Introduction

An appendiceal mucocele is a descriptive term for an obstruction of the appendiceal lumen and the accumulation of mucinous material. The accurate preoperative diagnosis of an appendiceal mucocele is very important, because rupture causes pseudomyxoma peritonei and is associated with a poor prognosis [1]. Ultrasonography (US) is useful for the preoperative diagnosis of an appendiceal mucocele [2, 3], and case reports with echogenic layers or a layered appearance of the internal contents have been described previously [2, 4–7]. Timor-Tritsch et al. [8] and Degani et al. [9] described US findings of this disease with a layered structure resembling the onion skin in the mass. In a case series, Caspi et al. [10] subsequently reported that a mass with findings on US of the ‘onion skin sign’ in the right lower quadrant of the abdomen in the presence of a normal ovary was strongly suggestive of a diagnosis of an appendiceal mucocele. Since then, various cases of appendiceal mucocele with the onion skin sign have been reported [11–14].

However, to the best of our knowledge, no investigation has evaluated the differential diagnoses to clarify whether the onion skin sign is a specific US marker of an appendiceal mucocele. Diseases of the small bowel [15, 16], ileocecal valve [17], cecum [18], appendix [3, 12, 17, 19, 20], mesentery [15], adnexa uteri [7, 8, 10, 12, 19, 21–30], or pelvic cavity outside the digestive, urinary or genital organs [15, 31] have been reported as differential diagnoses for appendiceal mucocele. The purpose of this study was to evaluate lesions in these locations to retrospectively determine whether the onion skin sign in the lower abdomen is specific for the diagnosis of an appendiceal mucocele.

Materials and methods

We conducted this study at a regional general hospital. Transabdominal US is performed over 11,000 times each year in our laboratory by one of the 12 experienced sonographers. Each organ, including those of the digestive tract, was scanned systematically. One of the two board-certified fellows of the Japan Society of Ultrasonics in Medicine (T.K., F.K.) performed US examinations to double check whenever the sonographers detected interesting and unusual findings, or when there was some difficulty interpreting the images and thus were requested to do so. After each examination, one of the fellows interpreted the acquired images and the findings reported by the sonographer. The findings were then revised to make them as accurate as possible when deemed necessary, and finally the US diagnoses were made either with or without comments.

Our study included 229 patients in whom transabdominal US detected lesions in the lower or middle-to-lower abdomen between January 2004 and March 2010, who underwent surgery and had definitive pathological diagnoses in the small bowel, ileocecal valve, cecum, appendix, mesentery, adnexa uteri or pelvic cavity outside the major organs. Patients with metastatic tumors in these locations were excluded from this study. The 229 patients comprised 83 males and 146 females, with a mean age of 44.2 years (range 6–92 years). Two of these patients showed a lesion in both ovaries.

We defined the onion skin sign as internal echogenic layers arranged like the circle of an onion or in concentric layers [10]. The layered structure of the wall of masses or digestive tract was not included in the definition. During the study period, we adopted the sign in daily practice based on the definition [14]. In this study, one of the fellows (T.K.) reviewed the US images and findings written on the report of transabdominal US in the 229 patients. There were no patients in whom the images had the onion skin sign and the report did not describe the presence of either an onion skin sign or a layered structure. In lesions with ‘a layered structure’ noted merely in the reports, the other fellow (F.K.) also reviewed the US images. We judged that the lesion had the onion skin sign, if the two fellows agreed that the layered structure was consistent with the sign. The fellows were not blinded to the pathological diagnoses. The sensitivity, specificity, and accuracy of the sign for the diagnosis of an appendiceal mucocele were calculated.

Each examination was performed using one of the seven US systems: the SSD-5000 or SSD-5500 (Aloka, Tokyo, Japan) with 5-MHz convex and 13-MHz linear transducers, the HDI 5000 (Advanced Technology Laboratories, Bothell, WA) with 2- to 5-MHz convex and 4- to 7-MHz linear transducers, the EUB-7500 (Hitachi Medical Corporation, Tokyo, Japan) with 3-MHz convex and 10-MHZ linear transducers, the SSA-700A or SSA-790A (Toshiba Medical Systems, Tochigi, Japan) with 3.5-MHz convex and 7.5-MHz linear transducers, or the LOGIQ 500 (General Electronic Medical Systems, Milwaukee, WI) with 3.8-MHz convex and 5- to 10-MHz linear transducers.

This study was performed under the approval of the ethics committee at our institution.

Results

The locations and pathological diagnoses of the lesions are shown in Table 1. The 231 lesions were located in the small bowel (n = 2, 0.9 %), ileocecal valve and/or cecum (n = 12, 5.2 %), appendix (n = 132, 57.1 %), mesentery (n = 6, 2.6 %), adnexa uteri (n = 76, 32.9 %), and pelvic cavity (n = 3, 1.3 %). Eight (6.1 %) of the 132 lesions in the appendix were diagnosed as an appendiceal mucocele, including pathological diagnoses of mucinous cystadenoma (n = 4) and mucinous cystadenocarcinoma (n = 4).

