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Journal of the Formosan Medical Association (2017) xx, 1e7

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Original Article

Extramedullary hematopoiesis involving the

thyroid: A rare cytologic finding in otherwise
healthy patients and review of literature
I-Shiow Jan a,b, Ming-Hsiang Weng b, Chih-Yuan Wang a,c,
Tien-Chun Chang a,c,d,e, Shyang-Rong Shih a,c,d,*

a
National Taiwan University College of Medicine, Taipei, Taiwan
b
Department of Laboratory Medicine, National Taiwan University Hospital, Taipei, Taiwan
c
Department of Internal Medicine, National Taiwan University Hospital, Taipei, Taiwan
d
Center of Anti-Aging and Health Consultation, National Taiwan University Hospital, Taipei, Taiwan
e
Far Eastern Polyclinic, Taipei, Taiwan

Received 18 September 2017; received in revised form 18 November 2017; accepted 20 December 2017

KEYWORDS Background/purpose: The thyroid gland is an uncommon site for the presence of extramedul-
Extramedullary lary hematopoiesis (EMH). We report the cases of four Taiwanese women with hematopoietic
hematopoiesis; elements on the smears of thyroid fine needle aspiration (FNA) samples and compare the find-
Fine needle ings with those of previously reported cases.
aspiration; Methods: We retrieved the data of cases in which thyroid FNA performed between January
Thyroid 2000 and December 2016. The clinical manifestations, laboratory data, and image findings
of cases with thyroid EMH were reported. A review of English literature was performed, and
the reported cases were compared with our series.
Results: During the study period, 63,361 specimens of thyroid FNAs were identified. Four spec-
imens contained hematopoietic elements from four women. Ultrasound study revealed calci-
fications in three patients. A review of English literature yielded 18 reports of thyroid EMH
involving 29 patients. Twenty-six patients were women, and three were men. Nodule calcifica-
tions were found in 13 patients. Four patients had primary myelofibrosis, and one had chronic
anemia. None had a thyroid malignancy.
Conclusion: Four patients were noted to have bone marrow elements on the smears among
63,361 thyroid FNA samples. These four Taiwanese women presented with nodular goiter
and foci of hematopoietic elements by thyroid FNA without any chronic disease of hematopoi-
etic tissue or any evidence of a thyroid malignancy.
Copyright ª 2018, Formosan Medical Association. Published by Elsevier Taiwan LLC. This is an
open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-
nc-nd/4.0/).

* Corresponding author. Department of Internal Medicine, National Taiwan University Hospital, No. 7, Chung-Shan South Road, Taipei,
10002, Taiwan. Fax: þ886 02 2322 4263.
E-mail address: srshih@ntu.edu.tw (S.-R. Shih).

