Bone Marrow Transplantation (2006) 38, 237–242

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ORIGINAL ARTICLE

A prospective study to evaluate a new dental management protocol before

hematopoietic stem cell transplantation

K Yamagata1, K Onizawa1, T Yanagawa1, Y Hasegawa2, H Kojima2, T Nagasawa2 and H Yoshida1

1
Department of Oral and Maxillofacial Surgery, Institute of Clinical Medicine, University of Tsukuba, Tsukuba, Japan and
2
Division of Hematology, Institute of Clinical Medicine, University of Tsukuba, Tsukuba, Japan

Pre-hematopoietic stem cell transplantation (HSCT) myelodysplastic syndromes and lymphomas.1,2 Although
dental treatment is essential to prevent serious infections HSCT is an effective treatment modality for these patients,
from oral sources during immunosuppression, in patients successful engraftment after HSCT requires adequate
who undergo HSCT therapy. This study was planned to immunosuppression of the recipient, which is accomplished
establish a dental management protocol for such patients. with total body irradiation, chemotherapy or a combina-
Forty-one patients scheduled for HSCT to treat hemato- tion of both. Their immunosuppressed status makes the
logical malignancies were consecutively enrolled in the patients more susceptible to infection, resulting in an
prospective trial. The dental status of all patients was increased risk of infectious complications, including the
evaluated by clinical and radiographic examination at a development of severe septicemia, that may be life-
median of 47 days before the commencement of HSCT threatening.2,3
therapy. Thirty-six patients had one or more dental The oral cavity is a potential site of such infectious
diseases; the remaining five had none. Caries was found in complications in patients receiving HSCT therapy, because
26 patients, apical periodontitis in 19, marginal period- it is an important port of entry for agents that can cause
ontitis in 24 and a partially erupted third molar in 11. Our systemic infections.4–7 To prevent these oral complications,
policy is to preserve patients’ teeth whenever possible, and pre-transplant comprehensive oral care has been incorpo-
therefore minimal dental intervention was planned. rated into the preparatory steps for patients scheduled to
Treatment was completed for all 36 patients with dental receive HSCT therapy. This approach is supported by the
pathologies, before the conditioning regimen began. All National Institute of Health consensus statement on oral
patients received the scheduled HSCT therapy without complications of cancer therapy (1989), which states,
alteration, interruption or delay, and did not show any ‘dental foci are potential sources of systemic infections
signs or symptoms associated with odontogenic infection that need to be eliminated or ameliorated before com-
while they were immunosuppressed. This protocol, there- mencement of anticancer therapy’.8 Therefore, to prevent
fore, appears to be appropriate for the pre-HSCT dental significant morbidity, all sources of potential infection
treatment of patients with hematological diseases. should be identified upon pre-transplant dental screening
Bone Marrow Transplantation (2006) 38, 237–242. and treated appropriately.2,9,10
doi:10.1038/sj.bmt.1705429 Not all previous studies have supported a need for pre-
Keywords: dental management; hematopoietic stem cell HSCT dental treatment. Melkos et al.11 reported that there
transplantation; apical periodontitis; marginal periodonti- was no significant difference in the occurrence of infection
tis; partially erupted third molar originating from oral disease during and after HSCT
therapy between patients, with and without pre-HSCT
dental treatments, but they did not describe in detail the
severity of the dental diseases of the patients in their study.
Introduction Toljanic et al.12 demonstrated that oncologic treatment
outcomes were unaffected by the presence of chronic dental
Hematopoietic stem cell transplantation (HSCT) has disease or acute exacerbations of these disease states in a
become an essential treatment for many patients with pilot study in which no chronic dental diseases were treated
malignant and non-malignant hematological diseases, regardless of severity, but the great majority of the patients
including acute and chronic leukemias, aplastic anemia, in their study received only chemotherapy, which does not
require the serious immunosuppression needed for HSCT
therapy. Given the limitations of these studies, pre-HCST
dental therapy is still indicated to prevent odontogenic
Correspondence: Dr H Yoshida, Department of Oral and Maxillofacial complications.
Surgery, Institute of Clinical Medicine, University of Tsukuba, 1-1-1
Tennodai, Tsukuba, Ibaraki 305-8575, Japan.
The potentially complicating oral conditions that have
E-mail: [email protected] been identified are as follows: dental caries, pulpitis, apical
Received 13 February 2006; revised 9 May 2006; accepted 23 May 2006 and marginal periodontitis and partially erupted third
 Pre-HSCT dental management protocol
K Yamagata et al
238
molar. Dental care for these disorders includes tooth Table 1 Oncologic diagnosis and medical treatment
brushing instruction, scaling, restoration, pulpectomy and No. of patients
endodontic treatment. Tooth extraction is recommended
for severe dental disease. Such pre-HSCT dental treatments Disease
