Journal of X-Ray Science and Technology 22 (2014) 493–501 DOI 10.3233/XST-140440 IOS Press
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Combination of CT imaging and endoscopy in diagnosis of appendicovesical fistula caused by appendiceal adenocarcinoma Wenying Wanga , Li Wangb , Jianfeng Xub , Shufang Shic , Ye Tiana,∗ and Yuanyuan Zhangd,∗ a Department
of Urology, Beijing Friendship Hospital, Capital Medical University, Beijing, China for Cancer Genomics, Wake Forest University School of Medicine, Winston-Salem, NC, USA c Department of Pathology, Beijing Friendship Hospital, Capital Medical University, Beijing, China d Institute for Regenerative Medicine, Wake Forest University, Winston-Salem, NC, USA b Center
Received 3 October 2013 Revised 21 January 2014 Accepted 16 March 2014 Abstract. The appendiceal diseases, particularly appendicitis, are the most common disorders in the digestive system localized at the right lower quadrant area. However, appendiceal carcinoma with vesico-appendiceal fistula is a rare clinical phenomenon. Lacking specific symptoms, appendiceal carcinomas with fistula formations are often misdiagnosed as acute appendicitis cases. The purpose of this study is to increase awareness of appendiceal neoplasms and appendicovesical fistulas. We reported our experiences in three complex cases related to digestive and urological systems, and reviewed the literature on diagnosis with various X-ray imaging techniques for this lesion. In this report, the first case failed to be diagnosed. The other two patients with appendicovesical fistulas secondary to appendiceal adenocarcinomas were successfully detected with computed tomography (CT) and cystoscopy. The patients recovered after right hemicolectomies and en bloc partial cystectomies and survived without tumor metastasis up to 7-year follow-up. In conclusion, a combined use of CT imaging and endoscopy techniques provides an accurate diagnostic alternative for appendicovesical fistula secondary to appendiceal adenocarcinoma. Keywords: Appendix adenocarcinoma, bladder, fistula
1. Introduction Appendix neoplasms are very rare entities in the digestive system and are found in only 0.9–1.4% of appendectomy specimens. The estimated age-adjusted incidence is only 12 cases per 100 million people per year [1]. Appendicovesical fistulas caused by the tumor often lack specific symptoms. By occasionally appearing as a right renal mass or chronic renal failure, they cause misdiagnosis pre-operatively [2]. In some cases, it presents urinary tract infections, dysuria, pyuria, frequencies, micturition pains, and gross hematurias, which is not encountered in most surgeons’ careers [3]. Clinicians are vulnerable to ∗
Corresponding authors: Ye Tian, Department of Urology, Beijing Friendship Hospital, Capital Medical University, 95 YongAn Road, Xicheng District, Beijing 100050, China. E-mail: [email protected]. Yuanyuan Zhang, Institute for Regenerative Medicine, Wake Forest University, Winston-Salem, NC 27157, USA. E-mail: [email protected]. c 2014 – IOS Press and the authors. All rights reserved 0895-3996/14/$27.50
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misdiagnosing other diseases with similar symptoms as appendicitis [4]. Histologically, two types of tumors exist in appendix tissues, i.e. carcinoid tumors that account for 32–85% of all appendiceal tumors and adenocarcinomas that account for only 4–6% of them. The adenocarcinomas are divided into three subtypes: mucinous, non-mucinous (colonic type), and signet-ring cell adenocarcinoma. The mucinous adenocarcinoma is predominant, composing 23%∼55% of all adenocarcinomas in the appendix [5]. Appendiceal adenocarcinoma, especially mucinous adenocarcinoma, is notorious for its spread to adjacent organs and forms the fistula to colon [6], uterus [7], and skin [8]. It is uncommon that an appendiceal adenocarcinoma penetrates into the bladder. To date, a total of fifteen cases of appendicovesical fistulas caused by adenocarcinoma have been reported since the first was described by Richie in 1977 [3]. Twelve cases resulted from mucinous adenocarcinoma type. The mucinous adenocarcinoma can easily perforate to the bladder via the fistulas because the appendix has a thin subserosa, muscles and serosa layer [9]. Although pre-operative diagnosis of appendiceal adenocarcinomas remains challenging, modern Xray imaging, endoscopic and pathological techniques make it possible to improve the diagnostic accuracy of appendiceal neoplasms. CT or magnetic resonance imaging (MRI) techniques are especially important for diagnosing the tumor and fistula within the appendix when combined with endoscopic examinations. Surgery alone, such as a right hemicolectomy, achieves a good 5-year survival in treatment of appendiceal adenocarcinomas [4]. Mucinous adenocarcinomas provide better long-term survival rates than nonmucinous tumors [4]. Therefore, an early and accurate pre-operative identification is critical for the clinical management of patients with appendiceal adenocarcinoma and fistulas. In this report, we presented three cases with appendiceal adenocarcinomas invading the bladder tissue, leading to the formation of fistulas. Preoperative diagnosis was made by the combined use of CT imaging and cystoscopy. We have discussed the value and features of different X-ray imaging techniques including barium enema, plain film, intravenous urogram (IVU) film, MRI, colonoscopy, CT, and cystoscopy used to diagnose this uncommon lesions related to two organs; the urinary tract and digestive system. 