https://doi.org/10.1016/j.jfma.2017.12.011
0929-6646/Copyright ª 2018, Formosan Medical Association. Published by Elsevier Taiwan LLC. This is an open access article under the
CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Jan I-S, et al., Extramedullary hematopoiesis involving the thyroid: A rare cytologic finding in otherwise
healthy patients and review of literature, Journal of the Formosan Medical Association (2017), https://doi.org/10.1016/
j.jfma.2017.12.011
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2 I.-S. Jan et al.
Introduction
Goiter is the most common thyroid disease worldwide. At a
medical center in Taiwan, the prevalence of goiter was
found to be 19.4% and 33.6% in male and female adults who
underwent health examination, respectively.1 Degenera-
tive changes such as hemorrhage, infarction, or fibrosis are
frequently observed in the goiter. Calcifications also can be
detected by ultrasonographic study of the thyroids.2 Fine
needle aspiration (FNA) of the thyroid gland is a well-
established diagnostic technique for the evaluation of
thyroid nodules.3 Extramedullary hematopoiesis (EMH) has
been described in every body organ other than the bone
marrow. The most common sites of EMH are the liver,
spleen, and lymph nodes.4 Other sites such as the nervous
system, lungs, breasts, adrenal glands, kidneys, perirenal
soft tissue, peritoneal surfaces, and gastrointestinal tract
may be affected. The thyroid gland is an uncommon loca-
tion for the presence of hematopoietic elements. A total of
18 reports of 29 patients with thyroid EMH were identified
by FNA cytology, and surgical pathology has been reported
in the English literature.5e22 Herein, we report four cases of
EMH in the thyroid gland and review the English literature
of thyroid EMH.
Methods
A total of 63,361 specimens of thyroid gland FNAs were
identified in a medical center between January 2000 and
December 2016. All FNAs were performed by endocrinolo-
gists or otolaryngologists, with or without ultrasound guid-
ance, depending on whether or not the thyroid nodules
were easily located by palpitation. All aspirates were
smeared onto slides. Some smears were air-dried, and then
Riu stain, a kind of Romanowsky stain, was performed.23
Some smears were fixed in 95% ethanol for Papanicolaou
stain. The clinical manifestations, laboratory data, and
image findings were reviewed.
The study protocol was approved by the Institutional
Review Board of the National Taiwan University Hospital,
Taiwan (No. 201603064RINB). The requirement for obtain-
ing informed consent from the patients was waived.
Results
Four out of 63,361 thyroid FNA specimens (0.006% inci-
dence) were found to contain hematopoietic elements. All
patients were women. Ages ranged from 58 to 76 years. The
clinical presentations were the thyroid nodules. The clin-
ical findings of our patients are summarized in Table 1. All
patients were otherwise healthy without hematological
disease and had no history of previous irradiation of the
head and neck.
Microscopically, FNA smears showed mature megakar-
yocytes, which had multilobulated nuclei and abundant
granular cytoplasm and were most easily noted on cytologic
smears (Figs. 1 and 2A). Various stages of myeloid and
erythroid cells were also present. No benign follicular cells
or Hürthle cells were identified in the four specimens. Also,
no thyroid malignancy was noted. The cytologic feature of
Please cite this article in press as: Jan I-S, et al., Extramedullary hematopoiesis involving the thyroid: A rare cytologic finding in otherwise
healthy patients and review of literature, Journal of the Formosan Medical Association (2017), https://doi.org/10.1016/
j.jfma.2017.12.011
patients’ samples was the presence of hematopoietic ele-
ments. Adipose tissue was found on the smears of case 2.
Details of the case history were as follows:
Case 1
A 58-year-old woman was referred from a local clinic to the
medical outpatient clinic with a chief complaint of right
nodular goiter noted for five months. Physical examination
disclosed a grade 0 nodule over the right thyroid.24 Labo-
ratory examinations revealed the following results: hemo-
globin (HB) 13.0 g/dL (10.8e14.9 g/dL), hematocrit (HCT)
39.7% (35.6e45.4%), mean corpuscular volume (MCV)
89.4 fL (80e100 fL), white blood cell (WBC) count 5.43 K/mL
(3.54e9.06 K/mL), and platelet (PLT) count 255 K/mL
(150e361 K/mL). A right thyroid nodule with annular-like
peripheral calcification was found by ultrasound study.
The thyroid nodule was 0.9 cm in diameter. Ultrasound-
guided FNA of the thyroid revealed negative for malig-
nancy. She was lost to follow-up one month after thyroid
FNA. No thyroid or hematological malignancy was found
during the follow-up period.
Case 2
A 71-year-old woman was referred to the medical outpa-
tient clinic with chief complaints of poor blood sugar con-
trol and body weight loss. Physical examination disclosed
thyroid nodules. Laboratory examinations gave the
following results: high-sensitivity thyroid-stimulating hor-
mone (hsTSH) 0.564 mIU/mL (0.1e4.5 mIU/mL), free
thyroxine 0.803 ng/dL (0.6e1.75 ng/dL), HB 13.7 g/dL, HCT
41.0%, MCV 96.7 fL, WBC count 4.61 K/mL, and PLT count
283 K/mL. Chest radiography revealed aortic knob calcifi-
cation. Bilateral multinodular goiters with micro-
calcification and bilateral cervical lymph nodes were found
by ultrasound examination. The largest thyroid nodule was
4.15 cm in diameter. Thyroid FNA result was negative for
malignancy but megakaryocytes and other hematopoietic
components were present. Some of the nodules were
enlarged during the follow-up period. Despite the failure to
detect malignancy by FNA, scheduled total thyroidectomy
was performed at the age of 73. Histopathology reported
bilateral nodular goiters, focal adenomatous changes,
hyalinized fibrosis, calcification, and old hemorrhage with
hemosiderin deposition. The patient has been followed up
since bilateral total thyroidectomy, and no thyroid or he-
matological malignancy has been found.
Case 3
A 59-year-old woman went to the medical outpatient clinic
with a chief complaint of a neck nodule. Physical exami-
nation disclosed a grade 0 and soft thyroids. Laboratory
examinations revealed the following results: hsTSH
0.610 mIU/mL (0.4e4 mIU/mL), free thyroxine 1.54 ng/dL
(0.89e1.76 ng/dL), HB 13.2 g/dL, HCT 40.5%, MCV 87.3 fL,
WBC count 6.09 K/mL, and PLT count 170 K/mL. An ultraso-
nographic study revealed bilateral multinodular goiter with
crescent-like peripheral calcification in the left lobe of the
thyroid gland (Fig. 3A). The calcified nodule was 0.92 cm in
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Thyroid extramedullary hematopoiesis and FNA 3

