Ophthalmic Surgery, Lasers and Imaging Retina

Clinical Science 

Choriocapillaris Changes Imaged by OCT Angiography After Half-Dose Photodynamic Therapy for Chronic Central Serous Chorioretinopathy

Kyoko Fujita, MD, PhD; Akiyuki Kawamura, MD, PhD; Mitsuko Yuzawa, MD, PhD

Abstract

BACKGROUND AND OBJECTIVE:

To evaluate the choriocapillaris using optical coherence tomographic angiography (OCTA) after half-dose verteporfin photodynamic therapy (hd-PDT) for chronic central serous chorioretinopathy (CSC).

PATIENTS AND METHODS:

We studied six eyes (six patients) with chronic CSC treated by hd-PDT. OCTA was performed before, 1 week after, and 1 month after hd-PDT. The area of flow abnormality at the choriocapillaris level within the PDT spot after hd-PDT was compared with that before hd-PDT.

RESULTS:

Serous retinal detachment was diminished in all eyes, with three achieving complete resolution at 1 month. On OCTA, all eyes showed irregular choriocapillaris flow before hd-PDT. The areas of abnormal flow shrank progressively at 1 month after hd-PDT.

CONCLUSION:

On OCTA, choriocapillaris flow tended to recover at 1 month after hd-PDT. OCTA may be clinically useful for evaluating choriocapillaris and the therapeutic effects of hd-PDT for chronic CSC.

[Ophthalmic Surg Lasers Imaging Retina. 2017;48:302–310.]

Abstract

BACKGROUND AND OBJECTIVE:

To evaluate the choriocapillaris using optical coherence tomographic angiography (OCTA) after half-dose verteporfin photodynamic therapy (hd-PDT) for chronic central serous chorioretinopathy (CSC).

PATIENTS AND METHODS:

We studied six eyes (six patients) with chronic CSC treated by hd-PDT. OCTA was performed before, 1 week after, and 1 month after hd-PDT. The area of flow abnormality at the choriocapillaris level within the PDT spot after hd-PDT was compared with that before hd-PDT.

RESULTS:

Serous retinal detachment was diminished in all eyes, with three achieving complete resolution at 1 month. On OCTA, all eyes showed irregular choriocapillaris flow before hd-PDT. The areas of abnormal flow shrank progressively at 1 month after hd-PDT.

CONCLUSION:

On OCTA, choriocapillaris flow tended to recover at 1 month after hd-PDT. OCTA may be clinically useful for evaluating choriocapillaris and the therapeutic effects of hd-PDT for chronic CSC.

[Ophthalmic Surg Lasers Imaging Retina. 2017;48:302–310.]

Introduction

Chronic central serous chorioretinopathy (CSC) is characterized by widespread alterations in the retinal pigment epithelium (RPE) as a result of persistent or recurrent serous retinal detachment (SRD) involving the macula. In eyes with CSC, the RPE may decompensate, leading to gradual deterioration of vision. Treatment should be considered prior to the development of irreversible retinal changes. In recent years, photodynamic therapy (PDT) has been recognized as an effective treatment option for most patients with CSC.1–5 Specifically, PDT using a reduced dose of verteporfin or a shortened time of laser emission minimizes the potential adverse effects while still achieving good treatment efficacy for chronic CSC.3–5

The mechanisms underlying PDT-induced vascular effects in chronic CSC remain unclear. Chan et al.2 speculated that PDT induces vascular endothelial damage and thrombus formation, causing short-term choriocapillaris occlusion and long-term choroidal vascular remodeling. These changes result in caliber normalization of dilated, congested choroidal vessels and are considered to be the mechanism by which PDT ameliorates CSC.

