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Non-haematopoietic malignancies metastasing

to the bone marrow: A 5 year record-based
descriptive study from a...

Article in Indian Journal of Cancer · June 2014

DOI: 10.4103/0019-509X.134614 · Source: PubMed

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Original Non-haematopoietic malignancies metastasing to the bone
Article marrow: A 5 year record-based descriptive study from a
tertiary care centre in South India
Mishra P, Das S, Kar R, Jacob SE, Basu D
Department of Pathology, Jawaharlal Institute of Postgraduate Medical Education and Research, Pondicherry, India
Correspondence to: Dr. Rakhee Kar, E-mail: drrakheekar@gmail.com

Abstract
INTRODUCTION: Bone marrow involvement by a non-haematological malignancy gives an opportunity to identify the lodgement, invasion of metastatic
cells and the response of the host to the tumor cells. The study was undertaken to assess the involvement of bone marrow with non-haematopoietic
malignancies and its significance in establishing primary diagnosis in clinically unsuspected cases. MATERIALS AND METHODS: This was a
descriptive study which included record review of the departmental archives for the last five years (January 2007 to December 2011). Eighty
four cases were studied; which included clinically diagnosed non-haematological malignancy for staging or symptomatic cytopenias/bony lesions
(group 1, n = 63), clinically suspected bone marrow metastasis of unknown primary malignancy due to symptomatic cytopenias/bony lesions
(group 2, n = 07) and clinically unsuspected malignancy with incidentally detected bone marrow metastasis (group 3, n = 14). RESULTS: Bone
marrow metastases of solid tumors were identified in 23 cases (27.3%) which included 9 cases from group 1, 14 cases from group 3 and nil in
group 2. Of the 14 cases in group 3, in 12 cases a definitive diagnosis could be made by correlating clinicoradiological findings with morphology
and immunohistochemistry. The most common tumor in pediatric cases were neuroblastoma and Ewing’s sarcoma (40%) and in adult’s
adenocarcinoma of gastrointestinal tract (30.7%) was the commonest. CONCLUSION: Bone marrow metastasis can masquerade as a primary
haematopoietic disorder; however its detection has both therapeutic and prognostic significance. Immunohistochemistry is a useful adjunct to
morphology in reaching a definitive diagnosis.
Key Words: Bone marrow, metastasis, non-haematopoietic malignancy

