literature review on breast cancer in nigeria

Barriers to Early Presentation and Diagnosis of Breast Cancer in Nigerian Women

Review article
Published: 09 July 2022
Volume 20 , article number 35 , ( 2022 )

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literature review on breast cancer in nigeria

Ibiwumi Damaris Kolawole 1 &
Thomas Prates Ong 1

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Breast cancer is the most occurring cancer and cause of cancer-related death in women globally with over 1.7million new cases and 18% death yearly. Although the incidence rate is almost three times higher in developed countries than developing countries, mortality rates are higher in developing countries. However, this cancer remains a complex disease and leading cause of cancer-related death In Nigerian women.

A compressive search of published articles was conducted on Science direct, Google scholar and PubMed with keywords Breast cancer, global presentation and diagnosis of breast cancer, incidence, burden of breast cancer in Nigeria, developed countries, and developing countries.

In Nigeria, approximately 28,380 new cases and 14,274 deaths of breast cancer were reported in 2020. Currently, breast cancer accounts for almost 26% of all cancer cases in Nigeria with 70% of women presenting at an advanced stage. Certain factors such as inadequate knowledge, poor health care system, cost of treatment, and fear are barriers to early detection of breast cancer in Nigeria and often result in lower survival rate.

Unless breast health education is initiated at both rural and urban areas to correct the misconception of breast cancer, Nigeria women will continue to present late for proper diagnosis and treatment.

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Advanced-stage breast cancer diagnosis and its determinants in Ethiopia: a systematic review and meta-analysis

Global Perceptions of Women on Breast Cancer and Barriers to Screening

Breast Cancer in Pakistan: Screening and Detection

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Acknowledgements

This study was funded by CNPq (Grant number 142373/2019-2).

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Ibiwumi Damaris Kolawole & Thomas Prates Ong

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IDK and TPO were responsible for the review design. IDK and TPO were responsible for data collection and appraising studies. IDK and TPO contributed to drafting the manuscript. IDK and TPO read and approved the final manuscript. TPO supervised the work.

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Kolawole, I.D., Ong, T.P. Barriers to Early Presentation and Diagnosis of Breast Cancer in Nigerian Women. Indian J Gynecol Oncolog 20 , 35 (2022). https://doi.org/10.1007/s40944-022-00637-w

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Received : 28 March 2022

Revised : 24 May 2022

Accepted : 15 June 2022

Published : 09 July 2022

DOI : https://doi.org/10.1007/s40944-022-00637-w

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Breast cancer in Nigeria

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1 Department of Surgery, University College Hospital, Ibadan, Nigeria.
PMID: 11126081

Breast cancer is now the commonest malignancy affecting women in Nigeria. It is likely to become an important public health issue in the next millennium. Recent years have witnessed an explosion in knowledge about the basic sciences of the disease, including the genetic basis and the pathology. These changes are leading to revisions in the management of the disease with a positive impact on prognosis. In this review, the recent developments in the various aspects of breast cancer are reviewed with reference to how they affect the disease in this environment.

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Shading indicates countries that provided terms and translation. The diagram was created with MapChart.

eTable. Characteristics of Survey Participants and Responses

eMethods. Comprehensive Methods for the Study

eFigure. Country Origins of Participants and Their Respective Languages

eAppendix. Survey

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Understanding Global Lived Experiences to Advance Oncology Care JAMA Network Open Invited Commentary August 30, 2024 Sudha Sivaram, DrPH; Satish Gopal, MD, MPH

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Simba H , Mutebi M , Galukande M, et al. Cancer Care Terminology in African Languages. JAMA Netw Open. 2024;7(8):e2431128. doi:10.1001/jamanetworkopen.2024.31128

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Cancer Care Terminology in African Languages

1 Environment and Lifestyle Epidemiology Branch, International Agency for Research on Cancer (IARC), World Health Organization (WHO), Lyon, France
2 Department of Global Health, Stellenbosch University, Cape Town, South Africa
3 Department of Surgery, Aga Khan University, Nairobi, Kenya
4 Department of Surgery, College of Health Sciences, Makerere University, Kampala, Uganda
5 Nutrition and Metabolism Branch, IARC, WHO, Lyon, France
6 Department of Epidemiology and Biostatistics, School of Public Health, Imperial College London, London, United Kingdom
7 Department of Preventive Medicine, School of Public Health, College of Health Sciences, Addis Ababa University, Addis Ababa, Ethiopia
8 Genetics Branch, IARC, WHO, Lyon, France
9 Epigenomics and Mechanisms Branch, IARC, WHO, Lyon, France
10 National Cancer Registry, National Health Laboratory Service, Johannesburg, South Africa
11 Cancer Surveillance Branch, IARC, WHO, Lyon, France
12 Strengthening Oncology Services Research Unit, Faculty of Health Sciences, University of the Witwatersrand, Johannesburg, South Africa
13 Department of Epidemiology & Biostatistics, Fred N. Binka School of Public Health, University of Health and Allied Sciences, Hohoe, Ghana
14 Department of Community Health, Institute of Public Health, Kilimanjaro Christian Medical University College, Moshi, Tanzania
15 Kilimanjaro Clinical Research Institute, Kilimanjaro Christian Medical Centre, Moshi, Tanzania
16 Department of Anthropology and Development Studies, University of Johannesburg, Gauteng, South Africa
Invited Commentary Understanding Global Lived Experiences to Advance Oncology Care Sudha Sivaram, DrPH; Satish Gopal, MD, MPH JAMA Network Open