2. Patients and methods Three patients (two females and one male) diagnosed with appendicovesical fistula were studied at our institute between July 2005 to September 2010 (Table 1). The mean age was 61 (45, 61, 78) years. The first patient presented with a one-year history of intermittent hematuria; the second patient was admitted with pyuria, urinary frequency and complaints of occasional mucus in the urine; the third patient was seen with a complaint of having had mucus in the urine for four months. All the patients did not have gastrointestinal tract symptoms such as pain, intestinal obstruction or melena. Past medical and surgical histories were all negative. Physical examination revealed a palpable mass 7cm in diameter in the right lower quadrant without tenderness in the first patient, and no abnormal findings were found in the rest two. Laboratory biochemical examinations were taken, including blood count, hemoglobin, white blood cell count and electrolytes, urine and fecal analysis, tumor markers including carcinoembryonic antigen (CEA) and alphafetoprotein (AFP). For the diagnosis of the appendiceal tumors, X-ray examinations were made, including plain abdominal, IVU film, barium enema and enhanced CT scanning. A 64-row multidetector CT (GE light Speed VCT scanner, GE Healthcare, Wis, USA) with working parameters of 120 kV/350 mA, 5-mm slice thickness, and 0.984:1 pitch was used to scan the kidneys, ureters and bladder of all the patients before the procedures. Non-ionic intravenous contrast agent (Iohexol injection, 75 ml:22.5 g, Yangtze River
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Table 1 Clinical characteristics of appendicovesical fistula caused by appendiceal adenocarcinom and appendicitis Variables Sex/Age (y) Symptoms Urine analysis
Case 1 M/61 Intermittent hematuria pyuria
Case 2 F/45 Pyuria, mucus in the urine Lots of WBC/HP, mucus in the urine
Case 3 F/78 Mucus in the urine More than 100 WBC/HP
Urine culture Serum CEA and AFP Physical examinations
− − −
Escherichia coli and fungi CEA (−) A palpable mass in the right lower quadrant
Escherichia coli CEA (−), AFP (−) −
Plain film and IVU Barium enema
− Appendix was not visible
− Extrinsic compression at the ileocecum
− −
CT scanning
A 3 cm × 4 cm solid mass on the right thicken bladder wall at the lesion side, an air bubble in the bladder lumen
A 7 cm solid mass with focal calcification on the bladder wall
A thickened right bladder wall, a tubular structure connected with the bladder, a fistula was seen
Cytology Cystoscopy
− A broad-based non papillary tumor, a fistula was seen
− Solid broad-based mass with a lot of mucus on the surface
− A fistula and a large amount of mucus can be seen
Biopsy
−
−
Pathology on surgical tissue samples
Colonic type adenocarcinoma
Mucinous adenocarcinoma
Adenocarcinoma suspicious for appendix origin Mucinous cystadenocarcinoma
Treatment
Appendectomy and partial cystectomy
Right hemicolectomy and partial cystectomy
Right hemicolectomy and partial cystectomy
Follow-up (yrs) 7 5 3 Recurrence, metastasis No No No Abbreviation note: WBC: white blood cell; HP: high powerfield; IVP: intravenous pyelography; CEA: carcinoembryonic antigen; AFP: alphafetoprotein; − negative.
Pharmaceutical Group, China) was used. In order to confirm the origin of the tumor, cystoscopy (rigid cystoscopy, Telescope “70” degree, Karl Storz, Germany,) and tumor biopsies were performed in all the patients. The pathological examination of the biopsy specimens were obtained in and around the fistula. The biopsied and resected specimens were fixed (10% neutral-buffed formalin for at least 24 h) and embedded in paraffin. The histological diagnosis was made using conventional hematoxylin and eosin staining and Immunohistochemistry.
3. Results Urinary analysis revealed 10–35 red blood cells and more than 100 white blood cells per high power field in all the patients. The small amount of white, loose, floating mucus were seen in urine samples in two patients (Table 1). Urine culture revealed Escherichia coli in both patients and fungi in one. Voided urinary cytology was negative. The fecal occult blood tests were negative. The blood electrolytes, alkaline phosphatase, liver enzymes, hemoglobin, and white blood cell count were normal. Tumor markers including CEA and AFP were on normal levels. Barium enema showed extrinsic compression at the ileocecum and the appendix was invisible (Fig. 1).
