Journal of the Formosan Medical Association (2021) 120, 226e233

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journal homepage: www.jfma-online.com

Original Article

Leukemia cutis in a medical center in

southern Taiwan: A retrospective study of 42
patients
Yung-Wei Chang a, Chih-Hung Lee a, Han-Chi Tseng a,b,*

a
Department of Dermatology, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung, Taiwan
b
Department of Cosmetic Applications and Management, Yuh Ying Junior College of Healthcare and
Management, Kaohsiung, Taiwan

Received 22 August 2019; received in revised form 5 February 2020; accepted 20 April 2020

KEYWORDS Background/Purpose: Leukemia cutis (LC), by definition, is the infiltration of neoplastic leuko-
Clinical cytes in the skin. The overall incidence of LC is rare. We aimed to investigate the association
characteristics; between clinical characteristics, classifications and prognosis among different types of LC in
Leukemia cutis; Taiwan.
Prognosis; Methods: We performed a retrospective analysis of forty-two patients with histopathology
Taiwan proven LC based on skin biopsies in a medical center in Southern Taiwan from 1997 to 2018.
The study involved medical records of the patients, clinical manifestations, and outcomes ac-
cording to different types of leukemia.
Results: This series consisted of 27 males and 15 females, and the mean age was 55.7 years
old. The most common cutaneous features were papules (38%) and nodules (29%), followed
by plaques (16%) and ulcers (10%). The most commonly affected sites were the trunk (33%)
and extremities (31.5%), although generalized distribution (14%) was not rare. The prognosis
of LC was very poor, 76.2% of patients (32/42) died during the follow-up, and the median sur-
vival time was 7.2 months (95% CI, 4.53e9.87 months). No statistical significance was found
(P Z 0.068 for survival curves) among different types of LC.
Conclusion: This study was the first large-scale research in regarding to LC of Han Chinese. The
commonest clinical presentations were papules and nodules, and the predilection sites were
trunk and extremities. Besides, there was the high frequency of LC from AML and MDS in
Taiwan. Clinicians should pay more attention to the leukemia patients with extramedullary
manifestations due to poor survival outcomes.
Copyright ª 2020, 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. No. 123, Ta-Pei Road, Niaosong District, 83301 Kaohsiung, Taiwan. Fax: þ886 7 7337612.
E-mail address: perkyjoy@hotmail.com (H.-C. Tseng).

