Bone Marrow Transplantation (2006) 37, 387–392
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ORIGINAL ARTICLE
A therapeutic platelet transfusion strategy is safe and feasible in patients
after autologous peripheral blood stem cell transplantation
H Wandt, K Schaefer-Eckart, M Frank, J Birkmann and M Wilhelm
BMT-Unit, Hematology/Oncology, Klinikum Nürnberg Nord, Nürnberg, Germany
Prophylactic platelet transfusions are considered as
standard in most hematology centers, but there is a
long-standing controversy as to whether standard prophylactic platelet transfusions are necessary or whether
this strategy could be replaced by a therapeutic transfusion strategy. In 106 consecutive cases of patients
receiving 140 autologous peripheral blood stem cell
transplantations, we used a therapeutic platelet transfusion protocol when patients were in a clinically
stable condition. Platelet transfusions were only used
when relevant bleeding occurred (more than petechial).
Median duration of thrombocytopenia o20 109/l and
o10 109/l was 6 and 3 days, which resulted in a total of
989 and 508 days, respectively. In only 26 out of 140
transplants (19%), we observed clinically relevant bleeding of minor or moderate severity. No severe or lifethreatening bleeding was registered. The median and mean
number of single donor platelet transfusions was one per
transplant (range 0–18). One-third of all transplants, and
47% after high-dose melphalan could be performed
without any platelet transfusion. Compared with a historical control group, we could reduce the number of platelet
transfusions by one half. This therapeutic platelet transfusion strategy can be performed safely resulting in a
considerable reduction in prophylactic platelet transfusions.
Bone Marrow Transplantation (2006) 37, 387–392.
doi:10.1038/sj.bmt.1705246; published online 9 January
2006
Keywords: platelet transfusion; autologous transplantation; bleeding complication
Introduction
There is an increasing demand for single donor platelet
transfusions due to intensive chemotherapy and blood stem
cell or bone marrow transplantation. Platelet transfusions
however are expensive and associated with a number of side
effects including febrile or allergic transfusion reactions,
Correspondence: Dr H Wandt, BMT-Unit, Hematology/Oncology,
Klinikum Nürnberg Nord, Nürnberg D-90419, Germany.
E-mail: [email protected]
Received 18 July 2005; revised 7 November 2005; accepted 8 November
2005; published online 9 January 2006
transmission of bacterial and viral infections, circulatory
congestion, transfusion-related acute lung injury and
alloimmunization.
During the last 10 years, it has been clearly shown by
several studies that severe thrombocytopenia after intensive
chemotherapy for acute myeloid leukemia can be safely
managed with a threshold of 10 109/l or even lower for
routine prophylactic platelet transfusion.1–4 On the basis
of these results, three clinical studies were performed with
a 10 109/l trigger in recipients of high-dose chemotherapy7total body irradiation (TBI), followed by hematopoietic stem cell support.5–7 All three studies proved the
safety of the 10 109/l trigger for prophylactic platelet
transfusion after autologous bone marrow or peripheral
blood stem cell transplantation (PBSCT).
A recent survey of transfusion practices at 18 transplant
centers in the US and Canada reported that five centers
used a threshold for prophylactic platelet transfusion of
o10–15 109/l. Most severe bleeding events occurred at
platelet counts of greater than 20 109/l and therefore
would not have been prevented even using this level as a
transfusion trigger.8
Virtually the same data were reported from an analysis of
1402 bone marrow transplants at Johns Hopkins Hospital.9
Therefore, the American Society of Clinical Oncology
recently published clinical practice guidelines with a
prophylactic platelet transfusion trigger of 10 109/l for
acute leukemia and hematopoietic cell transplantation.10
The use of peripheral blood stem cells instead of
bone marrow in autologous transplants has substantially
shortened the duration of severe thrombocytopenia. It is
still not known whether a prophylactic platelet transfusion
strategy is necessary, or whether a therapeutic transfusion
strategy is as safe and more cost effective. Therefore, we
started a prospective study with a new therapeutic platelet
transfusion protocol for all consecutive patients after
autologous PBSCT beginning in the year 2001.
The main objective of the study was the safety and
feasibility of a therapeutic transfusion strategy. The
study was approved by the institutional review board of
the Hematology/Oncology Department at the Klinikum
Nuremberg, Germany.
