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\begin{document}

\title{Splenic hemangiomas with different imaging findings: two
laparoscopically resected incidentalomas}



\author[1]{Kazuhiro Hiyama}%
\author[1]{Izumi Kirino}%
\author[1]{Yasuo Fukui}%
\author[1]{Hideo Terashima}%
\affil[1]{Atago Hospital}%


\vspace{-1em}



  
  \date{May 18, 2024}


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\selectlanguage{english}
\begin{abstract}
Although splenic tumors are relatively rare, we sometimes encounter
incidentalomas in the spleen. In such cases, we must plan treatment
based on imaging studies. Herein, we report two cases of splenic
hemangioma with different imaging findings, which were resected
laparoscopically.%
\end{abstract}%



\sloppy


\textbf{Splenic hemangiomas with different imaging findings: two
laparoscopically resected incidentalomas}

Kazuhiro Hiyama\textsuperscript{1}, Izumi Kirino\textsuperscript{1},
Yasuo Fukui\textsuperscript{1}, Hideo Terashima\textsuperscript{1}

1: Department of Surgery, Atago Hospital, Kochi, Japan

Keywords: splenic hemangioma, splenic incidentaloma, laparoscopic
splenectomy

Corresponding author

Kazuhiro Hiyama, MD

Department of Surgery, Atago Hospital

1-1-13, Atago-machi, Kochi, Japan

E-mail:\emph{hiyama@atago-hp.or.jp}

\textbf{Key Clinical Message (\textless{}50 words)}

Although splenic tumors are relatively rare, we sometimes encounter
incidentalomas. We must plan treatment based on imaging studies. In some
cases, we might have to consider detailed imaging study and/or tumor
biopsy.

\textbf{Introduction}

Splenic tumors are rare. They include benign primary tumors, such as
lymphangioma and hemangioma, and malignant primary tumors, such as
malignant lymphoma and angioblastoma. Also, solid cancers, such as
gastric, colon, and ovarian cancer sometimes metastasize to the spleen.
In 2013, Heller suggested a diagnostic and follow-up strategy for
splenic tumors as shown in Figure 1 (1); however, it is currently not
easy to differentiate between the various histological types of splenic
tumors and choose an appropriate treatment plan. Herein, we report two
cases of splenic hemangioma with different imaging findings. The tumors
mimicked malignant tumors, which led us to perform laparoscopic
splenectomy.

\textbf{Case history/ Examination}

\textbf{Case 1}

A female in her 50s presented to our internal medicine department to
undergo a work-up after multiple splenic tumors had been detected by
ultrasound during a health check-up. She did not have a fever or
abdominal pain. Her medical history was non-specific, and she had not
previously suffered from a panic disorder or appendicitis in childhood.
She had been taking clotiazepam for a while. She was not in acute
distress, and her vital signs were non-specific. On physical
examination, her spleen was not palpable, and she did not have
lymphadenopathy.

\textbf{Case 2}

A female in her 80s presented to our surgical department to undergo
follow-up examinations for ascending colon cancer, which had been
resected one year ago. She had a mild discomfort in the left upper
quadrant. She did not have a fever. She had undergone laparoscopic right
hemicolectomy for advanced ascending colon cancer (pT4a N1 M0, Stage
IIIa, according to the Japanese Classification of Colorectal,
Appendiceal, and Anal Carcinoma, Nineth English Edition) one year ago.
She had not received adjuvant chemotherapy according to her wishes.
Otherwise, her medical history was unremarkable and did not include
hypertension or hyperlipidemia. On physical examination, her spleen was
not palpable, and she did not have lymphadenopathy.

\textbf{Differential diagnosis, investigations, and treatment}

\textbf{Case 1}

A contrast-enhanced computed tomography (CT) scan (Fig. 2a, b) showed
innumerable splenic tumors, which were homogeneous, but poorly
demarcated. The maximum diameter of the largest tumor was 3 cm. The
tumors were not enhanced. The attending physician decided to perform a
follow-up CT scan 6 months later.

