Background:
The purposes of this study were to examine the oral tissues and caries prevalence of children undergoing liver transplantation, and to evaluate the relationship between tooth staining and serum bilirubin level.
Methods:
Thirty-four children (22 boys and 12 girls) under the age of 6 years with end-stage liver disease were referred from the Liver Transplantation Center at Kaohsiung Chang Gung Children's Hospital, Taiwan. Oral tissues were examined, and photographs taken to determine the green staining of the teeth and gingiva. A questionnaire was completed by their parents. Serum bilirubin levels were collected preoperatively in these children. Student's t-test was used to compare the mean decayed, missing, and filled tooth (dmft) difference between night-fed and non-night-fed groups, and to test the relationships between tooth staining and serum bilirubin levels.
Results:
The caries prevalence of the 34 children undergoing liver transplantation was 61.8%. The mean dmft score of children 2 to 6 years old who were night-fed was significantly higher than that of children who were not (10.1±1.2 vs. 6.3±1.2; p=0.038). Green staining of the teeth and gingiva was found in 61.3% of cases in children with biliary atresia. Total serum bilirubin levels were significantly higher in the green-stained group than in the non-stained group (17.87±2.50 vs. 2.20±0.65; p<0.01).
Conclusions:
Oral findings of children undergoing liver transplant presented significant green staining of the teeth and gingiva related to high serum bilirubin levels. Children who were night-fed showed an increased risk of developing caries suggesting that oral hygiene instructions should begin as early as possible before liver transplantation.
(Chang Gung Med J 2003;26:184-8)

Key words:
biliary atresia, caries prevalence.

METHODS

Thirty-four children (22 boys and 12 girls) under 6 years of age with end-stage liver disease were referred from the Liver Transplantation Center at Kaohsiung Chang Gung Children's Hospital, Taiwan from 2000 to 2001 for preoperative evaluation. The research protocol was recognized by the Hospital Research Committee, and an informed consent form for each patient was signed by their parents or guardians. The types of pediatric liver disorders were classified. Dental examinations were performed using an on-site dental chair, mirrors, and explorers under focused light. Dental caries was diagnosed based on the modified method of Rasike (1972) and assessed using decayed, missing, and filled tooth (dmft) and surface (dmfs) indices.(17) A questionnaire completed by their parents was designed to investigate the children's feeding habits.(18) Children were divided into night-fed and non-night-fed groups according to responses to questions concerning the habit and frequency of night-feeding practices. A child was assigned to the night-fed group if the answers indicated a nighttime bottle-feeding habit.
Oral tissues were examined, and photographs taken to determine the green staining of the teeth and gingiva in children with congenital biliary atresia. Photographs were projected on a screen and classified as green-stained and non-stained groups according to consensus reached by 2 examiners. Cases were classified into the non-stained group when the 2 examiners had an opposite opinion. Serum bilirubin levels including TB and DB were tested and data collected preoperatively in these children.
Student's t-test was used to compare the mean dmft difference between night-fed and non-night-fed groups, and to test the relationship between stained teeth and serum bilirubin levels. The level of significance (a) was set at 0.05.

RESULTS

Of the 34 children undergoing liver transplantation, 91.2% (31) had congenital biliary atresia. The caries prevalence of the 34 children undergoing liver transplantation was 61.8%. The mean dmft scores were 0±0 (0-2 years), 6.67±1.21 (2-4 years), and 10.44±1.16 (4-6 years), respectively (Table 1). The mean score of dmft for children 2 to 6 years old who were night-fed (n=11) was significantly higher than that of children who were not night-fed (n=10) (10.1±1.2 vs. 6.3±1.2; p=0.038). Green staining of the teeth and gingiva was found in 61.3% (19/31) of the children with congenital biliary atresia (Fig. 1). TB and DB were significantly higher in the green-stained group than in the non-stained group (p=0.003 and p=0.002, respectively) (Table 2).

DISCUSSION

As shown in Table 1, congenital biliary atresia accounted for 91.2% of pediatric liver transplants in this center compared to 40%-70% in other centers.(5) The affected children are often plagued by long-standing cholestasis and life-long jaundice. Other indications for pediatric liver transplantation include metabolic disorders associated with cirrhosis, fulminant hepatic failure, malignant tumors without extrahepatic metastases, and chronic liver disease leading to decompensated cirrhosis.(5) The types of liver transplants may include whole graft, reduced-size graft, split-liver graft, living-donor graft, and auxiliary transplantation. Early treatment with liver transplantation and immunosuppressive therapy (cyclosporine) after surgery provides a cure for such end-stage liver disease.
In this survey, the caries prevalence for the liver transplant children was 61.8%. The mean dmft scores of patients 2 to 6 years old were much higher when compared with the respective mean dmft scores of Taiwanese children (Table 1).(19) Morisaki et al. found rampant caries in 5 of 7 patients with congenital biliary atresia in their survey.(8,12) Enamel hypoplasia was generally found in most of these cases and was considered to be a predisposing factor for caries.(6,8,10) However, enamel hypoplasia may occur in children who have a history of unfavorable general health or nutritional problems in early infancy as in the chronic liver diseases shown here. This might not fully account for the higher caries indices in these children 2 to 6 years old. The present study showed that children who were night-fed had significantly higher dmft scores than children who were not. A prolonged night bottle-feeding habit is the other contributing factor causing tooth decay. The term "early childhood caries" describes this type of rampant dental caries in infants and toddlers, which is strongly related to the nursing habit.(20) It also highlights a number of issues, especially parental overindulgence of a child with a life-threatening disease.
It is therefore important that dentists, as a member of a team for liver transplantation, monitor the dental health of patients. Routine dental care and caries prevention programs need to be planned for those children during pre-liver or post-liver transplantation in order to reduce the risk of systemic infection arising from the oral cavity. Oral hygiene instructions to parents especially for eliminating the night bottle habit should begin as early as possible before liver transplantation.
Green staining of the teeth and gingiva was found in 61.3% of cases with biliary atresia. In this study, serum bilirubin levels (TB and DB) were significantly higher in the green-stained group than in the non-stained group (p=0.003 and p=0.002, respectively) (Table 2). Green staining of the teeth and gingiva appears to be associated with fetal or neonatal hyperbilirubinemia as a result of chronic liver failure. Stained cases showed various degrees of green staining in the primary dentition suggesting a correlation between the degree of tooth staining and the severity of disease. An extracted tooth of a stained case showed that the deeply stained portion of the root formed prior to liver transplantation was clearly demarcated from that normally formed after transplantation (Fig. 2). A histological study by Seow et al. demonstrated that dentin formed prior to liver transplantation had a larger number of irregular tubules compared to those fewer regular tubules formed after transplantation.(6,10) Further esthetic problems of stained teeth probably need to be solved by using composite resin, veneered crown, and laser whitening procedures as the children grow older.