Imaging the choriocapillaris in vivo is difficult because light is blocked by the choroidal and RPE melanocytes. Furthermore, the capillaries in the choriocapillaris are fenestrated, which makes high-resolution choriocapillaris imaging with fluorescein angiography (FA) and indocyanine green angiography (ICGA) highly challenging due to dye leakage.6 Optical coherence tomography angiography (OCTA) allows in vivo investigation of the choroidal vascular structure.7 There are some reports on the OCTA findings of CSC.8–11 However, to the best of our knowledge, there are no reports of OCTA findings after PDT for CSC. In this study, we used OCTA to evaluate changes in the choriocapillaris after half-dose verteporfin PDT (hd-PDT) in patients with chronic CSC by comparing with pre-PDT images.

Patients and Methods

This study adhered to the tenets of the Declaration of Helsinki and was approved by the Nihon University Hospital Institutional Review Board.

Consecutive patients with chronic CSC who underwent hd-PDT were enrolled between July and September 2015 at Nihon University Hospital. Informed consent was obtained from all subjects before treatment. CSC was diagnosed based on funduscopy, FA (TRC-50IX; Topcon, Tokyo, Japan), ICGA (TRC-50IX; Topcon, Tokyo, Japan), and swept-source OCT (SS-OCT) (Topcon, Tokyo, Japan) findings. Chronic CSC was diagnosed by the presence of SRD for at least 3 months. Patients were included in the analyses if the following two criteria were met: (1) presence of SRD involving the fovea on OCT; and (2) clear OCTA images available. Patients were excluded from analyses if: (1) there was a history of any prior treatment for CSC, or (2) other chorioretinal disorders, including age-related macular degeneration; polypoidal vasculopathy; pathologic myopia; or tilted disc syndrome, which may affect visual acuity, and/or foveal structures were present.

All patients underwent a complete examination that included best-corrected visual acuity (BCVA) measurement with Early Treatment Diabetic Retinopathy Study charts, intraocular pressure determination, anterior segment examination, and dilated fundus biomicroscopy. FA and ICGA were performed before PDT. SS-OCT and OCTA were performed before, and then at 1 week and 1 month after PDT. Subfoveal choroidal thickness, defined as the distance between the outer portion of the RPE and the inner surface of the sclera directly beneath the foveal center, was measured manually on fovea-centered horizontal and vertical OCT images using the built-in caliper tool. The average of horizontal and vertical scan measurements was used for analysis of subfoveal choroidal thickness.

OCTA and Image Analysis

The instrument used to obtain OCTA images was an RTVue XR Avanti (Optovue, Fremont, CA), employed for acquiring amplitude decorrelation angiography images. This instrument has a split-spectrum amplitude-decorrelation angiography software algorithm and is operated at 70,000 A-scans per second, using a light source centered on 840 nm with a bandwidth of 45 nm. Each OCTA volume contains 304 × 304 A-scans with two consecutive B-scans captured at each fixed position before proceeding to the next sampling location. Automatic segmentation of the choriocapillaris layer located between 30 μm and 60 μm below the RPE-Bruch's membrane complex was performed using the viewing software. The scan area was 6 mm × 6 mm and was centered on the fovea.

OCTA images were analyzed qualitatively to identify microstructural changes at the level of the choriocapillaris layer within the area of the PDT spot. The OCTA images acquired before and 1 week and 1 month after PDT were compared. If the PDT spot area was larger than the scan area of the OCTA image, only the 6 mm × 6 mm scan area was analyzed.

Photodynamic Therapy

The PDT was performed using half-dose verteporfin (Visudyne; Novartis AG, Bulach, Switzerland). The laser irradiation area was set to cover the hyperfluorescent area identified on images recorded during the middle to late phases of ICGA.

Statistical Analysis

Wilcoxon signed-rank test for paired data was used to compare pre- and post-PDT BCVA and subfoveal choroidal thickness. The level of statistical significance was set at a P value of less than .05.

