Radiological Manifestations of

Skeletal Lymphoma
John ONeill, MB, BAO, BCh, MRCPI, MSc, FRCR (UK),a,b
Karen Finlay, MD, FRCPC,a,b Eric Jurriaans, MD, FRCPC,a,b
and Lawrence Friedman, MBBCh, FRCPC, FACRa,b

Lymphoreticular neoplasms primarily arise in extraskeletal

locations with skeletal involvement usually secondary to
hematogenous spread or by direct invasion from surrounding involved lymph nodes or soft tissues. Primary lymphoma of bone is relatively rare in comparison. Lymphoma
encompasses Hodgkins and non-Hodgkins disease, Burkitts lymphoma, and mycosis fungoides. Skeletal disease
may present with symptoms localized to the site of bone
involvement, as an incidental finding on imaging for other
reasons, or as part of the staging of the disease. It is
important that the radiologist is cognizant of the many
presentations of skeletal lymphoma. We present a review
of the radiological imaging of skeletal lymphoma with
conventional radiographs, computed tomography, scintigraphic studies, and magnetic resonance imaging.

Primary lymphoma of bone is rare and skeletal changes

are more commonly encountered either as hematogenous
dissemination to bone from a primary extraskeletal site or
by direct invasion. These changes usually occur during
the course of the disease rather than a presenting feature.
Skeletal disease may present with symptoms localized to
the site of bone involvement, as an incidental finding on
imaging for other reasons, or as part of the staging of the
disease.
The classification of lymphoma is continuously
undergoing modification with the ultimate goal of
providing clinicians with a universal diagnostic basis
for therapeutic decisions. In 1994 the Revised European American Lymphoma classification was proFrom the aDepartment of Radiology, St. Josephs Healthcare Hamilton,
Ontario, Canada; and bMcMaster Health Sciences, Hamilton, Ontario, Canada.
Reprint requests: John ONeill, MB, BAO, BCh, MRCPI, MSc, FRCR
(UK), Radiology Department, St. Josephs Hospital, 50 Charlton Avenue
East, Hamilton, Ontario L8N 4A6, Canada. E-mail: joneill2@cogeco.ca.
Curr Probl Diagn Radiol 2009;38:228-236.
2009 Published by Mosby, Inc.
0363-0188/2009/$36.00 0
doi:10.1067/j.cpradiol.2008.07.001

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posed by the International Lymphomas Study Group

and has recently been incorporated into the World
Health Organization classification of tumors of hemopoietic and lymphoid tissues.1 It is predominantly
based on cell lineage and cell differentiation utilizing
genetic, immunophenotypic, biologic, and clinical features (Table 1). Cell type and degree of differentiation
may change during the course of the disease altering
treatment and prognosis.2 In basic broad categories,
lymphomas are divided into malignant lymphomas
and Hodgkins lymphoma, the former occurring three
times more frequently than the latter.
Skeletal involvement varies considerably depending on the cell type and method of detection.3 Examples include histiocytic and lymphocytic lymphomas,
which have a 21 and 12% rate of bone involvement,
respectively.4 Postmortem examination demonstrates
skeletal changes in 50% of Hodgkins lymphoma
cases with significantly less detected on radiographic
studies.3 The latter, however, varies considerably with
the method of imaging. The detection and recognition of
skeletal disease is essential in both the primary diagnosis
and the staging of the disease process and thus it is
important that the radiologist is cognizant of the many
presentations of skeletal lymphoma. We present a review
of the radiological imaging of skeletal lymphoma with
conventional radiographs, computed tomography (CT),
scintigraphic studies, and magnetic resonance imaging
(MRI) and have concentrated on the following categories: primary bone lymphoma, Hodgkins lymphoma,
non-Hodgkins lymphoma (NHL), Burkitts lymphoma,
and mycosis fungoides.

