C, Contrast-enhanced sonogram obtained 9 seconds after first arrival of contrast material to splenic artery clearly shows feeding pedicle (open arrows) entering into intrapancreatic accessory spleen (solid arrow) from splenic artery.
C,超声造影：注射造影剂9秒，造影剂到达脾动脉时，清楚显示来自脾动脉的供血蒂（空箭头示）进入胰腺内副脾（实箭头示）。
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D, Serial contrast-enhanced agent detection imaging (ADI software, Siemens Medical Solutions) sonograms, obtained 23 seconds (upper left), 37 seconds (upper right), 84 seconds (lower left), and 4 minutes (lower right) after contrast administration, show early heterogeneous enhancement (upper), late homogeneous enhancement (lower left), and delayed homogeneous and prolonged enhancement (lower right). Intrapancreatic accessory spleen (arrow) shows almost same echogenicity to main spleen (S) on all contrast-enhanced sonography phases. Both intrahepatic accessory spleen and main spleen show higher echogenicity than pancreas on all contrastenhanced sonography phases.
D,系列超声造影图(ADI software, Siemens Medical Solutions)：注射超声造影剂后23″、37″、84″和4分。显示动脉相早期不均匀增强（上图），动脉相晚期均匀增强（左下图），延迟期均匀增强且增强延长（下右图），胰腺内副脾（箭头示）与主脾在超声造影各相增强相同（S-脾）。在超声造影各相胰腺内副脾和主脾增强均高于胰腺。
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E and F, On unenhanced MR images, intrapancreatic accessory spleen (arrow) shows low signal intensity on T1-weighted image (E) and high signal intensity on fatsaturated T2-weighted image (F).
E、F, 未增强MR影像，胰腺内副脾（箭头示），T1为低信号(E)，T2为高信号(F)。
（缩略图，点击图片链接看原图）
G, Superparamagnetic iron oxide (SPIO)-enhanced T2*-weighted image obtained 10 minutes after SPIO administration shows signal drop similar in degree to that in lesion (arrow) and spleen (S).
G, 超顺磁性氧化铁(SPIO)增强，注射SPIO10分钟后T2加权影像显示病灶（箭头示）信号减弱程度与脾相似。S-脾。
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TABLE 1: Contrast-Enhanced Sonography Findings in Six Patients with Intrapancreatic Accessory Spleen
表1：6例胰腺内副脾的超声造影特征
（缩略图，点击图片链接看原图）
Discussion
With the widespread use of cross-sectional imaging techniques, such as sonography and CT, for evaluating abdominal diseases, it has become more common for radiologists to encounter nonsymptomatic benign solid lesions, including intrapancreatic accessory spleen in the pancreas. As several previous reports have indicated [2–4], however, it may still be difficult to differentiate intrapancreatic accessory spleen from pancreatic neoplasms such as islet cell tumor, solid pseudopapillary tumor, hypervascular metastasis, or even ductal adenocarcinoma and, accordingly, to make a correct diagnosis of intrapancreatic accessory spleen before surgery. In such circumstances, specific imaging of the functioning splenic tissue, such as 99mTc HDRBC scintigraphy, is necessary [10]. Although 99mTc scintigraphy allows selective splenic visualization with an excellent spleen-to-liver ratio, splenic visualization is still difficult in conditions in which minimal functioning splenic tissue is present, such as in cases of an accessory spleen [13]. Furthermore, a small accessory spleen of less than 1 cm in diameter may escape detection on scintigraphy because of low spatial resolution. Given that Levovist has a capability of being taken up by RES and sonography has high spatial and temporal resolution compared with scintigraphy, contrast-enhanced sonography using Levovist may be beneficial for the diagnosis of intrapancreatic accessory spleen.
