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Abstract

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. STATISTICAL ANALYSIS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

A prerequisite dental evaluation is usually recommended for potential organ transplant candidates. This is based on the premise that untreated dental disease may pose a risk for infection and sepsis, although there is no evidence that this has occurred in organ transplant candidates or recipients. The purpose of this study was to assess the prevalence of dental disease and oral health behaviors in a sample of liver transplant candidates (LTCs). Oral examinations were conducted on 300 LTCs for the presence of gingivitis, dental plaque, dental caries, periodontal disease, edentulism, and xerostomia. The prevalence of these conditions was compared with oral health data from national health surveys and examined for possible associations with most recent dental visit, smoking, and type of liver disease. Significant risk factors for plaque-related gingivitis included intervals of more than 1 yr since the last dental visit (P = 0.004), smoking (P = 0.03), and diuretic therapy (P = 0.005). Dental caries and periodontal disease were also significantly associated with intervals of more than 1 yr since the last dental visit (P = 0.004). LTCs with viral hepatitis or alcoholic cirrhosis had the highest smoking rate (78.8%). Higher rates of edentulism occurred among older LTCs who were less likely to have had a recent dental evaluation (mean 88 months). In conclusion, intervals of more than 1 yr since the last dental visit, smoking, and diuretic therapy appear to be the most significant determinants of dental disease and the need for a pretransplantation dental screening evaluation in LTCs. Edentulous patients should have periodic examinations for oral cancer. Liver Transpl 13:280–286, 2007. © 2007 AASLD.

It has been estimated that 60 to 80% of liver transplant recipients develop an infection, and infection can compromise the survival of any organ transplant recipient.1 Among the multiple causes of posttransplantation infection that are cited in the literature, however, dental sources have rarely been implicated.2, 3 This is unexpected when compared with the prevalence of untreated dental disease in the general population.4 Furthermore, a survey of U.S. organ transplant centers, conducted between 2003 and 2004, found that among the 294 respondents, 28 (9%) reported that they had encountered 1 or more incidents of sepsis from a dental source in a transplant recipient.5 In addition, 34 centers (11%) experienced 1 or more episodes of a dental infection prior to transplantation that necessitated cancellation or postponement of the surgery.5

To prevent such occurrences and to reduce the potential morbidity posed by dental infections, most transplant centers recommend a dental screening examination as part of the pretransplant evaluation process. Among the responders to our survey, 80% indicated that they routinely request such an evaluation.5 Although there are no equivalent protocols for liver transplantation, the 2001 Clinical Practice Guidelines for Renal Transplantation categorized the pretransplant oral examination as “C”. Category “C” denotes that there is “poor evidence regarding [its] inclusion” based on a lack of supporting literature and scientific evidence “but [the] recommendation may be made on other grounds.”6 This suggests that, in the absence of corroborative data relative to the risk of dental infections in recipients of other organ transplants, the prudent approach is to empirically recommend a routine pretransplantation dental screening examination.

The majority of liver transplants are performed for complications resulting from viral hepatitis or alcoholic cirrhosis. These diseases may be associated with lifestyles and behaviors that contribute to dental neglect and untreated dental disease.7 The purpose of this study was to evaluate the oral health status and oral health behaviors of potential candidates for liver transplantation. This information could be used to establish more definitive dental screening guidelines.

PATIENTS AND METHODS

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. STATISTICAL ANALYSIS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Oral examinations were performed on 300 consecutive patients between January 2004 and March 2005. All patients had been referred to the Starzl Transplant Institute for evaluation for a liver transplant. The examinations were conducted in conjunction with evaluations by transplant surgery, hepatology, anesthesiology, psychiatry, and social work. Consent to participate was based on approval by the university's institutional review board to allow all medical record information to be placed in a Transplant Research Registry. Data that were collected included age, gender, employment status, liver disease diagnosis, current smoking, dental insurance, interval since last dental visit, and diuretic use. The presence of xerostomia was based on 1 or more affirmative responses to 4 questions that relate to symptoms of a reduction in saliva as well as clinical signs of hyposalivation (Fig. 1).8

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Figure 1. Oral Evaluation Assessment Form.

