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Received: 13 June 2017    Revised: 10 August 2017    Accepted: 7 October 2017

DOI: 10.1111/tid.12832

ORIGINAL ARTICLE

Association between the time after transplantation and

different immunosuppressive medications with dental and
periodontal treatment need in patients after solid organ
transplantation

Gerhard Schmalz1 | Horst Wendorff1 | Lisa Berisha1 | Anja Meisel1 | 

Florian Widmer1 | Anna Marcinkowski1 | Helmut Teschler2 | 
Urte Sommerwerck2 | Rainer Haak1 | Otto Kollmar3 | Dirk Ziebolz1

1
Department of Cariology, Endodontology
and Periodontology, University of Leipzig,
Leipzig, Germany
2
Department of Pneumology, West German
Lung Center, Ruhrlandklinik, University
Hospital Essen, University Duisburg-Essen,
Essen, Germany
3
Department of General and Visceral
Surgery, HELIOS Dr. Horst Schmidt-Kliniken,
Wiesbaden, Germany
Correspondence
PD Dr. Dirk Ziebolz, MSc, Department
of Cariology, Endodontology and
Periodontology, University Leipzig, Leipzig,
Germany.
Email: dirk.ziebolz@medizin.uni-leipzig.de
Abstract
Objective: The aim of this study was to investigate the association of time after
transplantation and different immunosuppressive medications with dental and peri-
odontal treatment needs in patients after solid organ transplantation (SOT).
Methods: After lung, liver, or kidney transplantation, patients were included and di-
vided into subgroups based on the time after SOT (0-­1, 1-­3, 3-­6, 6-­10, and >10 years)
and immunosuppression (tacrolimus, cyclosporine, mycophenolate, glucocorticoids,
sirolimus, and monotherapy vs combination). Dental treatment need was determined
by the presence of carious lesions, while periodontal treatment need was diagnosed
based on a Periodontal Screening index score of 3-­4. The overall treatment need in-
cluded both the dental and/or periodontal treatment needs. Statistical analysis was
performed using the Kruskal-­Wallis test and chi-­squared test (P < .05).
Results: A total of 169 patients were included after SOT. A dental treatment need of
44%, a periodontal treatment need of 71%, and an overall treatment need of 84%
were detected in the total cohort. Only patients with >10 years after SOT had a lower
dental treatment need compared to the other groups (P = .02). All other comparisons
of dental, periodontal, and overall treatment needs were comparable between sub-
groups depending on time since SOT. Furthermore, no statistically significant differ-
ences were found in terms of the dental, periodontal, or overall treatment needs
following the administration of different immunosuppressive medications.
Conclusion: The high treatment need of patients after SOT, irrespective of the time
since transplantation, suggests insufficient dental and periodontal treatment before
and maintenance after organ transplantation. Furthermore, immunosuppressive
medication was not associated with the treatment need.

KEYWORDS
caries, dental treatment need, immunosuppression, oral health, organ transplantation,
periodontal treatment need, periodontitis