Results

Six eyes of six patients (six men) were studied. The patients ranged in age from 37 years to 53 years, with a mean age of 41 years (Table). ICGA revealed choroidal hyperfluorescence in the middle to late phases in all eyes. B-scan SS-OCT demonstrated the presence of SRD before PDT in all eyes. The PDT spot sizes ranged from 3,050 μm to 7,000 μm (mean ± standard deviation: 5,291.7 μm ± 1,511.2 μm). The SRD decreased in all eyes after PDT, and three eyes showed complete resolution at 1 month. Mean subfoveal choroidal thickness decreased from 395.6 μm ± 114.7 μm at baseline to 357.1 μm ± 118.5 μm at 1 week and 339.1 μm ± 106.9 μm at 1 month after treatment (P = .03 and .03, respectively, compared with baseline). The mean logMAR BCVA was 0.25 ± 0.35 before PDT and 0.11 ± 0.23 at 1 month after PDT. The difference between pre-PDT and 1-month post-PDT BCVA did not reach statistical significance (P = .06).

The OCTA images showed flow void area within the PDT spot area before PDT in all eyes. Abnormal choroidal vessels depicted as high-intensity lesions on OCTA in the choriocapillaris layer were observed inside or adjacent to the flow void area in all the affected eyes. The sizes and shapes of the foci varied among patients (Figures 16).

�A;Multimodal imaging of the right eye of Case 1. (A) Color fundus photograph shows serous retinal detachment and pigment epithelial detachment (PED) at the macula. (B) Middle phase of indocyanine green angiography shows hyperfluorescence at the macula. The PED is located at the upper fovea (white arrowhead). (C–E) Fluorescein angiography in early to middle phase (C), middle phase (D), and late phase (E). The PED is located at the upper fovea (white arrowhead). (F–H) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (F), 1 week after PDT (G), and 1 month after PDT (H). The PED is located at the upper fovea (white arrowhead). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels and flow void lesion are observed at the choriocapillaris layer (F). These findings are diminished progressively at 1 week and 1 month after PDT (G, H). (I–K) OCT before PDT (I), 1 week after PDT (J), and 1 month after PDT (K).

Figure 1.

Multimodal imaging of the right eye of Case 1. (A) Color fundus photograph shows serous retinal detachment and pigment epithelial detachment (PED) at the macula. (B) Middle phase of indocyanine green angiography shows hyperfluorescence at the macula. The PED is located at the upper fovea (white arrowhead). (C–E) Fluorescein angiography in early to middle phase (C), middle phase (D), and late phase (E). The PED is located at the upper fovea (white arrowhead). (F–H) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (F), 1 week after PDT (G), and 1 month after PDT (H). The PED is located at the upper fovea (white arrowhead). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels and flow void lesion are observed at the choriocapillaris layer (F). These findings are diminished progressively at 1 week and 1 month after PDT (G, H). (I–K) OCT before PDT (I), 1 week after PDT (J), and 1 month after PDT (K).

�A;Multimodal imaging of the right eye of Case 2. (A) Color fundus photograph shows serous retinal detachment at the macula. (B) Middle phase of indocyanine green angiography shows hyperfluorescence. (C–E) Fluorescein angiography in early to middle phase (C), middle phase (D), and late phase (E). (F–H) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (F), 1 week after PDT (G), and 1 month after PDT (H). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels and flow void lesion are observed at the choriocapillaris layer (F). These findings decrease progressively at 1 week and 1 month after PDT (G, H). (I–K) OCT before PDT (I), 1 week after PDT (J), and 1 month after PDT (K).

Figure 2.

Multimodal imaging of the right eye of Case 2. (A) Color fundus photograph shows serous retinal detachment at the macula. (B) Middle phase of indocyanine green angiography shows hyperfluorescence. (C–E) Fluorescein angiography in early to middle phase (C), middle phase (D), and late phase (E). (F–H) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (F), 1 week after PDT (G), and 1 month after PDT (H). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels and flow void lesion are observed at the choriocapillaris layer (F). These findings decrease progressively at 1 week and 1 month after PDT (G, H). (I–K) OCT before PDT (I), 1 week after PDT (J), and 1 month after PDT (K).

