Scand J Infect Dis 33: 815–817, 2001 ORIGINAL ARTICLE

Dental Caries is Common in Finnish ChildrenInfected with Helicobacter pyloriKAIJA-LEENA KOLHO1, PAÈ IVI HOÈ LTTAÈ 2, SATU ALALUUSUA2, HARRY LINDAHL1,ERKKI SAVILAHTI1 and HILPI RAUTELIN3

From the 1Hospital for Children and Adolescents, Helsinki Uni×ersity Central Hospital, Helsinki, 2The Department ofPedodontics and Orthodontics, Institute of Dentistry, Uni×ersity of Helsinki, Helsinki, and 3The Department ofBacteriology and Immunology, The Haartman Institute, Uni×ersity of Helsinki and Helsinki Uni×ersity Central HospitalDiagnostics, Helsinki, Finland

Childhood factors such as low socioeconomic status are risk factors for Helicobacter pylori infection and Streptococcusmutans-related dental caries. We examined whether H. pylori infection and dental caries are present today in the same groupof children examined previously. We reviewed the public dental health service � les of 21 H. pylori-positive children (uppergastrointestinal endoscopy at a median age of 13.5 y) and 27 H. pylori-negative children (endoscopy at a median age of 12.5y) examined during 1995–98 at the Helsinki University Central Hospital, Finland. All H. pylori-positive children hadexperienced dental caries in their primary or permanent teeth or in both whereas among H. pylori-negative children therespective proportion was 70% (pB0.01). At the age of 7 y, 18% (3 / 17) of the H. pylori-positive children had experiencedcaries in permanent teeth as compared to 0% among H. pylori-negative children (0 / 24; pB 0.05). At the age of 12 y, H.pylori-positive children had more decayed, missing or � lled permanent teeth than H. pylori-negative children (80% vs. 38%;pB0.05). Although a causal relationship between H. pylori and dental caries is unlikely, it is possible that H. pylori-infectedchildren have an increased risk of other health problems, such as dental caries, for which proper treatment is needed.

K.-L. Kolho, Hospital for Children and Adolescents, UniØersity of Helsinki, Box 281, FIN -00029 HYKS, Finland

INTRODUCTION

The prevalence of Helicobacter pylori infection is decreas-ing in developed countries (1). It has been estimated that atpresent : 5–10% of European children are infected (2, 3).Although the exact transmission route is unknown, it isassumed that the infection is transmitted either oro-orallyor feco-orally, most likely during early childhood (4). Itseems that living conditions during the � rst few years of lifeare of major importance for the acquisition of H. pyloriinfection, particularly in Finland. Above the age of 5 y, nomore than :0.3–0.5% of Finnish children become seropos-itive annually (5).

Dental caries is another health problem that is consid-ered to re� ect childhood living conditions and family man-ners. Prevalence of caries is declining in developedcountries, including Finland (6, 7). Streptococcus mutanshas a key role in the development of caries and the risk ofcaries is high if this bacterium is colonized on teeth early inlife (8). As S. mutans-related dental caries and H. pyloriinfection share similar risk factors, such as childhood livingconditions and low socioeconomic status (4, 9), it is possi-ble that these 2 bacterial diseases may coexist in the samegroup of children in Western societies. In Finland, dentalservices are free for all children from birth until the age of19 y, and the attendance of routine examinations in thepublic healthcare system is high (7). To study whether H.pylori-infected children have dental caries, we examined thepublic healthcare dental records of children with biopsy-proven H. pylori infection and their biopsy-negative con-

trols in order to compare the prevalence of caries in thesechildren.

MATERIALS AND METHODS

We reviewed data on children who underwent upper gastrointesti-nal endoscopy at the Hospital for Children and Adolescents,University of Helsinki, Helsinki, Finland during the period 1995–98. We found 22 H. pylori-infected children of Finnish origin witha permanent address in the Helsinki capital area, and these chil-dren formed the original study group. A control group (n¾34)consisted of age- and sex-matched children of Finnish originresident in the Helsinki capital area who underwent upper gas-trointestinal endoscopy at the same time at our hospital but werefound negative for H. pylori.