Transpl Infect Dis. 2018;20:e12832. wileyonlinelibrary.com/journal/tid © 2018 John Wiley & Sons A/S.  |  1 of 7
https://doi.org/10.1111/tid.12832 Published by John Wiley & Sons Ltd
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1 |  I NTRO D U C TI O N
In the past several decades, solid organ transplantation (SOT)
has become the standard therapy for patients with irreversible
1,2
organ failure. Owing to improvements in medical care and im-
munosuppressive therapy, the long-­term survival of patients after
SOT has increased, resulting in an expanding group of patients. 3,4
In addition to suffering different causal underlying diseases and
co-­morbidities, which might be relevant for dental care, these pa-
tients receive life-­long immunosuppressive therapy with different
medications. 5
The oral cavity is an important entry portal by which bacteria
can enter the bloodstream.6,7 Accordingly, dental care, especially
the treatment and prevention of oral infections and inflammation,
is of high importance in the vulnerable group of SOT recipients.
Therefore, the importance of early dental rehabilitation before SOT
and rigorous dental care after transplantation appear to be of great
importance.8-13
However, the reality is that there remains a great need for dental
care in this vulnerable patient group. Indeed, previous studies pub-
lished by this working group have demonstrated a high dental and
periodontal treatment need in patients after the transplantation of
different organs, including the kidney, heart, liver, and lung.12,14-16
Thus, patients from these organ groups have been investigated in-
dependently of the time span since transplantation or their form
of immunosuppression. As it is known that immunosuppressive
medication in combination with other factors might influence oral
diseases in transplant recipients,10,17,18 this factor might be of high
clinical relevance. Furthermore, it is unknown whether the high den-
tal and periodontal treatment needs of SOT recipients are caused
by a lack of treatment before SOT or of maintenance after SOT, or a
combination of the two.
Therefore, the aim of this study was to investigate the associ-
ation between the time after transplantation and different immu-
nosuppressive medications with dental and periodontal treatment
needs of patients after SOT. For this, a large group of SOT patients,
including three different organs (kidney, liver, and lung), from pre-
vious studies conducted by this working group should be investi-
gated.14-16 The prediction was that both the time after SOT and the
form of immunosuppression would be associated with the dental
and periodontal treatment needs in this patient group.
2 |  M E TH O DS
This clinical cross-­sectional study was reviewed and approved by
the ethics committee of the University Medical Center Goettingen,
Germany (No. 43/9/07) and by the ethics committee of the
University Hospital Essen (13-­5689-­BO). Research was conducted
in full accordance with the World Medical Association’s Declaration
of Helsinki. The patients were informed verbally, as well as in writ-
ing, about the study and provided written informed consent for
participation.
2.1 | Patients
Patients from 3 different previous studies conducted by this working
group,14-16 which fit specific inclusion criteria, were included. Following
liver and kidney transplantation procedures at the Department of
General, Visceral and Pediatric Surgery of the University Medical
Center Göttingen, patients were asked to participate in the study. They
were assessed during routine follow-­up care from February to July of
2012. Furthermore, patients were recruited after lung transplanta-
tion during routine outpatient visits to the lung transplant unit of the
Ruhrlandklinik, Essen, Germany, between February and October 2014.
The following inclusion criteria were required conditions for
participation in this study: solid organ transplantation (kidney, liver,
lung), any time span after transplantation and regular subsequent
appointments in one of the two transplant centers.
The exclusion criteria were as follows: age <18 years, the pres-
ence of any additional infectious diseases, especially HIV, seizure
and nervous disorders, and pregnancy. As specific dental exclusion
criteria, the inability to undergo complete oral investigation and
toothlessness were formulated.
2.2 | Patient questionnaires
To record the general and medical conditions of the patients, each
patient was given a questionnaire regarding the following points:
immunosuppression and further medication, diabetes status, smok-
ing habits (smoker, former smoker [non-­smoking for <5 years] and
non-­smoker), causal underlying disease for transplantation, and the
time since transplantation. Based on the time span after transplan-
tation, participants were divided into 5 groups (0-­1 year, 1-­3 years,
3-­6 years, 6-­10 years, and >10 years) for analysis. Furthermore, the
immunosuppressive drugs, which were taken by at least 15 patients,
were included in the further analysis. Additionally, the form of immu-
nosuppressive medication, ie, monotherapy or combination therapy,
was considered. Furthermore, patients were asked whether a dental
treatment was performed prior to SOT and if they visit their dentist
regularly.
2.3 | Oral examination
All patients were examined under standardized conditions by an
experienced dentist at the dental clinic of the University Medical
Center Göttingen (kidney and liver), or in the lung transplant unit
of the Ruhrlandklinik, Essen, Germany (lung). The investigation in-
cluded an examination of the teeth and periodontium.
2.3.1 | Dental examination (DMF-­T)
Based on a dental examination with a mirror and probe, all teeth show-
ing a suspected carious lesion of a cavity of the dentin layer, missing
teeth, and teeth with fillings or crowns were recorded. According to
the WHO 1997, the DMF-­T index was determined based on these
dental findings.19 In addition, the degree of caries restoration (%) was
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calculated to give the ratio of filled teeth (FT) to the carious (DT) plus
19
filled teeth (FT) (FT/(DT+FT) × 100). Patients with a degree of caries
restoration below 100% were classified to show their dental treat-
ment needs, as such patients had at least 1 untreated carious lesion.
maximum PSR/PSI value of ≤2 were classified as “no periodontal
treatment need.” A maximum value of 3 or 4 classified a patient for
“periodontal treatment need.”
Furthermore, patients showing dental and/or periodontal treat-
ment needs were classified as having an “overall treatment need.”

