Pattern of triple negative epithelial ovarian cancer in indigenous African women<b> </b>

Mustapha Akanji Ajani; Ayodeji Akeem Salami; Olutosin Alaba Awolude; Abideen Olayiwola Oluwasola

doi:10.12688/f1000research.9632.1

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Research Note

Pattern of triple negative epithelial ovarian cancer in indigenous African women

[version 1; peer review: 2 approved]

Mustapha Akanji Ajani¹, Ayodeji Akeem Salami¹, Olutosin Alaba Awolude², Abideen Olayiwola Oluwasola¹

PUBLISHED 28 Sep 2016

Author details Author details

¹ Department of Pathology, University College Hospital, Ibadan, Nigeria
² Department of Obstetrics and Gynaecology, University College Hospital, Ibadan, Nigeria

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Abstract

Background: Triple negative epithelial ovarian cancer (TNEOC) refers to ovarian carcinomas that do not express estrogen receptor (ER), progesterone receptor (PR) and human epidermal growth factor receptor- type 2 (HER-2/neu). The aim of this study is to determine the pattern of triple negative epithelial ovarian cancer in indigenous African women.

Methods: We performed a retrospective review of ER, PR and HER-2/neu expression in 90 Nigerian patients with histologically diagnosed epithelial ovarian cancer. Lack of expression of ER, PR and HER2/neu antigens was used to determine carcinomas that are among the TNEOC. We also compared the clinicopathological parameters (age, International Federation of Gynaecology and Obstetrics (FIGO) stage, grade and histological subtype) in patients with TNEOC and non- TNEOC .

Results: Thirty-eight (42.2%) of the 90 tumours diagnosed as EOC were negative for ER, PR and HER2/neu expression. There was no significant association between TNEOC with other parameters such as age, FIGO stage and histological grade. Sixteen (66.7%) of the 24 mucinous carcinomas were triple negative, while only 21 (33.3%) of the 63 serous carcinomas were triple-negative and one (50%) of the two endometrioid carcinomas was triple negative. There was a significant association between triple-negative tumours and histological subtypes of EOC (p = 0.034).

Conclusions: A subtype of epithelial ovarian cancer that is negative for ER, PR and HER-2/neu has been discovered in indigenous African women. TNEOC expression is high and is comparable to the triple negative breast cancer subtype seen in people of African ancestry. Future study of TNEOC in a large sample size should be considered.

Keywords

Estrogen Receptor, HER-2/neu expression, Immunohistochemistry, Ovarian carcinoma, Progesterone Receptor, Triple negative

Corresponding author: Mustapha Akanji Ajani

Competing interests: No competing interests were disclosed.

Grant information: The authors declared that no grants were involved in supporting this work.

Copyright: © 2016 Ajani MA et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication).

How to cite: Ajani MA, Salami AA, Awolude OA and Oluwasola AO. Pattern of triple negative epithelial ovarian cancer in indigenous African women [version 1; peer review: 2 approved]. F1000Research 2016, 5:2415 (https://doi.org/10.12688/f1000research.9632.1) First published: 28 Sep 2016, 5:2415 (https://doi.org/10.12688/f1000research.9632.1) Latest published: 28 Sep 2016, 5:2415 (https://doi.org/10.12688/f1000research.9632.1)

Introduction

Epithelial ovarian cancer (EOC) remains one of the leading causes of death in gynaecological malignancies in developed countries^1–4. The initial symptoms of ovarian cancer are often ambiguous, therefore it goes undiagnosed until after the disease is far advanced and has spread throughout the abdomen or to distant organs^5,6.

Steroid hormone receptors expression in epithelial ovarian cancers have been proposed to have therapeutic and prognostic relevance, as is the case in breast cancers⁷. The determination of tumour characteristics such as age, International Federation of Gynaecology and Obstetrics (FIGO) stage, grade and histological subtypes has been associated with clinical behaviour and impact on treatment and prognosis but have been found to be limited⁸. Among the biological parameters proposed as possible prognostic factors in ovarian cancer, estrogen receptor (ER), progesterone receptor (PR) and human epidermal growth factor receptor- type 2 (HER-2/neu) have been tested as potential biomarkers that guide individualized treatment of the cancer^5,6,9. Epithelial ovarian carcinoma results from repeated ovulations, where the cumulative effects of each minor trauma on the ovarian epithelium can lead to malignant transformation¹⁰. PR has been observed to predict better prognosis because of its protection against ovarian carcinoma development^11,12. On the other hand, overexpression of ER has been found to be associated with poor prognosis due to its contribution to initiation and/or promotion of ovarian carcinogenesis^10,13. The HER-2/neu has been shown to be over-expressed in approximately 20–30% of EOC with associated poor prognosis^14–16.

