Umbilical metastasis or Sister Mary Joseph\'s nodule

Review

Umbilical metastasis or Sister Mary Joseph’s nodule Aurelie Dubreuil, MD, Anne Dompmartin, MD, Philippe Barjot, MD, Sylvie Louvet, MD, and Dominique Leroy, MD

From the Department of Dermatology of Caen, France Correspondence Anne Dompmartin, MD, Service de Dermatologie, Centre Hospitalier Universitaire, Avenue Georges Clemenceau, 14033 Caen Cedex, France

Apart from hemopathies and sarcomas, the frequency of cutaneous metastasis ranges from 5% to 9%.1–3 Of these, metastatic tumors of the umbilicus are rare. The first case was reported in 1864 by Storer4 and called Sister Mary Joseph’s nodule. Three-hundred-and-sixty-eight cases were reported in the French and English literature between 1960 and 1995. Cases before 1960 will not be studied, because, in most of them, the primary tumor was unknown. The diagnosis is usually made with the histologic examination and the most common primary cancer is an adenocarcinoma of the stomach. The metastatic processes are numerous and condition the prognosis. History Sister Mary Joseph (1856–1939) was the first to draw a specific sign of intra-abdominal cancer and reported it to her chief Dr William Mayo: she noted that these patients presented a firm umbilical nodule. In recognition of her contribution to medicine, Hamilton Baily (1960) suggested that the name Sister Mary Joseph’s nodule should be given to the metastatic tumors of the umbilicus.5,6

Clinical manifestations The patients presenting umbilical metastasis were mainly women (176 cases);7–51 121 cases were men,7,10–13, 18,20,23,25,32,33,44,52–67 and in 71 cases the sex was not mentioned.22,33,68 Although there are no specific clinical features of umbilical metastasis, it is very important to examine carefully every patient’s umbilicus. It is usually a firm, irregular, and small nodule that may be painful and ulcerated, sometimes with pus, blood, or serous fluid as exudate (Fig. 1). Instead of a distinct nodule, it may also present as a diffuse induration of the subcutaneous tissue. The primary symptom of an internal cancer may be a © 1998 Blackwell Science Ltd

painless umbilical mass that is misdiagnosed as an umbilical hernia.19,31,32,35,48,51 Umbilical tumors can be the first symptom of an underlying cancer or an indication of a recurrence in a patient with a previous internal cancer.

Histology The diagnosis is based on the anatomicopathologic examination of the biopsy of the umbilical tumor; the histologic interpretation of the metastatic tumor can be used as an indication of the primary origin. With a fine needle aspiration of the nodule, a cytologic examination can be performed, especially in patients with previously documented malignancy. It provides a rapid and reliable diagnosis.13,20,29,32,53 Most cases involved metastasis of adenocarcinoma (278/ 368).7–13,15,16,18–30,32–37,41,42,44–49,53–64 Fifteen cases of squamous cell carcinoma were reported. In 13 cases, the primary site was determined: cervix, eight cases; 7,10,19,27,32,38–40 vagina;43 vulva;19 penis;7 lung;32 and ovary.31 Occasionally, other cancers were reported: four cases of undifferentiated carcinoma;10,19 three cases of carcinoid;14,17,22 two cases of leiomyosarcoma;27,52 one case of granulosa cell tumor;13 a myxoid liposarcoma of the stomach;33 a small cell carcinoma of the lung;65 a myeloma;66 two cases of peritoneal mesothelioma;50,51 an adenoacanthoma of the uterus;7 a hepatoma;7 one case of transitional cell carcinoma;13,67 and a mixed mu¨llerian tumor.19 In 58 cases, histologic examination of the primary tumor was not mentioned.10,68

Diagnosis The differential diagnosis comprises other acquired benign or malignant tumors of the umbilicus. International Journal of Dermatology 1998, 37, 7–13

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Figure 2 Primary sites of carcinomas in 121 men with a Sister Mary Joseph’s nodule