Patients and methods
Since 2001, a therapeutic platelet transfusion strategy
has been offered to all consecutive patients receiving
Therapeutic platelet transfusion strategy
H Wandt et al
388
myeloablative high-dose chemotherapy7TBI, followed
by autologous PBSCT. Patients with a diagnosis of
AL-amyloidosis, documented aspergillus infection, cerebral
lesions or life-threatening bleeding complications during
prior chemotherapy courses were excluded. All patients
gave their informed consent for stem cell transplantation
and our transfusion strategy.
Transfusion strategy
Therapeutic platelet transfusions were defined as transfusions to treat a patient with documented clinically relevant
bleeding during thrombocytopenia.
Petechias, retinal bleeding without impairment of visus
and minimal self-limiting nasal bleeding were not considered as clinically relevant.
In clinically stable patients, no prophylactic platelet
transfusions were performed irrespective of the morning
platelet count. These patients received only therapeutic
platelet transfusions when clinically relevant bleeding was
documented. In cases of significant bleeding (according
to the World Health Organisation (WHO) grade II or
greater), platelets were transfused within 3–4 h.
All platelet transfusions were random single donor
apheresis platelets, ABO compatible, with platelet concentrations according to German guidelines of the ‘Deutsche
Gesellschaft für Transfusionsmedizin und Immunhämatologie’ with 2–5 1011 platelets/unit. All transfusions were
leukocyte-reduced (o106 leukocytes). Platelet transfusions
were available 24 h a day.
In clinically unstable patients, platelet transfusions were
given prophylactically when the morning platelet count was
o10 109/l.
The definition of a clinically unstable patient was fever
438.51C and/or local infectious infiltrations suspicious for
invasive aspergillosis, sepsis syndrome or clinically relevant
plasmatic coagulation disorders. In case of surgery and
biopsies (except bone marrow), the platelet count should be
420 109/l.
Daily morning platelet count was performed until the
platelet count was self-supporting and greater than
20 109/l for 2–3 days. Blood counts were performed
on EDTA-anticoagulated blood using a hemocytometer
(Sysmex SF-3000, Sysmex Corp., Kobe, Japan). The
patients were examined twice daily for evidence of
hemorrhage. Fundoscopy was performed only in case of
impairment of vision.
Hemoglobulin levels were maintained at greater than
80 g/l by packed red cell transfusions.
Infection prophylaxis and treatment
Prophylactic oral antimycotics and antibiotics, as well as
the initiation of intravenous antibiotics for fever greater
than 38.51C, and the start of intravenous antimycotics were
applied according to the German guidelines.11 Granulocyte
colony-stimulating factor was given to all patients on
day þ 6 after transplantation until the leukocyte count
was above 1 109/l for 3 days. Aspirin and nonsteroidal
anti-inflammatory drugs were avoided. Paracetamol and
metamizol were used as antipyretics. All patients were
hospitalized during the study period.
Bone Marrow Transplantation
Bleeding and toxicity
During each therapy course, bleeding complications
according to WHO criteria (0, none; I, petechial; II, mild
blood loss; III, gross blood loss; IV, debilitating blood loss)
were recorded as well as the number of platelet transfusions
administered. Clinically relevant bleeding was defined as
melena, hematemesis, macrohematuria, hemoptysis, vaginal bleeding, epistaxis with gross blood loss, retinal
bleeding with impairment of vision or soft tissue bleeding
requiring blood transfusions. The bleeding complications
were recorded by the responsible physician. The examination for bleeding was performed twice daily. Bleeding
complications were reviewed by one senior physician (HW,
KS). Maximal bleeding per transplant was counted. Only
fevers greater than 38.51C were documented, as well as the
origin of fever and the underlying organisms in case of
septicemia. Mucositis was documented according to the
Bearman toxicity score.12
Statistics
Numbers of transplants without any platelet transfusion in
different groups were compared using the w2 test and
frequencies of transfusion between multiple myeloma
patients and other diagnoses or between the TBI and nonTBI group were calculated using the Mann–Whitney U-test
running on a computer-based program (STATISTICA for
Windows, 2001, Statsoft Inc., Tulsa, OK, USA).
Results
The study included 106 consecutive patients with a total
number of 140 transplantation procedures. Patients’
characteristics are listed in Table 1. The median age of
the patients was 54 years, with a range of 18–70 years. The
male to female ratio was about 2:1. The diagnoses were
multiple myeloma in 43%, malignant lymphoma in 32%
and acute leukemia in 16% of the cases. Only 8% of the
patients were transplanted because of a solid tumor.
