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10.12688/f1000research.110362.2
Case Report
Articles
Case Report: Incidental discovery of primary peritoneal psammocarcinoma
[version 2; peer review: 2 approved

Helal Imen Conceptualization Project Administration Validation Writing – Original Draft Preparation Writing – Review & Editing 12
Khanchel Fatma Methodology Visualization 12
Jouini Raja Methodology Visualization 12
Ben Thayer Maissa Formal Analysis Investigation https://orcid.org/0000-0002-8599-0888
a12
Mbarki Chaouki Investigation 23
Bettaieb Hajer Investigation 23
Rebii Saber Investigation 24
Ben Ismail Imen Investigation https://orcid.org/0000-0003-4924-3620
24
Ben Brahim Ehsen Methodology 12
Chedli-Debbiche Aschraf Methodology Supervision Validation 12
1 Department of Pathology, Habib Thameur Hospital, Tunis, 1008, Tunisia
2 Faculty of medicine of Tunis, Tunis El Manar University, Tunis, 1007, Tunisia
3 Department of Obstetrics and Gynecology, Yasminette's hospital, Ben Arous, 2063, Tunisia
4 Department of Surgery, Center for Traumatology and Major Burns, Ben Arous, 2013, Tunisia
a benthayerm@hotmail.com
No competing interests were disclosed.

16 10 2023
2022
11 69611 10 2023
Copyright: © 2023 Helal I et al.
2023
https://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Psammocarcinoma is an uncommon subtype of low-grade serous carcinoma. It is characterized by the presence of extensive psammoma bodies and can have either an ovarian or peritoneal origin. To our knowledge fewer than 30 cases of primary peritoneal psammocarcinoma (PPP) have been reported in the English literature. We report a rare case of  PPP in a 74-year-old female, discovered fortuitously within a laparotomy for gallbladder lithiasis. At laparotomy, multiple nodular implants involving the omentum, the peritoneum and a magma of intestinal loops in the right iliac fossa were noted. A biopsy from nodules was performed. Gross examination showed multiple nodules of different sizes in the fat tissue. Pathologic examination showed massive psammoma bodies representing more than 75% of the tumor. The final diagnosis was psammocarcinoma. Our patient was referred to the gynecologic department for further investigation and to ascertain whether the tumor arose from the ovaries or peritoneum. Hysterectomy, bilateral adnexectomy and omentectomy were performed. Macroscopic examination showed that both ovaries were intact having a normal size. No invasion of ovarian stroma was shown in microscopic examination. The patient died of SARS-CoV-2 (COVID-19) six days after the surgery.

PPP is a rare type of  low-grade serous carcinoma. The behavior of this tumor is unclear, and the treatment is not standardized because of its rarity and lack of long-term follow-up. More cases need to be studied for better understanding and improvement of the management protocols.

Primary peritoneal psammocarcinoma
psammocarcinoma
serous carcinoma
psammomatous bodies
case report
The author(s) declared that no grants were involved in supporting this work.Revised Amendments from Version 1

In accordance with the reviewers’ recommendations, minor modifications were made: The title was changed from “Case Report: Fortuitous discovery of primary peritoneal psammocarcinoma” from to “Case Report: Incidental discovery of primary peritoneal psammocarcinoma”.

Some parts of the abstract were reworded.

A more detailed description of the histological lesions was provided.

Prognosis, therapeutic strategies, and indications for adjuvant treatment, were discussed in detail in the revised version of the manuscript.
==== Body
pmcIntroduction

Psammocarcinoma, firstly reported by Kettle et al in 1916, is an extremely rare low-grade serous carcinoma. 1 , 2 Its diagnostic criteria have been clearly established, 74 years later, by Gilks et al. 1 Psammocarcinoma can arise from either the ovary or peritoneum. Primary peritoneal psammocarcinomas (PPP) are less common than ovarian psammocarcinomas, since fewer than 30 cases of PPP have been reported in the English literature. 3 – 6 In the majority of cases, PPP has a favorable prognosis, although some may show recurrences and metastases. 7 We report a rare case of primary peritoneal psammocarcinoma (PPP) in a 74-years-old female, discovered incidentally during a surgery for gallbladder lithiasis.

Case presentation

A 74-year-old postmenopausal woman, presented to the emergency department with fever and right upper abdominal pain. The patient, a Caucasian housewife, had no significant personal or family medical history. Physical examination on admission revealed tenderness and guarding of the right hypochondrium and a fever with a temperature of 38.2 degree Celsius. Her body mass index was 32. Routine laboratory tests were normal except for a leucocytosis and an increased C-reactive protein (CRP) level. Abdominal ultrasonography showed a lithiasic gallbladder with thickened walls (see Figure 1). The patient was referred to the surgery department for cholecystectomy for acute lithiasic cholecystitis.