Table 1 Summary of current cases of EMH in the thyroid gland.

Patient Age (y)/sex Location Size (cm) Ultrasound Calcification location/pattern TFT Hematological Histopathology
number disease
1 58/F Rt lobe 0.90 NG Right/peripheral calcification NS None ND
2 71/F Rt lobe 4.15 MNG Bilateral/microcalcification WNL None Nodular goiter
3 59/F Lt lobe 0.92 MNG Left/peripheral calcification WNL None ND
4 76/F Lt lobe 1.75 MNG None WNL None ND
Note: cm: centimeter; EMH: extramedullary hematopoiesis; F: female; Lt: left; MNG: multinodular goiter; ND: not done; NG: nodular
goiter; NS: not specified; Rt: right; TFT: thyroid function test; WNL: within normal limits; y: years old.

Figure 1 EMH and FNA cytology of the thyroids. (A) Various stages of myeloid (blast, black arrow; myelocyte, blue arrow) and
erythroid (polychromatic normoblast, black arrowhead; orthochromatic normoblast, blue arrowhead) cells in case 1 (Riu stain,
1000); one mature form megakaryocyte (B, C, D, black arrow) in the background of myeloid and erythroid cells. (B) Case 2, (C)
case 3, and (D) case 4 (Riu stain, 400).

diameter. The result of ultrasound-guided FNA of the thy-
roid was negative for malignancy but megakaryocytes and
other hematopoietic components were present. Repeated
ultrasonographic studies showed the same finding, and no
malignancy was noted by thyroid FNA. During the follow-up
period, no malignancy has been found for two years. No
surgical intervention of the thyroid was performed.
Case 4
A 76-year-old woman presented to the medical outpatient
clinic with a chief complaint of bilateral neck nodules. She
has been regularly followed up for multinodular goiter with
levothyroxine treatment for years. Physical examination
disclosed grade 0 and soft thyroids. Laboratory examina-
tions revealed the following results: hsTSH 2.6 mIU/mL
(0.4e4 mIU/mL), free thyroxine 0.759 ng/dL (0.89e1.76 ng/
dL), HB 13.8 g/dL, HCT 40.9%, MCV 86.3 fL, WBC count
5.46 K/mL, and PLT count 237 K/mL. Ultrasound study
showed bilateral multinodular goiter without calcification
(Fig. 3B). The largest thyroid nodule was 1.75 cm in diam-
eter. Ultrasound-guided FNA of the thyroid showed nega-
tive for malignancy except for the presence of
megakaryocytes. No malignancy has been found for one
year after hematopoietic cells were noted on thyroid FNA
smears. No surgical intervention of the thyroid was
performed.
Results of literature review
A review of the English literature yielded 18 reports of
thyroid EMH involving 29 patients. Twenty-six patients were
women, and three were men. Ages ranged from 28 to 82
years. The majority of the reports were single case reports.