Seventy-six patients received one transplant. In 26 and
four patients, respectively, a double or triple transplantation program was performed. The conditioning regimens
included chemotherapy and TBI in 19 patients, whereas the
other patients received high-dose chemotherapy-based
regimens alone. All of these regimens were established
myeloablative combination treatments (see Table 1).
Bleeding complications
The median number of days with platelets below 20 109/l
was 6 (range 0–92) and the median number of days with
platelets below 10 109/l was 3 (range 0–62). We observed
a total of 989 days with platelets below 20 109/l and 508
days with platelets below 10 109/l.
In 114 out of 140 transplants (81%), no clinically
relevant bleeding was observed. In 26 transplants (19%),
patients experienced maximal bleeding of WHO grade II.
WHO grade I (clinically not relevant) was registered in 28
transplants (20%). We observed no bleeding WHO grade
III and IV. Bleeding complications of WHO grad II were
caused by epistaxis in 12 out of 26 transplants (46%), and
Therapeutic platelet transfusion strategy
H Wandt et al
389
Table 1
Patients characteristics, diagnoses, conditioning regimen
Patients
PBSCTs
106
140
Number
Age (year)
Median (range)
Female/male
54 (18–70)
38/68
46
34
17
5
4
68
35
17
9
11
Conditioning regimens
Melphalan (140/200 mg/m2)
TBI/Cy
BEAM/CEAM/CEIAP/ICE
BuCy/BuCyVP16/Bu mono
Carbo/Treo/Tax/Mel
CarboPEC
46
19
18
15
4
4
68
19
21
15
11
6
NSGCT ¼ nonseminomatous germ cell tumor; TBI ¼ total body irradiation; BEAM ¼ busulfan, etoposide, cytarabine, melphalan; CEAM ¼
cyclophosphamide, etoposide, cytarabine, melphalan; CEIAP ¼ cyclophosphamide, etoposide, ifosfamide, cytarabine, cisplatinum; ICE ¼ ifosfamide,
cyclophosphamide, etoposide; BuCy ¼ busulfan, cyclophosphamide; BuCy
VP16 ¼ busulfan, cyclophosphamide, etoposide; Crabo/Treo/Tax/Mel ¼
carboplatin in combination with treosulfan, paclitaxel and melphalan;
CarboPEC ¼ carboplatin, etoposide, cyclophosphamide.
Table 2
Indications for prophylactic and therapeutic platelet
transfusion
Prophylactic
FUO
FUO and mucositis
Septicemia
Septicemia and mucositis
Pneumonia
Without indication
Mucositis only
Therapeutic
Bleeding WHO II
Epistaxis
Mucositis
Hematemesis
Pulmonary bleeding
Hematochezia
Vaginal bleeding
64
23
9
12
5
3
(100)
(36)
(14)
(19)
(8)
(5)
4 (4)
8 (12)
26
12
8
2
2
1
1
(100)
(46)
(30)
(8)
(8)
(4)
(4)
Transplants Transfusions
(no.)
(no.)
Multiple myeloma
Other diagnosis
Diagnoses
Multiple myeloma
Lymphoma
Acute leukemia
NSGCT
Ovarian cancer
No. of
transplantations (%)
Table 3
Number of transfusions related to diagnoses and
conditioning regimen
No. of
transfusions (%)
154
43
27
20
11
11
(100)
(28)
(18)
(13)
(7)
(7)
10 (6)
32 (21)
81
14
23
4
23
3
14
(100)
(17)
(28)
(5)
(28)
(4)
(17)
by mucosal bleeding due to mucositis in eight transplants
(30%) (Table 2).
Transfusions
The median and mean number of single donor platelet
transfusions was one per transplantation (range 0–18). The
TBI
Non-TBI
conditioning
Po0.05
Number of
platelet
transfusions
median (range)
68
72
87
148
1 (0–18)
1 (0–13)
Sign
19
121
69
166
3 (0–7)
1 (0–18)
Sign
median and mean number of therapeutic platelet transfusions per tranplantation was 0 (0–18) and of prophylactic
platelet transfusions was 1 (0–13), respectively.
Forty-eight out of 140 transplants (34%) could be
performed without any platelet transfusion. In patients
with normal marrow recovery (o14 days of duration of
platelet recovery to 420 109/l), even 42% of all
transplants could be performed without any platelet
transfusion.