Figure 1. Abdominal ultrasound.

The walls of the gallbladder (GB) are thickened, hyperechoic with a mobile gallstone.

At coelioscopy, multiple nodular implants involving the omentum, the peritoneum and a magma of intestinal loops in the right iliac fossa were noted. The nodules were sampled. Gross examination showed multiple nodules of different sizes in the fat tissue. Pathologic examination showed massive psammoma bodies representing more than 75% of the tumor invading the peritoneal fibro-adipose tissue (see Figure 2). Some papillary structures and isolated tumoral cells were seen. The epithelial cells had low to moderate nuclear grade features including small nuclei, inconspicuous nucleoli and rare mitoses. We haven’t identified any solid area of epithelial proliferation. Vascular emboli and perineural involvement were absent. The final diagnosis was psammocarcinoma.

Figure 2. Microscopic examination (Hematoxylin and eosin staining ×40).

Numerous psammoma bodies with small epithelial nests (see arrows) invading the peritoneum.

The patient was referred to gynecologic department for further investigation and to ascertain whether the tumor arose from ovaries or peritoneum. A computerized tomography scan was undergone and revealed: an uncomplicated sigmoid diverticulosis, an agglutination of the last ileal loops in contact with the anterior abdominal wall, an infiltration of the mesenteric fat and multiple mesenteric lymphadenopathies (see Figure 3). Hysterectomy, bilateral adnexectomy, omentectomy and lymph node dissection were performed. Macroscopic examination showed that both ovaries were intact, with a normal size (see Figure 4). No invasion of ovarian stroma was shown in microscopic examination. No lymph node invasion or distant metastasis had been identified. The final diagnosis was primary peritoneal psammocarcinoma (PPP). It was classified as stage III C carcinoma according to the International Federation of Gynecology and Obstetrics’ (FIGO) classification.

Figure 3. Abdominal computerized tomography scan.

Agglutination of the last ileal loops in contact with the anterior abdominal wall (see arrow), infiltration of the mesenteric fat and multiple mesenteric lymphadenopathies.

Figure 4. Macroscopic examination showed both ovaries with the circles indicating the normal size.

After a multidisciplinary meeting, the decision was made to complete the treatment by adjuvant chemotherapy. The patient died of SARS-CoV-2 (COVID-19), six days after the surgery. The diagnosis of COVID-19 was confirmed by a PCR test and a Computed Tomography.

Discussion

Psammocarcinomas of the peritoneum and the ovary are rare serous carcinomas sharing the same histologic characteristics, histogenesis, and treatment modalities. 8 PPP is an extremely rare peritoneal carcinoma. To the best of our knowledge, less than 30 cases of PPP have been reported in the literature. 3 – 6

The mean age for diagnosis in PPP is 52.1 years, ranging from 27 to 83 years. 9 Clinically, patients usually present with nonspecific symptoms, such as abdominal discomfort, increase in abdominal girth, nausea, or vomiting. 10 In 40% of cases, PPP is asymptomatic and is discovered incidentally, 11 similar to our case and the case described by Grinaldi et al. 3

The diagnosis of PPP is based on histopathological findings. First, Gilks et al defined psammocarcinoma by the association of four specific histologic criteria: (i) a destructive invasion of ovarian stroma, a vascular invasion, or, in the extraovarian cases, an invasion of intraperitoneal viscera; (ii) a mild to moderate nuclear atypia; (iii) an absence of area of solid epithelial proliferation, except for occasional nests with no more than 15 cells in diameter; (iv) at least 75% of papillae associated with or totally replaced by psammoma bodies. 1 , 3

Then, in 1994, Chen et al adapted the diagnostic criteria established by Gilks et al and had added the presence of an invasive pattern of the peritoneum, as a supplementary diagnosis criterion for the diagnosis of PPP. 12 Our case fulfilled all the criteria defined by Gilks and updated by Chen et al.

It is sometimes arduous to specify whether the psammocarcinoma is of peritoneal or ovarian origin. In such cases, only histologic examination can differentiate PPP from ovarian psammocarcinoma. The most important feature is ovarian stromal invasion seen in ovarian psammocarcinoma. 1 , 13 , 14 In PPP, psammoma bodies and nests of tumor cells may be seen in the serosal surface of ovaries but without any invasion of ovarian stroma.