Triple negative epithelial ovarian cancer (TNEOC) cases have been found to be more aggressive and display a worse prognosis than non-TNEOC cases¹⁷. This was similarly observed in the studies of triple negative breast cancer^18,19.

This study was designed to determine the pattern of TNEOC among indigenous African women and correlate it with clinicopathological parameters.

Methods

Patient selection

We performed a retrospective review of ER, PR and HER-2/neu expression in 90 patients with histologically diagnosed epithelial ovarian cancer seen at the University College Hospital, Ibadan, Nigeria between January 2006 and December 2012. Non-epithelial primary ovarian cancers and metastatic cancers in the ovary were not included in this study. The demographic data and clinical history of these cases were obtained from the case notes, surgical daybooks, surgical pathology request forms, post-mortem records and Cancer Registry data. Formalin-fixed paraffin-embedded tissue blocks of histologically diagnosed solid EOC between January 2006 and December 2012 were retrieved and used for the study. The microscopic grading (three-grade system) of Shimizu and Silverberg was used, which assesses architectural pattern, nuclear pleomorphism and mitotic activity²⁰. All histological classification of the EOC was based on the 2013 World Health Organisation (WHO) classification of ovarian tumours²¹. The FIGO staging of the cases used for this study was extracted from the case notes of the patients.

Ethics

The ethical clearance for this study was obtained from the Joint University of Ibadan/University College Hospital Ethical Review Committee (approval number UI/EC/13/0050) according to the Declaration of Helsinki.

Immunohistochemistry

The immunostaining procedure for HER-2/neu was carried out in accordance with the previously published article²². For the immunostaining procedure, three sections each for ER, PR and HER-2/neu at 5µm were cut from each of the paraffin-embedded tissue blocks after deparaffinization in xylene (two aliquots for five minutes each with the xylene covering the slide entirely). The sections were then rehydrated in graded alcohol concentrations (two aliquots each of 100% and 95% each and a single aliquot of 70%) in 250ml couplin jars. The antibodies used were monoclonal mouse anti-human ERα (Dako USA; clone ID5) and monoclonal mouse anti-human PR (Dako USA; clone PgR636) which identify the ER and PR nuclear protein antigens. The primary antibody used for HER-2/neu antigen was polyclonal rabbit anti-human C-erbB-2 (MBO/TEG, Dako USA, 1:800). The tissue sections were immersed in EDTA buffer (pH 9.0) for ER, citrate buffer (pH 6.0) for PR and in 1M Tris buffer (pH 9.0) for HER-2/neu. These slides were then incubated at room temperature for 20 minutes with primary monoclonal antibodies against ER (Dako USA, clone 1D5; 1:50), PR (Dako USA, clone PgR636; 1:50) and polyclonal rabbit anti-human C-erbB-2 (MBO/TEG, Dako USA, 1:800) followed by incubation in biotin-labelled secondary antibodies, polyclonal goat anti-mouse antibody for both ER and PR, (Dako USA, REF: K0675, LOT: 10081219) and polyclonal goat anti-rabbit antibody for HER-2/neu, (kitR, K5001, Dako Denmark) for 20 minutes and streptavidin-peroxidase complex (Dako USA, REF: K0675, LOT: 10084687) for another twenty minutes. The antigen-antibody complex was precipitated with di-aminobenzidine (DAB) for light microscopy with DAB substrate and DAB chromogen in the ratio of 1ml to 1 drop respectively. This was thereafter counterstained in Mayer’s haematoxylin (Dako USA). Dehydration of the sections was performed in ascending grades of alcohol and cleared in xylene. The slides were coversliped with DPX mountant. Known cases of breast cancer with positive reactions for ER, PR and HER-2/neu were used as a positive control. Negative controls were cases of tumour sections that were pretreated in Tris but without primary antibody immunostaining. All slides were reviewed independently by the three of the authors and cases with discordant scores were re-evaluated to have a consensus score. Grading of nuclear ER and PR staining was performed using an immunoreactive H-scoring system {none= 0 (negative); 1–25%=1+ (weak); 26–50%=2+ (moderate); >50%=3+(strong)}¹¹. HER-2/neu membrane staining was graded in according to the Hercep Test protocol system as 0, 1+, 2+ or 3+. Samples scored as 0 or 1+ were considered negative for HER-2/neu overexpression, 2+ was weakly positive and 3+ was strongly positive^22,23. Photomicrographs of the specimens were taken using Olympus digital camera, DP 21 at 400X magnification (Figure 1).