https://doi.org/10.1016/j.jfma.2020.04.025
0929-6646/Copyright ª 2020, 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/).
Leukemia cutis in Taiwan
Introduction
Leukemia cutis (LC), by definition, is the cutaneous infil-
tration of neoplastic leukocytes or precursors. The infil-
trated locations may include epidermis, dermis, or
hypodermis.1 The other term “leukemid” is not related to
leukemic cell infiltration but rather manifests as a cuta-
neous paraneoplastic disorder. It is defined as nonleukemic
cutaneous features of leukemia and is more common than
LC. More than 40% of leukemia patients will develop leu-
kemids. This condition is frequently the clinical presenta-
tion as the result of cytopenia owing to bone marrow failure
and drug eruptions. The cutaneous findings include throm-
bocytopenia - induced petechiae/purpura, leukocytoclastic
vasculitis, neutrophilic dermatoses such as pyoderma gan-
grenosum and Sweet’s syndrome. In addition, opportunistic
infections such as disseminated candidiasis and dissemi-
nated herpes zoster may also occur.2
Leukemia can be divided into many types based on the
immunophenotypic, morphologic, and cytogenetic fea-
tures: acute myeloid leukemia (AML), acute lymphoblastic
leukemia (ALL), chronic myeloid leukemia (CML), chronic
lymphocytic leukemia (CLL), hairy cell leukemia, and adult
T-cell leukemia/lymphoma (ATLL). However, the exact
overall incidence of LC is still unclear. Previous reports
revealed that the incidence of leukemia in United States is
average 1e2 cases per 100,000 populations. One study
retrospectively performed in Austria found that a preva-
lence of LC is 2.9e3.7% among 381 AML patients.3 Another
earlier research in New York, evaluated 877 patients with
AML during 1969e1986 and discovered 18 cases of LC, the
overall prevalence was 2%.4 AML (13%) and ATLL (40e70%)
are more likely to develop LC.5 According to the French-
American-British (FAB) classification for AML,6 it can be
categorized to M0-M7 subtypes, in which M4 and M5 have
the highest rates of cutaneous involvement, accounting for
30e50%.7
Myelodysplastic syndrome (MDS) is not a subtype of
leukemia; yet, it could also progress into acute myeloid
leukemia or present with cutaneous involvement. The FAB
classification for MDS is mainly based on the percentage of
myeloblast in bone marrow, which can be further divided to
the following five categories: refractory anemia (RA), re-
fractory anemia with ring sideroblasts (RARS), refractory
anemia with excess blasts (RAEB), refractory anemia with
excess blasts in transformation (RAEB-T), and chronic
myelomonocytic leukemia (CMML). The manifestations of
LC in MDS patients could imply concurrent or approaching
transformation to AML.8 Similarly, another retrospective
analysis including 108 patients of CMML from 2003 to 2010,
they found the occurrence of LC could foretell the AML
transformation.9
To date, several case series discussing about clinical
characteristics and associated prognosis of LC were con-
ducted at different countries.10e17 Among them, the largest
study of 75 patients of LC in Korea showed the male pre-
dominance and the mean age at diagnosis was 37.6 years.
The commonest cutaneous features were nodules and the
extremities were the most commonly involved.10 The
prognosis of LC is poor, one study in America showed that
88% of patients died within one year of diagnosis.18 Another
227
latest matched-cohort study in 2019, Wang et al. performed
a 1:3 ratio between 62 patients of AML with LC and 186
patients of AML without LC, they found those with LC
showed poorer overall survival and more extramedullary
involvement of internal organs.19
However, most of the studies only described the clinical
manifestations and lacked comparisons between the other
ones. Few studies evaluated their prognosis by using sur-
vival curve and no previous studies involving the data of LC
in Taiwan were reported. In this study, we aimed to
investigate the association between clinical characteris-
tics, distribution, and prognosis among different types of LC
in Taiwan by reviewing medical records, histopathology and
clinical photographs.
Methods
We performed a retrospective analysis. The medical re-
cords were collected from June 1997 to June 2018. Using
the pathological database of the Department of Derma-
tology at Kaohsiung Chang Gung Memorial Hospital, we
identified 42 LC patients. Our hospital is a 2700- beds
medical facility that serves as a tertiary referral center in
southern Taiwan. All cases were diagnosed histopathologi-
cally by pathologists and dermatologists. The study
involved clinical medical histories of the patients including
clinical manifestations and distribution, interval between
LC and systemic leukemia, and survival outcomes according
to different types of LC. All leukemia patients had under-
gone bone marrow examinations performed by hematolo-
gists and oncologists. They were further classified on the
basis of histopathology, morphology, immunohistochem-
istry and cytogenetics.
SPSS software (IBM SPSS Statistics for Windows, Version
22.0. Armonk, NY: IBM Corp.) was used to perform statis-
tical analyses. We conducted KaplaneMeier curve and log-
rank test to evaluate overall survival outcome and the
differences. The axis of time was defined as the interval
between diagnosis of LC and death. The patients who