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Fig. 1. Barium enema images of appendiceal adenocarcinoma. (A) Extrinsic compression at the ileocecum and the appendix is not visible (arrow) in Case 1; (B) in Case 2. (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/ XST-140440)
Fig. 2. CT scanning of adenocarcinoma of the appendix in three cases. (A) The bladder wall (thick arrow) and an air bubble within the bladder lumen (thin arrow, cross-sectional view). (B) A solid mass with calcification connecting with the ascending colon and extending to the bladder (thick arrow, longitudinal view). (C) A tumor mass in the right wall of the bladder (thick arrow) with a fistula leading to the bladder (thin arrow). (Colours are visible in the online version of the article; http://dx.doi.org/ 10.3233/XST-140440)
CT scans revealed a 3 cm × 4 cm solid mass on the right side (11 o’clock position) of the bladder wall with an air bubble within the bladder lumen in the first case; a 7 cm round solid mass with focal calcifications on the right side of the bladder wall in the second case; a thickened tissue with a channel structure connected with the right side of the bladder lumen in the third case (Fig. 2). Cystoscopy revealed that the tumors were located on the right side of the bladder attached with mucus, and the fistula opening to the bladder was observed in two patients (Fig. 3). The values for appendiceal tumors on noncontrast and contrast CT images were 30∼42 HU and 45∼70 HU respectively. The tissue biopsied by transurethral resection histologically revealed atypical dysplasia or adenocarcinoma suspicious but origins couldn’t be confirmed in each case. Surgical exploration revealed the tumors originated from the appendix and had grown into the bladder causing the fistula. The histologic
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Fig. 3. Cystoscopy examination of adenocarcinoma of the appendix. The opening of the fistula (arrow) was noted at 1 and 11 o’clock positions on the upper bladder wall (A). Mucus was seen from the fistula opening (B). (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/XST-140440)
Fig. 4. Histological examination of adenocarcinoma of the appendix. (A) Well differentiated colonic type adenocarcinoma in case 1. (B) Mucinous adenocarcinoma in case 2. (C) Well differentiated mucinous cystadenocarcinoma in case 3. (HE 20 × 10). (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/XST-140440)
Fig. 5. Immunohistological examination of adenocarcinoma of the appendix. (A) CK20 (+) in case 3. (B) CDx-2 (+) in case 3. (HE 20 × 10). (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/XST-140440)
diagnosis was that of a well-differentiated colonic type adenocarcinoma, mucinous adenocarcinoma and a well-differentiated mucinous cystadenocarcinoma respectively (Fig. 4). Immunohistological examination showed CK20 (+) and CDx-2 (+) in the third case (Fig. 5). The tumor tissues were removed by appendectomy and en bloc partial cystectomy in one case, and with a right hemicolectomy and en bloc partial cystectomy in two cases (Fig. 6). Neither postoperative radiotherapy nor chemotherapy was administered. All the patients survive after surgery with no tumor
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W. Wang et al. / Appendicovesical fistula caused by appendiceal adenocarcinoma Table 2 Clinical characteristics of appendicovesical fistula caused by appendiceal adenocarcinom and appendicitis
Variables Cases reported Sex affected Age Symptoms Tumor markers Plain film and IVP Fistula on MRI CT scanning
Appendiceal adenocarcinoma Extremely rare, 18 cases(including ours) Nearly the same (M:F = 1:1) 50–60 years old Urinary symptoms Seldom positive for CEA or AFP Usually unhelpful Less than 20% positive Soft-tissue mass in the right lower quadrant can be seen, loss of normal appendiceal tubular shape
Appendicitis Rare, more than 100 cases [20] M predominance (M:F = 3:1) [10] 10–40 years old Urinary symptoms, pneumaturia may occur − Calcification occasionally 40% positive An enlarged appendix that maintained its tubular structure, infiltration of periappendiceal fat by fluid or soft tissue strands
Barium enema Colonoscopy Biopsy
Appendix was not filled with contrast medium One case positive More than 30% positive, origin of tumor not identified sometimes
Flow of contrast medium was seen in a few cases − −
Cystoscopy Less than 40% positive 40%–60% positive [11] Treatment Right hemicolectomy and partial cystectomy Appendectomy and partial cystectomy Pathology Adenocarcinoma, mucinous (80% cases) Appendicitis Abbreviation note: IVU: intravenous urogram; CT: computed tomography; MRI: magnetic resonance imaging; − negative.
Fig. 6. he resected tissue specimens of appendiceal tumors connected to the bladder wall (black arrow). (A) Case 1. (B) Case 2 and (C) Case 3. Notes: 1 Appendiceal carcinoma. 2 Ileum. 3 Ascending colon. (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/XST-140440)
metastasis during the follow-up (3 to 7 years). Clinical characteristics, imaging examinations, perioperative variables and outcomes for three patients were listed at Table 1. 4. Discussion Appendiceal adenocarcinomas with appendicovesical fistulas [3] are rare and easily misdiagnosed as appendicitis case (Table 2). To date, only eighteen cases have been reported including ours [3,9–21]. Appendiceal adenocarcinoma most often presents in patients during their 50 s–60 s, significantly older than patients with appendicitis. The mean age of our patients was 61 years. Males are more frequently affected with appendiceal adenocarcinoma than females (3:1) [9], however, we found that, when the tumors infiltrated the bladder, males and females were equally affected. Differential diagnosis of appendiceal adenocarcinoma is highly important among the lesions with the pain and lower quadrant masses (Table 3). About 40% of patients with appendiceal adenocarcinoma have presented with acute appendicitis or incidental findings in resected specimens [10–13]. Pre-operative diagnosis is more difficult for patients with appendicovesical fistulas secondary to appendiceal adenocarcinoma, as the patients usually have no specific clinical manifestations. The patients usually do not have
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Table 3 Different diagnosis of right lower quadrant masses with clinical and imaging examination Variables Age predominance Gender affected most Main symptom Urine analysis Tumor markers Pregnancy test Ultrasound Plain film and IVU Barium enema CT MRI Colonoscopy Cystoscopy Biopsy Diagnostic laparoscopy
Ovarian cyst 30 years old F Abdominal pain − − − Hypoechoic − − useful Most useful − − Diagnostic Helpful
Ectopic pregnancy 20–30 years old F Abdominal pain − − + Hypoechoic − − Useful Useful − − N/A Helpful
Bladder carcinoma 65 years or older M Hematuria Hematuria + − Hypoechoic Helpful occasionally − Most useful Useful − + Diagnostic Not applicable
Bladder stone 65 years or older M Urinary tract infection Urinary tract infection − − Hyperechoic + − Useful Helpful − + N/A Not applicable
Glandular cystitis 30–40 years old M Hematuria Hematuria − − Hypoechoic Not helpful − Useful Useful − + Diagnostic Not applicable
Colonic carcinoma 60 years or older M Blood fecal − + − Hypoechoic − + Most useful Useful + − Diagnostic Helpful
Abbreviation note: CT: computed tomography; MRI: magnetic resonance imaging; IVU: intravenous urogram; F: female; M: male; − negative; + positive; N/A: not applicable.