Introduction from January 2007 to December 2011. A total of 2426

Metastasis of non-haematopoietic tumor cells to bone
marrow was reported as early as in 1834,[1] but a collected
series of such cases was not published until 1936. Rohr
and Hegglin,[2] studied sternal aspirates of 75 patients with
cancer and found marrow involvement in 11 of 13 patients
with bone metastases. In 1958, McFarland and Dameshek[3]
described a simplified technique for bone marrow biopsy,
and the ensuing experience demonstrated that one could
discover unsuspected malignant disease and in many cases
confirm the finding obtained by aspiration. Bone marrow
involvement by haematological malignancies is commonly
found; however, specially diagnosing a non-haematological
malignancy from marrow is a rare entity. Study of bone
marrow not only gives an opportunity to identify the
lodgement, invasion and extra vascular spread of metastatic
cells at a cellular level; it also gives information regarding
the reactions of the host marrow. Detection of metastatic
tumors in the bone marrow is crucial for clinical staging,
detecting response to treatment and the overall survival.
Recognition of metastasis in random biopsies presents
challenges to pathologists when diagnosing the primary
focus. [4] This study was undertaken to comprehensively
analyze bone marrow metastasis in non-haematological
malignancies diagnosed at a single tertiary care centre in
South India over the five years.
Materials and Methods
This was a descriptive cross-sectional study conducted
in the department of Pathology which included record
review of the departmental archives for the last five years
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bone marrow aspirations most of which also had biopsies,
were done during this period for the diagnosis of various
haematological and non-haematological disorders. Of these
2426 cases, there were 84 cases of non-haematological
malignancies in which bone marrow study was done. These
84 cases were selected for further study and were grouped
as under:
Group 1: Clinically diagnosed non-haematological malignancy
for staging or those who had symptomatic
cytopenias/bony lesions (n = 63).
Group 2: Clinically suspected bone marrow metastasis of
unknown primary malignancy due to symptomatic
cytopenias/bony lesions (n = 07).
Group  3: 
Clinically unsuspected malignancy with
incidentally detected bone marrow metastasis
(n = 14).
Bone marrow aspirate and biopsies were performed
from the posterior iliac spine. Bone marrow aspiration,
imprint smears and peripheral smears were stained by
Romanowsky stains, either by Giemsa or Leishman.
Trephine biopsies after standard processing were stained
with Haematoxylin and Eosin. Special stains like
Reticulin, Periodic Acid Schiff (PAS), Mucicarmine (MC)
and Alcian blue-PAS were done wherever necessary.
Morphological features like arrangement of tumor cells,
presence or absence of special features like rosettes,
pleomorphisim of tumor cells, and marrow response to
the tumor cell in the form of marrow necrosis, fibrosis
and osteomyelosclerosis were studied. Tumor burden was
assessed using the criteria put forth by Frisch et al. [5]
Immunohistochemistry (IHC) using standard technique
was used wherever required and the panel of markers
were chosen based on morphology and clinical history.
Standard descriptive statistics was used.
Results
The total number of positive cases showing marrow
metastasis was 23 which included 9 from group 1and
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Mishra, et al.: Bone marrow metastasis
14 from group 3 and none in group 2 [Table 1]. The
marrow aspiration, biopsy slides and the case records of
these 23 cases were studied in detail. Among the bone
marrow positive cases for metastasis (n = 23), there
were 15 males and 8 females; 10 were in paediatric age
group (<14 years), and 13 were in adult age group.
Lymphadenopathy was seen in 6 (26%) cases and
4 (17.3%) cases had hepatosplenomegaly. Peripheral smear
showed leucoerythroblastic picture in 6 (26%) cases.
Indication for bone marrow
Group 1: C onstituted 63 cases of known malignancy
the clinical diagnosis of which are summarised
in Table 2. Out of these 63 cases, primary
indication for bone marrow examination was
staging in the majority (54 cases). In the
remaining cases marrow was done due to
unexplained haematological abnormalities like
leucoerythroblastic anaemia, cytopenias (5 cases)
and bony lesions detected radio graphically like