2.3.2 | Periodontal examination (PSR/PSI)20,21

In the periodontal examination, periodontal probing depth (PPD)
and bleeding on probing (BOP: positive) were recorded using a
millimeter-­scaled periodontal probe (PCP 15; Hu-­Friedy, Chicago, IL,
USA) on 6 measurement points per tooth. The need for periodontal
treatment was defined in accordance with a PSR®/PSI score of 3 or
4 based on PPD (>3 mm).
The following criteria were used for classification:
• PSR®/PSI 0: if pocket depth <3.5 mm, no bleeding and no calculus.
• PSR®/PSI 1: if pocket depth <3.5 mm, bleeding on probing and no
calculus.
• PSR®/PSI 2: if pocket depth <3.5 mm, bleeding on probing and
calculus is present.
• PSR®/PSI 3: if pocket depth is 3.5-5.5 mm.
• PSR®/PSI 4: if pocket depth >5.5 mm.
For each patient, the maximum value of the PSR®/PSI score
was used for the classification of treatment need. Patients with a
2.4 | Statistical analysis
Statistical analysis was executed using SPSS for Windows, version
24.0 (SPSS Inc., Armonk, NY, USA). Metric variables were tested for
normal distribution with the Kolmogorow-­Smirnow test. None of
the investigated parameters were found to be normally distributed
by the Kolmogorow-­Smirnow test: (P < .05). Consequently, non-­
parametric tests for non-­normal distributed samples were chosen.
For the comparison of more than 2 independent non-­normal distrib-
uted samples, the Kruskal-­Wallis test or the chi-­squared test was
used. A two-­sided significance test was performed for all conducted
tests. The significance level was set at P < .05.
3 | R E S U LT S
3.1 | Patients
A total of 169 SOT patients, including 66 lung Tx, 70 liver Tx, and
33 kidney Tx recipients were included in this study. The mean age

TA B L E   1   Patient characteristics, including general parameters, their immunosuppressive medication, and the different transplanted
organs (lung, liver, and kidney)

Total (n = 169) Lung Tx (n = 66) Liver Tx (n = 70) Kidney Tx (n = 33) P-­value

General parameters
Age 55.44 ± 11.10 54.39 ± 9.71 56.36 ± 12.53 55.61 ± 10.62 .52
Gender female 43% (72/169) 49% (32/66) 37% (26/70) 42% (14/33) .41
Smoking status
Non-­smoker 63% (99/169) 36% (24/66) 78% (49/63) 90% (26/29) <.01
Former smoker 28% (44/169) 64% (42/66) 3% (2/63) 0% (0/29)
Smoker 9% (15/169) 0% (0/66) 19% (12/63) 10% (3/29)
Diabetes mellitus
Yes 24% (40/169) 20% (13/66) 33% (23/70) 12% (4/33) .04
No 76% (129/169) 80% (53/66) 67% (47/70) 88% (29/33)
Time since Tx 7.00 ± 5.72 5.86 ± 3.38 4.91 ± 4.29 13.70 ± 7.10 <.01
Immunosuppressive medication
Tacrolimus 59% (99/169) 64% (42/66) 66% (46/70) 34% (11/33) <.01
Cyclosporine 20% (33/169) 18% (12/66) 13% (9/70) 36% (12/33) .02
Mycophenolate 69% (116/169) 97% (64/66) 49% (34/70) 55% (18/33) <.01
Glucocorticoids 62% (105/169) 100% (66/66) 36% (25/70) 42% (14/33) <.01
Sirolimus 10% (17/169) 18% (12/66) 6% (4/70) 3% (1/33) .02
Monotherapy 23% (38/169) 0% (0/66) 37% (26/70) 36% (12/33) <.01
Combination therapy 77% (131/169) 100% (66/66) 63% (44/70) 64% (21/33)