The patient was referred to our surgical department to undergo a more
detailed consultation at that time. A laboratory workup demonstrated a
normal complete blood count, an elevated lactate dehydrogenase level
(404 IU/L), and a slightly elevated cancer antigen 19-9 (CA19-9) level
(58.1 U/mL), but a normal carcinoembryonic antigen (CEA) level (2.3
ng/mL). A follow-up contrast-enhanced CT scan showed slight enlargement
of the tumors (maximum diameter: 3.5 cm) without any findings that were
indicative of diseases affecting other organs, such as solid cancer
(Fig. 2c, d). No specific findings were noted during upper or lower
endoscopy. We could not rule out a malignant tumor because of the
following: 1. The tumors exhibited poor demarcation. 2. The tumors were
slightly enlarged. 3. The patient's CA19-9 level was slightly elevated.
Although Heller's strategy recommends positron emission tomography/CT or
a biopsy as a next step, since the tumors were innumerable and small, we
performed laparoscopic splenectomy as a ``diagnostic treatment'' (Fig.
3).

\textbf{Case 2}

A contrast-enhanced CT scan performed 6 months after the colon surgery
showed a solitary splenic tumor (maximum diameter: 2.0 cm) without any
other organ metastasis or dissemination. The tumor was homogenous and
well-demarcated (Fig. 4a, b). Twelve months later, a follow-up
contrast-enhanced CT scan showed marked enlargement of the splenic tumor
(maximum diameter: 2.5 cm), without any other organ metastasis or
dissemination (Fig. 4c, d). A laboratory workup demonstrated normal
tumor marker levels (CEA: 5.2 ng/mL, CA19-9: \textless{}0.5 U/mL). We
suspected metastatic cancer due to the rapid progression of the disease.
Since the patient did not have any other organ metastasis, we performed
laparoscopic splenectomy as a ``diagnostic treatment'' (Fig. 5).

\textbf{Outcome and follow up}

Both operations were performed without any postoperative complications.
Histopathologically, both tumors were diagnosed as hemangiomas. Case 1:
Multiple nodules were found in the spleen, which microscopically
consisted of proliferating blood vessels without epithelial
abnormalities (Fig. 6). Case 2: A cystic nodule was found in the spleen,
which microscopically consisted of proliferating blood vessels without
epithelial abnormalities (Fig. 7, 8). We followed the patients for 3
months after surgery.

\textbf{Discussion}

Splenic tumors are relatively rare. In fact, Bostick WL encountered 10
cases among 80,527 people (2). There are various histological types,
including benign primary tumors, such as lymphangioma, hamartoma, and
hemangioma; malignant primary tumors, such as malignant lymphoma and
angioblastoma; and metastatic tumors (3-5). The most common type of
primary benign splenic tumor is hemangioma, almost all of which occur as
solitary lesions (6). However, there have been a few reports about cases
involving multiple splenic tumors (7) (8). On the other hand, malignant
primary splenic tumors, such as angioblastoma, are very rare. However,
their prognosis is quite poor (6). The clinical presentation of splenic
tumors is highly variable (9); therefore, we must learn how to
differentiate among them. Although Heller suggested a diagnostic and
follow-up strategy for splenic tumors, which is currently used worldwide
(1), challenging cases are sometimes encountered.

We experienced two cases of splenic hemangioma with different clinical
presentations and imaging findings.

In case 1, we suspected angiosarcoma because of the following findings:
1. The tumors enlarged. 2. The tumors were heterogeneous and poorly
demarcated. (10) Although we initially considered hemangioma, large
splenic tumors sometimes mimic angioblastoma (11). In cases of splenic
angiosarcoma, surgery is the only curative treatment, and hence, the
chance to resect such tumors must not be missed. This was the reason why
we performed splenectomy. It might have been better to have conducted a
magnetic resonance imaging (MRI) scan. S.Y. Choi reported that
contrast-enhanced dynamic and diffusion-weighted MRI are useful for
distinguishing between benign and malignant splenic tumors (12).

In case 2, we suspected a metastatic tumor derived from adenocarcinoma
of the ascending colon because of both the patient's medical history and
the rapid enlargement of the tumor. Solitary splenic metastases are
rare, but they can occur in some cases (13). It may have been better to
perform a biopsy of the tumor. Although in Japan splenic biopsies are
hardly performed due to fears of causing intraabdominal bleeding or
tumor dissemination, they are reported to be a safe and effective way of
distinguishing among splenic tumors (14) (15) (16) (17) (18). Heller
recommended that biopsies should be performed as a second diagnostic
step for splenic tumors that are suspected of malignancy (1). On the
other hand, Cho reported a case in which severe complications occurred
after a biopsy of a splenic tumor (19). All things considered, biopsying
splenic tumors is quite effective; however, with recognition of the
potential complications, clinicians should take sufficient precautions
such as antibiotic therapy, and preparation for an urgent surgery
(splenectomy in some cases).