lytic or sclerotic lesions (4 cases). Among these
9 cases showed marrow metastasis.
Group 2: These seven cases were worked up for skeletal lytic
lesions with a clinical suspicion of bone metastasis.
However, no case was positive in this group.
Group 3: There were 14 cases in this group where bone
marrow metastasis was clinically unsuspected but
incidentally detected in all the cases. The bone
marrow was performed primary for unexplained
cytopenias and/or bony lesions. Morphologic
features coupled with IHC, detailed clinical and
radiological review helped in ascertaining the
primary site in 12 of these 14 cases.
Table 1: Group wise distribution of cases and
their positivity rate
Total
Groups
cases cases (%)
Group 1 (Clinically diagnosed) 63
Group 2 (Clinically suspected) 7 00 (0.0)
Group 3 (Clinically unsuspected) 14
Total 84
Table 2: Details of the cases with bone marrow
involvement in group 1
Clinical diagnosis Total cases Positive cases
Ewings sarcoma 28
Rhabdomyosarcoma 09
Neuroblastoma 05
Neuroendocrine carcinoma 05
Breast carcinoma 04
Lung carcinoma 03
Retinoblastoma 03
Carcinoma cervix 02
Gastrointestinal stromal tumor 01
Squamous cell carcinoma 01
Skin adnexal carcinoma 01
Ovarian carcinoma 01
Total 63
Indian Journal of Cancer | January–March 2014 | Volume 51 | Issue 1
The salient clinico-haematological profile of the 23 bone
marrow metastasis positive cases is summarized in Table 3.
Radiological findings
Of the 84 cases that were studied only in 17 cases there
was a radiological suspicion of marrow involvement by non
haematological malignancy, out of which 7 cases showed
metastatic deposits in bone marrow examination (positive
predictive value - 41.2%).
Bone marrow aspirate findings
Bone marrow aspiration was done in all the 84 cases and
biopsies were done in only 67 cases. The 17 cases where
biopsies were not done mostly belonged to the pediatric
age group. Bone marrow metastasis was found in 23 out
of 84 (27.3%) cases. In 19 cases, bone marrow aspiration
showed metastatic deposits, in two cases tumor was picked
up in the imprint smear and in two cases both aspirate and
imprint smears were negative; however, biopsy was positive.
Of the 23 positive cases, in 18 cases bone marrow biopsy
was done and all showed infiltration by malignant cells.
Of the 21 positive cases in bone marrow aspirate, 12 cases
showed small round cell morphology, five of them in
addition showed features like rosettes and neuropil
[Figure 1a and b] in the background. Five cases showed
features of adenocarcinoma, one of which showed signet ring
cell morphology. In the remaining four cases; cells exhibited
significant degree of pleomorphisim.
Most of the non-haematopoietic malignancies in children
metastasing to bone marrow were small round cell tumors
commonest being neuroblastoma and Ewing’s sarcoma each
comprising four cases, rhabdomyosarcoma in one case and
a single case reported as metastatic small round cell tumor
which could not be further sub classified. Of the 13 cases
in adults, eight cases were diagnosed as adenocarcinoma,
with primaries being located in GI tract in four; one in
Positive stomach and three from colon. There were also two cases
of lung adenocarcinoma, one case from breast and in one
09 (39.1) case the primary site of origin could not be ascertained.
The remaining five cases composed of two cases of Ewing’s
14 (60.9) sarcoma and one case each of neuroblastoma, clear cell
23 (100) sarcoma and choriocarcinoma.
Bone marrow biopsy findings
In the bone marrow biopsies, eosinophilia was seen in two
cases and reactive plasmacytosis was seen in one case as part
of tumor myelopathy. Stromal changes like fibrosis of grade 3
06 were seen in four cases. Osteomyelosclerosis was seen in four
- cases. Necrosis was seen in two cases. Assessment of tumor
02 burden in bone marrow biopsy was done in 18 cases and
- categorized based on the classification as proposed by Frisch
01 et al.[5] There was one case in category A, seven cases in
- category C, ten cases in category D and nil in category B.
- Immunohistochemistry
- The fourteen cases in group 3 were further worked up for
-
the primary tumor with the aid of clinical and radiological
-
findings coupled with an immunohistochemical panel.
-
Immunohistochemistry was done using the markers
-
Cytokeratin (CK)7, CK8, CK20, LCA, PLAP, CD99,
09
CA125, ER, PR, carcinoembryonic antigen (CEA), desmin
31
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Mishra, et al.: Bone marrow metastasis

