Dental Findings of Kidney and Liver Transplantation Patients from a Brazilian Oral Health Care Service

ABSTRACT

Objective:

To describe dental findings of kidney and liver, pre and post-transplant patients of an oral health care service from a Brazilian Southeast state.

Material and Methods:

A descriptive cross-sectional study was developed with a sample of patients attending the oral health care program for transplantation of Universidade Federal de Minas Gerais. Participants were divided into two groups according to the kind of transplantation-kidney or liver. Characteristics of the sample, sex (male/female), age (18-44; 45-54; 55-80), living region (Belo Horizonte, or outside), phase of transplantation (pre-Tx or post-Tx), and self-report of diabetes mellitus and hypertension were presented by frequencies. Dental caries experienced was measured by Decayed, Missing and Filled-Teeth (DMF-T) index.

Results:

185 patients, kidney (46; 24.9%), and liver (139; 75.1%) were included. Mean DMFT was 18.3 (20.0). DMFT scores of males (18.7; 20.0), females (17.2; 18.0), pre-transplanted (18.3; 20.0), and post-transplanted (18.1; 20.0) were similar. The liver transplantation group (19.3; 20.0) showed higher caries experience comparing to kidney´s (15.2; 17.0).

Conclusion:

Dental caries experience was high in kidney and liver patients under transplantation therapy. This highlights the demand for treatment need in this population.

Keywords:
Dental Caries; Kidney Transplantation; Liver Transplantation; Dental Health Services

Introduction

In December 1954, the kidney was the first human successfully solid organ transplantation (SOT). A couple of years ahead, in the 1960s, other SOT, such as liver, heart, and pancreas was performed [¹]. Since there, consistent improvements in the surgical approach and the immunosuppressive pharmacotherapy made transplantation the standard therapy for patients with irreversible liver failure and end-stage kidney disease (ESKD) [²,³]. Irreversible liver failure is caused by a range of conditions, for example, hepatitis C, alcoholic cirrhosis, and cancer [²]. ESKD indicates the demand for treatment by replacement therapy, either by dialysis or by transplantation. Uncontrolled hypertension and diabetes mellitus are the leading causes of ESKD [⁴,⁵].

In the patients ongoing pre-transplant (pre-Tx) and post-transplant (post-TX) therapy, some oral manifestations may be observed. Some studies reported alterations in the salivary composition, flow, buffering capacity, and the levels of immunoglobulins, IgA, for instance [⁶-⁸]. The colonization of the oral cavity by some microorganisms seems to be increased [⁷,⁹-¹¹]. Besides, the new lifestyle challenges by the transplantation may lead to a reduced priority for dental care [¹²]. These factors can increase the risk of dental caries.

Dental caries is a multifactorial biofilm-modulated disease determined by biological, socio-environmental, and behavioral factors that result in the destruction of the tooth hard tissues [¹³,¹⁴]. If not detected and managed in early stages, small caries lesions tend to increase the degree of tooth destruction reaching the pulp and inducing bacteremia in the periapical region [¹³,¹⁵]. Untreated oral conditions can represent a risk factor for infections [¹⁶,¹⁷]. Post-Tx patients are immunosuppressive to avoid grafting rejection, which makes them vulnerable to infectious diseases [¹⁸].

The omission of dental care before transplantation was associated with an elevated risk of infection [¹⁹]. A survey in the United States’ transplant centers reported that post-transplantation sepsis from a possible dental origin was acknowledged in 27% of the centers. Furthermore, due to dental infection, 38% of respondents stated that transplantations were postponed or canceled [²⁰]. A multinational cohort study reported that edentulousness, and Decayed, Missing and Filled Teeth (DMF-T) index greater than 14 were associated with early mortality in ESKD patients waiting for transplantation [²¹]. This highlights the relevance of dental practitioners in the multidisciplinary SOT team. The adoption of protocols for dental screening before and after transplantation is associated with reduced risk of infection in the oral cavity, decreased utilization of prescribed medicines, early dental rehabilitation, and increased oral health-related quality of life [¹⁷,²²].

During the years 2018 and 2019, 14,477 kidney and liver transplantations have been performed in Brazil [²³]. Previous studies worldwide have shown poor oral health status and high treatment need of patients under transplantation therapy [¹¹,¹²,²⁴-²⁶]. Although the expressive number of SOT in Brazil, little is known about the oral health status of candidates for transplantation in our country. In this manner, this research aimed to describe dental findings of kidney and liver, pre-Tx and post-Tx, patients of an oral health care service from a Brazilian Southeast state.

Material and Methods

Study Design

This is a descriptive cross-sectional study carried out in the state of Minas Gerais (MG), located in the Brazilian Southeast. MG is the second most populous state in the country (19,597,330 inhabitants), including 853 municipalities [²⁷]. According to the last epidemiological report published by MG Transplant - the institution responsible for coordinating the SOT and soft tissue transplantation policy in the state - 2,294 and 47 candidates were on the waiting list for kidney and liver grafting, respectively [²⁸].