Primary Lymphoma of Bone

Oberling first described this entity in 1928 and suggested the diagnosis of reticulum cell sarcoma but it

Curr Probl Diagn Radiol, September/October 2009

TABLE 1. Basic WHO classification of lymphomas

B-cell neoplasms
Precursor B-cell neoplasm
Mature B-cell neoplasms (incl. Burkitt lymphoma)
B-cell proliferations of uncertain malignant potential
T-cell and NK-cell neoplasms
Precursor T-cell neoplasms
Mature T-cell and NK-cell neoplasms (incl. Mycosis
fungoides)
T-cell proliferations of uncertain malignant potential
Hodgkin lymphoma

was not until 1939 that it was separated from Ewing

sarcoma by Parker and Jackson. In the same year it
was included in the Bone Sarcoma Registry by Ewing
under the heading of reticulum cell lymphosarcoma.5
Ivins and Dahlin introduced the term primary bone
lymphoma (PBL) in 1963.6 Diagnosis requires a primary focus in a single bone, histological confirmation,
and no evidence of distant lymph node or metastasis at
or within 6 months of presentation.7 Regional lymph
node disease is acceptable as is multifocal bone
involvement. PBL is responsible for less than 5% of
malignant bone tumors and less than 1% of NHL.8 The
majority of PBL are from NHL, usually a diffuse
B-cell subtype, with 6% arising from Hodgkins lymphoma.
Patients usually present with a long history of pain
localized to the site of involvement, or pathological
fracture (22%). In a large retrospective detailed imaging review of 237 patients with PBL, the following
features were recognized.7 The age ranged from 2 to
88 years with the majority evenly distributed between
the second and eighth decades at a mean of 42 years.
The male:female ratio was 1.8:1. Long bone involvement is more common than flat bone, 71% versus
22%, and is commonly metadiaphyseal (69%) with the
femur, tibia, and humerus the commonest bones involved. Lesions can be epiphyseal, metaphyseal, or
diaphyseal and may cross a joint space to involve the
opposing bone (4%) (Fig 1). Synovitis of adjacent
joint may occur and usually affects the knee. Conventional radiographic features include lytic (70%),
mixed (28%), and rarely, blastic (2%) patterns. The
commonest lytic pattern is permeative or moth-eaten.
Sequestra may occasionally be seen. Initial radiographs may be normal (5%), but abnormalities can be
demonstrated on bone scan or MRI before conventional radiographic changes. On average, conventional
radiographs become abnormal in this subgroup within
10 months. Periosteal reaction ranges from an inter-

Curr Probl Diagn Radiol, September/October 2009

rupted single or multiple layers to a single continuous

layer and is present in almost 50% of patients. Very
rarely disease may be confined to the periosteum.
Radionuclide bone scans are abnormal in the vast
majority of patients, 98%, demonstrating mild to
marked increased uptake. CT is excellent in delineating cortical destruction, whereas MRI is more sensitive than CT for assessing degree of soft tissue
involvement, 48%, which indicates a more aggressive
lesion with a poorer long-term outcome.
MRI signal characteristics were inhomogeneous
and variable with the majority of lesions isointense or
hypointense to muscle on T1 and hypo/iso/hyperintense to subcutaneous fat on T2. Low signal intensity
on both T1 and T2 is speculated to be related to a high
content of fibrous tissue.9 A recent MRI study of 29
patients with PBL marrow signal intensity were nonspecific intermediate on T1 and high signal on T2.10
Enhancement patterns were heterogeneous in 59%.
Soft-tissue extension was present in 76% and demonstrated a more homogenous appearance on T1, 90%
iso-intense to muscle, T2, 91% high signal intensity
(SI), and diffuse enhancement in 82%. Interestingly
cortical bone was abnormal in the majority, 93%, with
permeative cortical destruction with linear foci 52%.
Intramedullary extension is best assessed on MRI and
in this series a clear line of demarcation with normal
marrow was present in 55%.10 Rarely PBL may be
confined to the periosteum or cortex with diffuse
cortical thickening without medullary involvement.10
The differential diagnosis is dependent on the age at
presentation. In children, Ewings sarcoma, osteomyelitis, metastatic neuroblastoma, and Langerhans cell
histiocytosis should be considered, whereas in the
second decade lytic osteosarcoma should be included.
Adult differential includes metastatic disease and myeloma. Overall survival is 91% at 5 years and 87% at
10 years with combined modality of chemotherapy
and radiotherapy.11,12