Table 3: Clinicohaematological profile of the positive cases

Age Gender Clinical Indication Hb TLC/ PC PS BMA BMB Final
impression g/dl mm3 lakhs/ diagnosis
Other
mm3 Mets Mets Other Pattern
lineages
1 M US Cytopenia 5.8 12000 0.12 NC/NC + Suppressed + Necrosis C Mets SRCT
haematopoiesis
2 M US Cytopenia 3.5 4200 0.26 LEB picture + Suppressed ND ND RMS
haematopoiesis
2 F NB Staging 5.5 4700 2.05 MC/HC + Suppressed ND   ND NB
haematopoiesis
3 M ES Staging 11.7 6100 2.1 NC/NC + Normal active ND   ND ES
3 M NB Staging 11 11200 4.42 Neutrophilia + Normal active ND   ND NB
4 F US Cytopenia 4.1 9700 1.39 LEB picture + Suppressed + Fibrosis D NB
haematopoiesis
5 F ES Staging 9.8 10200 1.07 NC/NC + Suppressed ND   ND NB
haematopoiesis
9 M ES Staging 9.2 11900 8.83 Eosinophilia + Eosinophilia +   A ES
11 F ES Staging 9.8 8000 1.56 NC/NC + Eosinophilia +   C ES
13 M ES Staging 9.7 6600 2.2 NC/NC - Normal active +   C ES
19 M US Bony 4.1 19000 2.2 Neutrophilia + Suppressed +   D ES
lesions haematopoiesis
19 M US Cytopenia 4.8 20100 0.41 LEB picture + Suppressed + Oms D Adeno Ca
haematopoiesis Stomach
23 M ES Staging 9.9 14900 2 NC/NC + Reactive +   C ES
plasmacytosis
25 F US Cytopenia 10.4 25300 0.6 Eosinophilia + Suppressed + Necrosis D Chorio Ca
haematopoiesis
35 M US Bony 12.1 8000 2.6 Neutrophilia + Suppressed +   D CCS
lesions haematopoiesis
36 M US Cytopenia 6.4 14100 0.07 LEB picture + Normal active + C AdenoCa
colon
46 F Ca Breast Bony 10.6 3300 1.93 NC/NC + Normal active + Fibrosis D Ca Breast
lesions
50 F US Cytopenia 3.2 12300 0.39 LEB picture - Dilute + Oms D Adeno Ca
Colon
16 M US Bony 9.4 8000 1.97 NC/NC + Suppressed + C NB
lesions haematopoiesis
61 M US Cytopenia 5.4 9500 0.05 LEB picture + Suppressed + Fibrosis+ D Adeno Ca
haematopoiesis Oms Colon
45 F US Bony 9.8 12000 2.8 NC/NC + Normal active + C Adeno Ca
lesions Lung
65 M US Bony 13.7 17500 0.98 Neutrophilia + Normal active +   D Adeno sq
lesions Ca Lung
65 M US Bony 8.2 7400 3.12 NC/NC + Suppressed + Fibrosis+ D Mets
lesions haematopoiesis Oms Adeno Ca
BMA=Bone marrow aspiration; BMB=Bone marrow biopsy; M=Male; F=Female; US=Unsuspected; NB=Neuroblastoma; ES=Ewing’s sarcoma; RMS=Rhabdomyosarcoma;
CCS=Clear cell sarcoma; SRCT=Small round cell tumor; NC/NC=Normocytic normochromic; LEB=Leucoerythroblastic; MC/HC=Microcytic hypochromic; +present; absent;
ND=Not done; Oms=Osteomyelosclerosis; Ca=Carcinoma; PC=Platelet count

and synaptophysin depending on the morphology. In Discussion

12 cases a definitive opinion was possible. In the final
diagnosis we had one case each of Ewing’s sarcoma,
clear cell sarcoma, rhabdomyosarcoma, choriocarcinoma
[Figure 1c], two cases of neuroblastoma, one case of
metastatic adenocarcinoma from stomach and three cases
from colon [Figure 2a and b], and one case each of
adenosquamous [Figure 2c and d] and adenocarcinoma from
lung. In all these cases diagnosis was confirmed with the
primary site of tumor. In two cases, the primary site could
not be ascertained. These were reported as metastatic small
round cell tumor and metastatic adenocarcinoma respectively.
Clinical findings and immunohistochemistry of the above
cases are summarized in Table 4.
Of the 23 positive cases 6 (26%) had leucoerythroblastic
anaemia with immature granulocytes and nucleated red
cells in the peripheral smear. Contreras et al. [6] found
leucoerythroblastic reaction in 22% of their cases and Leland
and McPherson [7] in 33% of their cases. In our study,
nucleated red cell and immature granulocytes were not seen
in patients in whom the haemoglobin was 10% gm. or more
and usually not until the haemoglobin was reduced below
7.5% gm. [Table 3]. Presence of leucoerythoblastic anaemia
correlates with the degree of reactive bone marrow fibrosis
than with the extent of malignant infiltration.[8] In our study
4 out of these 6 cases showed marrow fibrosis.