intestinal symptoms. One explanation for this may be that in early stages, tumors of the appendix can invade the bladder before interfering with the intestinal passage. None of the three patients had typical symptoms of pneumaturia suggestive of appendicovesical fistula. As this disease was so rare, we had misdiagnosed the first case. Given the experience from the case, we made acute pre-surgical diagnoses in the remaining two patients. CT imaging examinations are often used in diagnosing the tumor in solid organs [22–24]. Despite ambiguous image structures in the hollow viscera, CT scans still provide valuable diagnostic information for appendiceal adenocarcinoma [25]. The presence of a solid or cystic mass in the area of the appendix with enhancing nodularity on CT usually suggests the possibility of malignancy. Wall thickness is also regarded as a differential point between neoplastic and non-neoplastic diseases. However, the presence of a relative thin wall can’t exclude malignancy. For all the three cases, CT’s showed a soft-tissue mass compressing the right bladder wall or focal bladder wall thickening. In addition, we observed the presence of air within the bladder, which suggested the existence of one fistula in one of our cases. Sometimes CTs were specific, but not sensitive for diagnosing appendiceal tumors; the appendix maintained its tubular structure without peri-appendiceal infiltration in a third of our cases. In addition, 64% of mucinous adenocarcinoma presented with appendiceal ruptures and peritoneal spreads [26,27]. However, none of the cases presented with pseudomyxoma peritonei on CT. Other X-ray imaging techniques are also helpful for diagnosing this type of tumor and fistulas. One case of a fistula was identified by barium enema [6]. MRI revealed the fistulous tract in three cases [9–11]. Cystoscopy can reveal fistula openings, and its diagnosis accuracy is about 40% [11]. In two cases of ours, we were able to clearly see the fistula on cystoscopy. The presence of mucus from the fistula on cystoscopy increased the likelihood that diagnosis would be mucinous adenocarcinoma. Transurethral biopsy and resection revealed adenocarcinoma or adenocarcinomatous tissue of probable colonic or appendiceal origin in six cases including one of our cases [3,9,11–13]. The fistula has rarely been seen on colonoscopy, so only one fistula was detected by colonoscopy [10]. Exploratory laparotomy can be helpful for diagnosis [14,15]. Taken together, the combined use of CT imaging and cystoscopy will increase the detection rate of this fistula. Immunohistochemical markers may help to identify the origin of the tumor. All the appendix mucous adenocarcinomas and bladder adenocarcinomas were positive for CK7 and CK20, but the latter was negative for beta-catenin [9].
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The main treatment for appendiceal adenocarcinoma with appendicovesical fistula is right hemicolectomy with partial cystectomy. Nitecki et al. [26] reported 68% and 20% 5-year survival rates for patients treated with right hemicolectomy and simple appendectomy respectively. Walters et al. [27] reported a similar 5-year survival rate with different surgical techniques (appendectomy vs hemicolectomy) for Stage 1 and 2 patients. For our patients, right hemicolectomy and simple appendectomy was performed on two patients and one patient respectively, which archived positive outcomes of long-term survival. 5. Conclusion In summary, we present three cases of appendiceal adenocarcinoma causing appendicovesical fistula. Although the lesion is rare, it should especially be considered in elderly patients suspected of intestinal carcinoma coupled with mucus in the urine. In cases with “bladder tumor”, especially those suspected to be of intestinal origin, one should examine the colon as well as the appendix. To avoid a misdiagnosis, the doctors must bear in mind that appendiceal adenocarcinomas, especially mucinous adenocarcinomas, can invade the bladder and form fistulas. A combined use of CT imaging, endoscopy techniques and tissue biopsy is essential for an accurate diagnosis. A suitable surgery of hemicolectomy and partial cystectomy archived a long-term survival in these three patients. Financial disclosure The authors declare that they have no relevant financial interests to disclose. References [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12]
A.S. ¸ Köksal, I.H. Kalkan, H. Yildiz, R.S. Ökten, G. Ne¸ss¸ar and N. Sa¸smaz, Direct visualization of an extremely rare malignancy: Adenocarcinoma of the appendix, Am J Gastroenterol 108 (2013), 149–150. K. Ahmed, R. Hoque, S. El-Tawil, M.S. Khan and M.L. George, Adenocarcinoma of the appendix presenting as bilateral ureteric obstruction, World J Surg Oncol 6 (2008), 23. J.P. Richie, Primary carcinoma of the appendix masquerading as primary bladder carcinoma, Arch Surg 112 (1977), 666–667. K.K. Turaga, S. Pappas and T.C. Gamblin, Right hemicolectomy for mucinous adenocarcinoma of the appendix: Just right or too much? Ann Surg Oncol 20 (2013), 1063–1067. N. Hananel, E. Powsner and Y. Wolloch, Adenocarcinoma of the appendix: an unusual disease, Eur J Surg 164 (1998), 859–862. Y. Miyakura, H. Iwai, K. Togashi, H. Horie, H. Nagai, Y. Kishaba, K. Sato and H. Azuma, Mucinous cystadenocarcinoma of the appendix invading the ascending colon with fistula formation: report of a case, Surg Today 37 (2007), 806–810. H. Tanaka, T. Kobayashi, K. Yoshida, T. Asakura, H. Taniguchi and Y. Mikami, Low-grade appendiceal mucinous neoplasm with disseminated peritoneal adenomucinosis involving the uterus, mimicking primary mucinous endometrial adenocarcinoma: a case report, J Obstet Gynaecol Res 37 (2011), 1726–1730. I. Mishin, G. Ghidirim and M. Vozian. Appendiceal mucinous cystadenocarcinoma with implantation metastasis to the incision scar and cutaneous fistula, J Gastrointest Cancer (2012), 349–353. R. Mistry, K. Ananthakrishnan, B.N. Hamid, C. Powell and G.E. Foster, Appendiceal carcinoma masquerading as recurrent urinary tract infections: Case report and review of literature, Urology 68 (2006), 428e1–428e3. H. Vidarsdottir, P.H. Moller, K.R. Benediktsdottir and G. Geirsson, Adenocarcinoma of the appendix with a fistula to the urinary bladder, Scand J Urol Nephrol 44 (2010), 354–356. I. Ikeda, T. Miura and I. Kondo, Case of vesico-appendiceal fistula secondary to mucinous adenocarcinoma of the appendix, J Urol 153 (1995), 1220–1221. S.E. Dahms, M. Hohenfellner, C. Eggersmann, A. Lampel, R. Golz and J.W. Thüroff, Appendix carcinoma invading the urinary bladder, Urol Int 58 (1997), 124–127.