Table 1 Locations and pathological diagnoses of 231 lesions in 229 patients
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Five (2.2 %) of the 231 lesions showed the US onion skin sign and all were diagnosed as an appendiceal mucocele, including diagnoses of mucinous cystadenoma (n = 3) and mucinous cystadenocarcinoma (n = 2) (Figs. 1, 2). The sensitivity, specificity, and accuracy of the sign for the diagnosis of an appendiceal mucocele were 63, 100, and 99 %, respectively.

Fig. 1
figure 1

A 58-year-old female with mucinous cystadenoma. Ultrasonography showed a sausage-shaped mass in the right lower abdomen, and the echogenic layered structure called the onion skin sign was shown in it (arrows). The continuity between the mass and the cecum was identified

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Fig. 2
figure 2

A 61-year-old male with mucinous cystadenocarcinoma. Ultrasonography showed a large cystic mass with the onion skin sign in the pelvic cavity (arrows)

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Discussion

The onion skin sign in the lower abdomen has been identified in the presence of appendiceal mucocele [10–14]. The process involved in the formation of this layered structure has yet to be elucidated. Degani et al. [9] reported that a macroscopic view of the appendix showed a heavy mucoid substance arranged in layers, and speculated that repeated sedimentation of the mucinous substance might result in the layered appearance. Caspi et al. [10] suggested that the gradual absorption of water and solutes might result in the gelation of the mucin after secretion into the appendiceal cavity, and that the layering phenomenon might result from fluctuations in the secretion of mucin into the cavity or in the degree of excretion blockage from the cavity.

An appendiceal mucocele was found in eight (6.1 %) of 132 appendiceal disease lesions detected with US, which was higher than the rate of 0.2–1.0 % of appendectomies reported in previous studies [19, 32–37]. At our institution, only computed tomography (CT) is performed in many patients for the diagnosis of acute appendicitis, which accounts for most cases of appendiceal diseases, while both CT and US are usually used for the precise evaluation of rare appendiceal diseases, such as an appendiceal mucocele.

In females, an appendiceal mucocele can sometimes be confused with a lesion of the adnexa because of their similarities in terms of both the clinical courses and US findings [8, 19, 21–29]. In our study, none of the 73 lesions in the ovary, including 16 lesions presenting as mucinous tumors, showed the onion skin sign on transabdominal US. Interestingly, the formation of an internal layered structure appears to be related to the mucinous substance in appendiceal mucinous tumors, but no such structure has been reported in association with ovarian mucinous tumors [38–46]. The presence of the US onion skin sign in the lower abdomen strongly suggests an appendiceal mucocele even when normal ovaries are not detected with transabdominal US.

Several limitations must be considered when interpreting the results of this study. First, the investigation was conducted retrospectively. An appendiceal mucocele is a rare entity, and conducting such studies prospectively is not easy. Second, we did not select all lesions detected in the lower abdomen on preoperative transabdominal US; we selected only lesions in the locations of previously reported differential diagnoses of appendiceal mucoceles. Third, a large number of patients who underwent surgery for an adnexal disease, the main differential diagnosis for appendiceal mucocele, did not undergo transabdominal US preoperatively in our laboratory. Most female patients who saw a gynecologist initially, and in whom the gynecologist detected an adnexal lesion on transvaginal US, did not have a chance to undergo transabdominal US in our laboratory for further evaluation, whereas patients who initially saw other specialists, such as emergency physicians, internists, surgeons or urologists, underwent transabdominal US for the evaluation of the abdominal or pelvic regions. Finally, the fellows who reviewed the US images were not blinded to the final diagnoses. Moreover, we reviewed static images. In our experience, real-time dynamic images were more impressive than static images for the presentation of the onion skin sign. Therefore, we cannot deny that the sign might have been missed by reviewing the static images in some cases.

Despite these limitations, it is significant that the onion skin sign was seen only in five lesions, all of which were diagnosed as appendiceal mucocele, among the 229 patients in whom transabdominal US detected a lesion in the lower abdomen, and who had definitive pathological diagnoses in the locations of previously reported differential diagnoses of appendiceal mucoceles.

Moreover, this US sign is unusual and very impressive; therefore, we think that recognition of the sign can facilitate a ‘snap diagnosis’.

Conclusions

The presence of the onion skin sign in the lower abdomen appears to be specific for the diagnosis of an appendiceal mucocele. In cases where the onion skin sign is obviously present in the lower abdomen on US, an appendiceal mucocele should be considered as the leading diagnosis.