There was a statistically significant difference in the
number of platelet transfusions according to diagnosis of
the patients, and whether they received a TBI or non-TBI
conditioning regimen (Table 3). The percentage of transplants without any platelet transfusion between patients
with multiple myeloma and other diagnoses was 47 versus
22%, and between patients with non-TBI and TBI regimens
37 and 0%, respectively.
During the study period, a total number of 154
prophylactic and 81 therapeutic platelet units were
transfused (see Table 2). The main indications for
prophylactic platelet transfusions were fever of unknown
origin (FUO) in 46% and septicemia with or without
mucositis in 20%. Forty-two out of 106 patients were
clinically unstable according to our definition and therefore
received platelet transfusions prophylactically.
Forty-two out of a total number of 235 transfusions
(27%) were given without a clear indication according to
the study protocol. This occurred during 16% of all
transplant procedures. Mucositis without relevant bleeding
was the indication in most (76%) of these transfusions (see
Table 2). Forty-two out of 106 patients were clinically
unstable according to our definition and therefore received
platelet transfusions prophylactically.
Major indications for therapeutic platelet transfusions
were epistaxis or mucositis with bleeding (76%) for which,
however, only 45% of all therapeutic transfusions were
needed (see Table 2).
There was no difference in the number of platelet units
transfused in patients below or above the median age of 54
years (data not shown).
Retrospective analysis
In a retrospective matched pair analysis, we compared the
first 60 transplant procedures in this prospective study with
60 historical peripheral blood stem cell transplants that
Bone Marrow Transplantation
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H Wandt et al
390
Table 4
Retrospective analysis
Prospective study
(50 pat, 60
PBSCTs)
Retrospective
analysis (54 pat,
60 PBSCTs)
55
18–67
49
17–61
21/29
41
10
9
25/29
41
10
9
5
5
Platelet transfusions
Median
Mean
Range
1
1.9
0–18
3
4
0–27
Total no of platelet transfusions
111
237
Age/years)
Median
Range
Female/male
Multiple myeloma/lymphoma
Acute leukemia
Solid tumor
Germ cell cancer
TBI conditioning
were performed during the year before we started our new
strategy. Our former strategy required platelet transfusions
routinely at a morning platelet count o10 109/l. Patients
were matched for gender, diagnosis and TBI conditioning.
The total number of transfused platelet units could be
reduced from 237 to 111, the median number of single
donor apheresis platelet transfusions per transplant was
decreased from 3 to 1 (Table 4).
Bleeding complications of WHO grade II and III were
registered in 20 and 1%, respectively, which was very
comparable to the incidence in our study patients. The
median number of red blood cell transfusions needed was 2
(range 0–6). This was exactly the same number and range
we needed in our study cohort.
Discussion
To our knowledge, this is the first clinical study that
replaced standard prophylactic platelet transfusion by a
therapeutic transfusion strategy in clinically stable patients
after autologous PBSCT regardless of the morning platelet
count.
With this prospective study, we could show in 106
patients that our therapeutic platelet transfusion strategy is
safe and more cost effective than the standard prophylactic
transfusion strategy with the 10 109/l trigger. No severe
bleeding (grade III and IV according to the WHO
classification) occurred during 140 transplants after highdose chemotherapy7TBI and 508 days of severe thrombocytopenia (o10 109/l). By the use of peripheral blood
stem cells, the median duration of severe thrombocytopenia
below 10 109/l or 20 109/l was a very short period of
3 and 6 days, respectively. The incidence of minor and
moderate bleeding (maximal WHO grade II) was only
19%. This bleeding incidence compares favorably with
moderate and severe bleeding events reported in the
literature for autologous transplants with a prophylactic
Bone Marrow Transplantation
platelet transfusion strategy.5,6,8,9 In the study of Bernstein
et al.,8 in patients after autologous PBSCT, only major,
severe and life-threatening bleeding was counted (corresponding to bleeding WHO grade III and IV). They
reported an incidence of 9%. In the analysis performed
with a prophylactic transfusion strategy at Johns Hopkins
Hospital, 18.5% moderate and severe bleeding was
reported for autologous transplants.9 This higher incidence
of severe bleeding events might be explained by the fact that
these transplants were performed with bone marrow
leading to a longer duration of leukocytopenia and
thrombocytopenia.