We have faced such difficulties in the case we present. For our patient, both ovaries were of normal size, small nests and psammoma bodies were present in serosal surface of ovaries but ovarian stroma was intact. The peritoneal involvement was greater than the involvement on the ovarian surface. Therefore, the diagnosis of PPP was confirmed.

The main differential diagnoses of PPP include the other epithelial serous neoplasms, such as cystadenofibromas and serous borderline tumors. 9 These tumors may present abundant psammoma bodies, but the invasion of surrounding structures excludes these diagnoses. Low-grade serous carcinoma with numerous psammomatous bodies is another differential diagnosis. The presence of several nests of more than 15 cells precludes the diagnosis of psammocarcinoma. The presence of marked nuclear atypia and numerous figures of mitosis distinguishes high-grade serous carcinoma from PPP.

Mesothelioma with massive psammoma bodies may simulate PPP but negativity of D2-40, calretinin and CK5/6 excludes the diagnosis of mesothelioma. 15

Calcified leiomyomatosis peritonealis disseminata (LPD), an infrequent subtype of leiomyomatosis occurring amongst young women with history of myomectomy, is another differential diagnosis of PPP. 16 We could rule out this diagnosis since our patient was 74 years-old with no history of myomectomy.

Given the rarity of theses tumors, management protocols are not standardized due to the rarity of these tumors. 17 Maximal cytoreductive surgery with hysterectomy, bilateral salpingo-oophorectomy and omentectomy, is the recommended treatment in the first instance. 1 , 16 , 17 For young women, conservative surgery can be discussed to preserve fertility. 3 Chemotherapy is thought to have a poor efficiency in PPP. 16 Chemotherapy is thought to have a poor efficiency in PPP. 16 In fact, recurrences were recorded in some patients who had received adjuvant chemotherapy. 5 However, follow-up adjuvant chemotherapy and hormonotherapy (tamoxifen), may be an option for residual diseases, PPP with aggressive behavior, and in case of recurrence, with positive results. 7 , 17 , 18 The chemotherapy protocols consisted of cyclophosphamide with cisplatin or carboplatin. 7 , 17 Complete response was obtained after adjuvant chemotherapy in an aggressive residual PPP in the case reported by Takahashi et al. 7 Complete response was also seen after the administration of Tamoxifen therapy in a recurrent PPP. 19

Given their rarity, we do not dispose enough elements to judge the scalability of PPPs. However, PPP is likely to have a high potential towards peritoneal recurrence, even after suitable treatment. 20 Some of the reported cases had developed several recurrences with a period of more than 5 or 10 years between those recurrences. 8

Although most of PPP seem to display an indolent clinical course, some may be very aggressive, with distant metastases. 7

One of the strengths of our study is that we were able to demonstrate with certainty that the primary origin of the psammocarcinoma was peritoneal and not ovarian. However, its major limitation consists in the lack of follow-up. In fact, since our patient had died of COVID-19 six days after the second surgery, we were not able to assess the response to treatment, the risk of recurrence and metastases and the prognosis of this tumor. The patient’s obesity might be a factor that favored the COVID-19 related early post operative death.

Conclusions

PPP is a rare type of low-grade serous carcinoma. The behavior of this tumor is unclear, and the treatment is not standardized because of its rarity and lack of long-term follow-up. The investigation of supplementary cases is imperative for a better comprehension of this entity and for the enhancement of management protocols.

Data availability

All data underlying the results are available as part of the article and no additional source data are required.

Consent

Written informed consent for publication of their clinical details and clinical images was obtained from the patient’s family.

10.5256/f1000research.157236.r271805
Reviewer response for version 2
Sapna Fnu 1Referee
1 Anatomic and Clinical Pathology, Montefiore Medical Center, Albert Einstein School of Medicine, Bronx, New york, USA
6 9 2024 Copyright: © 2024 Sapna F
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Version 2recommendationapprove-with-reservations
- History of SARS-CoV-2 infection is unclear. was the patient had SARS CoV-2 diagnosed before surgery? 

- No any pelvic imaging (CT/MRI) has been described before attempting hysterectomy and bilateral oophorectomy. 

- Data regarding presentation and treatment is insufficient. Can be added more. 

Additionally also there are few sentences can be rephrased. 

There is doubling of a sentence. I would suggest to make sure to correct all the typos and necessary edits. 

- Sizes of nodules in centimeters should be provided. It might affect the recurrence rate. 

Are enough details provided of any physical examination and diagnostic tests, treatment given and outcomes?

No

Is the case presented with sufficient detail to be useful for other practitioners?

Partly

Is sufficient discussion included of the importance of the findings and their relevance to future understanding of disease processes, diagnosis or treatment?