REFERENCES

1. Little JW, Rhodus NL. Dental treatment of the liver transplant patient. Oral Surg Oral Med Oral Pathol 1992;73: 419-26.
2. MacDougall BRD, Neuberger JM, Williams R. Patients for liver transplantation: assessment , survival, and rehabilitation. In: Farman JV, ed. Transplant surgery anaesthesia and perioperative care. New York: Elsevier Science Publishing 1988;343-61.
3. Svirsky JA, Saravia ME. Dental management of patients after liver transplantation. Oral Surg Oral Med Oral Pathol 1989;67:541-6.
4. Starzl TE, Iwatsuki S, Van Thiel DH, Gartner JC, Zitelli BJ, Malatack JJ, Schade RR, Shaw BW, Hakala TR, Rosenthal JT, Porter KA. Evolution of liver transplantation. Hepatology 1982;2:614-36.
5. Sheehy EC, Heaton N, Smith P, Roberts GJ. Dental management of children undergoing liver transplantation. Pediatr Dent 1999;21:272-80.
6. Seow WK, Shepherd RW, Ong TH. Oral changes associated with end-stage liver disease and liver transplantation: implications for dental management. J Dent Child 1991;58:474-80.
7. Herbert FL, Delcambre TJ. Unusual case of green teeth resulting from neonatal hyperbilirubinemia. J Dent Child 1987;54:54-6.
8. Morisaki I, Abe K, Tong LS, Kato K, Sobue S. Dental findings of children with biliary atresia: report of seven cases. J Dent Child 1990;57:220-3.
9. Belanger GK, Sanger R, Casamassimo PS, Bystrom EB. Oral and systemic findings in biliary atresia: report of 11 cases. Pediatric Dent 1982;4:322-26.
10. Shepherd RW. The treatment of end-stage liver disease in childhood. Aust Paediatr J 1988;24:213-6.
11. Odel GB. Neonatal hyperbilirubinemia. New York: Grune and Stratton, Inc., 1980.
12. Shapiro BM, Gallagher FE, Needleman HL. Dental management of the patient with biliary atresia. Report of two cases. Oral Surg 1975;40:742-7.
13. Morimoto A, Morimoto Y, Maki K, Nishida I, Kawahara K. Dental treatment of a prospective recipient of a liver transplant: a case report. J Clin Pediatr Dent 1998;23:75-8.
14. Funakoshi Y, Ohshita C, Moritani, Hieda T. Dental findings of patients who underwent liver transplantation. J Clin Pediatr Dent 1992;16:259-62.
15. Allman SD, McWhorter AG, Seale NS. Evaluation of cyclosporin-induced gingival overgrowth in the pediatric transplant patient. Pediatr Dent 1994;16:36-40.
16. Uemoto S, Tanaka, K, Honda K, Tokunaga Y, Sano K, Katoh H, Yamamoto E, Takada Y, Ozawa K. Experience with FK 506 in living-related liver transplantation. Transplant 1993;55:288-92.
17. Rasike AW. Criteria for diagnosis of dental caries. In Proceedings of the Conference on Clinical Testing of Cariostatic Agents. Chicago, October 14-16, 1968. Chicago: American Dental Association, 1972.
18. Lin YT, Tsai CL. Caries prevalence and bottle-feeding practices in 2-year-old children with cleft lip, cleft palate, or both in Taiwan. Cleft Palate-Craniofac J 1999;36:522-6.
19. Yao JH, Chang CS. Dental caries status of preschool children in Taipei. Chin Dent J 2001;20:283-96.
20. O悆ullivan DM, Tinanoff N. Social and biological factors contributing caries of the maxillary anterior teeth. Pediatr Dent 1993;15:41-4.
21. Rosenthal P, Ramos A, Mungo R. Management of children with hyperbilirubinemia and green teeth. J Pediatr 1986;108:103-5.

From the Department of Dentistry, 1Department of Surgery, Chang Gung Memorial Hospital, Kaohsiung.
Received: Aug. 29, 2002
Accepted: Nov. 25, 2002
Address for reprints: Dr. Yng-Tzer Lin, Department of Dentistry, Chang Gung Memorial Hospital. 123, Dabi Road, Niausung Shiang, Kaohsiung, Taiwan 833, R.O.C.
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