�A;Multimodal imaging of the left eye of Case 3. (A) Color fundus photograph. (B) Middle phase of indocyanine green angiography. (C–E) Fluorescein angiography in early to middle phase (C), middle phase (D), and late phase (E). (F–H) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (F), 1 week after PDT (G), and 1 month after PDT (H). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels, and flow void lesion at the choriocapillaris layer are observed (F). Flow void lesion increases at 1 week after PDT comparing with before PDT. The lesion decreases at 1 month (G and H). Before and 1 week after PDT, OCTA depicts relatively large choroidal vessels in the macular area and inferior to the macula (white arrow heads). These findings are diminished progressively at 1 week and 1 month after PDT (G, H). (I–K) OCT before PDT (I), 1 week after PDT (J), and 1 month after PDT (K).

Figure 3.

Multimodal imaging of the left eye of Case 3. (A) Color fundus photograph. (B) Middle phase of indocyanine green angiography. (C–E) Fluorescein angiography in early to middle phase (C), middle phase (D), and late phase (E). (F–H) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (F), 1 week after PDT (G), and 1 month after PDT (H). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels, and flow void lesion at the choriocapillaris layer are observed (F). Flow void lesion increases at 1 week after PDT comparing with before PDT. The lesion decreases at 1 month (G and H). Before and 1 week after PDT, OCTA depicts relatively large choroidal vessels in the macular area and inferior to the macula (white arrow heads). These findings are diminished progressively at 1 week and 1 month after PDT (G, H). (I–K) OCT before PDT (I), 1 week after PDT (J), and 1 month after PDT (K).

�A;Multimodal imaging of the left eye of Case 4. (A) Color fundus photograph. (B) Middle phase of indocyanine green angiography. (C–E) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (C), 1 week after PDT (D), and 1 month after PDT (E). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels and flow void lesion at the choriocapillaris layer are observed (C). These findings are diminished progressively at 1 week and 1 month after PDT (D, E). (F–H) OCT before PDT (F), 1 week after PDT (G), and 1 month after PDT (H). In this case, fluorescein angiography was not conducted due to fluorescein allergy.

Figure 4.

Multimodal imaging of the left eye of Case 4. (A) Color fundus photograph. (B) Middle phase of indocyanine green angiography. (C–E) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (C), 1 week after PDT (D), and 1 month after PDT (E). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels and flow void lesion at the choriocapillaris layer are observed (C). These findings are diminished progressively at 1 week and 1 month after PDT (D, E). (F–H) OCT before PDT (F), 1 week after PDT (G), and 1 month after PDT (H). In this case, fluorescein angiography was not conducted due to fluorescein allergy.

�A;Multimodal imaging of the left eye of Case 5. (A) Color fundus photograph. (B) Middle phase of indocyanine green angiography. (C–E) Fluorescein angiography in early to middle phase (C), middle phase (D), and late phase (E). (F–H) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (F), 1 week after PDT (G), and 1 month after PDT (H). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels, and flow void lesion at the choriocapillaris layer are observed (F). Flow void lesion increases 1 week after PDT comparing with before PDT. The lesion is diminished at 1 month (G, H). (I–K) OCT before PDT (I), 1 week after PDT (J), and 1 month after PDT (K).

Figure 5.

Multimodal imaging of the left eye of Case 5. (A) Color fundus photograph. (B) Middle phase of indocyanine green angiography. (C–E) Fluorescein angiography in early to middle phase (C), middle phase (D), and late phase (E). (F–H) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (F), 1 week after PDT (G), and 1 month after PDT (H). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels, and flow void lesion at the choriocapillaris layer are observed (F). Flow void lesion increases 1 week after PDT comparing with before PDT. The lesion is diminished at 1 month (G, H). (I–K) OCT before PDT (I), 1 week after PDT (J), and 1 month after PDT (K).