Figure 1 Nodular umbilical metastasis

Endometriosis The presence of extrauterine endometrial tissue is a relatively common condition, with an estimated prevalence of 10% of all women of childbearing age.69 It is a solitary blue, red, or brown nodule which increases in size, becomes painful, and may bleed during menses. The umbilicus is the most common site for this tumor. It can also occur as a secondary process in scars including the umbilicus.70 Benign tumors Foreign body granuloma,14 melanocytic nevi, papilloma, fibroma, epithelial inclusion cysts, epidermoid cysts, seborrheic keratosis, abscess,16,19,55 omphalitis,59 pilonidal sinus, keloid, hernia, myxoma, and many other tumors will be eliminated with the histologic examination. Primary umbilical carcinoma Primary malignant umbilical tumors, such as melanoma, squamous and basal cell carcinoma, sarcoma, and adenocarcinoma are rare.7,10,22 Clinically, they cannot be differentiated from secondary tumors of the umbilicus. Therefore, the diagnosis of primary adenocarcinoma of the umbilicus must always be looked at with care. Some umbilical adenocarcinomas have specific histologic features that enable a fairly confident prediction of the probable site of the primary tumor to be made. For instance, the linear distribution of the cells between adjacent collagen bundles International Journal of Dermatology 1998, 37, 7–13

is predictive of breast cancer, but similar patterns can exist in prostate or pancreas adenocarcinoma.71 A welldifferentiated glandular architecture is more typical of primary tumor of the large bowel or the rectum.1,71 Sometimes, there are no distinctive histopathologic features and, in these cases, immunocytochemical or electron-microscopic techniques may be of value.71 The diagnosis of primary umbilical carcinoma can be suspected when an alternative primary cancer has been searched for but not found by a complete check-up.

Etiology The umbilicus represents the site of predilection of metastasis for a host of intra-abdominal neoplasms. The umbilicus nodule may be the presenting symptom or the earliest sign of the tumor from which it originated. It can also be an indication of recurrence in a patient with a known disease. Stomach This was the major site of the primary lesion (96/368 cases; 26.1%),7–13,18,22,25,32,33,54–56,68 and the most important primary site in men (30%)7,10–13,18,25,32,54–56 (Fig. 2). In women, the frequency was less important (9%). Mainly adenocarcinomas were involved, except for one case of myxoid liposarcoma of the stomach.33 In 44 cases, the sex was not mentioned.22,33,68 Rectum, colon, and small bowel Of the 368 cases, colon, rectum, and small bowel are the primary site in 74 cases, i.e. 20.1%;7,10–23,25,32,33,52,57–59,68 six of them were secondary to a small bowel tumor. There were 22 women,7,10,12–21 30 men,7,10–13,18,20,23,32,33,52, 53,57–59 and in 22 cases the sex was unknown.22,25,68 For these sites, men were in the majority: 25% men and only 12% women. Mainly adenocarcinomas were involved, with the exception of three carcinoids: large and small © 1998 Blackwell Science Ltd

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because clinical, cytologic, histologic, radiologic, and surgical investigations of these patients were insufficient to provide supporting evidence: diffuse carcinosis, rapid death of the patient with no autopsy for instance. Physiopathology

Figure 3 Primary sites of carcinomas in 176 women with a Sister Mary Joseph’s nodule

bowel,14,22 cecum,17 and one case of leiomyosarcoma of the small intestine.52 Gynecologic carcinomas The ovary was the main primary site in women (Fig. 3) (59/176 cases; 34%)7,10–13,19,20,22–32 It also represented 63.4% of the gynecologic malignant tumors with umbilical metastasis (59/93 cases).7,10–13,19,20,22–43 The other sites were endometrium (12%)7,10,13,19,27,32–37 and cervix (5%).7,10,19,27,32,38–40 Mainly ovarian and endometrial adenocarcinomas were involved; however, one case of granulosa cell tumor of the ovary,13 one case of ovarian squamous cell carcinoma,31 one case of adenoacanthoma of the endometrium,7 one case of leiomyosarcoma of the endometrium,27 and two cases of carcinoma of the fallopian tube41,42 were also reported. The malignant tumors of the cervix, the vagina,43 and the vulva19 with umbilical metastasis were all squamous cell carcinomas. Therefore, an umbilical squamous cell carcinoma in a woman is usually a metastasis of a primary tumor of the cervix (8/14 cases). Pancreatic carcinoma The incidence was 10% (37/368 cases) of all the umbilical metastases.7,10,12,13,19,23,25,33,44,45,58,60–63 They occurred mainly in men (22/37 cases),7,10,12,13,23,44,58,60–63 with 14 women10,12,19,23,33,44,45 and one undetermined case.25 The histologic pattern was usually adenocarcinoma, except for one case of undifferentiated carcinoma.19 Other primary tumors The sites of the other primary tumors were as follows: gallbladder, 6 cases;10,22,46–49 breast, 6 cases;10,13 lung, 5 cases;10,12,32,65 prostate, 3 cases;10,33,64 penis, 1 case;7 peritoneum, 2 cases of mesothelioma;50,51 bladder, 1 case;67 kidney, 1 case;12 liver, 1 case;7 and myeloma, 1 case.66 Unknown primary tumor Of the 368 cases, 41 (11.2%) had an unknown etiology.7,10–13,22,32,33 The primary site was not established © 1998 Blackwell Science Ltd