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Clinical examinations were conducted by an experienced dental practitioner (J.G.) without dental radiographs. The assessments consisted of the presence and degree of gingival inflammation (gingivitis), the presence and degree of dental plaque accumulation, the number of carious and mobile teeth, rate of total edentulism, and manifestations of xerostomia. These findings were entered on the assessment form (Fig. 1) and in the patients' hospital charts. Patients were advised of the examination findings and whether or not they required dental treatment. The majority of the patients who were identified to have dental treatment needs chose to return to their local dentist for the recommended treatment. Follow-up was not possible to ascertain whether or not the liver transplant candidates (LTCs) complied with the dental care recommendations.

The oral assessment records were coded to deidentify participants, and the data were entered in a spreadsheet program (Microsoft Excel V. II. 3, Redmond, WA).

Patient demographics and liver disease diagnoses were compared with Organ Procurement and Transplantation Network databases from the United Network for Organ Sharing. Having dental insurance, interval since last dental visit, which was dichotomized as ≥12 months, presence of gingivitis, total edentulism, and current smoking were compared with data from the 1997 Behavioral Risk Factor Surveillance System Survey,9 the 1999 Behavioral Risk Factor Surveillance System Survey,10 the Third National Health and Nutrition Examination Survey,11 the Agency for Health Care Research and Quality,12 and Health 2004 from the U.S. National Center for Health Statistics,13 respectively. The severity of gingival inflammation was recorded on a 0–4 scale (Fig. 1) but was collapsed into 2 categories (present or absent) so that it could be compared with the national data.9 Dental plaque accumulation was similarly assessed and dichotomized. Criteria for untreated dental disease included the presence of gingivitis or dental plaque, and the number of mobile teeth (periodontal disease) or carious teeth. Characteristics of the totally edentulous patients were evaluated separately.

STATISTICAL ANALYSIS

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. STATISTICAL ANALYSIS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

The data were analyzed descriptively using percentages, means, and standard deviations. Tests of significance were performed using t-tests and χ2 (chi-squared) analyses as appropriate for the variables used in the comparisons. The 0.05 level was used as the criterion for statistical significance in all tests. All analyses were done with the Statistical Package for the Social Sciences for Windows (versions 13 and 14; SPSS, Chicago, IL).

RESULTS

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. STATISTICAL ANALYSIS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Patient Demographics and Dental Characteristics

Characteristics of the LTCs are compared with recent Organ Procurement and Transplantation Network transplant data in Table 1.14–17 These values were similar with nonsignificant deviations. Dental health features among dentate LTCs are compared with national dental health surveys in Table 29–11 and showed no significant differences. The presence of gingivitis in the LTCs, however, significantly increased in conjunction with the number of months since the patients' previous dental visits (P = 0.0004). Accumulations of dental plaque were detected in 147 of the patients (63.4%). The presence of dental plaque was significantly associated with diuretic use (P = 0.005). (A majority of the LTCs [70.3%] were taking 1 or more diuretic agents.) Dental plaque was also strongly related to the duration since last dental visit (P = 0.0004) and was more prevalent among current cigarette smokers (P = 0.03).

Table 1. Characteristics of the Liver Transplant Candidates
 Pittsburgh studyOPTN (%)
n%
  • Abbreviations: OPTN, Organ Procurement and Transplant Network; NASH, nonalcoholic steatohepatitis.

  • *

    Cryptogenic, postnecrotic, posthepatitis.

  • Autoimmune, primary biliary cirrhosis, primary sclerosing cholangitis.

  • Hepatocellular carcinoma, hemochromatosis, amyloid, sarcoid.

