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1 Indiana University School of Dentistry, Department of Periodontics and Allied Dental Programs, 1121 West Michigan Street, Indianapolis, IN 46202;
*corresponding author, mkowolik{at}iupui.edu
CONTROVERSY
The evidence supporting the role of the oral cavity as a significant reservoir of Helicobacter pylori is inconclusive. If the oral cavity is a reservoir for H. pylori, is this significant for subsequent gastric infection and thus disease risk? The authors contend that the answer lies, at least in part, in the conduct of studies using more appropriate methodology, designed to test the specific hypotheses being presented.
— Olav Alvares, Editor
Abstract Helicobacter pylori and Gastric Disease Detection of Oral H. pylori The Oral Cavity as a Reservoir for H. pylori Is the Mouth Significant in Gastric Infection? How is Oral H. pylori Transmitted? The Potential Significance of Oral H. pylori Acknowledgments REFERENCES
| Abstract |
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Key words. Helicobacter pylori, transmission, oral, mouth, dental plaque
| Helicobacter pylori and Gastric Disease |
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Although prevalence is decreasing, H. pylori infection remains one of the most common in man. Based on the results of serological tests that detect the presence of antibodies to H. pylori antigen, the carriage rate of H. pylori is reported to be 20-80% for adults in the developed world, and this figure may rise to more than 90% in the developing world (reviewed by Taylor and Blaser, 1991). These prevalence figures are primarily dependent upon age of the population under study, since, once H. pylori is acquired, it persists into old age unless eradicated by treatment. Crowded living conditions are also associated with increased carriage rates of H. pylori (Mendall et al., 1992), and, consequently, the socio-economic status of study subjects will also influence findings. While gastric H. pylori colonization appears prevalent, it is important to note that full-blown clinical disease develops in a minority of affected patients, where as-yet-undefined conditions, whether host- or bacteria-related, are conducive to disease. However, given its potential to cause disease and its widespread presence among human populations, the impact of H. pylori on health worldwide is still immense. The substantial literature relating to H. pylori since its discovery in 1983 (Marshall and Warren, 1983) serves to emphasize this; yet there still remains considerable controversy on a fundamental issue of the disease process—that is, How and from where is this bacterium acquired? Without such knowledge, we are surely unable to take a crucial step toward instigating measures to interrupt the spread of infection.
One would have expected that, should a significant non-human reservoir for H. pylori exist, it would have already been discovered. However, to date, there has been little success in identifying a consistent non-human source of infection, and one may then conclude that H. pylori is likely to be spread directly from person to person. Certainly, this is supported by increased prevalence in crowded living conditions and clustering of disease within family units (Drumm et al., 1990; Bamford et al., 1993). Nonetheless, the mode of transmission remains something of a mystery. Since blood-borne infection seems improbable, H. pylori must reach the stomach, its primary residence, via the oral cavity. This was most notably demonstrated by the pioneering efforts of Marshall et al.(1985), who, in an attempt to convince the then-many skeptics of the role of H. pylori in gastric disease, ingested H. pylori orally to confirm that it could indeed cause gastritis. The recognition of the oral cavity as the only feasible entry point for gastric H. pylori has led to a considerable interest concerning its role in the transmission process, with speculation of both oral-oral and fecal-oral transmission, with or without an intermediate step in this process. This article will discuss the evidence for a definitive role of the oral cavity in transmission and, more specifically, the role of the oral cavity as a reservoir for gastric H. pylori infection.
| Detection of Oral H. pylori |
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The currently accepted ’gold standard’ for the diagnosis of gastric H. pylori is culture, and this could provide a definitive method for the detection of oral H. pylori. The first documentation of the presence of H. pylori in the oral cavity was reported in 1989, when the bacterium was cultured from the dental plaque of one of 29 patients with H. pylori-associated gastric disease (Krajden et al., 1989). Since then, culture of oral H. pylori has also met with limited success. While the bacterium has been isolated from dental plaque and saliva samples, detection rates have been consistently low, as illustrated in Table 1
, although there are exceptions to this (Majmudar et al., 1990; D’Alessandro and Seri, 1992). In both of these studies, confirmation of isolate identity by means of molecular methods was not performed, and, as a result, there is a potential for false-positives (Namavar et al., 2001).