The umbilicus, because of its anatomic relations and its generous vascular and embryologic connections, is particularly prone to receive neoplastic cells. The metastatic processes to the umbilicus were studied with direct and indirect arguments. Propagation through lymph ducts The lymphatic drainage of the umbilicus is very important. There are lymphatic connections between the peri-umbilical skin and the deep lymphatic network: para-aortic, internal mammary, and external iliac nodes. There are also connections with the superficial lymphatic network: axillary and inguinal nodes. In the literature, connections with the axillary nodes60 and the inguinal lymph nodes15 were found in two cases. There are many variations of normal lymph drainage between patients, and several unusual patterns have been described with cutaneous lymphoscintigraphy. In one study,72 20% of patients had a lymphatic drainage from the peri-umbilical skin to the internal mammary nodes. The authors believe that the presence of this channel could explain the occurrence of umbilical metastasis and may have important implications for the surgical management and prognosis of these patients. In addition, Glover and Waugh73 demonstrated that there was an anterograde, but also a retrograde, dissemination of the neoplastic cells. Therefore, the umbilicus is a point of intersection of the lymphatic network; this explains the risk of lymphatic spread to the umbilicus and also the systemic dissemination from it. Finally, propagation through the lymph ducts seems to be the main etiology of umbilical metastasis. Propagation via the venous network The role of the veins in the cutaneous metastatic process is certainly very important. Batson74 isolated a vertebral vein system which consists of the epidural veins, the perivertebral veins, the veins of the thoraco-abdominal wall, the veins of the head and neck, and the veins of the vertebral column. These vessels are valveless and carry blood under low pressure. This vein system parallels, connects with, and provides bypasses for the portal, pulmonary, and caval system of veins. These vessels are very different from the lymphatic ones, which are smaller and have many valves; however, they can have a similar pattern, as observed after injections of roentgen opaque substances into the veins of the thoraco-abdominal wall. The numerous International Journal of Dermatology 1998, 37, 7–13

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connections of the venous network of the abdominal wall are probably very important in the genesis of umbilical metastasis.

these numerous anatomic connections, embryologic remnants may not play an important role in the genesis of umbilical metastasis.

Contiguous extension The umbilicus is a deep organ which is directly related to extraperitoneal tissue, so that direct extension from the anterior peritoneal surface is possible. In 1986, Goodheart et al.28 confirmed the contiguous extension of an ovarian carcinoma with peritoneal and umbilical metastasis. Histologically, the metastatic ovarian carcinoma had extended from a peritoneal fold to form an umbilical nodule. Definite vascular or lymphatic invasion was not seen. Since then, four other cases have been reported.31,33,57,59 Many authors observed multiple peritoneal nodules at laparotomy or autopsy, and 17 cases were clearly reported.8,11,16,17,24,29,33,35,37,42,51–54,56,58,61 It must be pointed out, however, that peritoneal mesothelioma rarely spreads to the anterior part of the abdominal wall, except on laparotomy scars or on local incisions for cytologic examination.51 It is rare for these tumors to penetrate into the umbilicus, and only two cases have been reported.50,51

In an umbilical hernia Occasionally, tumor cells may become implanted in an old umbilical hernia. Therefore, what appears to be acquired umbilical hernia in an otherwise asymptomatic patient should raise the suspicion of intra-abdominal malignancy. Seven cases (7/368) were clinically misdiagnosed as umbilical hernia.19,31,32,35,48,51