�A;Multimodal imaging of the left eye of Case 6. (A) Color fundus photograph. (B) Middle phase of indocyanine green angiography. (C–E) Fluorescein angiography in the early to middle phase (C), middle phase (D), and late phase (E). (F–H) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (F), 1 week after PDT (G), and 1 month after PDT (H). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels and flow void lesion at the choriocapillaris layer are observed (F). These findings decrease progressively at 1 week and 1 month after PDT (G, H). (I–K) OCT before PDT (I), 1 week after PDT (J), and 1 month after PDT (K).

Figure 6.

Multimodal imaging of the left eye of Case 6. (A) Color fundus photograph. (B) Middle phase of indocyanine green angiography. (C–E) Fluorescein angiography in the early to middle phase (C), middle phase (D), and late phase (E). (F–H) Optical coherence tomography angiography (OCTA) before photodynamic therapy (PDT) (F), 1 week after PDT (G), and 1 month after PDT (H). The PDT spot area is encircled by yellow dots. Before PDT, focal high-intensity lesion indicating abnormal choroidal vessels and flow void lesion at the choriocapillaris layer are observed (F). These findings decrease progressively at 1 week and 1 month after PDT (G, H). (I–K) OCT before PDT (I), 1 week after PDT (J), and 1 month after PDT (K).

Follow-up OCTA after PDT showed no flow void corresponding to the area of PDT spot in any of the patients. The flow void was reduced gradually at 1 week or 1 month after PDT. In two of six eyes (Case 3 and Case 5), the flow void lesion was enlarged at 1 week after PDT comparing with before PDT. At 1 month, those lesions did not enlarge, and a tendency of reduction was observed. Areas of abnormal choroidal vessels observed as high-intensity lesions on OCTA before PDT were reduced gradually at 1 week or 1 month after PDT and were replaced by homogenous flow patterns.

In one patient (Patient 3), relatively large choroidal vessels in the macular area and inferior region were observed on OCTA image (Figure 3). These lesions were diminished progressively at 1 week and 1 month after PDT.

�A;Clinical Characteristics and Changes in Visual Acuity, Serous Retinal Detachment, and Choroidal Thickness After Photodynamic Therapy

Table:

Clinical Characteristics and Changes in Visual Acuity, Serous Retinal Detachment, and Choroidal Thickness After Photodynamic Therapy

Discussion

In the present study, OCTA depicted progressive changes in choriocapillaris flow at the PDT-treated area at 1 week and 1 month after treatment. All eyes showed irregular choriocapillaris flow patterns before PDT. After PDT, however, the areas of irregular choriocapillaris flow patterns decreased and were replaced by homogenous flow patterns, indicating a tendency of recovery.

Schmidt-Erfurth et al.12 reported that the choriocapillaris became occluded due to histopathological changes following PDT in human eyes. Histopathologically, closure of the choriocapillaris was observed 1 week after PDT, and thereafter recanalization was detected in multiple areas of the primarily occluded choriocapillaris after PDT. Furthermore, FA and ICGA revealed homogenous hypofluorescence corresponding to the area of PDT spot.12 These changes resulted in choriocapillaris occlusion. In the present study, OCTA did not demonstrate homogenous low-flow findings corresponding to the PDT spot area at the choriocapillaris level at 1 week or 1 month after PDT. Differences in PDT intensity may account for the discrepant findings. Schmidt-Erfurth et al.12 also observed that the intensity of histopathological changes depended on laser intensity. Because we treated our patients with half-dose verteporfin, this case series might have manifested fewer changes than most PDT recipients. On the other hand, they observed recanalization of the choroid as early as 1 week after PDT,12 similar to our OCTA findings in this study.

