Benign metastasizing leiomyoma and 18‑FDG‑PET/CT: A case report and literature review

  • Authors:
    • Yusuke Sawai
    • Toshiki Shimizu
    • Yuta Yamanaka
    • Maiko Niki
    • Shosaku Nomura
  • View Affiliations

  • Published online on: July 19, 2017     https://doi.org/10.3892/ol.2017.6609
  • Pages: 3641-3646
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Abstract

Pulmonary benign metastasizing leiomyoma (PBML) is a rare disease entity that usually occurs in females of reproductive age with a previous history of uterine myoma. It is typically characterized by multiple pulmonary tumors consisting of benign leiomyoma cells. In the present study, two cases of PBML are discussed. The patient in each case underwent 2‑deoxy‑2‑(fluorine‑18)‑fluoro‑D‑glucose positron emission tomography/computed tomography (18‑FDG‑PET/CT) scans. One patient demonstrated a lack of 18‑FDG uptake and a quiescent clinical course. However, the second patient exhibited a markedly high uptake of 18‑FDG and aggressive cell proliferation. The two tumors revealed significant differences in metabolic behavior and in clinical course; however, they were similar with regard to cellular appearance. A review of previous studies concerning the findings of 18‑FDG‑PET/CT in published cases of PBML was also conducted and is presented here.

Introduction

Pulmonary benign metastasizing leiomyoma (PBML) is a rare disease entity that usually occurs in females of reproductive age with a prior history of uterine myoma. PBML was first described by Steiner in 1939 (1). PBML is typically characterized by multiple pulmonary tumors containing benign leiomyoma cells (2). Patients are usually asymptomatic and the tumors grow gradually (3). In the present study, two cases of PBML are presented, each of which include the results of 2-deoxy-2-(fluorine-18)-fluoro-D-glucose positron emission tomography/computed tomography (18-FDG-PET/CT) scans. The first patient demonstrated an absence of 18-FDG uptake and a quiescent clinical course. However, the second patient exhibited a markedly high uptake of 18-FDG and the aggressive proliferation of tumor cells was detected. The two tumors revealed significant differences in metabolic behavior and clinical course, yet were alike in regard to cellular appearance. A literature review on the findings of 18-FDG-PET/CT scans in previous published cases of PBML was also conducted and is discussed here.

Case

Case 1

A 38-year-old female was diagnosed with papillary adenocarcinoma of the thyroid gland following a fine-needle aspiration biopsy in Kansai Medical University Takii Hospital in July 2009. However, a CT scan of the chest revealed the presence of multiple nodules of varying sizes in each of the lungs (Fig. 1A). Consequently, an 18-FDG-PET/CT scan was performed. A lesion with high 18-FDG uptake [maximum standard uptake value (SUVmax), >4.9] was observed in the left lobe of the thyroid gland (Fig. 1B and C). However, the results revealed that none of the pulmonary nodules demonstrated 18-FDG uptake (SUVmax, <1.6; Fig. 1C and D). To elucidate whether the pulmonary nodules were metastatic, a CT-guided needle biopsy of the lungs was performed.

Histological examination was performed as part of routine clinical practice. Briefly, the 7-µm thick sections obtained from formalin-fixed and paraffin-embedded tissues were used for further examination. Resected tissue was fixed in 10% formalin neutral buffer solution (Muto Pure Chemicals Co., Ltd., Tokyo, Japan) at room temperature overnight. Hematoxylin and eosin (H&E) staining was used according to standard clinical histological examination. Light microscopy (BM43/DP27, original magnification, ×400; Olympus Corporation, Tokyo, Japan) was used for observation. H&E staining was performed with Tissue-Tek DRS Slide Stainer (Sakura Fine Tek Europe B.V., Flemingweg, Netherlands) according to manufacturer's protocol. Immunohistochemical staining for αSMA and Ki-67 was performed with Histofine Histostainer 36A (Nichirei Biosciences Inc., Tokyo, Japan) using primary antibodies against αSMA and Ki-67 according to manufacturer's protocol.