32 Indian Journal of Cancer | January–March 2014 | Volume 51 | Issue 1

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Mishra, et al.: Bone marrow metastasis
a b
Figure 1: (a) BMA of case 1 shows small round cells forming rosette in a neuropil background (Giemsa ×100). Inset shows higher magnification of the
same (Giemsa ×400); (b) BMB of the same case shows infiltration of the tumor cells; crush artefact and azzopardi effect (H and E, ×100); (c) BMB of case
8 shows pleomorphic tumor cells with necrosis (H and E, ×100). Inset shows higher magnification of the same (H and E, ×400)
a b
c d
Figure 2: (a) BMA of case 14 shows a solitary cluster of signet ring cells
(Giemsa × 100); (b) BMB of the same case (H and E, ×100). Upper and
lower right inset shows tumor cells are positive for MC (MC ×100) and
CEA (IHC × 100). Lower left inset shows tumor cells are positive for
CK 8 (IHC × 400); (c) BMA of case 10 shows sheet of pleomorphic cells
(Giemsa × 400); (d) BMB of the same case shows malignant squamous
islands along with clusters of pleomorphic cells arranged in glandular
pattern (H and E, ×100). Upper and lower right inset shows tumor cells are
positive for CK5/6 (IHC ×100) and CK8 (IHC ×400)
Bone marrow aspiration was done in 84 patients. Twenty
three cases showed metastatic deposits, (27.3%) which is
comparable to the previous studies in India.[9] Twenty one
cases were picked up in aspirates, one aspirate was diluted
and one was reported as normal active but biopsy showed
metastatic deposits. Bone marrow aspiration showed normal
or increased cellularity in 47.8% cases while in 52.2% cases
normal hemopoietic elements were reduced. Presence of
small round cells, neuropil in the background, clustering and
glandular arrangement of the cells were helpful findings to
clinch to a definitive diagnosis.
In our study the most common tumor in children that
metastasized to marrow was neuroblastoma and Ewing’s
sarcoma each being 40% and in adults was adenocarcinoma
of GI tract 30.7%. Similar findings were observed by
Ozkalemkas et al.,[10] where the most common histologic
subtype was adenocarcinoma gastrointestinal tract 42%.
However, a study conducted by Mohanty et al.,[11] showed
100% cases as neuroblastoma in pediatric population and
in adult population prostatic adenocarcinoma was the
most common malignancy metastasing to bone marrow
constituting 48% where as adenocarcinoma gastrointestinal
tract was 9%.
Indian Journal of Cancer | January–March 2014 | Volume 51 | Issue 1
c
There have been several previous studies pointing to
superiority of the bone marrow biopsy over aspirate smears
in diagnosis of metastatic tumor [12,13] as deposits in the
marrow are focal and may often elicit a fibrotic response
and therefore aspirates may be negative. Multiple sections
of the biopsy enable a much larger volume of the marrow
to be studied and allow infiltration to be recognized.[14]
Singh et al. [12] reported that bone marrow biopsy was
superior to aspiration in finding carcinoma (97% vs. 72%).
Similar findings were observed in our study where biopsy
vs. aspiration positivity is (100% vs. 91.3 %). However, a
study conducted by Sharma et al.,[15] showed an occasional
case where metastasis was detected only in aspiration.
Bearden et al.,[16] reported that bone marrow aspirates and
biopsies were complementary in diagnosis of various solid
tumors.
We had more numbers of positive cases in group 3,
i.e., clinically unsuspected than in group 1, i.e., staging
bone marrow. This may be attributed to the incomplete
clinical workup of these cases at the time of presentation.
Usually these patients presented at an advanced stage
with symptomatic cytopenias or bony lesions which was
misconstrued as a haematological malignancy at the outset.
Tumor burden was assessed in bone marrow biopsy and
classified into:[5] A- Microcolonies of single cells or clusters,
B- Multiple small tumor foci, C- One or more large masses
with preserved haematopoietic marrow and D- Total
marrow replacement by tumor. In our study we had one
case in category A, seven cases in category C, ten cases
in category D and nil in category B. Tumor myelopathy
like eosinophilia, plasmacytosis was seen in three cases and
10 cases were associated with stromal changes like necrosis,
fibrosis and osteomyelosclerosis. According to Mohanty
et al., [11] a number of associated features were observed
like osseous metaplasia, desmoplastic changes, necro
inflammatory reaction, granulomas and infections which may
help to suggest bone marrow metastasis, in the absence of
tumor cells in the bone marrow.
Immunohistochemistry was used as an adjunct to the
morphological findings in the marrow in elucidating the
primary site especially in clinically unsuspected cases.
Depending on the morphology of the tumor appropriate
immunohistochemistry panel was used to narrow down the
differentials as summarized below:
33
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Mishra, et al.: Bone marrow metastasis

