and dental plaque. J. Clin. Microbiol. 1989;27:2849–2850. [PMC free article: PMC267140] [PubMed: 2592545]
Sipponen P. Helicobacter pylori: a cohort phenomenon. Am. J. Surg. Pathol. 1995;19:S30–S36. [PubMed: 7762737]
Song O., Lange T., Spahr A., Adler G., Bode G. Characteristic distribution pattern of Helicobacter pylori in dental plaque and saliva detected with nested PCR. J. Med. Microbiol. 2000;49:349–353. [PubMed: 10755629]
Suzuki J., Muraoka H., Kobayasi I., Fujita T., Mine T. Rare incidence of interspousal transmission of Helicobacter pylori in asymptomatic individuals in Japan. J. Clin. Microbiol. 1999;37:4174–4176. [PMC free article: PMC85917] [PubMed: 10565957]
Teh B. H., Lin J. T., Pan W. H., Lin S. H., Wang L. Y., Lee T. K., Chen C. J. Seroprevalence and associated risk factors of Helicobacter pylori infection in Taiwan. Anticancer Res. 1994;14:1389–1392. [PubMed: 8067711]
Thomas J. E., Dale A., Harding M., Coward W. A., Cole T. J., Weaver L. T. Helicobacter pylori colonization in early life. Pediatr. Res. 1999;45:218–223. [PubMed: 10022593]
Thomas J. E., Gibson G. R., Darboe M. K., Dale A., Weaver L. T. Isolation of Helicobacter pylori from human faeces. Lancet. 1992;340:1194–1195. [PubMed: 1359263]
Tomb J. F., White O., Kerlavage A. R., Clayton R. A., Sutton G. G., Fleischmann R. D., Ketchum K. A., Klenk H. P., Gill S., Dougherty B. A., Nelson K., Quackenbush J., Zhou L. X., Kirkness E. F., Peterson S., Loftus B., Richardson D., Dodson R., Khalak H. G., Glodek A., Mckenney K., Fitzegerald L. M., Lee N., Adams M. D., Hickey E. K. The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature. 1997;388:539–547. [PubMed: 9252185]
Torres J., Lealherrera Y., Perez Perez G., Gomez A., Camorlingaponce M., Cedillorivera R., Tapiaconyer R., Munoz O. A community-based seroepidemiologic study of Helicobacter pylori infection in Mexico. J. Infect. Dis. 1998;178:1089–1094. [PubMed: 9806039]
Vaira D., D'Anastasio C., Holton J., Dowsett J. F., Londei M., Bertoni F., Beltrandi E., Grauenfels P., Salmon P. R., Gandolfi L. Campylobacter pylori in abattoir workers: is it a zoonosis? Lancet. 1988;ii:725–726. [PubMed: 2901576]
Van Zanten S. Do socio-economic status, marital status and occupation influence the prevalence of Helicobacter pylori infection? Aliment. Pharmacol. Ther. 1995;9:41–44. [PubMed: 8547527]
Vanzanten S. J. O. V., Pollak P. T., Best L. M., Bezanson G. S., Marrie T. Increasing prevalence of Helicobacter pylori infection with age—continuous risk of infection in adults rather than cohort effect. J. Infect. Dis. 1994;169:434–437. [PubMed: 8106778]
Vanzwet A. A., Thijs J. C., Koolstrasmid A. M. D., Schirm J., Snijder J. A. M. Use of PCR with feces for detection of Helicobacter pylori infections in patients. J. Clin. Microbiol. 1994;32:1346–1348. [PMC free article: PMC263696] [PubMed: 7519630]
Varoli O., Landini M. P., LaPlaca M., Tucci A., Corinaldesi R., Paparo G. F., Stanghellini V., Barbara L. Presence of Helicobacter pylori in gastric juice. Am. J. Gastroenterol. 1991;86:249. [PubMed: 1992647]
Velazquez M., Feirtag J. M. Helicobacter pylori: characteristics, pathogenicity, detection methods and mode of transmission implicating foods and water. Int. J. Food Microbiol. 1999;53:95–104. [PubMed: 10634701]
Vincent P., Gottrand F., Pernes P., Husson M. O., Lecomtehoucke M., Turck D., Leclerc H. High prevalence of Helicobacter pylori infection in cohabiting children—epidemiology of a cluster, with special emphasis on molecular typing. Gut. 1994;35:313–316. [PMC free article: PMC1374581] [PubMed: 8150338]
Webb P. M., Knight T., Greaves S., Wilson A., Newell D. G., Elder J., Forman D. Relation between infection with Helicobacter pylori and living conditions in childhood—evidence for person to person transmission in early life. Br. Med. J. 1994;308:750–753. [PMC free article: PMC2539652] [PubMed: 8142828]
Webb P. M., Knight T., Newell D. G., Elder J. B., Forman D. Helicobacter pylori transmission—evidence from a comparison with hepatitis A virus. Eur. J. Gastroenterol. Hepatol. 1996;8:439–441. [PubMed: 8804871]
Woodward M., Morrison C., McColl K. An investigation into factors associated with Helicobacter pylori infection. J. Clin. Epidemiol. 2000;53:175–181. [PubMed: 10729690]
Copyright © 2001, ASM Press.
Bookshelf ID: NBK2421PMID: 21290723


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