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Combination of CT imaging and endoscopy in diagnosis of appendicovesical fistula caused by appendiceal adenocarcinoma Wenying Wanga , Li Wangb , Jianfeng Xub , Shufang Shic , Ye Tiana,∗ and Yuanyuan Zhangd,∗ a Department
of Urology, Beijing Friendship Hospital, Capital Medical University, Beijing, China for Cancer Genomics, Wake Forest University School of Medicine, Winston-Salem, NC, USA c Department of Pathology, Beijing Friendship Hospital, Capital Medical University, Beijing, China d Institute for Regenerative Medicine, Wake Forest University, Winston-Salem, NC, USA b Center
Received 3 October 2013 Revised 21 January 2014 Accepted 16 March 2014 Abstract. The appendiceal diseases, particularly appendicitis, are the most common disorders in the digestive system localized at the right lower quadrant area. However, appendiceal carcinoma with vesico-appendiceal fistula is a rare clinical phenomenon. Lacking specific symptoms, appendiceal carcinomas with fistula formations are often misdiagnosed as acute appendicitis cases. The purpose of this study is to increase awareness of appendiceal neoplasms and appendicovesical fistulas. We reported our experiences in three complex cases related to digestive and urological systems, and reviewed the literature on diagnosis with various X-ray imaging techniques for this lesion. In this report, the first case failed to be diagnosed. The other two patients with appendicovesical fistulas secondary to appendiceal adenocarcinomas were successfully detected with computed tomography (CT) and cystoscopy. The patients recovered after right hemicolectomies and en bloc partial cystectomies and survived without tumor metastasis up to 7-year follow-up. In conclusion, a combined use of CT imaging and endoscopy techniques provides an accurate diagnostic alternative for appendicovesical fistula secondary to appendiceal adenocarcinoma. Keywords: Appendix adenocarcinoma, bladder, fistula
1. Introduction Appendix neoplasms are very rare entities in the digestive system and are found in only 0.9–1.4% of appendectomy specimens. The estimated age-adjusted incidence is only 12 cases per 100 million people per year [1]. Appendicovesical fistulas caused by the tumor often lack specific symptoms. By occasionally appearing as a right renal mass or chronic renal failure, they cause misdiagnosis pre-operatively [2]. In some cases, it presents urinary tract infections, dysuria, pyuria, frequencies, micturition pains, and gross hematurias, which is not encountered in most surgeons’ careers [3]. Clinicians are vulnerable to ∗
Corresponding authors: Ye Tian, Department of Urology, Beijing Friendship Hospital, Capital Medical University, 95 YongAn Road, Xicheng District, Beijing 100050, China. E-mail: [email protected]. Yuanyuan Zhang, Institute for Regenerative Medicine, Wake Forest University, Winston-Salem, NC 27157, USA. E-mail: [email protected]. c 2014 – IOS Press and the authors. All rights reserved 0895-3996/14/$27.50
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misdiagnosing other diseases with similar symptoms as appendicitis [4]. Histologically, two types of tumors exist in appendix tissues, i.e. carcinoid tumors that account for 32–85% of all appendiceal tumors and adenocarcinomas that account for only 4–6% of them. The adenocarcinomas are divided into three subtypes: mucinous, non-mucinous (colonic type), and signet-ring cell adenocarcinoma. The mucinous adenocarcinoma is predominant, composing 23%∼55% of all adenocarcinomas in the appendix [5]. Appendiceal adenocarcinoma, especially mucinous adenocarcinoma, is notorious for its spread to adjacent organs and forms the fistula to colon [6], uterus [7], and skin [8]. It is uncommon that an appendiceal adenocarcinoma penetrates into the bladder. To date, a total of fifteen cases of appendicovesical fistulas caused by adenocarcinoma have been reported since the first was described by Richie in 1977 [3]. Twelve cases resulted from mucinous adenocarcinoma type. The mucinous adenocarcinoma can easily perforate to the bladder via the fistulas because the appendix has a thin subserosa, muscles and serosa layer [9]. Although pre-operative diagnosis of appendiceal adenocarcinomas remains challenging, modern Xray imaging, endoscopic and pathological techniques make it possible to improve the diagnostic accuracy of appendiceal neoplasms. CT or magnetic resonance imaging (MRI) techniques are especially important for diagnosing the tumor and fistula within the appendix when combined with endoscopic examinations. Surgery alone, such as a right hemicolectomy, achieves a good 5-year survival in treatment of appendiceal adenocarcinomas [4]. Mucinous adenocarcinomas provide better long-term survival rates than nonmucinous tumors [4]. Therefore, an early and accurate pre-operative identification is critical for the clinical management of patients with appendiceal adenocarcinoma and fistulas. In this report, we presented three cases with appendiceal adenocarcinomas invading the bladder tissue, leading to the formation of fistulas. Preoperative diagnosis was made by the combined use of CT imaging and cystoscopy. We have discussed the value and features of different X-ray imaging techniques including barium enema, plain film, intravenous urogram (IVU) film, MRI, colonoscopy, CT, and cystoscopy used to diagnose this uncommon lesions related to two organs; the urinary tract and digestive system. 