Figure 1. Photomicrographs showing ER (left), PR (middle) and HER-2/neu (right) negative expression (TNEOC) (immunostaining, 400X).

Statistical analysis

The data obtained were subjected to statistical analysis using Statistical Package for Social Sciences (SPSS) version 20. Statistical analysis was used to evaluate statistical associations between TNEOC and clinicopathological parameters i.e. age, FIGO stage grade, and histological subtypes. Continuous variables were compared using the student’s T test and categorical variables were compared using the chi-square test, with the level of significance set at p <0.05.

Results

RAW DATA FOR PATTERN OF TRIPLE NEGATIVE EPITHELIAL OVARIAN CANCERS IN INDIGENOUS BLACK WOMEN
S/NO	AGE/years	BIOPSY SIDE	HISTOLOGICAL DIAGNOSIS	FIGO Stage	Histological Grading	Estrogen receptor (ER)	Progesterone receptor (PR)	HER-2/neu
1	55	Right	SEROUS CARCINOMA	II	II	negative	negative	negative
2	31	Right	MUCINOUS CARCINOMA	II	I	negative	negative	negative
3	72	Bilateral	SEROUS CARCINOMA	II	II	negative	weakly positive	weakly positive
4	50	Right	SEROUS CARCINOMA	II	I	weakly positive	strongly positive	strongly positive
5	59	Right	SEROUS CARCINOMA	II	I	strongly positive	negative	negative
6	60	Right	SEROUS CARCINOMA	II	II	negative	negative	strongly positive
7	44	Left	MUCINOUS CARCINOMA	I	II	negative	negative	negative
8	36	Right	SEROUS CARCINOMA	III	III	negative	negative	negative
9	52	Bilateral	SEROUS CARCINOMA	II	III	weakly positive	strongly positive	weakly positive
10	75	Bilateral	SEROUS CARCINOMA	III	II	negative	negative	negative
11	65	Left	SEROUS CARCINOMA	IV	III	weakly positive	weakly positive	strongly positive
12	48	Left	MUCINOUS CARCINOMA	II	I	negative	negative	weakly positive
13	54	Right	SEROUS CARCINOMA	II	III	weakly positive	negative	negative
14	37	Right	MALIGNANT BRENNER TUMOUR	I	I	strongly positive	negative	strongly positive
15	61	Bilateral	SEROUS CARCINOMA	II	II	strongly positive	weakly positive	weakly positive
16	43	Right	SEROUS CARCINOMA	II	I	negative	weakly positive	negative
17	41	Right	SEROUS CARCINOMA	IV	III	negative	negative	negative
18	49	Right	MUCINOUS CARCINOMA	III	II	negative	negative	negative
19	40	Left	MUCINOUS CARCINOMA	III	II	negative	weakly positive	negative
20	50	Right	SEROUS CARCINOMA	IV	III	negative	negative	strongly positive
21	26	Left	SEROUS CARCINOMA	II	III	negative	negative	negative
22	45	Bilateral	ENDOMETRIOID CARCINOMA	I	II	negative	negative	negative
23	30	Right	SEROUS CARCINOMA	IV	III	negative	negative	negative
24	47	Left	SEROUS CARCINOMA	III	III	negative	weakly positive	negative
25	38	Left	SEROUS CARCINOMA	II	II	weakly positive	strongly positive	negative
26	48	Left	SEROUS CARCINOMA	III	II	negative	strongly positive	strongly positive
27	45	Left	SEROUS CARCINOMA	II	II	weakly positive	weakly positive	negative
28	70	Right	SEROUS CARCINOMA	II	III	weakly positive	negative	negative
29	35	Bilateral	MUCINOUS CARCINOMA	III	III	weakly positive	negative	negative
30	53	Right	MUCINOUS CARCINOMA	IV	II	negative	negative	weakly positive
31	42	Bilateral	SEROUS CARCINOMA	III	I	negative	negative	negative
32	75	Bilateral	MUCINOUS CARCINOMA	III	I	negative	negative	negative
33	55	Bilateral	SEROUS CARCINOMA	IV	I	negative	negative	negative
34	50	Bilateral	SEROUS CARCINOMA	IV	III	strongly positive	negative	negative
35	65	Bilateral	SEROUS CARCINOMA	III	II	negative	negative	negative
36	49	Right	SEROUS CARCINOMA	III	III	strongly positive	srong	strongly positive
37	50	Right	SEROUS CARCINOMA	IV	III	negative	weakly positive	strongly positive
38	45	Left	SEROUS CARCINOMA	III	III	weakly positive	strongly positive	strongly positive