passed away were counted as events. And the patients
without events, including alive and lost to follow-up, were
censored at the time of the last follow-up. Statistical sig-
nificance was defined as a P-value <0.05, with a two-tailed
test. This study was approved by the Institutional Review
Board of Chang Gung Medical Foundation (IRB No:
201600976B0). The informed consents were exempted by
the board due to the retrospective nature of the study.
Results
Patient characteristics
Of the 42 Taiwanese patients with diagnosis of LC over the
period of 22 years, 27 males and 15 females were identified
(Fig. 1A). The male to female ratio was 1.8 to 1. On
average, there were two new cases diagnosed each year
over the past two decades. The most common was AML
(57%), followed by MDS (19%) and ATLL (12%). There were
also few cases of ALL, CML, and CLL. Three patients were
diagnosed as MDS initially but subsequently progressed into
228
Figure 1 (A) The demographic data including types and
gender distribution of LC. 27 male and 15 female patients were
shown. The most common type was AML (57%), followed by MDS
(19%) and ATLL (12%). (B) The age distribution of LC. Wide
range distribution was noted in AML cases. But there were
mostly old-aged cases among MDS and ATLL. The mean age was
about 55.7 years old (ranged from 16 to 85 years old). AML,
acute myeloid leukemia; ALL, acute lymphoblastic leukemia;
CML, chronic myeloid leukemia; CLL, chronic lymphocytic
leukemia; MDS, myelodysplastic syndrome; ATLL, adult T-cell
leukemia/lymphoma. RAEB, refractory anemia with excess
blasts; RAEB-T, refractory anemia with excess blasts in trans-
formation; CMML, chronic myelomonocytic leukemia. *The
cases were diagnosed as MDS firstly, but already progressed
into AML when LC was confirmed histopathologically.
AML, and afterwards evolved to LC. The mean age of LC at
diagnosis was about 55.7 years old (ranged from 16 to 85
years old) (Fig. 1B). The patients of AML had a wide range
of age distribution. On the contrary, ALL patients were
younger, and the cases of MDS and ATLL were mostly old-
aged.
Clinical features and distribution
We divided the cutaneous features of LC into six categories:
papules, nodules, plaques, macules, patches, and ulcers.
Y.-W. Chang et al.
By dermatologic definitions, a papule is a circumscribed
and elevated lesion less than 1 cm in diameter, which may
be solid or cystic. A nodule is a palpable larger and deeper
form of a papule, lesion greater than 1 cm with a spherical
or domed shape, which may be located in the epidermis,
dermis or hypodermis. A plaque is a solid, elevated, and
plateau-like lesion that has a diameter of 1 cm or larger,
which may be formed by a coalescence of papules or nod-
ules; the surface diameter is greater than its depth. A
macule is a flat and nonpalpable lesion that is even with the
surface level of surrounding skin; it is perceptible only by
change in surface color from the surrounding skin and less
than 1 cm in diameter. A patch is a larger form of a macule,
which is also flat and nonpalpable; it is perceivable with a
different color from its surrounding and larger than 1 cm in
diameter. An ulcer is a skin defect extending to epidermis
and dermis and sometimes even to subcutis.
As shown in the clinical pictures, LC could present as
papulonodules, noduloplaques, and ulcers (Fig. 2). Because
there could be more than one cutaneous findings in
different body parts in the same patient, we separated
each of the same cutaneous features into each category.
Our analysis showed the most common cutaneous features
of LC were papules and nodules, accounting for total 67%,
followed by plaques (16%) (Fig. 3A). Rarely, LC could pre-
sent as macules and/or patches which may be misdiagnosed
as viral exanthem.
We classified the sites of distribution into seven parts:
scalp, face, neck, trunk, extremities, genitalia, and
generalized. The generalized pattern was defined as the
combination of the involvement of the face, trunk and
extremities at the same time. Our study revealed the most
common parts were trunk and extremities, accounting for
total 65%, while 14% of LC cases were counted as general-
ized pattern (Fig. 3B).
Temporal association
LC may precede, accompany, or succeed with the devel-
opment of systemic leukemia. 55e77% of LC patients
develop after its systemic involvement. 23e38% of LC cases
occur concurrent with systemic leukemia. Interesting but
infrequently, LC may develop for at least 1 month previous
to the systemic involvement in peripheral blood or bone
marrow, which is termed as aleukemic LC,20 accounting for
about 7% of the patients. There were 3 cases of aleukemic
LC in our study. All three of them were diagnosed as MDS
initially and subsequently evolved to AML during the follow-
up. 12 cases occurred concomitantly with systemic leuke-
mia, and two-thirds of them were AML. Not surprisingly, LC
most commonly developed following systemic leukemia, 27
cases were identified and the percentage was 64.3%. The
mean interval between the diagnosis of systemic leukemia
and development of LC was about 16.3 months, and most of
them developed within 2 years (Fig. 4).
Survival outcomes
As mentioned previously, several studies have demon-
strated the presentation of LC is indicative of an unfavor-
able prognosis.10,14,18,19,21 In our study, 32 patients died
Leukemia cutis in Taiwan 229