The low incidence and severity of clinically relevant
bleeding (19% WHO grade II) in our study is the reason
why only a minority (34%) of all platelet transfusions was
performed for therapeutic purposes. Bleeding events were
mainly caused by epistaxis and mucositis (in 76%).
In patients treated with TBI-containing regimens, we
observed a more severe mucositis which lead to significantly
more transfusions compared with patients after chemotherapy-based regimens alone. Our experience is in accordance
with published data of patients with multiple myeloma
who were randomized to a TBI and non-TBI regimen.
Patients with TBI 8 Gy and melphalan 140 mg/m2 needed
twice the platelet transfusions compared with melphalan
200 mg/m2.13
In 46% of all prophylactic transfusions, fever of
unknown origin was the main trigger for transfusion. We
did not see an increased bleeding risk in those clinically
stable patients with fever. Therefore, we believe that fever
per se need not be a trigger for prophylactic platelet
transfusion in future transfusion protocols.
In 16% of all transplant procedures, platelet transfusions
were not performed in complete accordance with our
protocol. Seventy-six percent of these transfusions were
given prophylactically for mucositis without bleeding. This
experience shows the difficulty for the medical staff to
reduce prophylactic platelet transfusions even within a
protocol. For further multicenter studies, it is important to
educate physicians and nurses to follow strictly the guidelines of the therapeutic transfusion strategy, which was
proven to be safe in our study.
Despite 27% of all transfusions being given in violation
to the protocol guidelines, we could reduce the number of
apheresis platelet transfusions substantially (about one
half) by our new transfusion strategy compared to a
matched historical control group. Thirty-four percent of all
procedures and about half of the transplants for multiple
myeloma could be performed without a single platelet
transfusion.
A survey in 1991 conducted of institutional members
of the American Association of Blood Banks (hospitals)
in hematology/oncology patients has shown that about
20% of the hospitals did not administer prophylactic
transfusions, but rather used therapeutic platelet transfusions only in response to active bleeding.14 In 1987, there
were only a minority of 5% of leukemia and bone marrow
transplant services which did not transfuse platelets
prophylactially.15 However, the hospitals using platelets
prophylactically administered twice as many platelet
transfusions.
Therapeutic platelet transfusion strategy
H Wandt et al
391
Previous studies comparing bleeding risks in patients
with leukemia who received therapeutic rather than
prophylactic transfusions indicated that bleeding was
corrected in all patients. Thus, a therapeutic platelet
transfusion policy is a promising approach, but its actual
efficacy was unproven because of the small numbers of
patients included in these prior studies.16–18
There is a long-standing controversy in the scientific
community of hematologists and oncologists as to whether
standard prophylactic platelet transfusions are necessary or
whether this strategy should better be replaced by a
therapeutic transfusion strategy.10,17,19–22
During the last 20 years, the recommendations of the
American Society of Clinical Oncology reduced the trigger
for prophylactic platelet transfusion from 20 109/l down
to 10 109/l for thrombocytopenia following intensive
chemotherapy or after hematopoietic stem cell transplantation.10 The decision to administer platelet transfusions
should incorporate individual clinical characteristics of the
patient and not simply be a reflex to the morning platelet
count. Platelet transfusions are expensive and associated
with a number of side effects. Recently Ballen et al.23
reported autologous stem cell transplantations without the
use of blood product support in Jehovah’s Witnesses, a
religious group that refuses transfusion of any major blood
product. Of 26 patients, there was only one lethal cerebral
bleeding in a patient with a still active brain medulloblastoma. Another patient had life-threatening gastrointestinal
bleeding but the patient recovered after regeneration of
platelets. Three other patients had moderate bleeding with
epistaxis and/or hematuria. This report supports our
therapeutic platelet transfusion strategy since timely platelet transfusion could have corrected all major bleeding
events except in the case of the medullablastoma patient.
Patients with cerebral infiltrations, however, were excluded
from our therapeutic transfusion strategy.
A large prospective randomized trial is needed comparing the new therapeutic platelet transfusion strategy with
the standard prophylactic platelet transfusion strategy
using a morning trigger of 10 109/l for transfusion.
Therefore, we have now started such a multicenter trial in
Germany.
Acknowledgements
We thank Rex Nichols for preparing the manuscript and the
staff of the bone marrow transplant unit at the Nuremberg
hospital for the continuous support during the study.
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