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With the advances in molecular technology, the potential difficulties with culture have been circumvented by the use of the polymerase chain-reaction (PCR), which permits the amplification of a species-specific region of DNA for subsequent detection by agarose gel electrophoresis. PCR allows for the rapid detection of even small numbers of specific bacteria within a sample and obviates the need for viable organisms. By this method, H. pylori has been detected more frequently in oral samples, but results have been very variable, with a detection rate ranging from 0% to more than 90% (Tables 2, 3). Naturally, these results leave the scientific community as confused as ever, and there is a need to establish why such discrepancies exist. In this context, methodological differences between studies can most simply be divided into three areas: study population, oral sample collection, and laboratory detection procedure.
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based on this criterion. If H. pylori has a preferred oral niche such that it is unevenly distributed within the oral cavity, the chosen oral sample, whether supra- or subgingival plaque or from oral mucosa, as well as the number of sites sampled, is also likely to influence the results significantly. While choice of study population and sampling procedure are likely to contribute to the discrepancies found in the prevalence of H. pylori, it is important to use these differences to assist with our understanding of the role of the oral cavity as a reservoir for gastric H. pylori. Perhaps the most critical consideration in scrutinizing study results is that pertaining to the analysis of the oral sample. The lack of uniformity of laboratory procedures is likely to play a crucial role in the reported inconsistencies, and methods require standardization—for example, with respect to DNA extraction and purification and, most notably, choice of primers for PCR. To date, a host of primers has been used, including those based on the urease genes, 16S ribosomal RNA genes, a gene encoding a specific 26-K protein, and randomly selected DNA fragments. Unfortunately, the sensitivity and specificity differ among the primers (Lu et al., 1999; Song et al., 1999), and the most appropriate method for detection of oral H. pylori has yet to be established. Sensitivity and specificity can be increased by the use of a nested PCR method (Bamford et al., 1998; Jiang et al., 1998), in which a second set of primers specific for an internal region of the primary amplicon is used, and by Southern blot hybridization (Jiang et al., 1998), whereby the PCR amplicons separated by gel electrophoresis are blotted onto a membrane and detected by means of a labeled H. pylori-specific probe, but these procedures have not been consistently used. Most importantly, the use of appropriate positive and negative controls in the PCR reactions is essential, particularly with these heavily contaminated samples where low specificity is a potential problem.
| The Oral Cavity as a Reservoir for H. pylori |
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If a specific niche does exist for H. pylori, then one would expect to find the prevalence to differ between sites. H. pylori has been detected in supragingival plaque (Allaker et al., 2002; Kim et al., 2000; Song et al., 2000a,b), subgingival plaque (Pustorino et al., 1996; Dowsett et al., 1999; Riggio and Lennon, 1999), saliva (see Tables 1, 3) and oral lesions (Mravak-Stipetic et al., 1998; Birek et al., 1999), and on oral mucosa (Mravak-Stipetic et al., 1998; Dowsett et al., 1999; Allaker et al., 2002), but it is difficult to compare prevalence rates between these sites due to variations in methodology among studies. The prevalence of H. pylori in supragingival plaque has been shown to decrease from the molar to the premolar to the incisor region (Song et al., 2000b), suggesting that H. pylori has a distinct distribution within the oral cavity, but, again, this topic needs to be addressed more fully.