Figure 2 (A) Multiple erythematous papulonodules developed over trunk in a 60-year-old male patient with AML, M5. (B) An 85-
year-old male with CMML presented with diffuse noduloplaques over his back. (C) Ulcerative plaques occurred at lateral aspect of
right leg in a 79-year-old woman with MDS, RAEB type. She was diagnosed as AML 2 months later after LC development; therefore, a
case of aleukemic LC was identified. (D) An 84-year-old man with AML had multiple erythematous papules over his scalp. (E)
Multiple erythematous nodules developed at entire face in a 23-year-old male case of ALL. (F) A 55-year-old man with CLL pre-
sented with ulcers over glans penis for 3 months.

during the follow-up, and 74.3% (26/35) of patients passed
away within 1 year. 3 cases were transferred to other
medical centers for further management, while 4 cases
were lost to follow-up. There were only 3 patients alive
after chemotherapy or bone marrow transplantation.
KaplaneMeier curve was performed to evaluate the overall
survival outcomes, which showed that the median survival
time was only 7.2 months (95% CI, 4.53e9.87 months)
(Fig. 5A). Log-rank test was also conducted to evaluate the
differences of survival outcomes. We included AML, ATLL,
and MDS for the log-ranked test. The patients with AML had
a median survival time of 7.2 months (95% CI, 4.32e10.08
months). The median survival time was 1.5 months (95% CI,
0.64e2.36 months) in the group with ATLL and 3.5 months
(95% CI, 0.31e6.69 months) among those with MDS. This
results were not statistical significant (P Z 0.068 for sur-
vival curves).
Discussion
Leukemia cutis (LC) is the cutaneous infiltration of
neoplastic leukocytes or their precursors. In the past, there
are many terms used, which include primary extra-
medullary leukemia, chloroma, granulocytic sarcoma,
myeloid sarcoma and monocytic sarcoma. Although precise
overall incidence of LC is unclear, it appeared that there
was higher incidence of LC among children. Up to 25e30
percent of LC cases were found in congenital leukemia.22
The pathogenesis about how the leukemic cells infiltrate
into the skin still has not been well explained. In 2008, Cho-
Vega et al. proposed the hypothesis of migration of
leukemic cells into the cutaneous tissue on the basis of the
skin selective homing of memory T-cells. This deduction
highlighted that adhesion molecules, chemokine and
integrin may play an important role in the process of cell
migration.21 Furthermore, some environmental exposures
such as benzene, alkylating agents in chemotherapy,
ionizing radiation, and viral infection (e.g. ATLL caused by
HTLV-I infection) that may increase risks of developing
systemic leukemia, are also stand the same risk factors for
LC development.23
The diagnosis of LC needs to be proven by histopathol-
ogy. The following are some pitfalls that may result in
misdiagnoses. Firstly, single cutaneous nodule without
symptoms may lead to late detection; secondly,
230
Figure 3 (A) The percentage of cutaneous features. The
most common cutaneous presentations of LC were papules
(38%) and nodules (29%), followed by plaques (16%). (B) The
percentage of affected areas. The predilection sites were
trunk (33%) and extremities (32%), but generalized lesions also
accounted for some proportions.
Figure 4 The interval between the diagnosis of systemic
leukemia and development of LC. The mean interval was 16.3
months, and most of them developed within 2 years. However,
few cases may develop up to more than 9 years following
systemic leukemia.
Y.-W. Chang et al.
Figure 5 (A) The KaplaneMeier survival curve showed the
prognosis of LC was poor. The overall median survival time was
7.2 months (95% CI, 4.53e9.87 months). (B) Log-rank test
revealed survival differences between types of LC. The median
survival time of AML was 7.2 months (95% CI, 4.32e10.08
months), ATLL was 1.5 months (95% CI, 0.64e2.36 months), and
MDS was 3.5 months (95% CI, 0.31e6.69 months) (P Z 0.068 for
survival curves). The outcomes of all 42 patients: Death: 32;
Alive (including remission): 3; Transfer to other medical cen-
ters: 3; Lost to follow-up: 4.
maculopapular rash mimicking viral exanthem or drug
eruption; finally, aleukemic LC. In the above clinical set-
tings, clinicians should pay more attention to the medical
histories of the patients and perform skin biopsy if
necessary.14
Leukemia cutis in Taiwan 231

Table 1 Comparisons between cases series of leukemia cutis at different countries.

