Importance of oral health and dental treatment in organ transplant recipients

Abstract

Objectives: The purpose of the present study was to investigate which peri-transplant dental treatments were deemed necessary, and to determine retrospectively how often these treatments were actually performed, in patients who had received organ transplants. Materials and Methods: Medical records of the Department of Advanced General Dentistry at Yonsei University Dental Hospital were searched to identify liver or kidney transplant recipients who attended from 1st March 2014 to 31st December 2017. A total of 418 patients were identified, and their medical charts were reviewed. Sex, underlying systemic disease, oral hygiene status, dental treatment deemed necessary, dental treatment actually performed and durations of follow-up were tabulated. Results: More than half (53.8%) of the liver transplant recipients had poor oral hygiene, and poor oral hygiene was statistically significantly more prevalent in the liver transplant group than in the kidney transplant group (40.3%). In liver recipients in whom scaling was deemed to be required pre-transplant, the rate of it actually being performed pre-transplant was high (83.2%). By contrast, the rates of tooth extraction and prosthetic treatment actually being performed pre-transplant were low (12.8% and 0%, respectively). In kidney recipients, the rates of scaling, tooth extraction and prosthetic treatment actually performed pre-transplant, when deemed to be required, were 93.5%, 10.0% and 0.0%, respectively. Conclusions: We recommend that patients scheduled to receive an organ transplant be referred to a dental clinic as soon as possible beforehand, to remove any potential sources of oral infection. Educating physicians, as well as their patients, about the importance of early dental screening and pre-transplant dental treatment is essential.

Introduction

The survival rate of organ transplant recipients has increased markedly with the development of immunosuppressant drugs1., 2.. Unfortunately, infection frequently occurs in transplant recipients because of their immunosuppressed state, necessitating prophylactic management against future infection³. A systematic approach is required in transplant recipients to prevent infection, including proper dental treatment before and after the transplant. Uncontrolled intraoral infection can cause life-threatening abscesses and sepsis⁴. Dental treatment is therefore an important issue in organ transplant recipients that should not be overlooked.

Dental treatment in organ transplant recipients is divided into two phases: pre-transplantation; and post-transplantation. Pre-transplantation dental care involves eliminating possible sources of oral infection that could lead to systemic infection after the transplant. For example, periodontal disease and dental caries are potential sources of future infection. Pre-transplantation dental treatment and the treatment of dental emergencies have positive effects on the success of transplantation by reducing the possibility of infection. Recent studies suggest that local inflammation caused by intraoral factors can affect the prognosis of organ transplant recipients5., 6.. Post-transplantation dental treatment generally consists of dental caries treatment and prosthetic treatment, particularly because prostheses affect oral intake, and patients with good oral intake recover more rapidly⁷. Although various studies investigating dental treatment in organ transplant recipients have been reported8., 9., 10., 11., 12., 13., 14., 15. and awareness of the importance of dental treatment in this context has increased, few studies have directly investigated how dental treatments are actually provided to these patients.

The purpose of the present study was to investigate which peri-transplant dental treatments were deemed necessary, and to determine retrospectively how often these treatments were actually performed in patients who had received organ transplants. The study also aimed to generate useful information for dentists who evaluate and treat organ transplant recipients.

Materials and Methods

Ethics

The study protocol was approved by the Institutional Review Board at Yonsei University Dental Hospital (approval number 2-2018-0034) and the study was conducted in accordance with institutional guidelines and the guidelines of the Helsinki Declaration.

Patients

The medical records of the Department of Advanced General Dentistry at Yonsei University Dental Hospital were searched for organ transplant recipients who attended from 1 March 2014 to 31 December 2017. A total of 418 patients (256 male, 162 female) who were scheduled to receive either a liver transplant or a kidney transplant were identified, and their medical charts were reviewed. Sex, underlying systemic disease, oral hygiene status, dental treatment deemed necessary (including scaling, periodontal treatment, operative treatment, root canal treatment, tooth extraction, implant surgery and prosthetic treatment), dental treatment actually performed and follow-up duration were tabulated. To evaluate oral hygiene status, a consensus was reached by two experienced dentists based on a clinical oral examination and radiological data pertaining to factors such as gingival swelling, redness, dental calculus deposition and bleeding on probing.

Statistical analysis

Chi-square tests were used to determine the significance of differences in oral hygiene status between liver transplant recipients and kidney transplant recipients (IBM SPSS Statistics for Windows, Version 25.0, released 2017; IBM Corp., Armonk, NY, USA). A value of P < 0.05 was deemed to indicate statistical significance.

RESULTS

The 418 patients identified included 130 liver transplant recipients and 288 kidney transplant recipients. The causes of liver transplantation included cirrhosis (68/130; 52.3%) and liver cancer (62/130 patients, 47.7%). The causes of kidney transplantation included end-stage renal disease (267/288; 92.7%) and failure of a previous kidney transplant (13/288; 4.5%). More than half (70/130; 53.8%) of the liver transplant recipients had poor oral hygiene, and poor oral hygiene was statistically significantly more prevalent in the liver transplant group than in the kidney transplant group (χ² = 6.677, odds ratio 1.730, P = 0.010). Less than half (116/288; 40.3%) of the kidney transplant recipients had poor oral hygiene (Table 1).