39	52	Left	SEROUS CARCINOMA	II	II	weakly positive	negative	negative
40	56	Right	SEROUS CARCINOMA	II	III	negative	negative	negative
41	46	Bilateral	MUCINOUS CARCINOMA	II	II	negative	strongly positive	negative
42	16	Bilateral	MUCINOUS CARCINOMA	II	II	negative	negative	negative
43	55	Left	MUCINOUS CARCINOMA	II	I	negative	negative	negative
44	59	Bilateral	SEROUS CARCINOMA	III	I	negative	negative	negative
45	69	Bilateral	SEROUS CARCINOMA	III	III	weakly positive	weakly positive	weakly positive
46	47	Bilateral	SEROUS CARCINOMA	III	II	negative	negative	negative
47	82	Right	MUCINOUS CARCINOMA	II	III	negative	negative	negative
48	44	Left	MUCINOUS CARCINOMA	II	I	negative	negative	negative
49	44	Right	ENDOMETRIOID CARCINOMA	II	II	negative	strongly positive	weakly positive
50	60	Left	SEROUS CARCINOMA	IV	II	negative	negative	strongly positive
51	32	Right	MUCINOUS CARCINOMA	I	I	negative	negative	negative
52	59	Bilateral	MUCINOUS CARCINOMA	II	II	negative	negative	negative
53	68	Right	SEROUS CARCINOMA	III	III	weakly positive	weakly positive	weakly positive
54	57	Left	SEROUS CARCINOMA	III	III	negative	negative	weakly positive
55	36	Left	MUCINOUS CARCINOMA	I	I	negative	negative	negative
56	49	Right	SEROUS CARCINOMA	I	I	negative	negative	strongly positive
57	39	Left	MUCINOUS CARCINOMA	II	II	negative	negative	negative
58	65	Right	SEROUS CARCINOMA	III	I	negative	negative	negative
59	64	Left	SEROUS CARCINOMA	IV	III	negative	weakly positive	negative
60	75	Bilateral	MUCINOUS CARCINOMA	II	I	weakly positive	negative	strongly positive
61	47	Bilateral	MUCINOUS CARCINOMA	II	II	negative	negative	negative
62	51	Left	SEROUS CARCINOMA	IV	III	negative	negative	negative
63	50	Right	MUCINOUS CARCINOMA	III	III	negative	negative	negative
64	28	Right	SEROUS CARCINOMA	III	III	negative	negative	weakly positive
65	53	Right	SEROUS CARCINOMA	IV	III	negative	negative	negative
66	46	Left	SEROUS CARCINOMA	III	II	weakly positive	weakly positive	negative
67	69	Left	SEROUS CARCINOMA	IV	III	negative	weakly positive	negative
68	40	Right	SEROUS CARCINOMA	III	III	negative	weakly positive	negative
69	75	Right	SEROUS CARCINOMA	III	II	negative	negative	strongly positive
70	52	Right	SEROUS CARCINOMA	III	II	negative	negative	strongly positive
71	47	Bilateral	SEROUS CARCINOMA	IV	III	negative	weakly positive	weakly positive
72	69	Bilateral	MUCINOUS CARCINOMA	I	I	negative	weakly positive	weakly positive
73	56	Bilateral	SEROUS CARCINOMA	II	II	negative	negative	negative
74	66	Right	SEROUS CARCINOMA	II	III	negative	weakly positive	negative
75	40	Left	SEROUS CARCINOMA	II	III	negative	negative	negative
76	60	Right	SEROUS CARCINOMA	II	III	negative	negative	negative
77	54	Bilateral	SEROUS CARCINOMA	III	III	weakly positive	strongly positive	negative
78	54	Right	SEROUS CARCINOMA	IV	II	negative	negative	weakly positive
79	58	Right	MUCINOUS CARCINOMA	II	II	negative	negative	negative
80	53	Bilateral	SEROUS CARCINOMA	IV	II	negative	negative	strongly positive
81	64	Bilateral	SEROUS CARCINOMA	IV	III	strongly positive	strongly positive	strongly positive
82	57	Right	SEROUS CARCINOMA	III	III	negative	negative	negative
83	54	Left	MUCINOUS CARCINOMA	II	I	negative	negative	strongly positive
84	42	Right	SEROUS CARCINOMA	III	III	negative	strongly positive	weakly positive
85	35	Left	SEROUS CARCINOMA	II	II	negative	negative	negative
86	60	Bilateral	SEROUS CARCINOMA	II	II	negative	negative	weakly positive
87	62	Bilateral	SEROUS CARCINOMA	IV	III	negative	strongly positive	strongly positive
88	67	Bilateral	SEROUS CARCINOMA	III	II	negative	negative	negative
89	56	Bilateral	MUCINOUS CARCINOMA	II	II	negative	negative	negative