2. Patients and methods Three patients (two females and one male) diagnosed with appendicovesical fistula were studied at our institute between July 2005 to September 2010 (Table 1). The mean age was 61 (45, 61, 78) years. The first patient presented with a one-year history of intermittent hematuria; the second patient was admitted with pyuria, urinary frequency and complaints of occasional mucus in the urine; the third patient was seen with a complaint of having had mucus in the urine for four months. All the patients did not have gastrointestinal tract symptoms such as pain, intestinal obstruction or melena. Past medical and surgical histories were all negative. Physical examination revealed a palpable mass 7cm in diameter in the right lower quadrant without tenderness in the first patient, and no abnormal findings were found in the rest two. Laboratory biochemical examinations were taken, including blood count, hemoglobin, white blood cell count and electrolytes, urine and fecal analysis, tumor markers including carcinoembryonic antigen (CEA) and alphafetoprotein (AFP). For the diagnosis of the appendiceal tumors, X-ray examinations were made, including plain abdominal, IVU film, barium enema and enhanced CT scanning. A 64-row multidetector CT (GE light Speed VCT scanner, GE Healthcare, Wis, USA) with working parameters of 120 kV/350 mA, 5-mm slice thickness, and 0.984:1 pitch was used to scan the kidneys, ureters and bladder of all the patients before the procedures. Non-ionic intravenous contrast agent (Iohexol injection, 75 ml:22.5 g, Yangtze River
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Table 1 Clinical characteristics of appendicovesical fistula caused by appendiceal adenocarcinom and appendicitis Variables Sex/Age (y) Symptoms Urine analysis
Case 1 M/61 Intermittent hematuria pyuria
Case 2 F/45 Pyuria, mucus in the urine Lots of WBC/HP, mucus in the urine
Case 3 F/78 Mucus in the urine More than 100 WBC/HP
Urine culture Serum CEA and AFP Physical examinations
− − −
Escherichia coli and fungi CEA (−) A palpable mass in the right lower quadrant
Escherichia coli CEA (−), AFP (−) −
Plain film and IVU Barium enema
− Appendix was not visible
− Extrinsic compression at the ileocecum
− −
CT scanning
A 3 cm × 4 cm solid mass on the right thicken bladder wall at the lesion side, an air bubble in the bladder lumen
A 7 cm solid mass with focal calcification on the bladder wall
A thickened right bladder wall, a tubular structure connected with the bladder, a fistula was seen
Cytology Cystoscopy
− A broad-based non papillary tumor, a fistula was seen
− Solid broad-based mass with a lot of mucus on the surface
− A fistula and a large amount of mucus can be seen
Biopsy
−
−
Pathology on surgical tissue samples
Colonic type adenocarcinoma
Mucinous adenocarcinoma
Adenocarcinoma suspicious for appendix origin Mucinous cystadenocarcinoma
Treatment
Appendectomy and partial cystectomy
Right hemicolectomy and partial cystectomy
Right hemicolectomy and partial cystectomy
Follow-up (yrs) 7 5 3 Recurrence, metastasis No No No Abbreviation note: WBC: white blood cell; HP: high powerfield; IVP: intravenous pyelography; CEA: carcinoembryonic antigen; AFP: alphafetoprotein; − negative.
Pharmaceutical Group, China) was used. In order to confirm the origin of the tumor, cystoscopy (rigid cystoscopy, Telescope “70” degree, Karl Storz, Germany,) and tumor biopsies were performed in all the patients. The pathological examination of the biopsy specimens were obtained in and around the fistula. The biopsied and resected specimens were fixed (10% neutral-buffed formalin for at least 24 h) and embedded in paraffin. The histological diagnosis was made using conventional hematoxylin and eosin staining and Immunohistochemistry.
3. Results Urinary analysis revealed 10–35 red blood cells and more than 100 white blood cells per high power field in all the patients. The small amount of white, loose, floating mucus were seen in urine samples in two patients (Table 1). Urine culture revealed Escherichia coli in both patients and fungi in one. Voided urinary cytology was negative. The fecal occult blood tests were negative. The blood electrolytes, alkaline phosphatase, liver enzymes, hemoglobin, and white blood cell count were normal. Tumor markers including CEA and AFP were on normal levels. Barium enema showed extrinsic compression at the ileocecum and the appendix was invisible (Fig. 1).