are anticipated to decrease the risk of local and systemic CML 14
ML 7
odontogenic infections during patient immunosuppression.
AML 4
Considering the limited period available for pre-HSCT NHL 4
dental treatment,13 minimal dental intervention to treat MDS 4
only the sources of potential infection is recommended. MM 3
However, treatment protocols that clearly define the best ALL 3
Others 2
treatment modality for patients at their pre-HSCT dental
assessment are needed. We previously used retrospective Medical treatment
data to construct a brief dental management protocol for BMT 28
patients scheduled to undergo HSCT therapy for hemato- PBSCT 13
logic diseases and evaluated its usefulness.14 However, a
Abbreviations: ALL ¼ acute lymphoid leukemia; AML ¼ acute myeloid
protocol defining the appropriate detailed treatment leukemia; BMT ¼ bone marrow transplant; CML ¼ chronic myeloid
modality according to the severity of each dental disorder leukemia; MDS ¼ myelodysplastic syndrome; ML ¼ malignant lymphoma;
remains to be described. This study was prospectively MM ¼ multiple myeloma; NHL ¼ non-Hodgkin’s lymphoma; PBSCT ¼
carried out to establish detailed treatment criteria for peripheral blood stem cell transplant.
minimal intervention in potentially detrimental dental
disorders and to judge the effectiveness of the protocol.
into account a patient’s status and treatment schedule. We
describe the details of the protocol below:
Teeth with mild or moderate caries are restored in
Patients and methods patients with sufficient time for dental treatment, but
observed in those with insufficient time. Decayed teeth with
Seventy-one candidates for HSCT therapy were referred pulpitis are treated by pulpectomy and root canal filling.
from the Division of Hematology, Tsukuba University The residual roots are extracted.
Hospital to the Division of Oral and Maxillofacial Surgery, Teeth with recently symptomatic apical periodontitis or
which is the same hospital that carried out the screening of asymptomatic apical periodontitis and periapical radio-
dental pathology between 1998 and 2004. Of 71 patients lucency of the maximal diameter greater than 5 mm are
with hematological malignancies, 41 underwent HSCT treated with root canal in patients whose schedule permits,
therapy; 30 did not because their general condition was but the teeth are removed if there is insufficient time for
poor or because no appropriate donor could be found. The treatment. Asymptomatic apical periodontitis with peria-
41 patients were consecutively enrolled into the prospective pical radiolucency of less than 5 mm is not treated.
trial. Subjects were 22 males and 19 females, ranging in Marginal periodontitis, teeth with gingival swelling, pain
age from 17 to 58 years with a mean of 41.3 years. All and purulent discharge, a probing depth greater than 8 mm
participants gave informed consent before proceeding with or severe mobility are removed, whereas teeth with
treatment. Hematologic diagnoses were as follows: 14 marginal periodontitis but without these signs and symp-
patients had chronic myeloid leukemia, seven had malig- toms are observed and tooth brushing instruction and/or
nant lymphoma, four had acute myeloid leukemia, four scaling is provided.
had non-Hodgkin’s lymphoma, four had myelodysplastic Partially erupted third molars with pericoronitis or
syndrome, three had multiple myeloma, three had acute purulent drainage are extracted, and asymptomatic third
lymphoblastic leukemia and two had other malignancies. molars are not treated.
Hematopoietic stem cells were collected from the bone All patients, including those without dental foci, are
marrow of 28 patients and from the peripheral blood of 13 given tooth brushing instructions to exfoliate dental
(Table 1). plaque.
The dental status of all patients was evaluated at the For the HSCT procedure, all patients were admitted to a
initial visit before HSCT by one experienced dentist. The disinfected room. During the conditioning period, each
screening examination consisted of a clinical examination patient experienced at least one episode of a temperature
of the hard and soft oral tissues and a radiographic survey, higher than 381C and an absolute white blood cell count
including panoramic and occasional periapical films for (WBC) of less than 1000/ml lasting several days, as
symptomatic teeth. All dental diseases encountered, includ- manifestations of their immunosuppressed status. Dental
ing caries, apical periodontitis, marginal periodontitis and follow-up was conducted during the only HSCT hospita-
impacted third molar, were recorded for each patient. lization, which was approximately 3 weeks long. Any
Dental foci were defined as caries, apical and marginal patient with local signs and symptoms consistent with
periodontitis and partially erupted third molar. odontogenic infections, such as swelling, pain, redness and
A new protocol was designed to preserve diseased teeth sensitivity of the gingiva surrounding the teeth had a dental
whenever possible, compared with the previous protocol14 consultation and was given treatment as necessary. The
(see Figure 1). This protocol defines the pre-HSCT dental frequency and occurrence of oral complaints and complica-
treatment modality for the dental foci identified, taking tions were recorded on the patients’ medical charts and