All our cases showed irregular choriocapillaris flow patterns before PDT. Teussink et al.8 reported that choriocapillary flow patterns in chronic CSC depicted on OCTA consisted of both reduced flow and hyperperfusion, in contrast to the fairly homogenous appearance of a healthy choriocapillary layer. In this study, abnormal choroidal vessels were seen adjacent to flow void areas in the choriocapillaris layer in all eyes before PDT, and these changes were reduced after PDT. Furthermore, subfoveal choroidal thickness decreased after PDT. The term “pachychoroid” has been proposed to describe increase in choroidal thickness.13 Eyes with pachychoroid change often manifest dilatation of large choroidal vessels compressing the Sattler's layer and choriocapillaris.14 In this study, the abnormal choroidal vessels and flow void area on OCTA in the choriocapillaris layer were diminished after PDT, consistent with the decrease in choroidal thickness. We suspect that circulation of the choriocapillaris was improved because compression by the large choroidal vessels was removed by PDT. There were two eyes (Case 3 and Case 5) in which flow void increased 1 week after PDT compared with before PDT, but decreased at 1 month. We speculated that recovery from PDT-induced damage to the choroidal vessels might be delayed in these two cases.

Limitations of this study include the small number of subjects and short follow-up period. The OCTA findings that can be assessed qualitatively have not been fully described or explored. Further study with larger sample size and longer follow-up are required.

In conclusion, OCTA demonstrated changes in choriocapillaris flow after PDT compared to pre-PDT images. Patterns of abnormal choroidal vessels at the choriocapillaris layer observed before PDT tended to recover to a homogeneous pattern at 1 month after PDT. OCTA may be clinically useful for evaluating choriocapillaris flow and the therapeutic effects of PDT for chronic CSC.

References

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  8. Teussink MM, Breukink MB, van Grinsven MJ, et al. OCT angiography compared to fluorescein and indocyanine green angiography in chronic central serous chorioretinopathy. Invest Ophthalmol Vis Sci. 2015;56(9):5229–5237. doi:10.1167/iovs.15-17140 [CrossRef]
  9. Shinojima A, Kawamura A, Mori R, Fujita K, Yuzawa M. Findings of optical coherence tomographic angiography at the choriocapillaris level in central serous chorioretinopathy. Ophthalmologica. 2016;236(2):108–113.
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Clinical Characteristics and Changes in Visual Acuity, Serous Retinal Detachment, and Choroidal Thickness After Photodynamic Therapy

Patient No. Gender Age (Years) Treated Eye Symptom Duration (Months) PDT Spot Size (μm) BCVA logMAR Serous Retinal Detachment Choroidal Thickness (μm)
Pre 1-Month Post 1-Week Post 1-Month Post Pre 1-Week Post 1-MonthPost
1 Male 53 Right 36 6,200 −0.08 −0.08 Decreased None 304.0 252.5 256.5
2 Male 43 Right 10 3,500 0.10 0 None None 291.0 250.0 241.5
3 Male 41 Left 36 3,050 0.06 0.02 Decreased Decreased 387.0 383.0 380.5
4 Male 37 Left 60 6,600 0.14 0.08 Decreased Decreased 524.5 437.5 386.0
5 Male 43 Left 24 7,000 1.00 0.62 Decreased Decreased 575.0 566.5 533.5
6 Male 41 Left 60 5,400 0.30 0.04 Decreased None 292.0 253.0 236.5
Authors

From Kansai Medical University, Hirakata City, Osaka, Japan (KF); and Nihon University, Chiyoda, Tokyo (AK, MY).

Dr. Yuzawa reports grants, personal fees, and non-financial support from Novartis and Santen; grants and personal fees from Alcon Japan; grants from Pfizer; personal fees from Senju, Astellas Pharma, Japan Focus Company, and Janssen Japan; and personal fees and non-financial support from Bayer and Baush & Lomb Japan outside the submitted work. Dr. Fujita reports personal fees from Novartis outside the submitted work. Dr. Kawamura reports no relevant financial disclosures.

Address correspondence to Kyoko Fujita, MD, PhD, Kansai Medical University, 2-5-1 Shinmachi, Hirakata City, Osaka 573-1010, Japan; email: fujitak@hirakata.kmu.ac.jp.

Received: September 24, 2016
Accepted: January 23, 2017

10.3928/23258160-20170329-04

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