Laparoscopic splenectomy for hemangioma was first performed by Hodge in
1895 (8). Due to a fear of bleeding, the hand-assisted method is usually
selected in the cases involving giant splenomegaly. For splenic tumors,
laparoscopic splenectomy is superior to classical open surgery because
the laparoscope makes it possible to see the whole abdomen from various
angles. This was particularly useful in our case 2, as we initially
suspected that the tumor was a metastatic lesion, and hence, it was
important to rule out other types of metastases, such as dissemination.

In summary, there are a wide variety of splenic tumors. The Heller's
diagnostic pathway (Fig. 1) is helpful as a diagnostic tool in them (1).
For further evaluation, contrast-enhanced MRI and tumor biopsies should
be considered. Also, patients should be informed that even benign tumors
(which mainly measure \textgreater{}1 cm) can rupture (20) and cause
acute abdomen. In cases of splenomegaly, laparoscopic resection
with/without the hand-assisted method should be considered.

\textbf{Figure Legends}

Figure 1

The Heller's Diagnostic and follow-up strategy. (1) *Cyst: imperceptible
wall, near-water attenuation (\textless{}10 HU), no enhancement. +:
Hemangioma: discontinuous, peripheral, centripetal enhancement (findings
that are uncommon in splenic hemangiomas). ++: Benign imaging features:
homogeneous, low attenuation (\textless{}20 HU), no enhancement, smooth
mar- gins. \selectlanguage{ngerman}§: Evaluate: PET vs. MRI vs. biopsy. ll: Suspicious imaging
features: heterogeneous, enhancement, irregular margins, necrosis,
splenic parenchymal or vascular invasion, substantial enlargement. ¶:
Indeterminate imaging features: heterogeneous, intermediate attenuation
(\textgreater{}20 HU), enhancement, smooth margins. \#: Follow-up MRI in
6 and 12 months.

Figure 2

Contrast-enhanced computed tomography (CT) scans obtained in case 1

Initial visit: (a) arterial phase; (b) delayed phase

Innumerable splenic tumors were seen.

Six months later: (c) arterial phase; (d) delayed phase

The tumors had enlarged.

Figure 3

Laparoscopic image of the tumors in case 1

Innumerable whitish splenic tumors were seen (arrows).

Figure 4

Contrast-enhanced CT scans obtained in case 2

Initial visit: (a) arterial phase; (b) delayed phase

A solitary splenic tumor (maximum diameter: 2.0 cm) was seen.

Twelve months later: (c) arterial phase; (d) delayed phase

The tumor had enlarged (maximum diameter: 2.5 cm).

Figure 5

Laparoscopic image of the tumor in case 2

A solitary, slightly hard tumor was seen (arrow).

Figure 6

Resected spleen (case 1)

Multiple nodules, consisting of proliferating blood vessels, were found
in the spleen.

Figure 7

Resected spleen (case 2)

A cystic nodule was found in the spleen.

Figure 8

Histopathological findings of the resected spleen (case 2)

The tumor consisted of proliferating blood vessels without any
epithelial abnormalities. These findings were consistent with
hemangioma.

\textbf{Conflicts of Interest Statement}

The authors declare that they have no conflict of interests and that
there are no relevant financial disclosures to report.

\textbf{Authors' contributions}

Kazuhiro Hiyama made substantial contributions to the data acquisition
and the study conception, design, and interpretation. He was also
involved in the initial drafting of the manuscript and critically
revising the final manuscript.

The other authors were involved in revising the final manuscript. All of
the authors have reviewed the final manuscript and gave their approval
to the version to be published. In addition, they agree to be
accountable for all aspects of the work, including for ensuring that
questions related to the accuracy or integrity of any part of the work
are appropriately investigated and resolved.

\textbf{List of abbreviations}

CA19-9: cancer antigen 19-9, CEA: carcinoembryonic antigen, CT: computed
tomography, MRI: magnetic resonance imaging

\textbf{Consent}

Written informed consent was obtained from the patient prior to
submission.

\textbf{References}

1. Heller MT, Harisinghani M, Neitlich JD, Yeghiayan P, Berland LL.
Managing incidental findings on abdominal and pelvic CT and MRI, part 3:
white paper of the ACR Incidental Findings Committee II on splenic and
nodal findings. J Am Coll Radiol. 2013;10(11):833-9.