Tx, transplantation. The results are given as the mean values ± standard deviation or as % (n). Significant findings are highlighted in bold (signifi-
cance level P < .05)
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TA B L E   2   Treatment needs of the study participants in the total cohort and separated between the different transplanted organs (lung,
liver, and kidney). The results are given as the mean values ± standard deviation or as % (n). Significant findings are highlighted in bold
(significance level P < .05)

Total (n = 169) Lung Tx (n = 66) Liver Tx (n = 70) Kidney Tx (n = 33) P-­value

DMF-­T 21.01 ± 5.64 21.21 ± 5.31 22.41 ± 5.25 17.61 ± 5.81 <.01

Degree of caries 89.68 ± 19.34 91.90 ± 14.81 85.57 ± 24.41 93.95 ± 12.91 .24
restoration
Dental treatment need
Yes 44% (74) 41% (27) 50% (35) 36% (12) .36
No 56% (95) 59% (36) 50% (35) 64% (21)
Periodontal treatment need
Yes 71% (120) 83% (55) 57% (40) 76% (25) <.01
No 29% (49) 17% (11) 43% (30) 24% (8)
Overall treatment need
Yes 84% (142) 91% (60) 79% (55) 82% (27) .14
No 16% (27) 9% (6) 21% (15) 18% (6)

DMF-­T, decayed-­, missing-­ and filled-­ teeth index, Tx, transplantation.

TA B L E   3   Dental, periodontal, and overall treatment needs depending on the time since organ transplantation

Time since transplantation in years

0-­1 1-­3 3-­6 6-­10 >10 P-­value

Dental treatment need

Yes 43% (9/21) 56% (22/39) 50% (17/34) 49% (19/39) 20% (7/36) .02
No 57% (12/21) 44% (17/39) 50% (17/34) 51% (20/39) 80% (29/36)
Periodontal treatment need
Yes 76% (16/21) 67% (26/39) 79% (27/34) 67% (26/39) 69% (25/36) .70
No 24% (5/21) 33% (13/39) 21(7/34) 33% (13/39) 31% (11/36)
Overall treatment need
Yes 81% (17/21) 85% (33/39) 97% (33/34) 85% (33/39) 72% (26/36) .08
No 19% (4/21) 15% (6/39) 3% (1/34) 15% (33/39) 18% (10/36)

The results are given as the % (n). Significant findings are highlighted in bold (significance level P < .05).

of the group was 55.44 ± 11.10 years, without statistically signifi-
cant differences between the single organ groups (P = .52). The
average time since organ transplantation was 7.00 ± 5.72 years
for all SOT patients. However, regarding smoking habits, diabe-
tes status, time since transplantation, and different immunosup-
pressive medication, and significant differences between the
single organs (lung, liver, kidney) were detected (P < .05, Table 1).
A total of 71% of the patients stated that they had received a
dental treatment prior to their transplantation. Moreover, 77%
of the patients stated that they were in regular contact with their
dentist.
3.2 | Oral examination
The DMF-­T, degree of caries restoration, and the dental, peri-
odontal, and overall treatment needs are shown in Table 2. A den-
tal treatment need of 44%, a periodontal treatment need of 71%,
and an overall treatment need of 84% were detected in the patient
group. The patients were thereby divided into subgroups depend-
ing on the single organ. After liver transplants, patients were found
to present a lower periodontal treatment need compared to the
lung and kidney transplant patients (P < .01).
3.3 | Treatment need depending on the time since
transplantation
The treatment according to the time since transplantation is pre-
sented in Table 3. Only the dental treatment need was signifi-
cantly different between the different subgroups (P = .02). Thus,
patients who received organ Tx more than 10 years ago were
found to have fewer dental treatment needs compared to the
other subgroups. Furthermore, a high periodontal and high over-
all treatment need was found for the patients, while differences
between the subgroups were not statistically significant (P > .05).
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TA B L E   4   Dental, periodontal, and