Dataset 1.Raw data for ‘Pattern of triple negative epithelial ovarian cancer in indigenous African women’.

Thirty-eight (42.2%) of the 90 epithelial ovarian cancers (EOC) were negative for ER, PR and HER-2/neu expression (Figure 1). There was no significant association between triple-negative EOC and age (p = 0.218), FIGO stage (p = 0.425) and histological grade (p= 0.269). There were more TNEOC cases seen in patients older than 40 years than those below 40 years of age. Of 38 cases of TNEOC, 21 (55.3%) were found in the early stage (FIGO stage I and II) of epithelial ovarian cancer and 17 (44.7%) were at the advanced stage.

However, sixteen (66.7%) of the 24 mucinous carcinomas were triple-negative, while only 21 (33.3%) of the 63 serous carcinomas were triple-negative and one (50%) of the two endometrioid carcinomas was triple-negative (Table 1). There was therefore a significant association between triple-negative tumours and histological subtypes of EOC (p = 0.034).

Table 1. Correlation between triple negative epithelial ovarian cancer and clinicopathological parameters.

	TNEOC	Non-TNEOC	Total	P value
Age
<40	9	4	13
>40	29	48	77	0.218
FIGO Stage
I-II	21	22	43
III-IV	17	30	47	0.425
Histological grade
I	10	9	19
II	16	18	34
III	12	25	37
Histological subtypes
Serous Carcinoma	21	42	63
Mucinous Carcinoma	16	8	24
Endometrioid Carcinoma	1	1	2
Malignant Brenner tumour	0	1	1	0.034
Total	38	52	90

Discussion

A subgroup of epithelial ovarian cancer that is negative for ER, PR and HER-2/neu expression has been identified among indigenous African women. This subgroup is known as triple negative epithelial ovarian cancer (TNEOC). According to ER, PR, and HER-2/neu expressions, a breast cancer subtype known as triple negative breast cancer (TNBC) has been identified²⁴.

In our study, triple negative tumours accounted for 42.2% of EOC. This value contrasts with the results of other studies^17,25 and compares with the results of previous study²⁶. A significant percentage (66.7%) of mucinous carcinoma were negative for ER, PR and HER-2/neu and this was statistically significant (p=0.034). This finding contrasts what was found from previous studies where there was no significant association between the TNEOC and histological subtypes^17,25,26. No significant association was also found between the TNEOC and histological grade unlike what was observed by Liu et al.¹⁷ and de Toledo et al.²⁶ where TNEOC was significantly correlated with histological grade. There was no significant association between TNEOC and age and FIGO stage compared to the findings of other studies^17,25,26.

Our findings were comparable with what was found by Huo et al. in the population differences in breast cancer where triple negativity was predominant (27%)¹⁹. In view of the fact that triple-negative breast cancers are more often seen in black Africans and African-Americans and are associated with a poorer prognosis than non-triple-negative breast cancers, further studies of TNEOC in different environments are required.

Conclusions

A subtype of epithelial ovarian cancer that is negative for ER, PR and HER-2/neu has been discovered in Nigeria. Its (TNEOC) expression is high and is comparable to the triple negative breast cancer subtype seen in people of African ancestry. Future study of TNEOC in a large sample size should be considered.

Data availability

F1000Research: Dataset 1. Raw data for ‘Pattern of triple negative epithelial ovarian cancer in indigenous African women’, 10.5256/f1000research.9632.d136777²⁷

Author contributions

MAA conceived and designed the study. MAA, AAS and AOO carried out the research. MAA and AOO prepared the first draft of the manuscript. All authors contributed to the experimental design and preparation of the manuscript. All authors were involved in the revision of the draft manuscript and have agreed to the final content.