Primary Multifocal Bone Lymphoma

Primary multifocal bone lymphoma is a subtype of
primary bone lymphoma and comprises between 11
and 33% of PBL.13,14 Diagnosis requires the involvement of multiple bone sites without distant lymph
node or visceral involvement for 6 months post presentation. Patient presentation and imaging characteristics are similar to those in PBL, allowing for multiple
bone involvement, although there are no large

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FIG 1. Primary bone lymphomaNHL: (A) AP and (B) lateral distal femur in a 73-year-old female with a 2-month history of localized pain to distal
femur. Predominantly lytic destructive process of metadiaphysis extending to joint with scattered foci sclerotic reaction, cortical destruction, and
periosteal reaction.

studies reviewing this particular subgroup.15 One

study reviewed eight patients with a total of 63
lesions. The femur, tibia, and spine were the commonest sites of involvement. Permeative lytic lesions are predominant with all lesions demonstrating uniform uptake by bone scan. Extraosseous
soft-tissue mass and pathological fractures may be
present as seen in PBL. Radiographs underestimated
the extent of disease with MRI more sensitive than
bone scan for extent of bone marrow involvement
(Fig 2). Overall survival is worse than PBL.

Hodgkins Lymphoma
Hodgkins lymphoma (HD) comprises 25% of all lymphomas. The ReedSternberg cell, usually a B-cell, is the
malignant cell. Incidence of HD by age shows a bimodal
distribution. In industrialized nations, the first peak occurs in people aged approximately 20 years, while the

230

second peak is observed in patients aged 55 years or

older. In developing countries, the first peak is shifted
into childhood, usually before adolescence.
Initial skeletal presentation of Hodgkins lymphoma is
seen in only 1 to 4% of cases. However, during the
course of the disease, between 5 and 32% will develop
bone marrow involvement.16,17 Osseous disease may be
from direct spread from contiguous lymph node involvement and is commonly spinal. Hematogenous dissemination is associated with a poorer prognosis due to higher
association with the more unfavorable histological subtypes.8,18 Primary bone involvement is rare and accounts
for approximately 6% of primary bone lymphoma as
discussed above. It is important to differentiate between
PBL and secondary involvement, as the former is Stage
1 and the latter is Stage 4 disease in the Ann Arbor
classification.
Multiple osseous lesions, 66%, are more common
than single lesions with adults more commonly affected

Curr Probl Diagn Radiol, September/October 2009

FIG 2. Multifocal primary bone lymphomaHD. 40-year-old male with 3-month history of multifocal back pain. (A) Lateral lower thoracic spine
demonstrating wedge compression fracture with increased AP diameter of a 10th thoracic vertebra. Corresponding sagittal T2 (B) thoracic spine
with diffuse increase signal intensity and collapse of T10, T4, and L1 with secondary spinal stenosis at T4. Signal intensity was of uniform low signal
on T1 (not shown).

than children. Presentation is usually with local pain and

tenderness. The dorsolumbar spine, pelvis, ribs, femora,
and sternum are the commonest sites in order of frequency.19 Osteolytic lesions are commonest but lesions may
be mixed or sclerotic. The latter occur between 15 and
45%. An ivory vertebra represents diffuse sclerosis,
homogenous or heterogenous, of a vertebral body. Vertebra plana, a flattened vertebral body, is a less common
finding but both may occur and are not limited to
lymphoma. Localized sclerosis of a vertebra, sternum, or
pelvis secondary to adjacent to lymph node disease is
common. Anterior erosion may occur from involvement
of paravertebral lymphadenopathy. Diffuse skeletal osteosclerosis may occur in response to extensive marrow
disease or diffuse bone marrow fibrosis. Ill-defined ostiolytic lesions, which may have a sclerotic rim, are often
associated with a periosteal reaction, lamellated or with a
sunburst pattern.19 Rarely, hypertrophic osteoarthrop-

Curr Probl Diagn Radiol, September/October 2009

athy occurs, usually in patients with mediastinal involvement.