Please cite this article in press as: Jan I-S, et al., Extramedullary hematopoiesis involving the thyroid: A rare cytologic finding in otherwise
healthy patients and review of literature, Journal of the Formosan Medical Association (2017), https://doi.org/10.1016/
j.jfma.2017.12.011
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4 I.-S. Jan et al.
Figure 2 FNA cytology of the thyroids. One mature form
megakaryocyte (A, black arrow) was present in a background of
myeloid and erythroid cells on the smear from case 1. Because
of the presence of multinucleated giant cells, the cytologic
presentation might be misinterpreted as anaplastic thyroid
carcinoma. Thyroid FNA of anaplastic carcinoma showed
multinucleated giant cells (B, black arrow) with more cellular
pleomorphism and atypia in a background of neutrophil infil-
tration. (Riu stain, 400).
Thyroid EMH was detected by FNA cytology and/or surgical
pathology. At least 24 patients were observed to have
multinodular goiter. EMH was associated with some form of
calcifications by ultrasound study in the majority of cases,
with most being described as mature bone formation on
surgical pathology. Four patients without calcifications by
ultrasound or calcium deposition by surgical pathology had
agnogenic myeloid metaplasia (AMM), which is also known
as primary myelofibrosis (PMF). Two patients without cal-
cifications by ultrasound had chronic anemia and diabetes,
respectively. In addition, there was no thyroid malignancy
in all of the reported cases. Table 2 summarizes the liter-
ature findings.
Discussion
EMH refers to the production of trilineage bone marrow
elements at sites outside of the bone marrow and typically
Please cite this article in press as: Jan I-S, et al., Extramedullary hematopoiesis involving the thyroid: A rare cytologic finding in otherwise
healthy patients and review of literature, Journal of the Formosan Medical Association (2017), https://doi.org/10.1016/
j.jfma.2017.12.011
occurs in organs, which are responsible for fetal hemato-
poiesis in lymph nodes, liver, and spleen. This process has
been described for every organ. However, cases that
involve the thyroid gland are extremely rare. In our series,
the incidence of EMH noted on thyroid FNAs was 0.006% (4/
63,361), which is very close to the finding (9/
172,939 Z 0.005%) by Been et al.11 To our knowledge,
thyroid EMH diagnosed by FNA has been reported in seven
series including 16 cases.5e11 In 2016, Been et al. reported
the highest number of cases of thyroid EMH diagnosed with
FNA.11 Another six series only documented seven cases of
thyroid EMH by FNA. Herein, we present the cytologic and
clinical features of four cases, whose thyroid FNAs showed
hematopoietic elements. To our knowledge, this is the most
abundant case series of thyroid EMH reported in an Asian
hospital to date.
The predominant cytologic features in our series were
those of trilineage bone marrow elements, such as mega-
karyocytes, blasts, promyelocytes, myelocytes, meta-
myelocytes, bands and segmented forms of granulocytes,
erythroid precursors, nucleated erythrocytes, and eryth-
rocytes (Fig. 1). No follicular cells, Hürthle cells, or colloid
was seen. No architectural or cytologic atypia was present
in any one specimen. The presence of numerous giant cells
was the most unusual and predominant finding on the
smears of our cases (Figs. 1BeD and 2A). The differential
diagnosis included infection, inflammation, therapeutic
changes, and neoplasms. The recognition of megakaryo-
cytes, multinucleated cells with a large amount of cyto-
plasm, and irregular nuclei without nucleoli, by
Romanowsky-type stain, was critical to obtain a correct
interpretation of our thyroid FNA smears. Multinucleated
giant cells on the smear of thyroid FNA especially should be
differentiated from anaplastic thyroid carcinoma cells
(Fig. 2). Fassina et al. have reported a case of thyroid EMH
diagnosed as anaplastic thyroid carcinoma at a local hos-
pital before evaluation at their institution.8 In this setting,
the identification of scattered mononuclear myeloid and
erythroid precursors will indicate thyroid EMH (Fig. 2A). For
anaplastic thyroid carcinoma, there are the spectrum of
cellular atypia and tumor diathesis background (Fig. 2B).
All of our cases did not show follicular cells or colloid on
the cytologic smears. The possibility could be explained by
inadvertent sampling of adjacent structures or sampling of
pure population of hematopoietic cells in the focus of
myeloid metaplasia within the thyroid gland. The former
does not seem likely as most thyroid FNAs were performed
by expert clinicians. Furthermore, the thyroid FNAs of case
1, 3 and 4 were performed by the ultrasound-guided pro-
cedure. The size of the aspirated nodule of case 2 was
4.15 cm, which could be identified by palpation. For the
group of thyroid EMH diagnosis by cytology, the cytologic
smears from two of 16 cases, like our current four cases,
revealed the hematopoietic cells, but did not show any
follicular cells, Hurthle cells or colloid.11 Another two
cases’ smears just showed the colloid. No follicular cells or
Hurthle cells could be found on the smears of these two
reported cases.5,11
EMH was associated with calcium deposition in some
cases. In our series, thyroid ultrasound examination iden-
tified calcifications in cases 1, 2, and 3. The calcifications
may display a variety of patterns in the ultrasound
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Thyroid extramedullary hematopoiesis and FNA 5