Country Taiwan Korea Koreaa Austria Spain China United Kingdom
Years 1997e2018 1988e2011 1980e1999 1968e1996 1994e2014 2002e2015 1992e2004
Case numbers 42 75 62 26 17 10 8
Male/Female 27/15 51/24 38/24 12/14 11/6 6/4 5/3
M/F ratio 1.8 2.1 1.6 0.86 1.8 1.5 1.7
Mean age (years) 55.7 37.6 33.2 55.4 62.5 49.3 61.3
Types (No.)
AML 24 49 38 17 10 9 5
ALL 3 18 11 0 0 0 0
CML 1 7 10 9 0 0 2
CLL 1 0 0 0 1 0 1
MDS 8 1 3 0 4 1 0
ATLL 5 0 0 0 0 0 0
Clinical distribution (%)
Scalp 7 10 13 7 0 0 6
Face 9 14 14 3 9 25 19
Neck 2 5 4 0 0 0 6
Trunk 33 28 32 37 23 31 31
Extremities 32 37 33 13 36 31 25
Genitalia 4 1 2 3 5 6 0
Generalized 14 6 2 37 27 6 13
Cutaneous features (%)
Papules 38 31 33 38 33 31 31
Nodules 29 34 28 32 33 61 46
Plaques 16 17 18 10 22 0 15
Macules 6 9 19 18 6 8 8
Patches 1 8 0 0 0 0 0
Ulcers 10 1 2 2 6 0 0
Temporal relation (NA Z 17) (NA Z 5)
Before (aleukemic LC) 3 4 7b 1 5 1 0
Simultaneous 12 13 7b 8 12c 2 3
After 27 58 31b 12 7 5
Intervald (months) 16.3 16.2 NA 23.8 NA 28.9 19.5
Intervale (months) 7.9 8.3 4.3b 8.0 NA 5.6 14
Reference Our study 10 11e13 14 15 16 17
NA: data not available. The bold number in the Table 1 means the highest percentage in each studies.
a
From 3 studies (17 cases from 1980-198911, 22 cases from 1988-199512, and 23 cases from 1989-199913).
b
From 2 studies conducted by Jang IG et al.12 and Jang KA et al.13
c
12 cases include LC occurs simultaneously and after the systemic leukemia.
d
Mean interval between the diagnosis of LC and systemic leukemia.
e
Mean interval between the diagnosis of LC and death.