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 Pre-HSCT dental management protocol
K Yamagata et al
239
Present protocol Previous protocol14
Caries Caries

Severity Mild to moderate

Severe Severity Mild to moderate Severe
Treatment Sufficient Insufficient
period

Restoration Pulpectomy or
Treatment or Extraction
Restoration No treatment Pulpectomy No treatment
Treatment

Apical Periodontitis Apical Periodontitis

Symptom Present Absent Symptom Present Absent

5mm < 5mm 2mm < 2mm

Periapical
Periapical
radiolucency
radiolucency
(diameter)
(diameter)

Root canal Treatment No treatment

Treatment No treatment Extraction
Extraction treatment

Marginal Periodontitis Marginal Periodontitis

Symptom Severity Mild to moderate Severe

Present Absent

Probing
depth 8mm < 8mm
Severe Treatment Teeth brushing instruction
Mild or Scaling Extraction
Tooth to
moderate
mobility

Treatment Teeth brushing instruction

Extraction or Scaling

Partially erupted third molar Partially erupted third molar

Symptom Present Absent
Symptom Present Absent

Treatment
Treatment Extraction No treatment
Extraction No treatment

Figure 1 Dental treatment protocol for HSCT candidates.

investigated throughout the course of HSCT therapy, and be completed 10 days before HSCT therapy, to give the
the effectiveness of the new detailed protocol was assessed patient time to undergo the conditioning regimen for
by the attending dentists and hematologists. HSCT. The time available for dental treatment was less
than 1 month for 13 patients, from 1 to 2 months for 11,
from 2 to 3 months for seven and more than 3 months for
Results 10. The patients with duration of more than 2 months
between dental examination and the commencement of
The dental status of all patients was evaluated between 7 HSCT therapy were re-examined to check for new dental
and 240 days before the commencement of HSCT therapy, disease within 1 month before HSCT therapy. Thirty-eight
with a median of 47 days. Dental treatment was required to of the 41 patients (92.7%) had one or more dental diseases.

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K Yamagata et al
240
Table 2 Dental diseases The median number of days in which patients’ tempera-
Dental disease No. of patients a
No. of teeth
ture was higher than 381C during HSCT was 4, ranging
from 0 to 60 days, with no significant difference between
Caries 26 101 bone marrow transplantation (BMT) and peripheral blood
Pulpitis 2 5 stem cell transplantation (PBSCT). The median number of
Apical periodontitis 19 43
days where patients had a WBC of less than 1000/ml was
Marginal periodontitis 24 94
Partially erupted third molar 11 21 17, ranging from 6 to 75 days for BMT, and 10 ranging
from 0 to 12 days for PBSCT. There was a statistical
a
More than one odontogenic disorder was diagnosed in some patients. difference in the number of days of WBC less than 1000/ml
between the two HSCT modalities.
Only two of the 41 patients (4.9%) experienced gingival
Table 3 Dental treatment outcome pain before and during HSCT therapy. One was a 31-year-
old female who complained of mild pain at the lower
Dental treatment No. of patients No. of teeth
anterior gingiva, where gingivitis had been induced by
Restoration 12 40 anticancer agents. Another was a 30-year-old male who
Scaling 24 complained of mild pain at the gingiva of the upper third
Professional tooth brushing instruction 21
molar, which was under observation as asymptomatic. In
Extraction 10 14 both cases, there were no symptoms except pain, and there
Apical periodontitis 7 7 was no possibility of odontogenic infection. Pain resolved
Marginal periodontitis 5 6 spontaneously in both patients without treatment, and the
Partially erupted third molar 2 3 scheduled HSCT therapy continued. Thus, no alteration,
Pulpectomy 2 5
interruption or delay of HSCT therapy was required for
Endodontic treatment 4 5 any patient.