Through embryologic remnants The umbilicus is a scar which remains after the fall of the umbilical cord; it is connected to multiple embryologic remnants: the vitelline duct, which becomes the Meckel’s diverticulum (2%–4% of the general population), and is sometimes connected to the distal part of the umbilicus;75 the urachus or the allantoid canal between the umbilicus and the roof of the bladder; the umbilical vein between the umbilicus and the cava, which becomes the falciform ligament; and the umbilical arteries, which become the vesico-umbilical ligaments on the sides of the urachus. In the literature, the embryological remnants were suspected to be the main routes of metastasis from the primary sites to the umbilicus; however, only two authors documented metastatic adenocarcinoma arising in an embryologic remnant of patients presenting umbilical metastasis. In a patient presenting adenocarcinoma of the gallbladder with umbilical metastasis, McElfpatrick and Toll46 also demonstrated metastatic lesions of the mesothelium and the vascular spaces of the falciform ligament. Scarpa et al.23 also reported the involvement of the ligament teres of a patient presenting adenocarcinoma of the tail of the pancreas. Although the falciform ligament directly connects the umbilicus to the liver, umbilical metastasis from a primary carcinoma of the liver is very rare; only one case7 has been reported. In addition, although the allantoid canal connects directly the umbilicus to the urinary bladder, only one case67 of bladder carcinoma with umbilical metastasis has been reported in a patient presenting multiple other metastases. Therefore, despite International Journal of Dermatology 1998, 37, 7–13

Arterial spread Extravasation of the malignant cells from the circulation and invasion of target organs, such as the umbilicus, is another pattern of metastasis.76 Iatrogenic umbilical metastasis A few cases of umbilical metastasis after laparoscopy have been reported.40,48,49 The metastases were present on the laparoscopy site and were not always associated with intraperitoneal malignant disease.40 Clinicians need to be informed of the possibility of laparoscopy site tumor implantation and the implications for the management of occult intra-abdominal malignancies. Prognosis In 152 cases (152/368), umbilical metastasis was discovered before the diagnosis of primary cancer;7,8,10–33,35,39,41, 42,44,46,47,50–56,58–63 Sister Mary Joseph’s nodule was the only initial presentation of internal malignancy in 97 of these 152 cases.7,11–16,18,19,21–33,35,41,44,46,47,50,51,55,56,61,63 In 88 cases, the umbilical metastasis was discovered after the beginning of the treatment of the primary tumor; 7,9–13,18–20,22,25,27,29,32–34,36–38,40,43,45,48,49,57,58,64–66 in 22 patients (22/88; 23.5%), with a previous internal cancer, umbilical metastasis was the first indication of recurrence.9–11,20,25,32–34,36–38,40,43,45,48,49,64 The average time27,38 between the treatment of the primary cancer and the occurrence of umbilical metastasis was 22 months, ranging from 1 month to 10 years. Mainly endometrial,19,27,34,36,37 cervical,19,38 and ovarian25 malignancies were associated with umbilical metastasis late after the treatment of the primary tumor. Therefore, umbilical deposits in a patient who has previously been treated for a gynecologic malignancy may be an umbilical metastasis. The presence of umbilical metastasis usually represents advanced metastatic disease with an associated poor prognosis. The average survival time is 11 months. Only 13.5% of patients with umbilical metastasis are alive after 2 years, thus emphasizing the ominous significance of this metastatic location.7,10,12,19,23,25,37,38,51 One patient10 was alive 18 © 1998 Blackwell Science Ltd

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years after the appearance of the umbilical metastasis. Long-term survival can occur when the nodule of the umbilicus is a solitary metastasis; in these patients, aggressive surgery and chemotherapy are warranted.25

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Umbilical metastasis or Sister Mary Joseph’s nodule may be the first presenting sign in a patient with an unknown malignant disease. In a man, metastatic adenocarcinoma of the umbilicus is most often related to the stomach; metastatic squamous cell carcinoma is usually related to the lung or the penis. In a woman, the main primary tumor is an ovarian adenocarcinoma; a squamous cell carcinoma is usually related to the cervix. The metastatic process to the umbilicus through the lymph ducts and the venous network seems to play the main role in the genesis of Sister Mary Joseph’s nodule: the umbilicus is a point of intersection between anterograde and retrograde dissemination of the neoplastic cells. Umbilical metastasis is usually associated with extensive metastatic disease and the prognosis is poor; however, long-term survival is possible if Sister Mary Joseph’s nodule is a solitary metastasis.

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Tatto art by Kandi Everett, Honolulu, Hawaii. From the world of Tattoos Collection, Norman Goldstein, MD, Honolulu, Hawaii.

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