Table 4: Clinico-radiological correlation with immunohistochemistry findings of the unsuspected cases with
the clinical diagnosis (group 3)
Age Sex Clinical diagnosis BMBx Clinical evaluation IHC Final diagnosis
4 F Storage disorder Neuroblastoma Abdominal mass, osteolytic NSE+, S100+ Neuroblastoma
lesions
19 M MM Ewings sarcoma X-ray-multiple lytic lesions CD99+, NSE+ Ewings sarcoma
of long bones, skull
35 M NHL Clear cell sarcoma Ankle swelling Non contributary Clear cell sarcoma
61 M Leukaemia Adenocarcinoma Per rectal bleeding CK20/8+CK7- Adenocarcinoma colon
2 M Leukaemia ND Proptosis left eye ND Rhabdomyosarcoma
65 M MM Adenocarcinoma Bonescan-vertebral collapse PAN CK+ Adenocarcinoma ?unknown site
1 M Leukaemia Mets SRCT Lymphadenopathy Non contributary Mets SRCT
25 F CML Metastatic Vaginal nodule: USG-liver CK7/8+ Choriocarcinoma
carcinoma mets CEA+
PLAP-
50 F ITP Adenocarcinoma USG-liver mets CK20/8+ Adenocarcinoma colon
colon CK7-
65 M MM Poorly differentiated X-ray-lung mass CK5/6+ Adenosquamous lung
carcinoma ,CK8+
CK7/20-
16 M Leukaemia Neuroblastoma X-ray-lytic lesion Chromogranin+ Neuroblastoma
45 F MM Metastatic X-ray-lytic lesion CK8+ Adenocarcinoma lung
adenocarcinoma Mediastinal widen
ing
19 M NHL Poorly differentiated Gastric Bx-adenocarcinoma CK7/8+ Adenocarcinoma stomach
carcinoma CK20-
PLAP-
36 M NHL Adenocarcinoma Abdominal distension CK8+ Adenocarcinoma colon
colon USG-Ascitis CEA+CK7/20-
M=Male; F=Female; BMB=Bone marrow biopsy; MM=Multiple myeloma; CML=Chronic myeloid leukaemia; ND=Not done; USG=Ultrasonography; SRCT=Small round cell
tumor

Undifferentiated carcinoma: Pan CK, EMA, Chromogranin,
LCA, S100
Pleomorphic sarcoma: Vimentin, Desmin, SMA, CD117,
S100, CD99, CD68
Round cell tumor: Pan CK, Vimentin, Desmin, CD99,
NSE, LCA, Chromogranin
At times immunohistochemistry can be non-contributory
owing to extensive necrosis with lack of viable tissue
and sections with scanty tissue. In our study in one case
immunohistochemistry was not much of help because of
extensive necrosis.
Conclusion
Detection of metastasis in the bone marrow has both
therapeutic and prognostic significance. Clinical history,
radiological findings, morphology and immunohistochemistry
with a panel of antibodies is useful to arrive at a definitive
diagnosis. In addition immunohistochemistry has a special
role to play in biopsies especially where the nature of the
primary tumor is unknown.
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