We retrieved data on all dental examinations carried out in thepublic healthcare system up until April 1999 in the 56 childrende� ned above. Dental � les were obtained from 48 children (86%)referred for upper gastrointestinal endoscopy because of abdomi-nal pain or suspicion of H. pylori infection (n¾33), suspicion ofgastrointestinal re� ux (n¾5) or other reasons (n¾10). Twenty-one children (12 females) were considered H. pylori-infected (uppergastrointestinal endoscopy performed at a median age of 13.5 y;range 4.5–16 y) and 27 children (11 females) H. pylori-negative(upper gastrointestinal endoscopy at a median age of 12.5 y; range4.2–16 y). The age difference between the H. pylori-positive and-negative groups was not signi� cant (p\0.05). H. pylori infectionwas veri� ed in 19 children as positive � ndings in at least two of thefollowing tests: rapid urease test (Jatrox; Procter & Gamble Phar-maceuticals, Weiterstadt, Germany); histologic examination; andserum antibodies to H. pylori in an in-house enzyme immunoassaywith a sensitivity of 88% in children (10, 11). In addition, 2children with chronic gastritis and positive serology and nodularityin the antrum suggestive for H. pylori infection but negativehistologic examination for H. pylori were considered H. pylori-positive. Among the non-infected children, there were no macro-

© 2001 Taylor & Francis. ISSN 0036-5548 DOI: 10.1080:00365540110076624

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Scand J Infect Dis 33K.-L. Kolho et al.816

scopic � ndings in the stomach and histologic examination andresults of serology for H. pylori (n¾22) or rapid urease test(n¾23) were negative (each of the 27 non-infected children under-went serological assessment or rapid urease test or both).

Dental � les

All dental � les were reviewed by one of the authors (P.H.), whowas unaware of the H. pylori infection status of the children. Dataon dental follow-up in the public healthcare system were availableuntil a median age of 15 y (range 5–19 y) for H. pylori-positivechildren and until a median age of 14 y (range 5–18 y) for H.pylori-negative children. The number of decayed, missing and � lledteeth (dmft index for primary teeth and DMFT index for perma-nent teeth; WHO, 1987) was used for describing the prevalence ofcaries. Cumulative caries prevalence was assessed as a combinationof the two indices. Periodontal health was assessed using therecords for Community Periodontal Index of Treatment Needs(CPITN; WHO, 1987). This index is based on the examination of6 index teeth in the permanent dentition and separates healthy(CPITN¾0) and infected (bleeding) periodontium (CPITN¾1),and teeth with dental calculus (CPITN¾2).

Ethics

The study protocol was approved by the Ethics Committee of theMinistry of Social Affairs and Health and by the Ethics Committeeof the Health Department of the City of Helsinki.

Statistical analyses

The Mann–Whitney U-test was used to analyse the correlationbetween the presence or absence of H. pylori infection and eitherthe dmft, DMFT or CPITN indices. Fisher’s exact test was used inthe other statistical analyses. A p-valueB0.05 was consideredsigni� cant.

RESULTS

All H. pylori-positive children had experienced dentalcaries in their primary or permanent dentition or both,compared to 70% of H. pylori-negative children (pB0.01;Table I). The total number of affected teeth did not differbetween H. pylori-positive and -negative children. At theage of 7 y, 75% (36:48) of the children had complete datafor calculation of the dmft index. Caries prevalence of theprimary teeth was 58% (21:36) in these children (dmft index]1; Table I), and showed no signi� cant difference betweenthe H. pylori-positive and -negative groups. At this age,none of the H. pylori-negative children (0:24) but 18%(3:17) of the H. pylori-positive children had experienced

caries in their permanent teeth (pB0.05 for DMFT indexrelated to H. pylori positivity). At the age of 12 y, 80% ofthe H. pylori-positive children and 38% of the H. pylori-negative children had experienced caries in permanent teeth(DMFT index ]1; pB0.05; Table I). At this age, themedian number of affected permanent teeth was 1 (range0–5) in the H. pylori-positive group and 0 (range 0–12) inthe H. pylori-negative group (pB0.05). Eight of the H.pylori-negative children had excellent dental healththroughout the dental follow-up as both dentitions wereintact. The CPITN indices did not differ between H. pylori-positive and -negative children.

DISCUSSION

In this cross-sectional study, all H. pylori-positive childrenhad experienced caries in primary or permanent teeth (orboth), and this proportion was signi� cantly greater thanthat seen among the H. pylori-negative children. At the ageof 7 y, H. pylori-positive children had experienced morecaries in their permanent teeth but there was no differencein the dental health of primary dentition. At this age, thenormal shedding of primary teeth had occurred in manychildren, limiting the data on the health of primary teethand possibly leading to underestimation of caries preva-lence in primary teeth (as the health of missing primaryteeth could not be assessed). The cumulative caries preva-lence in primary and permanent teeth was related to H.pylori positivity but the cumulative number of decayedteeth did not show such a correlation. The number ofdecayed teeth is dependent on the length of follow-up asthe appearance of caries in a single tooth is associated withseveral teeth being affected during the following years (12).In our series, the length of dental follow-up and the agedistribution of H. pylori-positive and -negative childrenwere similar and it is therefore conceivable that there wasno signi� cant difference in the cumulative number of de-cayed teeth.