Sample and Data Collection

The sample of this study was composed of patients attending the oral health care program for transplantation of Universidade Federal de Minas Gerais, located in Belo Horizonte, capital of the state of MG. This program started in 2002 with blood narrow patients ongoing transplantation. About ten years later, the program initiated oral health care management in liver transplantation patients and, more recently, renal. The program's main goals include comprehensive, efficient, and quick oral treatment for patients on transplantation therapy. This kind/type of service, with the diversity of procedures available, maybe is unique in Brazil.

A secondary database produced with patients' dental records from March 2012 to March 2020 was analyzed in this study. The database includes patient’s dental caries experience, socio-demographic and clinical characteristics. Dental caries was measured by the DMF-T index, according to the recommendations for oral health surveys from the World Health Organization [²⁹]. Undergraduate students performed clinical exams, but all diagnoses were checked by a professor of the program. Other variables included sex (male/female), age (18-44; 45-54; 55-80), living region (Belo Horizonte, or outside), phase of transplantation (pre-Tx or post-Tx) and self-report of diabetes mellitus and hypertension. The following inclusion criteria were required for this research: kidney and liver pre-Tx or, post-Tx patients. Subjects under the age of 18 years and the cases without information on caries experience, socio-demographic and clinical characteristics were excluded.

Data Analysis

Descriptive statistics was performed using the Statistical Package for the Social Sciences (SPSS for Windows version 25.0, SPSS Inc., Chicago, USA). The characteristics of the sample are presented by frequency and proportion. Dental caries experience is presented as mean and median DMFT scores.

Ethical Clearance

The study was approved by ethics committee of Universidade Federal de Minas Gerais (Protocol number CAAE-77375517.9.0000.5149). The participants were verbally informed about the research and provided written informed consent for participation.

Results

A total of 185 patients, including 46 (24.9%) kidney (pre-Tx=37 [80.4%]; post-Tx=9 [19.6%]), and 139 (75.1%) liver (pre-Tx=109 [78.4%]; post-Tx=30 [21.6%]), were included in this study. 71.4% (n=132) were male. Table 1 shows the characteristics of the sample.

Table 1
Characteristics of the sample.

Variables	Kidney Tx	Liver Tx	Kidney Tx + Liver Tx
	N (%)	N (%)	N (%)
Sex
Male	27 (58.7%)	105 (75.5%)	132 (71.4%)
Female	19 (41.3%)	34 (24.5%)	53 (28.6%)
Age (Years)
18 to 44	20 (43.5%)	31 (22.3%)	51 (27.6%)
45 to 54	10 (21.7%)	32 (23.0%)	42 (22.7%)
55 to 80	16 (34.8%)	76 (54.7%)	92 (49.7%)
Living Region
Belo Horizonte	26 (56.5%)	73 (52.5%)	99 (53.5%)
Outside Belo Horizonte	20 (43.5%)	66 (47.5%)	86 (46.5%)
Phase of Transplantation
Pre-Tx	37 (80.4%)	109 (78.4%)	146 (78.9%)
Post- Tx	9 (19.6%)	30 (21.6%)	39 (21.1%)
Diabetes Mellitus
No	37 (80.4%)	103 (74.1%)	140 (75.7%)
Yes	9 (19.6%)	36 (25.9%)	45 (24.3%)
Hypertension
No	14 (30.4%)	90 (64.7%)	104 (56.2%)
Yes	32 (69.6%)	49 (35.3%)	81 (43.8%)
Total	46 (24.9)	139 (75.1)	185 (100.0)

Mean DMFT was 18.3 (Median = 20.0), decayed teeth (1.6; 1.0), missing teeth (9.1; 7.0), filled teeth (7.6; 6.0). Edentulous accounted for 3.8% (n=7), while only 1 (0.5%) participant was caries-free. Mean DMFT scores of males (18.7; 20.0), females (17.2; 18.0), pre-Tx (18.3; 20.0), and post-TX (18.1; 20.0) were similar. Dental caries experience increased with age, ranging from mean 12.7 (13.0) affected teeth in the age bracket of 18-44 years to 21.2 (23.0) affected teeth in the age bracket of 55-80 years. Higher caries experience was observed in the liver transplantation group (19.3; 20.0) compared to kidney´s (15.2; 17.0). DMFT scores are presented for kidney and liver transplantation groups and the whole sample in Table 2.

Table 2
Decayed, Missing, and Filled Teeth (DMF-T) index of kidney and liver patients under transplantation therapy.