Figure 3 Ultrasonographic picture of the thyroids. (A) left thyroid nodule with crescent-like peripheral calcification (arrow) of
case 3; (B) left thyroid nodule without calcification of case 4.

examination, including macrocalcifications, micro-
calcifications, and rim calcifications. They may cause dif-
ficulty in performing thyroid FNA in some cases. The most
often seen histology of these calcifications is mature bone
formation, which can manifest as bone marrow fat on
cytologic smears.11 In our series, thyroid FNA in case 2
showed adipose tissue and hematopoietic elements. How-
ever, the pathologic report of thyroidectomy only disclosed
calcifications. Neither mature bone formation nor he-
matopoietic elements were found on the tissue section of
thyroid glands. However, the pathology also showed bilat-
eral nodular goiters, focal adenomatous changes, hyali-
nized fibrosis, and old hemorrhage with hemosiderin
deposition. These degenerative changes will reach the
stage of dystrophic calcification.16 For this case, matura-
tion of calcified tissue to mature bone formation did not
happen to the patient. Therefore, no mature bone forma-
tion was identified on the tissue sections. In addition, there
may be some tiny foci of hematopoietic elements that were
not caught on tissue sections.
One of our cases did not have calcifications detected by
ultrasound examination, and no one has had a hematolog-
ical disorder since documentation of thyroid EMH by FNA.
Been et al. reported that two out of nine cases did not have
calcifications by ultrasound examination, and neither one
had a hematological disease at that time.11 On the other
hand, one patient without calcifications detected by ul-
trasound examination had chronic anemia in the report
conducted by Leung et al.7
EMH can be seen in the thyroid without calcifications or
mature bone formation, which was reported one each by
Lazzi et al., Fassina et al., Schmid et al., and Leoni
et al.6,8,13,14 In their case reports, their patients had AMM/
PMF, a disease associated with EMH. Active EMH normally
occurs in fetal development. On the other hand, passive
EMH occurs on hematological disorders, including AMM/

Please cite this article in press as: Jan I-S, et al., Extramedullary hematopoiesis involving the thyroid: A rare cytologic finding in otherwise
healthy patients and review of literature, Journal of the Formosan Medical Association (2017), https://doi.org/10.1016/
j.jfma.2017.12.011
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6 I.-S. Jan et al.