2. Bostick WL. Primary Splenic Neoplasms. Am J Pathol.
1945;21(6):1143-65.

3. Kaza RK, Azar S, Al-Hawary MM, Francis IR. Primary and secondary
neoplasms of the spleen. Cancer Imaging. 2010;10(1):173-82.

4. Vancauwenberghe T, Snoeckx A, Vanbeckevoort D, Dymarkowski S,
Vanhoenacker FM. Imaging of the spleen: what the clinician needs to
know. Singapore Med J. 2015;56(3):133-44.

5. Ricci ZJ, Mazzariol FS, Flusberg M, Chernyak V, Oh SK, Kaul B, et al.
Improving diagnosis of atraumatic splenic lesions, part II: benign
neoplasms/nonneoplastic mass-like lesions. Clin Imaging.
2016;40(4):691-704.

6. Abbott RM, Levy AD, Aguilera NS, Gorospe L, Thompson WM. From the
archives of the AFIP: primary vascular neoplasms of the spleen:
radiologic-pathologic correlation. Radiographics. 2004;24(4):1137-63.

7. Steininger H, Pfofe D, Marquardt L, Sauer H, Markwat R. Isolated
diffuse hemangiomatosis of the spleen: case report and review of
literature. Pathol Res Pract. 2004;200(6):479-85.

8. Shinde J, Pandit S, Kolte S, Singh SP. Laparoscopic splenectomy for
haemangioma of the spleen. J Minim Access Surg. 2014;10(1):42-4.

9. Abrishami A, Khalili N, Kooraki S, Abrishami Y, Grenacher L, Kauczor
HU. Evaluation of cross-sectional imaging features that aid in the
differentiation of benign and malignant splenic lesions. Eur J Radiol.
2021;136:109549.

10. Thipphavong S, Duigenan S, Schindera ST, Gee MS, Philips S.
Nonneoplastic, benign, and malignant splenic diseases: cross-sectional
imaging findings and rare disease entities. AJR Am J Roentgenol.
2014;203(2):315-22.

11. Misawa T, Shiba H, Fujiwara Y, Futagawa Y, Harada T, Ikegami M, et
al. Massive splenomegaly caused by cavernous hemangiomas associated with
Klippel-Trenaunay syndrome: report of a case. Surg Today.
2014;44(1):197-200.

12. Choi SY, Kim SH, Jang KM, Kang TW, Song KD, Moon JY, et al. The
value of contrast-enhanced dynamic and diffusion-weighted MR imaging for
distinguishing benign and malignant splenic masses. Br J Radiol.
2016;89(1063):20160054.

13. Obana A, Komatsu N, Aiba K, Nakanishi S, Abe M, Yamaguchi T, et al.
A case of long-term survival after splenectomy for solitary splenic
metastasis from gastric cancer. World J Surg Oncol. 2020;18(1):250.

14. Keogan MT, Freed KS, Paulson EK, Nelson RC, Dodd LG. Imaging-guided
percutaneous biopsy of focal splenic lesions: update on safety and
effectiveness. AJR Am J Roentgenol. 1999;172(4):933-7.

15. Lucey BC, Boland GW, Maher MM, Hahn PF, Gervais DA, Mueller PR.
Percutaneous nonvascular splenic intervention: a 10-year review. AJR Am
J Roentgenol. 2002;179(6):1591-6.

16. McInnes MD, Kielar AZ, Macdonald DB. Percutaneous image-guided
biopsy of the spleen: systematic review and meta-analysis of the
complication rate and diagnostic accuracy. Radiology.
2011;260(3):699-708.

17. Singh AK, Shankar S, Gervais DA, Hahn PF, Mueller PR. Image-guided
percutaneous splenic interventions. Radiographics. 2012;32(2):523-34.

18. Patel N, Dawe G, Tung K. Ultrasound-guided percutaneous splenic
biopsy using an 18-G core biopsy needle: our experience with 52 cases.
Br J Radiol. 2015;88(1055):20150400.

19. Cho SY, Cho E, Park CH, Kim HJ, Koo JY. Septic shock due to
Granulicatella adiacens after endoscopic ultrasound-guided biopsy of a
splenic mass: A case report. World J Gastroenterol. 2021;27(8):751-9.

20. Karakayali F, Basaran C, Soy EA, Karakus S, Yabanoglu H, Moray G, et
al. Spontaneous spleen rupture and rectus sheath hematoma in a patient
with Klippel-Trenaunay syndrome: report of a case. Surg Today.
2010;40(2):154-7.

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