Caries was discovered in 101 teeth in 26 patients, pulpitis in Discussion

five teeth in two patients, apical periodontitis in 43 teeth in
19 patients, marginal periodontitis in 94 teeth in 24 patients Pre-HSCT dental screening to identify and treat potential
and partially erupted third molar in 21 teeth in 11 patients oral sources of infection has become standard care in
(Table 2). Three patients had no dental disease. patients scheduled for HSCT therapy.3,7 The principal aim
Using the new protocol, 36 patients received one or more of screening is to reduce morbidity and mortality, which
kinds of dental treatment. Of 101 caries in 26 patients, may arise from oral complications associated with HSCT
40 cases in 12 patients were restored, and the remaining therapy during immunosuppression. Although all potential
61 teeth of 14 patients were not treated. All five cases of sources of oral infection should be eliminated by dental
pulpitis were treated with pulpectomy and root canal filling. treatment before initiation of conditioning, time limitations
Of 43 teeth with apical periodontitis in 19 patients, 41 were and the patient’s disease status frequently interfere with
asymptomatic and two were symptomatic. Periapical complete treatment.3,6,7,13 Given this restriction, the re-
lesions greater than 5 mm were observed in 10 teeth in moval of potentially preservable diseased teeth may be the
eight patients and lesions smaller than 5 mm in 33 teeth in only viable treatment option, resulting in oral care that
11. Seven teeth with asymptomatic lesions greater than does not best serve the long-term oral needs of the patients,
5 mm in seven patients were removed, five teeth in four because removal of multiple teeth may compromise
patients, including two that were symptomatic and three nutrition during and after HSCT therapy.15 As a further
that were asymptomatic, that had a lesion of over 5 mm complication of extraction, there is an associated increased
were treated endodontically, and the remaining 31 teeth in risk of infection, bleeding or delayed wound healing that
13 patients with asymptomatic apical periodontitis and could require postponing the scheduled HSCT therapy.16–18
periapical lesions of less than 5 mm were followed without A comparison between patients with no dental foci or
treatment. Of 94 teeth affected with marginal periodontitis, completed dental treatment and those with dental foci or
six teeth of five patients were removed, and the remaining no dental interventions demonstrated that the impact of
88 teeth of 24 patients were preserved with scaling and dental foci on the occurrence of post-HSCT infections was
professional tooth brushing instruction. Only three of 21 not statistically significant.11 Patients with chronic dental
partially erupted third molars were symptomatic. One pathology were reported to be safe to proceed with
patient had two symptomatic lower third molars. All three chemotherapy without dental intervention, as the conver-
symptomatic teeth were extracted, and eight upper and 10 sion of chronic dental disease to an acute state during
lower asymptomatic third molars were not treated chemotherapy occurs infrequently.12 These reports suggest
(Table 3). The planned dental treatment was completed that intensive pre-HSCT dental treatment is not necessary.
for 36 patients before initiation of the conditioning Furthermore, patients should avoid the additional morbid-
regimen. There was no new dental pathology at re- ity or mortality associated with needless treatment. Con-
examination. All 41 patients, including the five that did sequently, minimal dental intervention is recommended.
not require dental treatment, underwent HSCT therapy Our previous dental management protocol was evaluated
without showing signs or symptoms associated with as significantly beneficial as pre-HSCT dental treatment for
odontogenic infection. patients scheduled to undergo HSCT therapy, but included