Male17357.758.814
Female12742.341.2
Age distribution (yr)   
 35–499130.824.315
 50–6414448.863.1
 ≥656020.312.6
Employment status   
 Working full-time6321.930.116
 Unemployed103.50.3
 Disabled by disease14751.058.4
 Retired6823.611.2
Liver disease   
 Viral hepatitis B or C9531.741.817
 Alcoholic cirrhosis8026.721.8
 Other cirrhosis*4515.011.0
 Cholestatic liver disease3411.314.9
 NASH268.73.0
 Other206.67.4
Table 2. Dental Health Characteristics
AgePittsburgh studyNational surveys (%)
n%
  1. NOTE: Age adjusted.

Dental insurance   
 18–34240.058.19
 35–541046564
 ≥554332.341.7
Dental visit within past 12 months   
 18–442150.068.110
 45–649564.670.6
 ≥65337562.8
Gingivitis   
 30–39538.549.111
 40–493549.349.7
 50–594045.954.1
 60–692351.152.7
 70–79850.055.0

Edentulism

Total edentulism occurred in 67 LTCs (22.3%). The edentulism rate for LTCs aged 50–69 yr was significantly greater than national rates in 2000 (Table 3A).12 The mean age at which the edentulous LTCs lost their teeth was 40 yr. Edentulism was significantly associated with smoking (P = 0.026). The mean number of months since the last dental visit for the edentulous group was 88.9 months as compared with 27.4 months for the dentate patients (P = 0.0004; Table 3B). An inverse relationship between being dentate or edentulous and having had a dental visit during the previous 12 months was also evident (Table 3B). Among the edentulous patients, 42% indicated that they had dental insurance.

Table 3A. Total Edentulism by Age
Age (yr)Pittsburgh studyNational12
n%%P
30–3911.55.30.766
40–491014.96.80.093
50–592435.813.00.015
60–692943.222.20.001
≥7034.531.50.226
Table 3B. Interval Since Last Dental Visit by Dental Status
 DentateEdentulous
n%n%
  1. NOTE: Age adjusted.

  2. Abbreviation: SD, standard deviation.

1–6 months9440.51218.5
7–12 months5523.7913.8
<12 months8335.84467.7
 Dentate (%)Edentulous (%)
1–12 months64.232.3
>12 months35.867.7
Mean # of months27.4 (SD 46.46)88.9 (SD 121.85)

Smoking

LTCs in all age brackets except the ≥65-yr-old group were currently smoking cigarettes at a higher rate than the national rates in 2002 (Table 4).13 There were significantly more smokers among men and women in the 45- to 64-yr-old age group (P = 0.005). LTCs with hepatitis C or alcoholic cirrhosis were also more likely to smoke (78.8%; P = 0.0004).

Table 4. Current Smoking Rates
Age (yr)Pittsburgh studyNational rates13P
 MaleFemaleMale (%)Female (%)
n%n%
  1. NOTE: Age adjusted.

25–34150133.328.124.10.767
35–44940.9633.329.724.50.556
45–645850.43342.324.421.50.005
≥6539.427.19.38.50.994

Severe Dental Disease

We established that the presence of 2 or more carious teeth and/or 2 or more teeth that were mobile due to periodontal disease were indicators of severe dental disease as well as neglect of oral health. Among the dentate LTCs, 74 patients (31.8%) met these criteria. The predominant risk factor for having severe dental disease was an interval of ≥12 months since the last dental visit (P = 0.001).

Dental Disease and Liver Disease

Among the 300 LTCs, 95 (31.7%) had viral hepatitis and 80 (26.7%) had alcoholic cirrhosis as their primary liver disease. The prevalence of dental disease in this subset of patients did not differ significantly from that of the LTCs with other liver disorders. LTCs with viral hepatitis or alcoholic cirrhosis were, however, more likely to smoke (P = 0.0004). This increases susceptibility to the accumulation of dental plaque, which is a precursor to the development of dental caries and periodontal disease. Smoking was also significantly associated with edentulism (P = 0.026).