讨论
断面影像技术已广泛使用，如超声、CT，用于评估腹部疾病，放射医师经常遇见无症状的良性肿块，其中包括胰腺内副脾。然而，从以往的报导看[2-4]，胰腺内副脾与胰腺内新生物还是很难鉴别的，如胰岛细胞瘤、实性假性乳头状瘤、高血管转移灶、甚至导管腺癌，因此只有术后才能做出准确的诊断。在这种情形下，功能性脾组织的特殊影像，如99mTc HDRBC核素扫描是必要的[10]。虽然99mTc核素扫描选择脾组织显像，且有良好的肝脾对比度，但在较小功能性脾组织时，脾的显像还是困难的，如副脾[13]。由于核素扫描的低空间分辨率，直径小于1cm的副脾可能漏诊。造影剂Levovist可以被RES所摄取，与核素扫描相比，超声检查有较高的空间和时间分辨率，使用Levovist进行超声造影有助于胰腺内副脾的诊断。
In this study, contrast-enhanced sonography showed characteristic enhancement features that allowed the diagnosis of intrapancreatic accessory spleen. During the four phases of contrast-enhanced sonography, intrapancreatic accessory spleens showed enhancement patterns identical to those of the spleen. In particular, prolonged enhancement of the intrapancreatic accessory spleen on the hepatosplenic parenchymal phase, similar to that of the spleen, was observed in all patients. Although the mechanism of this trapping of Levovist in the spleen and liver on the hepatosplenic parenchymal phase is not yet completely understood, phagocytosis of the microbubbles by the cells of the RES, including Kupffer cells, has been proposed as a most likely explanation [14]. This mechanism of enhancement of splenic tissue on the hepatosplenic phase of contrast-enhanced sonography is theoretically similar to those of 99mTc HDRBC scintigraphy [10] and SPIO-enhanced MRI [5]. Given that sonography offers superior spatial resolution to scintigraphy without the risk of radiation exposure, is more cost-effective, and requires less imaging acquisition time than MRI, sonography may be a valuable alternative to scintigraphy or MRI.
在此研究中，超声造影显示了特殊增强的特性，可以诊断胰腺内副脾。在超声造影四个时相中，胰腺内副脾增强模式与脾脏一致，特别是在肝脾实质相的延长增强，所有病例均是如此。虽然在内肝脾实质相的Levovist陷阱机制并不完全清晰，RES包括Kupffer细胞对微泡的吞噬是最有可能的解释[14]。超声造影肝脾相脾组织增强的机制理论上与99mTc HDRBC核素扫描[10]和SPIO增强MRI [5]类似。超声造影可提供比核素扫描跟高的空间分辨率且没有放射性，有更高的性价比；比MRI用时更少，因此超声造影是除核素或MRI检查以外的另一种有价值的方法。
In addition, we also observed inhomogeneous enhancement in all intrapancreatic accessory spleens on the vascular phase and in most intrapancreatic accessory spleens on the arterial phase. According to Catalano et al. [12], between the 12 seconds after contrast material bolus injection when splenic artery opacification usually begins and 50 seconds after contrast material bolus injection, there is inhomogeneous enhancement of the splenic parenchyma resembling the well-known arciform or zebra-striped pattern seen on dynamic CT or MRI [14]. The inhomogeneous enhancement of the spleen on the early phase (within 50–70 seconds) is known to be related to the different flow rates through the red and white pulp [15]. Therefore, inhomogeneous enhancement on the early phase could provide another clue to the diagnosis of intrapancreatic accessory spleen.
此外，我们同样观察到所有胰腺内副脾在血管相为不均匀增强，在动脉相大部分为不均匀增强。根据Catalano等[12]，在造影剂注射后12″脾动脉开始显影到50″脾实质不均匀增强与动态CT或MRI的弓形或斑马条纹形式相似[14]。在造影早期相（57-70″）脾不均匀增强是与脾脏实质内的红髓和白髓血流量不同相关[15]。因此，造影早期相的不均匀增强可提供另一个诊断胰腺内副脾的线索。
Multiphasic CT or dynamic MRI can provide hemodynamic data of focal pancreatic lesions; this would allow most intrapancreatic accessory spleens to be diagnosed by showing a similar enhancement pattern to that of the spleen on all phases. However, contrast-enhanced sonography may provide many advantages over CT. First, it allows real-time scanning with a greater time window (more than four phases) than that of CT without any risk related to radiation exposure and the use of iodinated contrast material. Furthermore, although we used a high mechanical index, contrast-enhanced sonography technique, and Levovist, a combineduse of second-generation sonography contrast agents and the low-mechanical-index technology allows real-time scanning and therefore provides more accurate hemodynamic information [12]. Therefore, in the clinical scenario in which a hypervascular lesion in the pancreatic tail is seen on singlephase CT, contrast-enhanced sonography can be used instead of additional acquisition of multiphasic CT images.