Table 2 Thyroid EMH diagnosis by FNA cytology and/or surgical pathology in the English literature.
Reference Patients Age (y)/sex Location Size (cm) Ca US/CT Mature bone Associated disease
5
Gay et al., 1985 2 47/F NS NS NS ND MNG
68/F Rt lobe NS NS ND MNG
Lazzi et al., 19966 1 78/F Rt lobe 2.1 NS ND AMM/PMF
Leung et al., 19987 1 49/F Rt Inf 1.8 None ND Chronic anemia
Fassina et al., 19998 1 82/M Rt lobe NS NS ND AMM/PMF
Magalhaes et al., 20079 1 68/F NS 0.9 None ND Diabetes
Gupta et al., 201610 1 71/M Rt lobe 1.0 Present ND MNG
Been et al., 201611 9 77/F Isthmus 3.0 None ND NS
34/F Isthmus 0.8 Rim, micro ND NS
61/F Rt Inf 2.0 Present ND NS
66/F Lt Inf 1.6 Micro ND NS
70/M Rt Mid 2.0 None ND MNG
71/F Lt Inf 1.6 Micro ND NS
59/F Lt Mid 1.3 Micro ND MNG
52/F Lt Inf 1.6 Micro ND NS
76/F Lt Inf 1.9 Present ND NS
Tzanakakis et al., 198912 1 47/F Rt Mid 1.5 NS þ MNG
Schmid et al., 198913 1 82/F Lt lobe 3 NS  AMM/PMF
Leoni et al., 199614 1 67/F NS NS NS  AMM/PMF
Ardito et al., 200915 1 28/F Lt Inf 3 NS þ FA
Pontikides et al., 200316 1 34/F Rt lobe 7.5 Present þ MNG
Westhoff et al., 200817 1 34/F Rt lobe 3 NS þ MNG
Harsh et al., 200918 1 50/F Lt lobe 2 Present þ FA
Akbulut et al., 201119 1 54/F Rt Inf 2 Present þ MNG
Basbuga et al., 201220 1 65/F Bilateral NS Present þ MNG
Chun et al., 201321 3 41/F Rt Inf 1 NS þ MNG
49/F Rt lobe NS NS þ MNG
72/F Bilateral NS NS þ MNG
Sayar et al., 201422 1 57/F Bilateral NS Present þ MNG
Note: AMM/PMF: agnogenic myeloid metaplasia/primary myelofibrosis; Ca: calcification; cm: centimeter; EMH: extramedullary hema-
topoiesis; F: female; FA: follicular adenoma; FNA: fine needle aspiration; Inf: inferior; Lt; left; M: male; Mid: midportion; MNG: mul-
tinodular goiter; ND: not done; NS: not specified; Rt: right; US/CT: ultrasound/computed tomography; y: years old; þ: positive; :
negative.

PMF, anemias, myeloproliferative disorders, leukemias, Acknowledgments

lymphomas, and myelomas. The liver and spleen are the
most common sites of active and passive EMH. Less than 5%
of EMH cases develop outside these organs.25 The pre-
requisites for the development of EMH foci are presumably
the presence of stem cells that have hematopoietic po-
tential and a suitable microenvironment consisting of
stromal cells, extracellular matrix, and growth factors.7
With the reactive changes accompanying degenerative al-
terations within the nodule, a suitable microenvironment
may be provided by mesenchymal stem cells and capil-
laries, which contribute to focal EMH.13
In conclusion, the detection of EMH in the thyroid gland
is extremely rare. We report four Taiwanese women with
nodular goiter and the presence of foci of hematopoietic
elements by thyroid FNA without any chronic disease of
hematopoietic tissue or any evidence of a thyroid malig-
nancy. This is the most abundant case series of thyroid EMH
reported in an Asian Hospital.
Conflicts of interest
The authors have no conflicts of interest relevant to this
article.
We thank the Eighth Core Lab, Department of Medical
Research, National Taiwan University Hospital for the sup-
port during the study.
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healthy patients and review of literature, Journal of the Formosan Medical Association (2017), https://doi.org/10.1016/
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