Finally, if the oral cavity is a reservoir for H. pylori, it is unclear whether it is a permanent or transient reservoir, but this is likely to have implications in terms of the interpretation of study findings as well as the understanding of its role in gastric infection.
| Is the Mouth Significant in Gastric Infection? |
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While there may well be a positive correlation between oral and gastric H. pylori carriage, more convincing support for the role of the oral cavity in gastric infection would come from demonstrating that the oral cavity and stomach harbor identical or closely related strains of H. pylori. Today, this is invariably addressed by molecular typing, which involves comparison of isolates at the DNA level to look for differences that would indicate different strains. The H. pylori genome displays considerable diversity (Taylor et al., 1992), so that isolates from unrelated patients are likely to be differentiated by these methods. Consequently, it is expected that identification of identical or closely related strains in one or more sites or subjects would suggest transmission between these sites/subjects, or a common source of infection. More specifically, identification of the same strain in the mouth and stomach would support the role of the oral cavity as a reservoir for gastric H. pylori. Molecular typing methods for H. pylori have included restriction fragment length polymorphism (RFLP) analysis, whereby extracted chromosomal DNA is digested with high-frequency cutting restriction endonucleases, and the digested fragments are separated by agarose gel electrophoresis to reveal distinct digest patterns between strains. Since interpretation of the complex band patterns is difficult, this method is often combined with Southern hybridization—for example, using a labeled ribosomal RNA gene probe (ribotyping).
Typing of both oral and gastric H. pylori was first performed by Shames et al.(1989), who used RFLP analysis to determine if oral and gastric isolates from the same subject were identical or closely related. The group reported that H. pylori previously isolated from the dental plaque of one gastric patient (Krajden et al., 1989) was indistinguishable from the gastric isolate, but that strains differed between patients. These results were later confirmed by others (Khandaker et al., 1993; Cellini et al., 1995; Parsonnet et al., 1999). More recently, however, Song et al.(2000c) used nested PCR followed by DNA sequencing of the amplicon to demonstrate that, in the three patients studied, the H. pylori strains detected in the mouth differed from those detected in the gastric samples.
Ferguson et al.(1993) isolated H. pylori from saliva of one of nine patients with gastric H. pylori and again found that it was the same strain as that isolated from the stomach. In this case, both soluble-protein electrophoresis and PCR-restriction endonuclease analysis (PCR-REA) were used for H. pylori typing. In the latter case, the PCR amplicon, rather than chromosomal DNA, is digested with restriction endonucleases, and the simpler pattern is then observed by agarose gel electrophoresis. PCR-REA thus obviates the need for culture, and, with the previously addressed difficulties in culturing oral H. pylori, this facilitates matters immensely. More recently, PCR-REA has been used to type H. pylori detected in both dental plaque and the stomach, and results revealed that, in 13 of 15 cases, the restriction digest patterns of the PCR amplicon from both sites were identical (Oshowo et al., 1998), although only one restriction endonuclease was used, thus limiting the ability to discriminate between strains.
Overall, there is indeed support for the existence of the same strain in both the oral cavity and stomach, but this evidence is far from strong, and additional data are needed. Moreover, there are further issues that should be considered with respect to finding identical or closely related strains of H. pylori in both the oral cavity and the stomach. Since there is evidence that more than one strain of H. pylori may be present in the stomach (van der Ende et al., 1996), the H. pylori strain derived from the oral cavity is not necessarily that responsible for gastric pathology. Furthermore, while finding the same oral and gastric strains in the same subject may suggest that the oral cavity is a reservoir for gastric infection, it may be equally likely that this results from a common source of infection. Alternatively, the source of oral H. pylori may be the stomach, with gastric H. pylori reaching the mouth via vomitus or gastric reflux. This gastro-oral transmission route has certainly been reported, and the subject has been reviewed (Axon, 1995).
| How is Oral H. pylori Transmitted? |
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Oral-oral transmission would most likely involve transfer of H. pylori between individuals via infected saliva. In support of oral-oral transmission, Megraud (1995) found an increased prevalence of H. pylori in children of African mothers who pre-masticate the infants’ food, and gnotobiotic beagle puppies infected with Helicobacter felis, again with a primarily gastric niche, have been demonstrated to transmit the bacteria by licking uninfected animals (Lee et al., 1991). The use of chopsticks in Chinese immigrants in Australia has been associated with a higher prevalence of H. pylori infection, as diagnosed by serology (Chow et al., 1995), and this is presumed to be the result of sharing of chopsticks and H. pylori transmission through saliva.