The cumulative prevalence of caries in our series washigh, as 100% of the H. pylori-positive and 70% of the H.pylori-negative children had experienced caries during theirdental follow-up. At the age of 12 y, however, 20% of theH. pylori-positive and 62% of the H. pylori-negative chil-

Table I. Dental follow-up for the presence of decayed (d :D), missing (m :M) or � lled (f:F) teeth (dmft index for primary teeth and DMFTindex for permanent teeth) of 21 Finnish children with biopsy-pro×en H. pylori infection and their biopsy-negati×e controls (n¾27)

H. pylori-positive children H. pylori-negative children (dentalfollow-up at a median age of(dental follow-up at a median age of14 y; range 5–18 y)15 y; range 5–19 y) p

21:21 (100%) 19:27 (70%) B0.01dmft»DMFT\0 at the end ofdental follow-up

dmft\0 at the age of 7 y 9:15 (60%) 12:21 (57%) \0.05(primary teeth)

DMFT\0 at the age of 12 y 12:15 (80%) 8:21 (38%) B0.05(permanent teeth)

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H. pylori and dental decayScand J Infect Dis 33 817

dren in our series had caries-free permanent teeth. InHelsinki City, : 30% of 12-y-old children examined inpublic health centres between 1995 and 1998 had intactteeth (Public dental care statistics, Helsinki). As poor in-come and lower social class are associated with highercaries prevalence it would be important to know whetherchildren infected with H. pylori differed in this respectfrom those who were not infected. Social class could notbe assessed in this study but the variance in incomeamong Finnish households is among the smallest inWestern societies. In the Helsinki area, the majority ofFinnish children who are H. pylori-positive at endoscopyseem to come from families with high socioeconomicstatus and good housing (13). All children in our serieslived in the Helsinki capital area, which has a municipalwater supply, and there was no difference between the H.pylori-negative and -positive groups in terms of the areainhabited. Therefore it is unlikely that there was a majordifference in the living standard of the 2 groups of chil-dren at the time of the study. The socioeconomic statusat the time of our series, however, is not necessarily thesame as that during the � rst years of life, which is themost susceptible period for transmission of H. pylori andS. mutans infections. The question of whether there wasa difference in social class between the groups during theearly years remains unanswered.

Reports on the oral health of H. pylori-infected pa-tients are few and we found no such reports on H. py-lori-positive children. One epidemiologic study in theadult population of San Marino showed that seropositiv-ity for H. pylori was associated with the presence ofdental prostheses (14), probably re� ecting poor dentaltreatment during previous decades. Another report statedthat oral hygiene and the presence of periodontal diseasein adults did not correlate with the presence of biopsy-proven H. pylori infection (15). Studies on oral healthand H. pylori have mainly focused on the possible role ofthe oral cavity as a transmission route for H. pylori in-fection. Several groups have reported positive � ndings ofeither DNA of H. pylori or culture in samples obtainedfrom dental plaque but contradictory data also exist [fora review, see Thomas et al. (16)]. It is possible that H.pylori is a transient microorganism in the oral cavity (17)and it is unlikely that the high prevalence of dental cariesin H. pylori-positive children is associated with the pres-ence of H. pylori in the oral cavity per se. Other factors,so far unknown, are more likely to be related to thisphenomenon.

In summary, dental caries was invariably present in H.pylori-positive Finnish children living in the capital area.Although a causal relationship between H. pylori anddental caries is unlikely, it is possible that H. pylori-in-fected children may have other health problems as well,such as dental caries, for which proper treatment isneeded.

ACKNOWLEDGEMENTS

This study was supported by the University of Helsinki and by theSigrid Juselius Foundation, Helsinki, Finland.

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9. Vargas CM, Crall JJ, Schneider DA. Sociodemographic distri-bution of pediatric dental caries: NHANES III, 1988-1994. JAm Dent Assoc 1998; 129: 1229–38.

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12. Utriainen P, Pahkala K, Kentala J, Laippala P, Mattila K.Changes in the oral health of adolescents treated by theFinnish public dental services between the ages of 13 and 15years. Commun Dent Oral Epidemiol 1998; 26: 149–54.

13. Kolho K-L, Rautelin H, Lindahl H, Savilahti E. Helicobacterpylori-positive gastritis in pediatric patients with chronic in� -ammatory bowel disease. J Pediatr Gastroenterol Nutr 1998;27: 292–5.

14. Gasbarrini G, Pretolani S, Bonvicini F, Gatto MRA, TonelliE, Megraud F, et al. A population based study of Helicobacterpylori infection in a European country: the San Marino Study.Relations with gastrointestinal diseases. Gut 1995; 36: 838–44.

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Submitted March 5, 2001; accepted May 9, 2001

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