Dental treatment Periodontal treatment Overall
overall treatment needs depending on the
need need treatment need
immunosuppressive medications used
Tacrolimus
Yes 43% (43/99) 70% (68/99) 83% (82/99)
No 45% (31/69) 73% (50/69) 86% (59/69)
P-­value .88 .73 .68
Cyclosporine
Yes 42% (14/33) 76% (25/33) 91% (30/33)
No 44% (60/136) 70% (95/136) 82% (112/136)
P-­value 1.00 .67 .30
Mycophenolate
Yes 43% (50/116) 74% (86/116) 84% (97/116)
No 45% (24/53) 64% (34/53) 85% (45/53)
P-­value .87 .20 1.00
Glucocorticoids
Yes 43% (45/105) 74% (78/105) 86% (90/105)
No 45% (29/64) 66% (42/64) 81% (52/64)
P-­value .87 .29 .52
Sirolimus
Yes 47% (8/17) 77% (13/17) 88% (15/17)
No 43% (66/152) 70% (107/152) 84% (127/152)
P-­value .80 .78 1.00
Form of therapy
Monotherapy 40% (15/38) 71% (27/38) 84% (32/38)
Combination 45% (58/130) 71% (92/130) 84% (109/130)
P-­value .45 .81 .91

The results are given as % (n). The significance level was P < .05.