Candidiasis

Oral manifestations of candidiasis were seen in 17 patients (5.7%). Each of these patients had 2 or more predisposing factors for candidal overgrowth, which included xerostomia or diuretic therapy (N = 17), having a denture (N = 12), or smoking (N = 6).

Xerostomia

One or more symptoms of dry mouth were reported by 130 LTCs (43%), clinical manifestations of a lack of saliva were found in 86 (28%), and 48 (16%) had both. A reduction in saliva could, in part, be related to diuretic medications that were being taken by 70% of the LTCs. Patients on diuretic therapy were more likely to have accumulations of dental plaque (P = 0.005). In addition, all 17 patients with clinical candidiasis had manifestations of xerostomia or were taking diuretics.

DISCUSSION

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. STATISTICAL ANALYSIS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES

Our findings suggest that this sample of 300 LTCs had dental health attributes that were similar to those of the general population. A number of LTCs, however, presented with neglected oral health, untreated dental conditions, or behaviors that were potential precursors to dental disease. In this group, the significant risk factors for dental disease that were identified are summarized in Table 5. Among these, 12 months or longer since the patients' previous visit to a dentist appears to be the most significant factor that was attributable to untreated dental disease.

Table 5. Potential Risk Factors for Dental Disease in Liver Transplant Candidates
Risk factorOutcomeP
>12 months since last dental visitGingivitis0.0004
>12 months since last dental visitDental plaque0.0004
>12 months since last dental visit≥2 carious teeth0.0004
>12 months since last dental visit≥2 mobile teeth0.0004
>12 months since last dental visit≥2 carious or mobile teeth0.001
Diuretic useDental plaque0.0054
Ages 45–64 yrSmoking0.005
Viral hepatitis or alcoholic cirrhosisSmoking0.0004
SmokingDental plaque0.0344
SmokingEdentulism0.0264
Ages 50–59 yrEdentulism0.0156
Ages 60–69 yrEdentulism0.0012
Edentulism≥12 months since last visit0.0004
Viral hepatitis or alcoholic cirrhosis≥12 months since last visit0.575
Viral hepatitis or alcoholic cirrhosisEdentulism0.4590
Viral hepatitis or alcoholic cirrhosisInsurance0.7250
Viral hepatitis or alcoholic cirrhosis≥2 carious teeth0.343
Viral hepatitis or alcoholic cirrhosis≥2 mobile teeth0.432

A number of other factors that may have important health implications for LTCs were also identified.

Manifestations of a reduction in saliva were found in 56% of the LTCs. A number of features associated with advanced liver disease can diminish the amount of saliva, which in turn, promotes the deposition and retention of dental plaque.18, 19 The management of ascites and/or edema, frequent complications of cirrhosis, may require the use of diuretic agents that can reduce saliva production. The development of ascites has also been recognized as a possible indication for liver transplantation.20 In the present study, 70% of the LTCs were taking 1 or more diuretic agents, and this was significantly associated with the presence of dental plaque. LTCs may require mood modifiers, and those with anticholinergic activity may decrease saliva. (The likelihood of xerostomia increases with the number of medications being taken.)21 Furthermore, chronic active hepatitis, autoimmune hepatitis, and primary biliary cirrhosis have been associated with Sjögren's syndrome, another cause of xerostomia.18

Candidiasis, which may arise from colonization in the oropharynx, can be a significant source of infection in liver transplant recipients.1, 22 We identified 17 LTCs with oral candidal lesions. All 17 patients had risk factors for candidiasis, including symptoms of xerostomia or diuretic therapy, and 15 of the 17 (88%) were smokers or had a denture. A number of our LTCs also had diabetes, which, in addition to the above, is another contributing factor to candidal overgrowth.23

The potential impact of these complications of xerostomia could be compounded by a prolonged period on the transplant waiting list. (As of February, 2006, this ranged from a median of 790 to 926 days.)24