	Kidney Tx				Liver Tx				Kidney Tx + Liver Tx
Variables	DT (Me/Md)	MT (Me/Md)	FT (Me/Md)	DMF-T (Me/Md)	DT (Me/Md)	MT (Me/Md)	FT (Me/Md)	DMF-T (Me/Md)	DT (Me/Md)	MT (Me/Md)	FT (Me/Md)	DMF-T (Me/Md)
Sex
Male	2.4 (1.0)	5.1 (3.0)	6.7 (5.0)	14.2 (15.0)	1.6 (1.0)	11.1 (9.0)	7.2 (6.0)	19.9 (21.0)	1.8 (1.0)	9.9 (8.0)	7.1 (6.0)	18.7 (20.0)
Female	1.0 (1.0)	6.7 (5.0)	8.9 (9.0)	16.7 (18.0)	1.3 (1.0)	7.7 (4.5)	8.8 (9.5)	17.4 (18.0)	1.2 (1.0)	7.3 (5.0)	8.8 (9.0)	17.2 (18.0)
Age (Years)
18 to 44	3.0 (1.5)	3.3 (1.0)	6.6 (3.5)	12.8 (12.5)	1.8 (1.0)	4.0 (3.0)	6.8 (5.0)	12.6 (13.0)	2.3 (1.0)	3.7 (2.0)	6.7 (5.0)	12.7 (13.0)
45 to 54	1.0 (1.0)	4.4 (3.5)	10.0 (10.5)	15.6 (17.0)	1.9 (2.0)	9.6 (8.5)	7.9 (6.5)	19.4 (19.0)	1.7 (1.0)	8.4 (7.5)	8.4 (8.0)	18.5 (19.0)
55 to 80	0.9 (0.5)	9.8 (7.0)	7.4 (7.5)	18.1 (18.5)	1.2 (0.0)	13.1 (13.0)	7.7 (6.5)	21.9 (23.0)	1.2 (0.0)	12.5 (12.0)	7.6 (6.5)	21.2 (23.0)
Living Region
Belo Horizonte	1.7 (1.0)	4.5 (3.0)	7.9 (7.0)	14.1 (17.0)	1.5 (1.0)	9.8 (8.0)	8.1 (8.0)	19.2 (20.0)	1.5 (1.0)	8.4 (5.0)	8.0 (8.0)	17.9 (19.0)
Outside Belo Horizonte	2.1 (1.5)	7.5 (5.0)	7.2 (6.0)	16.8 (16.5)	1.5 (1.0)	10.8 (9.0)	7.0 (5.0)	19.3 (20.0)	1.7 (1.0)	10.0 (8.0)	7.0 (6.0)	18.7 (20.0)
Phase of Transplantation
Pre-transplantation	1.6 (1.0)	5.8 (4.0)	6.9 (5.0)	14.3 (16.0)	1.6 (1.0)	10.8 (9.0)	7.3 (5.0)	19.7 (21.0)	1.6 (1.0)	9.5 (7.0)	7.2 (5.0)	18.3 (20.0)
Post-transplantation	2.7 (1.0)	5.9 (3.0)	10.6 (9.0)	19.0 (18.0)	1.3 (0.5)	8.2 (6.5)	8.3 (8.0)	17.8 (20.0)	1.6 (1.0)	7.7 (6.0)	8.8 (9.0)	18.1 (20.0)
Diabetes Mellitus
No	2.0 (1.0)	5.9 (3.0)	8.1 (9.0)	16.0 (18.0)	1.6 (1.0)	9.8 (8.0)	7.7 (6.0)	19.0 (20.0)	1.7 (1.0)	8.8 (6.0)	7.8 (7.0)	18.2 (19.5)
Yes	1.2 (1.0)	5.3 (4.0)	5.4 (4.0)	12.2 (11.0)	1.2 (0.5)	11.6 (9.5)	7.1 (6.0)	20.0 (21.5)	1.2 (1.0)	10.4 (9.0)	6.8 (6.0)	18.4 (20.0)
Hypertension
No	2.9 (1.0)	3.0 (1.0)	7.8 (7.5)	13.6 (14.0)	1.5 (1.0)	9.7 (8.0)	7.9 (6.5)	18.9 (20.0)	1.7 (1.0)	8.8 (7.0)	7.9 (6.5)	18.2 (19.5)
Yes	1.4 (1.0)	7.0 (4.0)	7.5 (6.0)	15.9 (18.0)	1.6 (1.0)	11.3 (10.0)	7.0 (6.0)	19.9 (20.0)	1.5 (1.0)	9.6 (6.0)	7.2 (6.0)	18.3 (20.0)
Total	1.8 (1.0)	5.8 (3.5)	7.6 (6.0)	15.2 (17.0)	1.5 (1.0)	10.3 (8.0)	7.6 (6.0)	19.3 (20.0)	1.6 (1.0)	9.1 (7.0)	7.6 (6.0)	18.3 (20.0)

• Me = Mean; Md = Median; DT= Decayed Teeth; MT= Missing Teeth; FT= Filled Teeth;

Discussion

This study described dental findings from 185 kidney and liver, pre-Tx and post-Tx, patients. The majority were male candidates for a liver. The prevalence of dental caries was high in both groups. However, the mean DMF-T was smaller in the kidney transplantation patients. Also, dental caries experience and severity increased with age.