The 4 µm thick sections obtained from formalin-fixed and paraffin-embedded tissues were deparaffinized in xylene and rehydrated in a graded series of alcohol to water. Antigen retrieval was performed using 10 mM citrate buffer (pH 6.0) at 121°C for 15 min. Sections were washed in TBS. Antigen retrieval was not performed when examining the expression of αSMA. Sections were blocked with 3% H2O2 at room temperature for 10 min and then incubated for 1 h at room temperature with the antibodies against αSMA (catalog no. 712021; clone no. 1A4; pre-diluted working solution for Histostainer) or Ki-67 (catalog no. 718017; clone no. SP6; pre-diluted working solution for Histostainer) (both from Nichirei Biosciences Inc., Tokyo, Japan).

The sections were subsequently incubated with the Histofine Simple Stain MAX PO (Nichirei Biosciences Inc.) for 30 min at room temperature according to the manufacturer's protocol. Staining was visualized by adding 3,3′diaminobenzidine (K5007; Dako; Agilent Technologies, Inc., Santa Clara, CA, USA) for 10 min at room temperature. Sections were counterstained with haematoxylin for 1 min and then dehydrated with a series of alcohols and xylene.

The lung biopsy tissue specimen revealed a disordered arrangement of spindle-shaped tumor cells (Fig. 2A), and immunohistochemical examination indicated that the cells stained positive for α-smooth muscle actin (α-SMA). The Ki-67 ratio was <1% (Fig. 2B and C). These findings were consistent with the phenotypic characteristics of benign leiomyoma (1). At the age of 37, the patient had experienced extensive genital bleeding due to a uterine myoma, and an emergency total hysterectomy with a right oophorectomy was performed. Histological examination of the preexisting uterine myoma tissue specimens, which were obtained during a previous surgical resection (Japan Community Health Care Organization Hoshigaoka Medical Center, Osaka, Japan), was performed as aforementioned. The results of the histological examination revealed the presence of intravascular leiomyomatosis, which is associated with the pathogenesis of PBML (4). Thus, a definitive diagnosis of PBML was established.

As the pulmonary lesions were not attributable to metastases of thyroid cancer, the patient underwent a subtotal thyroidectomy with a curative intention. The tumor-node-metastasis classification pathological stage of the tumor was identified to be pT1aN1aM0 (5). With regard to PBML, observation without the use of aggressive therapy is recommended when the tumor is clinically quiescent (3).

Case 2

A 62-year-old post-menopausal female was referred to Kansai Medical University Takii Hospital for an investigation due to the presence of numerous pulmonary nodules detected in a routine chest radiography in August 2013. The patient had experienced bilateral upper back pain for two weeks prior to the first appointment at this hospital. The patient had no history of uterine myoma. A chest CT revealed the presence of a tumor in the right upper lung that was 60 mm in diameter and numerous nodular lesions of varying sizes in each of the lungs, in addition to a soft tissue mass that was 70 mm in diameter in the left second rib (Fig. 3A). The parameters assessed included complete blood count and standard clinical laboratory examinations, and the expression levels of specific tumor markers were within normal limits, including carcinoembryonic antigen, serum cytokeratin-19 fragments and Pro-gastrin-releasing pepetide. Contrast-enhanced magnetic resonance imaging of the head revealed a tumor in the left parietal lobe that was 20 mm in diameter, with an edema. As the patient was suspected to have a lung cancer with pulmonary, bone and brain metastases, an 18-FDG-PET/CT scan was performed. The results indicated abnormally high 18-FDG uptake in the right upper lung tumor, the left third rib tumor, atlas vertebra, fourth thoracic vertebra, bilateral ilia and multiple bilateral pulmonary nodules in the lungs (Fig. 3B-D; SUVmax, 20.1). Subsequently, a CT-guided needle biopsy of the right upper lung tumor was performed. Histological examination of the lung biopsy tissue specimen revealed a disordered arrangement of spindle-shaped tumor cells with mild atypia (Fig. 2D). Immunohistochemical examination revealed that the cells stained positive for α-SMA (Fig. 2E). By contrast, CD34, S-100, estrogen receptor (ER) and progesterone receptor (PgR) expression was not detected in these cells. The Ki-67 ratio was <1% (Fig. 2F). These findings are consistent with the phenotypic characteristics of benign leiomyoma. In order to confirm the pathological diagnosis, an additional CT-guided needle biopsy of the tumor of the left rib was performed. The results of the second biopsy tissue specimen from the tumor of the left rib corroborated the findings from the first biopsy specimen obtained from the tumor in the right lung. Consequently, a definitive diagnosis of PBML was established. The patient received whole brain irradiation followed by palliative irradiation for the pulmonary nodules in the right upper lung and left second rib. However, no treatment response was observed and the tumors were identified to be growing (Fig. 4). After three months, the patient was re-admitted to hospital due to a consciousness disorder. Corticosteroids and glycerin were administered, and the neurological symptoms were temporarily improved. However, the patient succumbed to septicemia with Clostridium perfringens.