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Fig. 1. Barium enema images of appendiceal adenocarcinoma. (A) Extrinsic compression at the ileocecum and the appendix is not visible (arrow) in Case 1; (B) in Case 2. (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/ XST-140440)
Fig. 2. CT scanning of adenocarcinoma of the appendix in three cases. (A) The bladder wall (thick arrow) and an air bubble within the bladder lumen (thin arrow, cross-sectional view). (B) A solid mass with calcification connecting with the ascending colon and extending to the bladder (thick arrow, longitudinal view). (C) A tumor mass in the right wall of the bladder (thick arrow) with a fistula leading to the bladder (thin arrow). (Colours are visible in the online version of the article; http://dx.doi.org/ 10.3233/XST-140440)
CT scans revealed a 3 cm × 4 cm solid mass on the right side (11 o’clock position) of the bladder wall with an air bubble within the bladder lumen in the first case; a 7 cm round solid mass with focal calcifications on the right side of the bladder wall in the second case; a thickened tissue with a channel structure connected with the right side of the bladder lumen in the third case (Fig. 2). Cystoscopy revealed that the tumors were located on the right side of the bladder attached with mucus, and the fistula opening to the bladder was observed in two patients (Fig. 3). The values for appendiceal tumors on noncontrast and contrast CT images were 30∼42 HU and 45∼70 HU respectively. The tissue biopsied by transurethral resection histologically revealed atypical dysplasia or adenocarcinoma suspicious but origins couldn’t be confirmed in each case. Surgical exploration revealed the tumors originated from the appendix and had grown into the bladder causing the fistula. The histologic
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Fig. 3. Cystoscopy examination of adenocarcinoma of the appendix. The opening of the fistula (arrow) was noted at 1 and 11 o’clock positions on the upper bladder wall (A). Mucus was seen from the fistula opening (B). (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/XST-140440)
Fig. 4. Histological examination of adenocarcinoma of the appendix. (A) Well differentiated colonic type adenocarcinoma in case 1. (B) Mucinous adenocarcinoma in case 2. (C) Well differentiated mucinous cystadenocarcinoma in case 3. (HE 20 × 10). (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/XST-140440)
Fig. 5. Immunohistological examination of adenocarcinoma of the appendix. (A) CK20 (+) in case 3. (B) CDx-2 (+) in case 3. (HE 20 × 10). (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/XST-140440)
diagnosis was that of a well-differentiated colonic type adenocarcinoma, mucinous adenocarcinoma and a well-differentiated mucinous cystadenocarcinoma respectively (Fig. 4). Immunohistological examination showed CK20 (+) and CDx-2 (+) in the third case (Fig. 5). The tumor tissues were removed by appendectomy and en bloc partial cystectomy in one case, and with a right hemicolectomy and en bloc partial cystectomy in two cases (Fig. 6). Neither postoperative radiotherapy nor chemotherapy was administered. All the patients survive after surgery with no tumor
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W. Wang et al. / Appendicovesical fistula caused by appendiceal adenocarcinoma Table 2 Clinical characteristics of appendicovesical fistula caused by appendiceal adenocarcinom and appendicitis
Variables Cases reported Sex affected Age Symptoms Tumor markers Plain film and IVP Fistula on MRI CT scanning
Appendiceal adenocarcinoma Extremely rare, 18 cases(including ours) Nearly the same (M:F = 1:1) 50–60 years old Urinary symptoms Seldom positive for CEA or AFP Usually unhelpful Less than 20% positive Soft-tissue mass in the right lower quadrant can be seen, loss of normal appendiceal tubular shape
Appendicitis Rare, more than 100 cases [20] M predominance (M:F = 3:1) [10] 10–40 years old Urinary symptoms, pneumaturia may occur − Calcification occasionally 40% positive An enlarged appendix that maintained its tubular structure, infiltration of periappendiceal fat by fluid or soft tissue strands
Barium enema Colonoscopy Biopsy
Appendix was not filled with contrast medium One case positive More than 30% positive, origin of tumor not identified sometimes
Flow of contrast medium was seen in a few cases − −
Cystoscopy Less than 40% positive 40%–60% positive [11] Treatment Right hemicolectomy and partial cystectomy Appendectomy and partial cystectomy Pathology Adenocarcinoma, mucinous (80% cases) Appendicitis Abbreviation note: IVU: intravenous urogram; CT: computed tomography; MRI: magnetic resonance imaging; − negative.