多相CT或动态MRI可提供局部病灶的血液动力学数据；通过显示与脾相似的各相增强模式可诊断大部分胰腺内副脾。然而，超声造影较CT有很多的优势。第一：可实时扫查，较CT具有较大时间窗（超过4相），没有任何放射线，没有使用碘化造影剂，Levovist为复合型第二代超声造影剂，在低机械指数技术下可实时扫查，因此可提供更准确的血液动力学信息[12]。因此，在临床上发现胰腺尾部单相CT高血管病灶，超声造影可用于代替进一步的多相CT检查。
In addition, all intrapancreatic accessory spleens showed hyperechogenicity to the pancreas and isoechogenicity to the spleen in all four enhanced sonography phases. Although some other hypervascular tumors, such as islet cell tumor, may show a similar enhancement pattern, they usually become low- or isoechoic to the pancreas on the portal or delayed phase [16, 17]. Therefore, the prolonged enhancement relative to the pancreas on contrast-enhanced sonography provides another clue to the correct diagnosis. Furthermore, islet cell tumor can show a ringlike enhancement on the arterial phase that differs from the homogeneous enhancement pattern of intrapancreatic accessory spleen [16].
此外，在超声造影的四相中，所有胰腺内副脾显示为比胰腺回声高，与脾脏为等回声。虽然其它一些高血管肿瘤，如胰岛细胞瘤为相似的增强模式，在静脉相和延迟相，与胰腺相比通常变为低或等回声[16,17]。因此副脾相当胰腺超声造影是增强延长，是正确诊断的另一个线索。此外胰岛细胞瘤在动脉相时可显示为环样增强，与胰腺内副脾的均匀增强模式不同[16]。
Our study has some limitations. First, the inherent limitation of pancreatic sonography, which is a poor sonic window for the pancreas, also clearly persists on contrast-enhanced studies. However, because intrapancreatic accessory spleen is exclusively located in the pancreatic tail, the sonic window for the pancreatic tail could be achieved through the spleen with little difficulty. Indeed, all cases in our study could be clearly depicted on both baseline and contrast-enhanced sonography. Second, because we used a high-mechanical-index harmonic technique and Levovist in this study, intermittent scanning was necessary to avoid excessive bubble destruction. Such intermittent scanning requires much operator skill and may therefore be responsible for making contrast-enhanced sonography difficult to perform. Although continuous real-time scanning using low-mechanical-index technology and more stable second-generation sonography contrast agents could provide better information regarding the hemodynamics of intrapancreatic accessory spleen, we believe that the intermittent scanning technique using Levovist, which has an RES-specific uptake, remains a valuable option for the diagnosis of intrapancreatic accessory spleen.
我们的研究有一定局限性，首选，胰腺超声检查本身的超声窗不是很理想，因此持续的超声造影研究也受到限制。然而，胰腺内副脾只位于胰腺尾部，通过胰腺尾部的超声窗并不是很困难。的确我们所有研究的病例，在基波超声和超声造影时都可有清晰显示。其次，因为我们使用的是高机械指数和Levovist超声造影剂，使用间歇扫查以避免微泡的过渡破坏。间断扫查需要操作者技术更熟练，因此超声造影有一定难度。虽然使用低机械指数连续扫查技术和更稳定的第二代造影剂可提供更好的胰腺内副脾的信息，但我们认为使用Levovist和间歇扫描技术，利用RES的特殊摄取，对胰腺内副脾的诊断仍然是有价值的。
In conclusion, Levovist-enhanced sonography revealed the characteristic enhancement features of intrapancreatic accessory spleen and allowed the specific diagnosis of intrapancreatic accessory spleen to be made. The characteristic features of intrapancreatic accessory spleen on contrast-enhanced sonography were an inhomogeneous enhancement on the early vascular phase, similar enhancement to the spleen during the postvascular phase, and prolonged enhancement on the hepatosplenic parenchymal phase.
结论，Levovist超声造影，可显示胰腺内副脾的增强特征，可对胰腺内副脾做出诊断。胰腺内副脾超声造影特征是：早期血管相为不均匀增强，血管后相与脾增强类似，肝脾实质相增强延长。