Discussion

To date, the metabolic behavior of PBML in 18-FDG-PET/CT has attracted a high degree of interest. A number of previous reports have demonstrated that there is a lack of 18-FDG uptake in PBML. However, to the best of our knowledge, there has not yet been a systematic review with respect to the 18-FDG-PET/CT findings for PBML. Therefore, a literature review of prior case reports concerning patients with PBML and 18-FDG-PET/CT findings was conducted. In total, 34 cases were identified in 29 reports (3,633). In addition to these 34 cases, the present two cases were added and a total of 36 cases of PBML were reviewed. The results are summarized in Table I. The median age of the patients included was 47 years (range, 34–69 years). A total of 5 patients were pre-menopausal, 2 were post-menopausal and 19 patients had previously received a hysterectomy. The conditions of the reproductive systems of the remaining 10 patients were unconfirmed. All of the total 36 cases were of benign leiomyoma. However, only one patient exhibited malignant transformation (16). With regard to the 18-FDG-PET/CT findings, the accumulation of 18-FDG varied significantly. According to the discretion of the researchers, the patients were assigned into the following three groups: No (minimal) uptake, low (moderate) uptake and high (positive) uptake. A total of 25 patients (69.4%) were assigned to the no uptake group, 8 patients (22.2%) were assigned to the low uptake group and 3 patients (8.3%) were assigned to the high uptake group. However, only one patient out of those 3 had a tumor that demonstrated aggressive behavior. The SUVmax values were identified in 13/36 cases and the median value was determined to be 2.2 (range, 1.4–20.1). The Ki-67 proliferation index ranged from 0–5% in those 13 cases and a total of 7/13 cases had a Ki-67 index <1%. Consequently, there was no significant correlation observed between the uptake of 18-FDG in the tumors and the Ki-67 index. The expression of ER and PgR within the tumors was also assessed. In total, 21/23 patient tissue samples exhibited positive staining for ER (91.3%) and 20/21 had positive staining for PgR (95.2%). However, the patient in case 2 was determined to be double negative for ER and PgR.

Table I.

Characteristics of patients with PBML with 18-FDG-PET/CT findings.

Table I.

Characteristics of patients with PBML with 18-FDG-PET/CT findings.