LC could present with a wide range of clinical features.
Generally speaking, the cutaneous findings are erythema-
tous to purplish, violaceous papules, nodules or plaques.
Sometimes the central parts may show ulcerative change.
Occasionally, the tumors may look like greenish masses
because of myeloperoxidase (MPO) related green pigmen-
tation, resulting in the term “chloroma”. In one study by Su
et al. in the America in 1984, it revealed over half of LC
cases presented with papules and nodules, accounting for
60%, followed by infiltrated plaques (26%).18 Previous re-
ports revealed that most of the skin lesions were usually
asymptomatic, however, extremely pruritus may present.
Similarly, most of our LC cases remained asymptomatic
except some case presented with painful ulcers.
In addition to the typical cutaneous manifestations,
unusual atypical findings of LC may resemble leonine
facies,24 figurate cutaneous lesions,25 fingertip hypertro-
phy,26 erythema nodosum,27 guttate psoriasis,28 chronic
paronychia,29 leukemic vasculitis,30 and rarely, Sister Mary
Joseph’s nodule.31 LC presented as diffuse papulovesicles
mimicking disseminated herpes simplex in a 45-year-old
male patient of AML (M2 type) had also been reported.32
Oral mucosal involvement could present with gingival hy-
perplasia. In a study conducted by Kaddu et al., they found
41% of AML patients presented gingival hyperplasia, and
most of them derived from subtypes of M4 or M5.14 In pe-
diatric cases, congenital leukemia patients may present as
“blueberry muffin” appearance.33
Herein, we compared with other studies at different
countries (Table 1). To date, of all literatures focusing on
LC, we had the second largest case numbers. The ratios of
male to female ranged from 1.5 to 2.1 except more females
232
found in Austria. The mean ages were mostly around 50e60
years old but younger in the Korean studies. Among the
types of LC, undoubtedly, the commonest type was AML,
but we appeared to have more patients of MDS with LC. On
the contrary, fewer cases of ALL and CML were identified
compared to the Korean studies. Previously, more propor-
tion of M4 and M5 subtypes of AML had been reported.14
However, our study revealed that different subtypes of
AML occurred in nearly the same proportions (Fig. 1A).
In an earlier study conducted in 1984, no predilection
sites of LC were reported.18 But in our review, trunk and
extremities were the largest proportions among all of the
studies. Interestingly, more cases of generalized pattern
were reported in our study compared with those in Korea
and China. Papules and nodules were the leading two
cutaneous lesions in regard to the clinical features but ul-
cers were much more common in our study as compared
with the other ones.
As mentioned previously, LC may occur before, concur-
rently, or after the development of systemic leukemia.
Most of the studies revealed LC developed following sys-
temic leukemia. The mean interval was about 1e2 years
until the skin eruption. And the mean interval between the
diagnosis of LC and death was mostly within 8 months,
showing the unfavorable prognosis. In our study, there were
three cases of aleukemic LC, and the average interval of
transformation to AML was 6 months. This result was
consistent with Longacre and Smoller’s research in 1993.
They analyzed 50 cases of LC with MDS and determined the
mean time evolving to systemic leukemia was 6 months
after LC development.34
Intriguingly, only one case with CLL was identified in our
study, and the interval between the diagnosis of leukemia
and LC development was more than 10 years (126.9 months).
This result was similar with a CLL case in the United Kingdom,
the interval was reported 9.5 years (114 months).17 Accord-
ing to the latest matched-cohort study in 2019, it revealed
the group with LC had a worse overall five-year survival rate
(8.6%) compared to the group without LC (28.3%).19
The management of LC is directed to the treatment of
the underlying systemic leukemia, including systemic
chemotherapy or local therapy.21 If the cases are refractory
to treatments or tending to be palliative, local radiation
therapy such as total skin electron beam therapy could be a
treatment option, especially AML cases.35 Resolution of skin
lesions is usually followed by the remission of systemic
hematological disorders. In addition to conventional
chemotherapy, autologous or allogeneic stem cell trans-
plantation often leads to more favorable outcome.3
In conclusion, this study was the first retrospective case
series to investigate LC in Taiwan and the first large-scale
research in regarding to LC of Han Chinese. It revealed the
preponderance in males and most types were AML and MDS.
The commonest clinical features were papules and nodules,
and more ulcers were identified. The predilection sites
were trunk and extremities. LC often indicates an advanced
status with poor prognosis and is a marker of rapid pro-
gression of underlying hematological diseases. Rarely, it
could present as aleukemic LC. Therefore, it is very
important that clinicians should be familiar with the cuta-
neous features and make timely diagnosis of the extra-
medullary involvement.
Y.-W. Chang et al.
Limitations
The major limitations of our research include its retro-
spective nature without control groups and restriction to a
single tertiary referral center. The case numbers may be
underestimated because only skin biopsy-proven ones are
included. We are not able to compare the incidence of LC
according to the different types of systemic leukemia
because of unavailable epidemiological data at our hospi-
tal. Further studies are needed in the future.
Contributors
C.H. Lee provided the original conception. C.H. Lee and
H.C. Tseng designed the study. Y.W. Chang and H.C. Tseng
collected the data, analyzed the data, and drafted the
article. All authors (Y.W. Chang, C.H. Lee, and H.C. Tseng)
contributed to the data interpretation, revised the manu-
script for important intellectual content, and approved the
final version of the manuscript.
Declaration of Competing Interest
The authors have no conflicts of interest relevant to this
article.
Appendix A. Supplementary data
Supplementary data to this article can be found online at
https://doi.org/10.1016/j.jfma.2020.04.025.
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