The prevalence of cigarette smoking among LTCs is another cause for concern,25, 26 and rates of 33 to 78.8% were observed in the present study. More men and women in all age brackets except the ≥65-yr-old group, and twice as many 45- to 64-yr-old men were smoking than national estimates in 2002.13 The highest rate of smoking (78.8%) occurred among LTCs who had hepatitis C or alcoholic cirrhosis. This is attributable to the high degree of previously established associations among smoking, alcohol, and/or drug abuse.25, 27, 28 Smoking accelerates the progression of periodontal disease and subsequent tooth loss.29–31 The LTCs who smoked were more likely to have dental plaque, and there were significantly more smokers who had become edentulous.

Liver transplant recipients have been shown to be at greater risk of developing squamous cell carcinoma of the upper aerodigestive tract.32, 33 The development of this tumor may, in part, to be related to immunosuppression but may be primarily attributable to smoking. The older age of LTCs, combined with the cumulative number of years smoked, particularly among the greater representation of patients with alcoholic cirrhosis or hepatitis C, may be significant components of the cancer risk.34 (We have previously shown that patients who developed head and neck cancers who had heavier daily alcohol consumption also had smoked a greater number of pack years.)35 No precancerous lesions were found in the present study.

Although the overall rate of edentulism among the LTCs was comparable to that of the U.S. population (22%), there were significantly more edentulous individuals in the 50- to 69-yr-old age group. In addition, smokers were significantly overrepresented among edentulous LTCs. Edentulism among smokers is another disturbing finding relative to the development of head and neck tumors in liver transplant recipients. Edentulous individuals are typically less likely to have regular oral examinations.36 Among our edentulous LTCs, 67% had not seen a dentist for more than 1 yr, and the mean interval since their last dental visit was 89 months, despite the fact that 42% reported having dental insurance. This behavior pattern could result in a failure to detect the development of premalignant leukoplakias or early tumors in the oral cavity.

Other physical, behavioral, and/or social comorbidities among LTCs that could contribute to untreated dental disease, as well as tooth loss, include their older age, disability with loss of insurance, preoccupation with medical issues, lack of motivation, anxiety and/or depression, poor health behaviors, or an inability to comply with obligatory health regimens.37–39 Although these components did not appear to have a significant impact on the majority of the LTCs in the present study, patients with hepatitis C or alcohol abuse may particularly be at risk. These factors could also have added impact if the patients have a prolonged period on the waiting list.

It is noteworthy that several of our patients had postponed dental visits or reported that their dentists were reluctant to provide dental care out of concern for clotting problems. These, however, can be readily managed with antifibrinolytic agents including aminocaproic acid (Amicar) administered orally preoperatively or postoperatively as an oral rinse, or tranexamic acid (Cyklokapron) orally pre- or postoperatively.40, 41

Following liver transplantation, modifications in lifestyle, additional financial burdens, and obligatory adherence to treatment regimens may result in compromises in dental care priorities. Physicians and transplant coordinators who provide care for transplant recipients must remind patients of the importance of adhering to daily oral health maintenance regimens. They should also reemphasize the need for compliance with regular dental evaluations. Members of the dental health professions should also be apprised of the oral health care needs of transplant patients.

Conclusions

The risk of infection or sepsis from dental disease prior or subsequent to organ transplantation has not been established but may be significant for some patients. Based on the findings from this study, individuals who have not had a dental evaluation for more than 1 yr are significantly more likely to have dental disease. Current smoking and xerostomia are prevalent in LTCs and represent potential contributory factors to dental disease and oral candidiasis. Edentulous patients should be advised to undergo a periodic oral cancer screening examination.

REFERENCES

  1. Top of page
  2. Abstract
  3. PATIENTS AND METHODS
  4. STATISTICAL ANALYSIS
  5. RESULTS
  6. DISCUSSION
  7. REFERENCES
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