Fecal-oral transmission is also feasible. Certainly, H. pylori has been cultured from stools, both of children in The Gambia (Thomas et al., 1992), and of adults in England (Kelly et al., 1994) and the USA (Parsonnet et al., 1999). However, as with oral samples, culturing H. pylori from these samples harboring an abundant flora has met with only limited success, and this problem is only exacerbated by the potentially toxic effects of feces on the bacterium. H. pylori has also been detected by PCR in fecal samples (Mapstone et al., 1993b; Shimada et al., 1994; Li et al., 1996; Namavar et al., 2001). Again, detection rates have been consistently low, generally even lower than those reported for oral samples, and, while this could challenge the potential significance of fecal-oral transmission, it has also been attributed in part to inhibition of the PCR reaction by fecal contaminants (Bamford et al., 1998). Fecal-oral transmission is indirectly supported by results of studies performed in South America, which have suggested that water supplies may harbor H. pylori (Klein et al., 1991; Hulten et al., 1996), and consumption of raw vegetables fertilized with human feces is associated with an increased risk of infection (Hopkins et al., 1993). The potential for flies as vectors for enteric disease has been known for years, and, if fecal-oral transmission does occur, the housefly could play a role in this capacity. Indeed, PCR has detected H. pylori in the housefly (Grubel et al., 1998), although not consistently (Osato et al., 1998).
Since there is support for both oral-oral or fecal-oral transmission, it has been proposed that H. pylori can be spread in both manners, and that the principal mode of transmission is likely to be population-dependent. Whether oral-oral or fecal-oral, there is potential for an intermediate step in H. pylori transmission. The possible roles of chopsticks in oral-oral transmission and of water or the housefly in fecal-oral transmission have been mentioned. H. pylori has also been detected, by PCR, beneath the fingernails of indigenous Indians from rural Guatemala (Dowsett et al., 1999), and, more importantly, there was a significant positive association between tongue and fingernail carriage, suggesting a role of finger-mouth contact in the transmission process.
| The Potential Significance of Oral H. pylori |
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The impact of H. pylori oral carriage on the gastric patient has been discussed, but how do these data influence the dental profession? One might hypothesize that those working close to the oral cavity may be at increased risk of H. pylori infection. However, while studies are few, there appears to be little evidence in support of this. Japanese dentists have been reported to be at higher risk for H. pylori infection than age-matched controls, although, for indiscernible reasons, the risk appears to be greater in younger dentists (Honda et al., 2001). By contrast, data reported by Banatvala et al.(1995) indicated that dentists do not appear to have a higher carriage rate than pre-clinical dental students. In terms of patient care, H. pylori seropositivity has been significantly associated with higher plaque levels (Peach et al., 1997) and less frequent visits to the dentists (Gasbarrini et al., 1995), although this has not been consistently found (Nguyen et al., 1993). However, one can do little harm in reinforcing oral hygiene measures and encouraging dental attendance, particularly given the recent interest in an association between oral and general health.
In summary, there is increasing evidence for a role of the oral cavity in transmission of H. pylori, and new methods of detection continue to support this (Young et al., 2001). However, this subject requires considerably more investigation before definite involvement of the oral cavity can be confirmed and preventive measures can be tailored toward the prevention of oral spread. More specifically, more extensive studies to confirm identical or closely related strains in the mouth and stomach are required. Also, a specific niche for H. pylori should be identified in the oral cavity, and the association of H. pylori with other members of the oral microflora needs to be addressed. More successful culturing techniques for oral H. pylori are also needed to confirm its viability and thus infectious status.
For those skeptics among us, if H. pylori were a typical member of the oral flora, one would expect it to be recovered more frequently than has so far been reported, but it may be that oral carriage is population-dependent or is only transient. This will need to be addressed in appropriate population-comparison studies and longitudinal investigations, respectively. However, if the oral cavity is a reservoir for gastric infection, in even a minority of individuals, this should be sufficient to warrant a preventive approach that encompasses consideration of the oral reservoir.
| Acknowledgments |
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