Table 1.

Medical history and oral hygiene status of organ transplant recipients

Organ transplanted	Past medical history	Good oral hygiene, n (%)	Poor oral hygiene, n (%)	Total, n
Liver	Liver cirrhosis	36 (52.94)	32 (47.06)	68
	Liver cancer	24 (38.71)	38 (61.29)	62
	Total	60 (46.15)	70 (53.85)	130
Kidney	End-stage renal disease	156 (58.43)	111 (41.57)	267
	Failure of a previous kidney transplant	10 (76.92)	3 (23.08)	13
	Other	6 (75.00)	2 (25.00)	8
	Total	172 (59.72)	116 (40.28)	288

The dental treatments deemed necessary pre-transplant and the dental treatments actually performed pre-transplant are shown in Table 2. In liver recipients in whom scaling was deemed to be required pre-transplant, the rate of it actually being performed pre-transplant was high (83.2%). By contrast, the corresponding rates of actual performance pre-transplant were low for tooth extraction (12.8%) and prosthetic treatment (0.0%). In kidney recipients, the rates of actual performance pre-transplant for procedures deemed necessary were 93.5% for scaling, 10.0% for tooth extraction and 0.0% for prosthetic treatment. The performance rates of scheduled dental treatments post-transplant are shown in Table 3. The overall performance rate was low post-transplant (both kidney and liver) compared with pre-transplant, but the rates of prosthetic treatment and implant surgery increased post-transplant.

Table 2.

Necessary dental treatments and dental treatments actually performed before transplantation

Type of treatment	Liver transplantation			Kidney transplantation
	Necessary (n)	Performed (n)	Performance rate (%)	Necessary (n)	Performed (n)	Performance rate (%)
Scaling	125	104	83.20	276	258	93.48
Periodontal treatment	13	8	61.54	25	10	40.00
Operative treatment	39	9	23.08	67	16	23.88
Root canal treatment	14	3	21.43	13	3	23.08
Extraction	65	8	12.82	110	11	10.00
Prosthetic treatment	37	0	0.00	46	0	0.00
Total	293	132	45.05	537	298	55.49

Table 3.

Scheduled dental treatments and dental treatments actually performed after transplantation

Type of treatment	Liver transplantation			Kidney transplantation
	Scheduled (n)	Performed (n)	Performance rate (%)	Scheduled (n)	Performed (n)	Performance rate (%)
Scaling	25	7	28.00	50	17	34.00
Periodontal treatment	6	0	0.00	18	1	5.56
Operative treatment	31	2	6.45	57	4	7.02
Root canal treatment	13	0	0.00	14	2	14.29
Extraction	50	5	10.00	92	8	8.70
Implant surgery	11	0	0.00	21	1	4.76
Prosthetic treatment	36	4	11.11	38	8	21.05
Total	172	18	10.47	290	41	14.14

Most of the immunosuppressive regimens were tacrolimus-based, and these variously included low-dose steroid and/or antimetabolites or mammalian target of rapamycin (mTOR) inhibitors. No patients were managed with cyclosporine. Only 19/130 (14.6%) liver recipients and 33/288 (11.5%) kidney recipients underwent follow-up dental visits (Table 4). Fifteen (14/130 liver recipients and 1/288 kidney recipients) of the 418 organ recipients died. Of the 14 liver recipients who died, in seven cases death was caused by sepsis and three of those seven patients had oral infections that had been identified pre-transplantation. Although the definite origin of sepsis could not be identified via their medical records, oral factors may have contributed to sepsis in these patients.

Table 4.

Follow-up of organ transplant recipients

Organ transplanted	Followed up (n = 52)				Not followed up (n = 366)
	Follow-up period
	0–3 months	3–6 months	>6 months	Total (%)	Death	No operation	Other*	Total (%)
Liver	5	5	9	19 (14.62)	14	5	92	111 (85.38)
Kidney	3	8	22	33 (11.46)	1	6	248	255 (88.54)

^*Other: unknown or appointment cancelled.

DISCUSSION

Several studies have shown that actively controlling infection can affect the prognoses of organ transplant recipients16., 17.. Post-transplant infections can include periodontal diseases and other oral diseases. Dental caries that migrates into the dental pulp can cause severe pain, difficulty eating and malaise. Such situations can result in oral bacteria reaching the alveolar bone around the root apex via the pulp¹⁸, which then becomes an ongoing source of infection. In severe cases, such infections can lead to resorption of the alveolar bone and form a fistula in the buccal gingiva, or cause an abscess in the vestibular space¹⁹. The gingival sulcus and periodontal pocket are susceptible to microbial colonisation²⁰. Uncontrolled periodontal disease – particularly periodontitis – can lead to tooth loss as a result of alveolar bone loss, and it can be a source of wider infection.