Author, yearAgeStatusFDG uptake (SUVmax)Ki-67 indexERPgR(Refs.)
Chan et al, 2005 (6)
  Case 149PreNo uptake (ca. 1.4)NE++
  Case 245HRTno uptake (ca. 2.0)NENENE
Moon et al, 200952PostNo uptake (NE)NE++(7)
di Scioscio et al, 200964HRTno uptake (NE)<1%++(8)
Lee, 200751NENo uptake (NE)NENENE(9)
Londero et al, 200852HRTlow uptake (NE)NE++(10)
Kasai et al, 200953HRTNo uptake (NE)NE+(11)
Lin et al, 2010 (12)
  Case 138NElow uptake (0.2–2.2)NENENE
  Case 237HRTNon avid (0.7–2.9)NENENE
Clément-Duchêne et al, 201055HRTno uptake (NE)NENENE(13)
Lin and Bradshaw, 201044PreNo uptake (NE)NE++(14)
Caminati et al, 201169NEno uptake (NE)NE++(15)
Ogawa et al, 201165NELow uptake (ca. 3.8)NENENE(16)
Yoon et al, 201134Prefaint uptake (NE)NENENE(17)
Ni et al, 201246NENon avid (ca. 3.1)NENENE(18)
Nakajo et al, 201250HRTno uptake (ca. 1.5)<1%++(19)
Fu et al, 201246HRTNo uptake (NE)<5%NE+(20)
Alraiyes et al, 201340HRTno uptake (NE)NE++(21)
Okabe et al, 201347PreNo uptake (NE)NE+NE(22)
Tsunooka et al, 2013 (23)
  Case 151NEno uptake (NE)<1%++
  Case 258HRTNo uptake (NE)<1%++
Mogi et al, 201335NEno uptake (NE)NE++(24)
Chen et al, 2013 (25)
  Case 147NENo uptake (NE)NE++
  Case 247HRTmoderately (NE)<3%++
  Case 353NEModerately (NE)<5%++
Ağaçkiran et al, 201344HRTincreased (1.92–4.60)<3%++(26)
Loukeri et al, 201447PreLow uptake (ca. 2.2)<3%+NE(27)
Jeon et al, 201357HRTlow uptake (NE)NE++(28)
Okita et al, 201344HRTNo uptake (NE)NENENE(29)
Jin et al, 201343HRTminimal (0.9–1.8)<1%++(30)
Taftaf et al, 201452HRTPositive uptake (NE)NE+NE(31)
Ma and Cao, 201545HRTno uptake (NE)<1%++(32)
Wei et al, 201547HRTNo uptake (NE)<5%NENE(3)
Wang et al, 201648NElow uptake (0.5–2.1)NENENE(33)
Present case-138HRTNo uptake (<1.6)<1%NENE
Present case-262Posthigh uptake (20.1)<1%

[i] ER, estrogen receptor; PgR, progesterone receptor; HRT, hysterectomy; Pre, premenopausal; Post, postmenopausal; NE, not evaluated; ca, circa; 18-FDG-PET/CT, 2-deoxy-2-(fluorine-18)-fluoro-D-glucose positron emission tomography/computed tomography; SUVmax, maximum standard uptake value.

It has previously been reported that 18-FDG-PET/CT is useful for distinguishing malignant leiomyosarcoma from benign leiomyoma (34,35). In general, SUV values for leiomyosarcoma were observed to be significantly greater than those for leiomyoma. However, numerous reports for 18-FDG-avid leiomyoma were also identified (3638). Furthermore, a series of comprehensive analyses for those patients who underwent 18-FDG-PET/CT revealed that small proportion of benign uterine leiomyomas exhibited positive 18-FDG uptake. In the present study, a case of 18-FDG-avid PBML is detailed. Summarizing previous studies indicated that 33 PBML cases involved 18-FDG non-avid tumors, and only 3 were 18-FDG-avid tumors. No particular phenotype was identified to be associated with 18-FDG-avid PBML. Further investigations are required in order to improve present understanding of the biological characteristics of PBML, thus leading to its optimal management.

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APA
Sawai, Y., Shimizu, T., Yamanaka, Y., Niki, M., & Nomura, S. (2017). Benign metastasizing leiomyoma and 18‑FDG‑PET/CT: A case report and literature review. Oncology Letters, 14, 3641-3646. https://doi.org/10.3892/ol.2017.6609
MLA
Sawai, Y., Shimizu, T., Yamanaka, Y., Niki, M., Nomura, S."Benign metastasizing leiomyoma and 18‑FDG‑PET/CT: A case report and literature review". Oncology Letters 14.3 (2017): 3641-3646.
Chicago
Sawai, Y., Shimizu, T., Yamanaka, Y., Niki, M., Nomura, S."Benign metastasizing leiomyoma and 18‑FDG‑PET/CT: A case report and literature review". Oncology Letters 14, no. 3 (2017): 3641-3646. https://doi.org/10.3892/ol.2017.6609