Bone marrow disease is often focal in nature and
thus may not be identified on bilateral iliac crest
marrow sampling. MRI is beneficial in these cases as
it is sensitive in demonstrating marrow infiltration and
in addition may help in guiding biopsy.17,18 In a study
assessing the value of MRI versus bone marrow
biopsy involving 26 patients, MRI identified seven
cases of spinal disease, only three of which were
positive on crest biopsy. MRI-positive patients had a
higher relapse rate in the 24-month follow-up period
than the MRI-negative patients.17
Lymphocytic-predominant and nodular sclerosis are
less aggressive histological subtypes than mixed cellularity and depleted lymphocytes and carries a better
prognosis. The latter has a greater incidence of bone
involvement and aggressive osteolytic lesions. The dif-

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FIG 3. Secondary Hodgkins lymphoma: 25-year-old male with known history. Hodgkins lymphoma presented with left scapular pain. (A) AP
scapula demonstrates a well-defined lucent lesion with a nonsclerotic border of the body of the scapula extending to the glenohumeral joint and
acromion. Localized increased uptake on bone scan (B), with decreased signal on T1 (C), and increased signal on T2 (D) in the corresponding
area seen on conventional radiograph.

ferential diagnosis for new bone lesions occurring in

treated HD includes recurrent disease, development of
NHL, and osteomyelitis due to immunosuppression. The
overall 5-year survival for all stages of Hodgkins disease
is 91% with higher stage disease survival as low as 70%.

232

Non-Hodgkins Lymphoma
NHL is the most prevalent hematopoietic neoplasm and
includes many clinicopathologic subtypes, the majority
of which are of B-cell origin. Each subtype has its own

Curr Probl Diagn Radiol, September/October 2009

FIG 4. Secondary NHL: 68-year-old male with known NHL. AP right hip baseline (A), 6 weeks (B), and 3 months later (C). Initial radiograph is normal,
progresses to diffuse permeative subtle changes, and finally to diffuse osteolysis, superolateral femoral neck cortical destruction, and pathological
inter-trochanteric fracture. Bone scan (D) at 6 weeks with diffuse radiotracer uptake right proximal femur, bilateral distal femurs, and left clavicle.
Remaining areas increased uptake was confirmed as degenerative in nature. Coronal bilateral (E) and unilateral (F) coronal T1 and bilateral coronal
short tau inversion recovery (STIR) hips (G), performed at 2 months. Diffuse heterogeneous low signal intensity within the femoral neck and proximal right
femoral shaft on T1 with mixed low and high signal on STIR bilaterally with right diaphyseal periosteal reaction.

Curr Probl Diagn Radiol, September/October 2009

233

FIG 5. Primary bone lymphoma: 60-year-old male with left ankle tenderness post trauma. (A) AP ankle demonstrating a subtle permeative
destruction distal tibial diametaphysis initially thought normal. Repeat radiograph (B) at 10 weeks shows rapid progression with diffuse osteolysis
extending into diaphysis with exuberant periosteal reaction. Coronal T1 (C) and sagittal STIR (D) MRI sequences correlate with above findings with
diffuse low signal intensity on T1 and high signal on STIR with cortical destruction on medial and lateral borders. Extensive soft-tissue infiltration,
low on T1, and high signal on STIR, not appreciated on radiographs. This example stresses the initial subtle changes that may progress rapidly.

distinct epidemiology, etiology, morphology, immunophenotype, genetics, clinical features, and response to
therapy.20 In general, those of a large cell type with
diffuse rather than nodular type growth have a more

234

aggressive pattern of growth. It is more common in

males, 1.4:1, and affects all ages with a median age of 55
years. Patients predisposed to developing NHL include
those with congenital immunosuppression, those with

Curr Probl Diagn Radiol, September/October 2009

multiple lytic lesions, hypercalcemia, and renal failure.21 The 5-year relative survival rate of patients with
NHL is approximately 50%.