Competing interests

No competing interests were disclosed.

Grant information

The author(s) declared that no grants were involved in supporting this work.

Acknowledgements

Special thanks to Mr S Ajagboye and Mr SP Otegbade of the Department of Pathology, University of Ibadan and University College Hospital respectively for the technical assistance they rendered with the slides used for this study and Mr Abayomi Odetunde of Institute for Advanced Medical Research and Training, College of Medicine, University of Ibadan for carrying out the immunohistochemical staining on the cases.

Faculty Opinions recommended

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¹ Department of Pathology, University College Hospital, Ibadan, Nigeria
² Department of Obstetrics and Gynaecology, University College Hospital, Ibadan, Nigeria

Competing interests

No competing interests were disclosed.

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The authors declared that no grants were involved in supporting this work.

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© 2016 Ajani MA et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication).

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Ajani MA, Salami AA, Awolude OA and Oluwasola AO. Pattern of triple negative epithelial ovarian cancer in indigenous African women [version 1; peer review: 2 approved]. F1000Research 2016, 5:2415 (https://doi.org/10.12688/f1000research.9632.1)

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Reviewer Report 13 Oct 2016

Saad Aliyu Ahmed, Department of Pathology, Ahmadu Bello University Teaching Hospital (ABUTH), Zaria, Nigeria

Approved

https://doi.org/10.5256/f1000research.10379.r16697

This is an interesting manuscript, well conceived and has addressed the objective of the research.
The methodology is simple and reproducible.
Result was clearly outlined and discussion

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Reviewer Report 11 Oct 2016

Akinwumi Komolafe, Department of Morbid Anatomy and Forensic Medicine, Obafemi Awolowo University, Ilé-Ifẹ̀, Nigeria

Approved

https://doi.org/10.5256/f1000research.10379.r16923

I have gone through the whole paper and these are my comments:

It is a well conceived and conducted research paper with the aims and objectives and rationale for the study well spelled out.

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VERSION 1 PUBLISHED 28 Sep 2016

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Akinwumi Komolafe, Obafemi Awolowo University, Ilé-Ifẹ̀, Nigeria
Saad Aliyu Ahmed, Ahmadu Bello University Teaching Hospital (ABUTH), Zaria, Nigeria

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Reviewer Report

9 Views

13 Oct 2016 | for Version 1

Saad Aliyu Ahmed, Department of Pathology, Ahmadu Bello University Teaching Hospital (ABUTH), Zaria, Nigeria

9 Views Cite this report Responses(0)

Approved

This is an interesting manuscript, well conceived and has addressed the objective of the research.
The methodology is simple and reproducible.
Result was clearly outlined and discussion was adequate.
Conclusion is apt.

This research finding will add to the few literature on TNEOC in the population studied. It will serve as a baseline for future reference and interestingly the research has prognostic and therapeutic implications.

Competing Interests

No competing interests were disclosed.

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.

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Reviewer Report

9 Views

11 Oct 2016 | for Version 1

Akinwumi Komolafe, Department of Morbid Anatomy and Forensic Medicine, Obafemi Awolowo University, Ilé-Ifẹ̀, Nigeria

9 Views Cite this report Responses(0)

Approved

I have gone through the whole paper and these are my comments:

It is a well conceived and conducted research paper with the aims and objectives and rationale for the study well spelled out.
It addresses the peculiarities of the African race which is fundamental to adequate care.
The authors are very clear and consistent in the message that they aimed to convey and have passed this through.
All parts of the research work have fulfilled the guidelines for sound scientific work.
The discussion addresses crucial details.
The conclusion is a brilliant and excellent summation of the author's scientific work.

Competing Interests

No competing interests were disclosed.

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.

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Pattern of triple negative epithelial ovarian cancer in indigenous African women

Abstract

Keywords

Introduction

Methods

Patient selection

Ethics

Immunohistochemistry

Figure 1. Photomicrographs showing ER (left), PR (middle) and HER-2/neu (right) negative expression (TNEOC) (immunostaining, 400X).

Statistical analysis

Results

Table 1. Correlation between triple negative epithelial ovarian cancer and clinicopathological parameters.

Discussion

Conclusions

Data availability

Author contributions

Competing interests

Grant information

Acknowledgements

References

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