Partly

Is the background of the case’s history and progression described in sufficient detail?

Partly

Reviewer Expertise:

Gynecologic and Breast Pathology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

10.5256/f1000research.157236.r215712
Reviewer response for version 2
Braham Marouen 1Referee https://orcid.org/0000-0002-8861-3471

1 Aziza Othmana University hospital, Tunis, Tunisia
3 9 2024 Copyright: © 2024 Braham M
2024
https://creativecommons.org/licenses/by/4.0/ This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Version 2recommendationapprove
Most corrections have been made . the paper is ready for indexing in this new version.

Are enough details provided of any physical examination and diagnostic tests, treatment given and outcomes?

Partly

Is the case presented with sufficient detail to be useful for other practitioners?

Yes

Is sufficient discussion included of the importance of the findings and their relevance to future understanding of disease processes, diagnosis or treatment?

Partly

Is the background of the case’s history and progression described in sufficient detail?

Yes

Reviewer Expertise:

Reproductive Medicine / Gynecology Surgery / Fertility preservation

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

10.5256/f1000research.157236.r215711
Reviewer response for version 2
Otsuka Isao 1Referee https://orcid.org/0000-0002-5136-3050

1 Kameda Medical Center, Kamogawa, Chiba Prefecture, Japan
26 10 2023 Copyright: © 2023 Otsuka I
2023
https://creativecommons.org/licenses/by/4.0/ This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Version 2recommendationapprove
The revisions are appropriate, however, I have only one comment. As the title has been changed, the word "fortuitous" should be replaced by "incidental" in the abstract.

Are enough details provided of any physical examination and diagnostic tests, treatment given and outcomes?

Partly

Is the case presented with sufficient detail to be useful for other practitioners?

Partly

Is sufficient discussion included of the importance of the findings and their relevance to future understanding of disease processes, diagnosis or treatment?

Yes

Is the background of the case’s history and progression described in sufficient detail?

Partly

Reviewer Expertise:

gynecologic oncology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

10.5256/f1000research.121959.r195525
Reviewer response for version 1
Otsuka Isao 1Referee https://orcid.org/0000-0002-5136-3050

1 Kameda Medical Center, Kamogawa, Chiba Prefecture, Japan
29 8 2023 Copyright: © 2023 Otsuka I
2023
https://creativecommons.org/licenses/by/4.0/ This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Version 1recommendationapprove-with-reservations
The authors report a case of primary peritoneal psammocarcinoma (PPP) incidentally discovered during a laparotomy (written in Abstract) for gallbladder lithiasis. After the coelioscopy (written in Case Presentation), the patient underwent surgical staging consisting of hysterectomy, bilateral adnexectomy, and omentectomy. The patient died six days after the surgery.

This manuscript reports a rare case of stage IIIC PPP. Some flaws need to be revised.

Major comments The authors wrote, "Macroscopic examination showed that both ovaries were intact having a normal size (see Figure 4)." However, "small nests and psammoma bodies were present in serosal surface of ovaries." Papillary excrescences may be seen on the surface of both ovaries (Figure 4). Were both ovaries truly intact on macroscopic examination?

Was the surgery for gallbladder lithiasis a laparotomy or a laparoscopy? (see above)

The authors wrote, "No lymph node invasion." Was lymphadenectomy performed?

The authors need to explain factors associated with early post-operative death due to COVID-19 infection. What was her body mass index (Figure 3 may indicate the patient was obese)?

The title of this case report is "Fortuitous discovery of PPP". However, the patient died six days after the surgical staging for stage IIIC PPP. As the word fortuitous implies "advantage [Cambridge Dictionary]", the title might be changed.

Minor comments Case presentation. a temperature of 38.2 degrees "Celsius".

Figure 2. Where is the arrow?

Figure 3. The figures should carry an arrow pointing to "agglutination of the last ileal loops."

Are enough details provided of any physical examination and diagnostic tests, treatment given and outcomes?

Partly

Is the case presented with sufficient detail to be useful for other practitioners?

Partly

Is sufficient discussion included of the importance of the findings and their relevance to future understanding of disease processes, diagnosis or treatment?

Yes

Is the background of the case’s history and progression described in sufficient detail?

Partly

Reviewer Expertise:

gynecologic oncology

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Ben Thayer Maissa faculty of medecine of tunis, Tunisia

8 10 2023 We are very grateful for your precious time and effort in reviewing our paper and providing valuable comments. The authors have carefully considered the comments and tried our best to address every one of them. We have incorporated most of the suggestions. We hope the manuscript after careful revisions will meet your high standards. The authors welcome further constructive comments and feedback. Point-by-point response to the reviewer’s comments and concerns are provided below. The adjustments were highlighted in yellow in the revised manuscript. The authors wrote “Macroscopic examination showed that both ovaries were intact having a normal size. However, “small nests and psammoma bodies were present in serosal surface of ovaries”. Were both ovaries truly intact on macroscopic examination?