Several previous studies have shown insufficient oral health

3.4 | Treatment needs depending on
immunosuppression
The results for the treatment need depending on medication with
tacrolimus, cyclosporine, mycophenolate, glucocorticoids, or
­sirolimus as well as the form of immunosuppression (monotherapy
vs combination) are shown in Table 4. No statistically significant
findings were detected in terms of the dental, periodontal, or overall
treatment needs.
4 | D I S CU S S I O N
The aim of this study was to investigate the association between
the time after transplantation and the different immunosuppressive
medications with dental and periodontal treatment needs of pa-
tients after SOT. In the current study, the investigated patients after
SOT presented with high periodontal and overall treatment needs.
Only the dental treatment need was found to be associated with the
time since transplantation, whereby patients more than 10 years
after transplantation were found to show significantly fewer dental
treatment needs compared to the other groups (P = .02).
conditions of adult patients after kidney, lung, or liver trans-
plants.14-17,22-24 Only one study showed poor oral health in a mixed
cohort of 20 patients with different SOT.12 A factor of the highest
clinical relevance appears to be the dental and periodontal treat-
ment need of the patients, which shows the current necessity for
dental intervention. This parameter has often not been assessed ex-
plicitly in available studies but was chosen as the main focus of the
current study.
The importance of dental care for organ transplant patients
has been known for many years; as early as 1993, Glassman stated
that patients after liver transplantation must receive dental in-
vestigation, dental treatment, and preventive care. 25 Accordingly,
the importance of the role of dentists in caregiver team SOT has
grown for more than 20 years. 26 Currently, a clear demand for
early dental rehabilitation and sufficient maintenance can be de-
rived from recent literature. 8-13 Considering the results of the
current study, a dental treatment need of approximately 44%, a
periodontal treatment need of 76%, and an overall treatment need
of 81% were found in patients who had undergone a transplan-
tation in the previous year (the 0-­1 year category). In particular,
the first year after surgery was found to be a vulnerable period
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6 of 7       SCHMALZ et al.
for transplanted patients. 27 The presence of such a high treatment
need immediately after transplantation suggests that the demand
for dental rehabilitation prior to transplantation appears not to
be fulfilled. Furthermore, it appears contradictory to the fact that
71% of patients received dental treatment prior to Tx. However,
the periodontal treatment need appears especially high. This might
lead to the assumption that the patients are dentally, but not peri-
odontally, rehabilitated before Tx. It is thereby unclear if this could
be caused by lack of time, insufficient knowledge, or inadequate
sensitization of the dentists and/or transplant centers or if there is
also a compliance problem with the patients. The treatment need
was found to be consistently high in SOT patients after long-­term
follow-­up. This suggests that the demand of a sufficient mainte-
nance after transplantation is also not fulfilled, which also appears
to contradict the fact that at least 77% of patients stated that they
visit their dentist regularly. However, just visiting the dentist does
not necessarily ensure that adequate maintenance is being com-
pleted. Therefore, as a clinical implication, a greater focus on den-
tal and especially periodontal examination and treatment before
SOT and consequent maintenance after SOT is necessary. The only
exception is that more than 10 years after transplantation, patients
were found to show significantly fewer dental treatment needs
compared to the other groups.
The second aspect is the potential influence of different immuno-
suppressive medications on the treatment need. It has been shown
that immunosuppressive medications, in combination with other
factors, might influence oral diseases in transplant recipients.10,17,18
In this context, differences were reported between different medi-
cations. 22,23 The current study did not find any association between
different immunosuppressive drugs and the dental, periodontal, and
overall treatment need. Therefore, the influence of different medi-
cations on oral health parameters might be of low clinical relevance
in terms of the treatment need.
4.1 | Strengths and limitations
To the best of the authors’ knowledge, this is the first study inves-
tigating the association between the time after transplantation
and the use of different immunosuppressive medications with
dental and periodontal treatment needs in post-­S OT patients.
The major strength of this study is the high number of patients
enrolled, consisting of different transplanted organ groups. The
included patients have already been investigated separately
regarding their oral health, and oral health deficiencies were
found.14-16 The current study uses this large cohort of patients
as 1 group to investigate potential factors influencing this unsat-
isfying situation. Thus, it was possible to show for the first time
that patients immediately after SOT have high treatment needs
comparable to patients who underwent SOT many years prior. Of
course, this is limited by the fact that the subgroups were formed
within a cross-­
s ectional study and no longitudinal evaluation
was executed. Accordingly, differences between the subgroups
regarding smoking status, diabetes mellitus, transplanted organ,
and further factors might influence the findings. Nevertheless,
the exclusion of patients to adjust the subgroups would have re-
duced the case number enormously and would reduce the mean-
ingfulness of the results.
5 | CO N C LU S I O N
Post-­SOT patients show a high treatment need, regardless of the time
since transplantation and the form of immunosuppression. These
findings could suggest insufficient dental and periodontal treatment
before and maintenance after organ transplantation. Consequently,
the dental care of patients after SOT must be improved to fulfill
their need for early dental rehabilitation and sufficient maintenance
of this patient group. Consequent collaboration between dentists
and transplant centers appears necessary, and guidelines should be
formed and implicated in the dental care of SOT recipients.
AC K N OW L E D G E M E N T S
The authors thank Dr. Tanja Kottmann for the statistical analysis.
C O N FL I C T O F I N T E R E S T S TAT E M E N T
The authors declare no conflicts of interest.
AU T H O R C O N T R I B U T I O N S
Gerhard Schmalz interpreted the data and wrote the manuscript.
Horst Wendorff participated in the data interpretation and criti-
cally revised the manuscript. Lisa Berisha participated in data col-
lection and revised the manuscript. Anja Meisel, Florian Widmer,
Anna Marcinkowski Helmut Teschler, Urte Sommerwerck, Rainer
Haak, and Otto Kollmar participated in data collection and inter-
pretation and revised the manuscript. Dirk Ziebolz was the primary
investigator, participated in the data interpretation and drafted the
manuscript. All authors denied having any conflicts of interest and
gave their final approval for the manuscript.
ORCID
Dirk Ziebolz  http://orcid.org/0000-0002-9810-2368
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How to cite this article: Schmalz G, Wendorff H, Berisha L,
et al. Association between the time after transplantation and
different immunosuppressive medications with dental and
periodontal treatment need in patients after solid organ
transplantation. Transpl Infect Dis. 2018;20:e12832.
https://doi.org/10.1111/tid.12832
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