Fig. 6. he resected tissue specimens of appendiceal tumors connected to the bladder wall (black arrow). (A) Case 1. (B) Case 2 and (C) Case 3. Notes: 1 Appendiceal carcinoma. 2 Ileum. 3 Ascending colon. (Colours are visible in the online version of the article; http://dx.doi.org/10.3233/XST-140440)
metastasis during the follow-up (3 to 7 years). Clinical characteristics, imaging examinations, perioperative variables and outcomes for three patients were listed at Table 1. 4. Discussion Appendiceal adenocarcinomas with appendicovesical fistulas [3] are rare and easily misdiagnosed as appendicitis case (Table 2). To date, only eighteen cases have been reported including ours [3,9–21]. Appendiceal adenocarcinoma most often presents in patients during their 50 s–60 s, significantly older than patients with appendicitis. The mean age of our patients was 61 years. Males are more frequently affected with appendiceal adenocarcinoma than females (3:1) [9], however, we found that, when the tumors infiltrated the bladder, males and females were equally affected. Differential diagnosis of appendiceal adenocarcinoma is highly important among the lesions with the pain and lower quadrant masses (Table 3). About 40% of patients with appendiceal adenocarcinoma have presented with acute appendicitis or incidental findings in resected specimens [10–13]. Pre-operative diagnosis is more difficult for patients with appendicovesical fistulas secondary to appendiceal adenocarcinoma, as the patients usually have no specific clinical manifestations. The patients usually do not have
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Table 3 Different diagnosis of right lower quadrant masses with clinical and imaging examination Variables Age predominance Gender affected most Main symptom Urine analysis Tumor markers Pregnancy test Ultrasound Plain film and IVU Barium enema CT MRI Colonoscopy Cystoscopy Biopsy Diagnostic laparoscopy
Ovarian cyst 30 years old F Abdominal pain − − − Hypoechoic − − useful Most useful − − Diagnostic Helpful
Ectopic pregnancy 20–30 years old F Abdominal pain − − + Hypoechoic − − Useful Useful − − N/A Helpful
Bladder carcinoma 65 years or older M Hematuria Hematuria + − Hypoechoic Helpful occasionally − Most useful Useful − + Diagnostic Not applicable
Bladder stone 65 years or older M Urinary tract infection Urinary tract infection − − Hyperechoic + − Useful Helpful − + N/A Not applicable
Glandular cystitis 30–40 years old M Hematuria Hematuria − − Hypoechoic Not helpful − Useful Useful − + Diagnostic Not applicable
Colonic carcinoma 60 years or older M Blood fecal − + − Hypoechoic − + Most useful Useful + − Diagnostic Helpful
Abbreviation note: CT: computed tomography; MRI: magnetic resonance imaging; IVU: intravenous urogram; F: female; M: male; − negative; + positive; N/A: not applicable.
intestinal symptoms. One explanation for this may be that in early stages, tumors of the appendix can invade the bladder before interfering with the intestinal passage. None of the three patients had typical symptoms of pneumaturia suggestive of appendicovesical fistula. As this disease was so rare, we had misdiagnosed the first case. Given the experience from the case, we made acute pre-surgical diagnoses in the remaining two patients. CT imaging examinations are often used in diagnosing the tumor in solid organs [22–24]. Despite ambiguous image structures in the hollow viscera, CT scans still provide valuable diagnostic information for appendiceal adenocarcinoma [25]. The presence of a solid or cystic mass in the area of the appendix with enhancing nodularity on CT usually suggests the possibility of malignancy. Wall thickness is also regarded as a differential point between neoplastic and non-neoplastic diseases. However, the presence of a relative thin wall can’t exclude malignancy. For all the three cases, CT’s showed a soft-tissue mass compressing the right bladder wall or focal bladder wall thickening. In addition, we observed the presence of air within the bladder, which suggested the existence of one fistula in one of our cases. Sometimes CTs were specific, but not sensitive for diagnosing appendiceal tumors; the appendix maintained its tubular structure without peri-appendiceal infiltration in a third of our cases. In addition, 64% of mucinous adenocarcinoma presented with appendiceal ruptures and peritoneal spreads [26,27]. However, none of the cases presented with pseudomyxoma peritonei on CT. Other X-ray imaging techniques are also helpful for diagnosing this type of tumor and fistulas. One case of a fistula was identified by barium enema [6]. MRI revealed the fistulous tract in three cases [9–11]. Cystoscopy can reveal fistula openings, and its diagnosis accuracy is about 40% [11]. In two cases of ours, we were able to clearly see the fistula on cystoscopy. The presence of mucus from the fistula on cystoscopy increased the likelihood that diagnosis would be mucinous adenocarcinoma. Transurethral biopsy and resection revealed adenocarcinoma or adenocarcinomatous tissue of probable colonic or appendiceal origin in six cases including one of our cases [3,9,11–13]. The fistula has rarely been seen on colonoscopy, so only one fistula was detected by colonoscopy [10]. Exploratory laparotomy can be helpful for diagnosis [14,15]. Taken together, the combined use of CT imaging and cystoscopy will increase the detection rate of this fistula. Immunohistochemical markers may help to identify the origin of the tumor. All the appendix mucous adenocarcinomas and bladder adenocarcinomas were positive for CK7 and CK20, but the latter was negative for beta-catenin [9].
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The main treatment for appendiceal adenocarcinoma with appendicovesical fistula is right hemicolectomy with partial cystectomy. Nitecki et al. [26] reported 68% and 20% 5-year survival rates for patients treated with right hemicolectomy and simple appendectomy respectively. Walters et al. [27] reported a similar 5-year survival rate with different surgical techniques (appendectomy vs hemicolectomy) for Stage 1 and 2 patients. For our patients, right hemicolectomy and simple appendectomy was performed on two patients and one patient respectively, which archived positive outcomes of long-term survival. 5. Conclusion In summary, we present three cases of appendiceal adenocarcinoma causing appendicovesical fistula. Although the lesion is rare, it should especially be considered in elderly patients suspected of intestinal carcinoma coupled with mucus in the urine. In cases with “bladder tumor”, especially those suspected to be of intestinal origin, one should examine the colon as well as the appendix. To avoid a misdiagnosis, the doctors must bear in mind that appendiceal adenocarcinomas, especially mucinous adenocarcinomas, can invade the bladder and form fistulas. A combined use of CT imaging, endoscopy techniques and tissue biopsy is essential for an accurate diagnosis. A suitable surgery of hemicolectomy and partial cystectomy archived a long-term survival in these three patients. Financial disclosure The authors declare that they have no relevant financial interests to disclose. References [1] [2] [3] [4] [5] [6] [7] [8] [9] [10] [11] [12]
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