Authors’ response:  As shown in Figure 4, there were no macroscopically detectable abnormalities in either ovary. The psammomas observed on the surface of the ovaries on microscopic examination are sub-millimetric and cannot be visualized with the naked eye. Was the surgery for gallbladder lithiasis a laparotomy or a laparoscopy?

Authors’ response:  The cholecystectomy was performed laparoscopically. The authors wrote “No lymph node invasion. Was lymphadenectomy performed?

Authors’ response:  A lymph node dissection was performed. We added this detail in the case presentation’s description in the revised version. The authors need to explain factors associated with early post-operative death due to the COVID-19 infection. What was her body mass index?

Authors’ response:  We discussed factors favoring the early post-operative death due to the COVID-19 infection. Indeed, the patient was obese with a BMI of 32. The title of this report is “Fortuitous discovery of PPP”. However, the patient died six days after the surgical staging for PPP. As the word fortuitous implies ‘advantage’, the title might be changed.

     Authors’ response:  We replaced the title in the revised version by “Case             Report: Incidental discovery of primary peritoneal psammocarcinoma” Case presentation: a temperature of 38.2 degrees “Celsius”

Authors’ response:  The term “Celsius” was added in the revised manuscript. Figure 2: where is the arrow?

Authors’ response:  the arrow was added in Figure 2 Figure 3: the figure should carry out an arrow pointing the agglutination of the last ileal loops.

Authors’ response:  The arrow pointing the agglutination of the last ileal loops was added in Figure 3.

10.5256/f1000research.121959.r144608
Reviewer response for version 1
Braham Marouen 1Referee https://orcid.org/0000-0002-8861-3471

1 Aziza Othmana University hospital, Tunis, Tunisia
22 8 2022 Copyright: © 2022 Braham M
2022
https://creativecommons.org/licenses/by/4.0/ This is an open access peer review report distributed under the terms of the Creative Commons Attribution Licence, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Version 1recommendationapprove-with-reservations
This case report shows the approach in front of a suspicion of peritoneal psammocarcinoma, diagonostic difficulty and etiological research, the subject is interesting because primary peritoneal psammocarcinoma is a very rare pathology and the diagnosis is not obvious.

Recommendations: Could you add pictures from the 1st or 2nd surgery?

Could you elaborate on the anatomopathological examination with more detailed description?

Regarding the discussion, could you note the prognosis in the literature and chemotherapy used in theses cases?

Are enough details provided of any physical examination and diagnostic tests, treatment given and outcomes?

Partly

Is the case presented with sufficient detail to be useful for other practitioners?

Yes

Is sufficient discussion included of the importance of the findings and their relevance to future understanding of disease processes, diagnosis or treatment?

Partly

Is the background of the case’s history and progression described in sufficient detail?

Yes

Reviewer Expertise:

Reproductive Medicine / Gynecology Surgery / Fertility preservation

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

Ben Thayer Maissa faculty of medecine of tunis, Tunisia

8 10 2023 We are very grateful for your precious time and effort in reviewing our paper and providing valuable comments. The authors have carefully considered the comments and tried our best to address every one of them. We have incorporated most of the suggestions.  We hope the manuscript after careful revisions will meet your high standards. The authors welcome further constructive comments and feedback. Point-by-point response to the reviewer’s comments and concerns are provided below. The adjustments were highlighted in yellow in the revised manuscript. Could you add pictures from the first and second surgery?

Authors’ response:  Unfortunately, no intraoperative images were available. We had to make do with the photos taken during the gross examination. Could you elaborate on the anatomopathological examination with a more detailed description?

Authors’ response:  A more detailed description of the histological lesions was provided in the revised version of the manuscript. Regarding the discussion, could you note the prognosis in the literature and chemotherapy used in this case?

Prognosis, therapeutic strategies, and indications for adjuvant treatment, including chemotherapy, were discussed in detail in the revised version.

Competing interests: No competing interests were disclosed.

Competing interests: No competing interests were disclosed.

Competing interests: No competing interests were disclosed.

Competing interests: No competing interests were disclosed.

Competing interests: No competing interests were disclosed.

Competing interests: No competing interests were disclosed.

Competing interests: No competing interests were disclosed.
==== Refs
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