Considering the entire sample, we found high values of DMF-T. In a previous study [¹²] developed with SOT (heart, liver, and kidney) patients, mean DMF-T pre-transplantation (18.1 ± 5.3) and post-transplantation (16.8 ± 8.3) showed similarity with our findings. Several studies reported poor habits of oral hygiene and poor oral health status among adults under transplantation therapy [¹¹,²⁵,³⁰-³²]. Factors, such as modifications in lifestyle, usage of medicines that reduce salivary flow, and the high burden of ESKD and chronic liver disease in pre-Tx candidates, seem to reduce dental care priorities in this population, increasing the development of caries lesions [³²].

In the reviewed literature, we found two studies developed in the Brazilian Northeast that evaluated oral health status of kidney and liver pre-Tx patients. Menezes et al. [¹⁰] reported a mean DMF-T in patients under dialysis therapy in the state of Maranhão, Brazil, similar to our findings. However, D-component and M-component were higher but, F-component was smaller than our findings. Considering liver pre-Tx, Lins et al. [³²] reported a mean DMF-T in accordance with our results. Nonetheless, mean D-component was high compared to our data, and mean F-component, was small.

In comparison to the Southeast region, the Northeast presents higher levels of poverty [²⁷]. It has been reported earlier [³³,³⁴] there is a relationship between inequalities and the burden of oral diseases and dental caries, access to, and utilization of oral health care services. This may partially explain the higher values of D and M-components but low values of F-component of DMF-T index in the Northeast. National epidemiological surveys showed similar trends within the general population [³⁵]. In this matter, multicenter studies among patients under transplantation therapy in different regions of Brazil could provide evidence about the inequalities in the burden of oral diseases in this group.

Published research regarding dental caries experience in patients under transplantation therapy is controversial. Similar, low, and high DMF-T indices among pre-Tx and post-Tx groups have been reported [⁷,¹⁰-¹²,²⁵,³¹]. In the kidney group, our findings showed higher DMF-T scores in post-Tx. Differently, Schmalz et al. [¹¹] described higher DMF-T in the kidney pre-Tx group (19.47 ± 5.84) compared to post-Tx (17.61 ± 5.81). Considering the liver group, we found small DMF-T scores in the post-Tx. Similar results were reported by one study conducted in Germany, which mean DMF-T of liver pre-Tx (23.7 ± 4.0) was higher than post-Tx (22.8 ± 5.2) [²⁵]. It is noteworthy that, in our research and both discussed studies [¹¹,²⁵], different patients under pre-Tx and post-Tx therapy were assessed. Therefore, this limits comparisons. Moreover, discrepancies in dental caries experience may be explained by different studied populations and methodologies, age groups and, characteristics of health care services in the countries.

This study has some limitations that should be addressed. The limited level of evidence produced by the cross-sectional design. Different kidney and liver, pre-Tx, and post-Tx patients were investigated in this study; therefore, the results must be interpreted with caution. We used a secondary database, which data was not collected specifically for this research. Associated factors to dental caries in transplanted patients, such as the use of medicines that decrease salivary flow and immunosuppressors, could not be assessed. Furthermore, the time in the waiting list and after SOT seems to be associated with dental caries experience; however, this information was not available.

Dental screening, treatment, and rehabilitation should be part of the pre-operative care protocol for patients in the transplant waiting list [¹¹,²⁵,³⁰]. Patients under transplantation therapy usually are systemically compromised, present underlying conditions, and use several medicines. It is possible that general dentists feel insecure to provide dental care to this population [³²]. To our knowledge, there are few specialized transplantation oral health care centers in Brazil. In this context, it is important to identify oral health demands of this population to nurture policymakers' decisions. In this matter, this study provided some insight into the oral health status from both, kidney and liver patients under transplantation therapy attending an oral health care program in a populous state in Brazil.

Conclusion

Dental caries experience was high in kidney and liver, pre-Tx and post-Tx, patients. This highlights the demand for treatment need in this population.

• Financial Support
  None.
• Data Availability
  The data used to support the findings of this study can be made available upon request to the corresponding author.

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Edited by

Academic Editor: Alessandro Leite Cavalcanti

Publication Dates

• Publication in this collection
  02 Apr 2021
• Date of issue
  2021

History

• Received
  20 Aug 2020
• Reviewed
  22 Sept 2020
• Accepted
  12 Oct 2020