The Department of Advanced General Dentistry at Yonsei University Dental Hospital has established a cooperative programme with the Departments of Gastroenterology, Nephrology and Transplantation Surgery. The aims of the programme are to develop and implement routine examination of the oral condition of organ transplant recipients, and eliminate sources of oral infection prior to transplantation. Patients are typically admitted to the hospital 2 or 3 days before the transplant, allowing them time to visit the dental hospital. In the current study the oral hygiene status of organ transplant recipients was generally poor. Compared with kidney recipients, a higher percentage of liver recipients had poor oral hygiene status. The reason for this is unclear, but we suspect that the general health condition may differ between liver transplant recipients and kidney transplant recipients. Pinson et al.²¹ assessed Karnofsky Performance scores in patients before and after organ transplantation. This scoring system measures a patient’s capacity to perform daily activities on a scale from 1 to 100, where 80–100 corresponds to the capacity to perform normal activity (‘able’), 50–79 corresponds to requirement for assistance and an inability to work (‘unable’) and 0–49 corresponds to requirement for specialised care and hospitalisation (‘disabled’)²². In Pinson et al.²¹, the performance scores of recipients before liver transplantation were as follows: 13% were able, 57% were unable and 30% were disabled (mean score 53% ± 3%). The performance scores of recipients before kidney transplantation were relatively better, with 56% able, 44% unable and none disabled (mean score 75% ± 1%). Because oral hygiene habits are included in the daily activities measured using the Karnofsky score, the low performance status of liver transplant recipients (i.e., the majority feeling unable or disabled) could explain the comparatively poor oral hygiene status of these patients.

Because prospective organ transplant recipients were referred to the dental hospital just 2 or 3 days before undergoing transplantation, performing any pre-transplant dental treatment was difficult. Moreover, transplantation surgeons were concerned about the deterioration of a patient’s condition after invasive dental treatments, such as periodontal surgery and tooth extraction, which could delay the transplantation surgery. As a result, patients only received some of the dental treatments that were deemed to be required, and most patients only underwent minimal non-invasive dental treatments, such as scaling. To improve this situation, patients should be referred for dental examinations and treatments on an outpatient basis long before organ transplantation. In patients for whom invasive procedures (such as tooth extraction) are required, the invasiveness of the procedure itself should not be a concern. Instead, immediate treatment should be undertaken because of the risk of life-threatening abscess and sepsis from an infection originating in the oral cavity⁴.

In the present study, most post-transplant dental treatments were not performed as scheduled, and the majority of patients were lost during follow-up. This may have been because of a relative lack of patient and/or doctor awareness of the importance of post-transplant dental treatment. Post-transplant prosthetic treatment can improve quality of life by enhancing the capacity for oral intake. Post-transplant dental treatment can be undertaken once the general health of a patient has improved. In cases of invasive dental treatment involving bone surgery, delays of 3–6 months are typically required after transplantation8., 9., 12.. However, even in cases where a patient recovers without complications, invasive dental treatments need to be administered with caution.

Most patients who receive organ transplants require immunosuppressive drugs thereafter, which render them vulnerable to infection after dental treatment23., 24.. The use of prophylactic antibiotics to counter the risk of unknown infection is therefore recommended, under consultation with both the patient’s physician and the surgeon. In the past, cyclosporine was the most commonly used post-transplant immunosuppressive agent, but tacrolimus has since replaced it. Cyclosporine can cause gingival hyperplasia²⁵, resulting in patient discomfort and difficulty brushing teeth, whereas tacrolimus has no adverse dental effects²⁶. The use of tacrolimus has dramatically reduced the incidence of gingival hyperplasia in transplant recipients. None of the patients in the current study was prescribed cyclosporine, and there were no cases of gingival enlargement.

In conclusion, we recommend that patients scheduled to receive an organ transplant should be referred to a dental clinic as soon as possible beforehand, for identification and removal of any potential sources of oral infection. This is particularly important in prospective liver recipients, who may have comparatively poor oral hygiene. Educating physicians, as well as their patients, about the importance of early dental screening and pre-transplant dental treatment is essential. After receiving a transplant, patients should be regularly reminded of the necessity for regular dental check-ups and dental treatment, to improve prognosis. Success of these objectives can only be accomplished via a comprehensive oral care programme with full cooperation among patients, physicians and dentists.

Funding

This research was supported by Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Education (NRF-2017R1D1A1B03033657).

Conflict of interest

None.

Author contributions

Eun-Jung Kwak: Substantial contributions to the conception or design of the work; or the analysis, or interpretation of data for the work; AND Drafting the work or revising it critically for important intellectual content; AND Final approval of the version to be published; AND Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Dong-Jin Kim: Substantial contributions to the acquisition of data for the work; AND Final approval of the version to be published; AND Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Yisel Choi: Final approval of the version to be published; AND Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Dong-Jin Joo: Final approval of the version to be published; AND Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. Wonse Park: Substantial contributions to the conception of the work; AND Final approval of the version to be published; AND Agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.