Burkitts Lymphoma

FIG 6. Burkitts Lymphoma: 28-year-old male with known history of

nonendemic Burkitts lymphoma with 4-week history of lower fibular
pain and tenderness. AP distal tibia and fibula with permeative
destruction diaphysis fibula.

organ transplant immunosuppressed patients, and those

with human immunodeficiency virus infection. The same
staging system (Ann Arbor) is used as in Hodgkins
disease. As outlined above, the involvement of bone is
related to the subtype with the more aggressive subtypes
more commonly affecting bone.
Skeletal lesions may represent primary or secondary disease from hematogenous dissemination or local
invasion (Figs 3-5). Although PBL is predominantly
NHL (94%), it is less common than secondary disease.
PBL is discussed in greater detail above. In secondary
disease, children are more commonly affected than
adults, 20 to 30% versus 10 to 20%.3 Axial skeletal
involvement particularly predominates the spine, pelvis, skull, ribs, and facial bone involvement. HD
osteolytic lesions, which are more frequently multiple,
with permeative or moth-eaten pattern of destruction,
are common. Osteosclerotic lesions, local or diffuse,
are less commonly seen than in HD. Vertebral involvement with anterior erosion from adjacent lymphadenopathy, ivory vertebra, and vertebral plana may
occur. Periosteal reaction is less frequent than in HD.
Rarely, NHL may simulate multiple myeloma with

Curr Probl Diagn Radiol, September/October 2009

Burkitts lymphoma (BL) is a high-grade B-cell neoplasm and is named after Burkitt, who mapped its
geographic distribution across Africa. BL has two
forms, the endemic (African) form and the nonendemic or sporadic form. The relative frequency compared with other NHLs is 6%.21 The endemic form is
the commonest malignant childhood disease in tropical Africa. There is a strong association with the
EpsteinBarr virus in the endemic (African) form and
is related in approximately 20% in the nonendemic or
sporadic form. Both are commoner in children and in
males, 2:1. The African form commonly presents with
swelling of the facial bones, loosening of the teeth, and
rapidly enlarging nontender lymph nodes. The maxilla
and mandible are the commonest affected bones with
multiple sites in 10%. Early features include loss of
the lamina dura, particularly of the lower molars, and
follicular cortex of a developing tooth. Root resorption, loss trabecular pattern of cancellous bone with
eventual bone destruction with an infiltrative margin
leading to cortical destruction with associated softtissue mass and floating teeth sign on radiographs. BL
is a rapid proliferative disease and bony destruction
can take place over a short period of time. Other facial
bones may be involved and may develop extradural
extension. The sporadic form usually presents with
abdominal tumors but may develop jaw lesions as
described in up to 16%.21-24
The long bones, predominantly the femur and tibia,
and pelvis are infrequently involved. The lesions may
be multiple and bilateral and affect the diaphysic,
metaphysic, or epiphyseal. Focal osteolytic lesions
coalesce with destruction of the cortex and induce a
periosteal reaction (Fig 6) and a soft-tissue mass. Bone
marrow involvement is a poor prognostic indicator
occurring in up to 54% in advanced cases in endemic
form but is often present at an earlier stage in sporadic
form. Children fare better than adults, as do those with
limited disease.

Mycosis Fungoides
Mycosis fungoides (MF) is part of a heterogeneous
group of malignant T-cell lymphomas termed cutane-

235

ous T-cell lymphoma (CTCL). MF is the most common type of CTCL. Sezary syndrome is a variant of
MF occurring in 5% of cases. The skin is the primary
site of involvement. Stage IVB disease is characterized by visceral, including skeletal, involvement. The
disease occurs more frequently in men, 2:1, and may
occur in all age groups, but patients are commonly in
the sixth decade with a mean age at presentation of 50
years.
Three separate types of bone lesion occur and
predominantly affect the appendicular skeleton: osteolytic, osteoblastic, and diffuse osteoporosis.25-27 Cortical bone destruction with associated soft-tissue mass
and periostitis may occur. Sezary syndrome is the
leukemic phase of MF with generalized erythroderma.28 It is associated with a symmetrical seronegative
polyarthritis secondary to malignant synovial infiltration.29 Marrow involvement occurs in up to 20% of
patients with CTCL and is often present at the time of
diagnosis and may be nodular localized or infiltrative.
When the latter is present, it is associated with diffuse
dissemination and a shortened survival time.29 Stage
IVB disease has a mean survival of 18 months.

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