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K Yamagata et al
241
removing potentially salvageable teeth to prevent the mobility were extracted; teeth without these symptoms were
occurrence of infection during the therapy.14 From our treated with scaling, and the patient was instructed in
experience and the desire to preserve teeth if possible, proper brushing technique. There was no occurrence of
we designed a new protocol for minimal intervention, in infectious complications in these patients. These outcomes
which the treatment modality is decided according to the indicate that teeth with chronic marginal periodontitis,
severity of the disease, and only severely diseased teeth are except for actively infected teeth, can be treated conserva-
extracted. The time available to treat dental disorders in the tively.
current study was longer than in other reports,13 resulting There are two basic treatment options for managing an
in the completion of planned dental treatments before impacted, asymptomatic third molar. Some advocate
conditioning in all patients. It is important that the planned prophylactic extraction as soon as possible,22,25 whereas
treatment be completed before HSCT therapy, even if others prefer a more conservative approach,17,26 because
minimal dental intervention is adopted, so early dental the risk of developing diseases associated with the third
screening and treatment is essential. However patients with molar may be further reduced if the patient has good oral
a duration of more than 2 months between dental hygiene. In one study, 40% of patients who underwent
examination and commencement of HSCT therapy had prophylactic removal of partially erupted or impacted third
the possibility of developing new dental disease after dental molars, which were symptomatic or asymptomatic, experi-
examination. We therefore considered that re-examination enced post-operative complications, such as bleeding,
should be carried out in order to identify new dental disease alveolitis, trismus or infection, in the course of intensive
within 1 month before HSCT therapy. cancer therapy, including BMT.17 The complication rate
Most studies and the current protocol agree concerning among these patients was much higher than that reported
treatment modality for caries, symptomatic periapical in the healthy population.27 In that report, the symptoms of
lesion, severe advanced marginal periodontitis and sympto- most non-extracted symptomatic third molars were treated
matic partially erupted third molar.3,7,17,19,20 However, with antibiotics and analgesics, but the impact on outcome
considerable controversy remains as to the best treatment of scheduled HSCT therapy was not described. In the
for asymptomatic periapical lesion, chronic marginal current protocol, symptomatic third molars were removed,
periodontitis and asymptomatic partially erupted and asymptomatic third molars were untreated, and there
third molar, and practitioners manage these pathologies was no occurrence of odontogenic infection.17 Outcomes
with approaches that vary from very conservative to using this management approach indicate that extraction
aggressive. for symptomatic third molars and non-intervention for
As regards asymptomatic apical periodontitis, one study asymptomatic ones is safe.
suggests that there is no increase in the incidence of After completing dental treatments, which followed the
infectious complications during HSCT therapy when teeth newly designed protocol, all the patients received their
with post-endodontic periapical radiolucencies of greater scheduled HSCT therapy without alteration, interruption
than 1.5 mm are not treated.19 Our previous study also or delay, and did not experience signs or symptoms
showed that untreated periapical radiolucencies smaller associated with odontogenic infection during immunosup-
than 2 mm did not convert to the acute stage during HSCT pression. Consequently, the new protocol is likely to be
therapy.14 However, treatment is commonly required for appropriate for guiding the pre-HSCT dental treatment of
large periapical lesions in the healthy population. In the patients with hematological diseases.
present study, we did not treat asymptomatic periapical Some studies report that systemic oral assessment,
periodontitis with apical radiolucencies that were smaller regular encouragement of patient self-care, and consistent
than 5 mm, and there was no occurrence of conversion to oral care may be the most important factors related to the
the acute stage or of infectious complications. Patient prevention or amelioration of oral infection during HSCT
outcomes in the present study suggest that it is safe not to therapy.7,21,28 In addition to the management of oral
treat asymptomatic apical lesions smaller than 5 mm before diseases, patient caregivers should provide careful instruc-
immunosuppressive conditioning. tion in advance about oral care during immunosuppression.
Chronic marginal periodontitis is the most common Before dental treatment, all patients in the present study
significant dental infection, which affects HSCT pa- were educated to exfoliate dental plaque, which produces
tients.4,6,21 A retrospective investigation reported that dental caries and marginal periodontitis. The extent to
64% of patients with chronic periodontal disease had which dental instruction influenced the absence of oral
positive blood cultures associated with clinical signs of infection in the present study is unknown, but we believe
septicemia during the initial 100 days after HSCT.15 the instruction was beneficial. Further studies with a larger
However, because little data are available about the effect sample are required to confirm the appropriateness of the
of pre-HSCT dental treatment for chronic periodontitis on newly designed dental treatment protocol.
the incidence of infectious complications, the treatment
modality has varied from observing the affected teeth to
removing asymptomatic teeth.22–24 Teeth with a poor
periodontal prognosis are generally extracted, but no References
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