Question Does cancer care terminology exist in African languages, and if so, what do these translations mean within their cultural context?

Findings This survey study of 107 health care workers and cancer researchers revealed diverse cancer terminology in 44 African languages across 32 countries in Africa. Translations of key terms including cancer , malignant , chronic , and radiotherapy commonly conveyed elements of fear and tragedy.

Meaning The findings highlight ethno-linguistic diversity and how the language used to communicate about cancer can potentially contribute to fear, stigma, and communication challenges between patients and health care workers.

Importance Effective communication between patients and health care teams is essential in the health care setting for delivering optimal cancer care and increasing cancer awareness. While the significance of communication in health care is widely acknowledged, the topic is largely understudied within African settings.

Objective To assess how the medical language of cancer and oncology translates into African languages and what these translations mean within their cultural context.

Design, Setting, and Participants In this multinational survey study in Africa, health professionals, community health workers, researchers, and scientists involved in cancer care and research and traditional healers were invited to participate in an online survey on a voluntary basis through online platforms. The survey provided 16 cancer and oncologic terms used in cancer diagnosis and treatment (eg, cancer , radiotherapy ) to participants, mostly health care workers, who were asked to provide these terms in their local languages (if the terms existed) followed by a direct or close translation of the meaning in English. The survey was open from February to April 2023.

Main Outcomes and Measures Patterns of meaning that recurred across languages were identified using thematic analysis of 16 English-translated terms categorized into 5 themes (neutral, negative, positive, phonetic or borrowed, and unknown).

Results A total of 107 responses (response rate was unavailable given the open and widespread distribution strategy) were collected from 32 countries spanning 44 African languages, with most participants (63 [59%]) aged 18 to 40 years; 54 (50%) were female. Translations for cancer were classified as phonetic or borrowed (34 [32%]), unknown (30 [28%]), neutral (24 [22%]), and negative (19 [18%]), with the latter category including universal connotations of fear, tragedy, incurability, and fatality. Similar elements connoting fear or tragedy were found in translations of terms such as malignant , chronic , and radiotherapy . The term radiotherapy yielded a high percentage of negative connotations (24 [22%]), with a prevailing theme of describing the treatment as being burned or burning with fire, heat, or electricity, which may potentially hinder treatment.

Conclusions and Relevance In this survey study of cancer communication and the translation of oncology terminology in African languages, the findings suggest that the terminology may contribute to fear, health disparities, and barriers to care and pose communication difficulties for health professionals. The results reinforce the need for culturally sensitive cancer terminology for improving cancer awareness and communication.

An estimated 801 000 incident cancer cases and 520 000 cancer deaths occurred in Africa in 2020. 1 , 2 The cancer burden in this region is increasing faster than in any other region of the world 3 ; thus, cancer surveillance, research, and control programs for prevention are major priorities. Effective communication between patients and care teams is essential for empowering primary and secondary cancer prevention as well as enhancing patient engagement and treatment adherence. Despite this importance, communication has been given insufficient attention in the African context. Barriers in cancer communication can contribute to stigma and disempowerment, impacting both patients and health care workers (HCWs). 4 - 6 Communication challenges between HCWs and patients are not confined to a specific region; they are prevalent issues globally, cutting across cultures and sociodemographic groups within a highly mobile globalized world. Health care workers face challenges in conveying information to patients due to linguistic differences. 7 , 8

Language, with its transformative power, can either empower individuals to actively participate in their care or disenfranchise them, impeding their engagement with the health care system. The way cancer is discussed and how cancer communication translates in terms of meaning are important given that language intricately shapes actions, exerting influence from symptom recognition to the proactive pursuit of treatment and care. In specific cultural contexts, the linguistic portrayal of a patient’s experience with cancer and cancer care often uses metaphors of warfare and violence. 9 , 10 Metaphors such as fighting cancer , survivors , and losing the battle are commonly used in the health care setting, patient narratives, and the broader community. 9 Individuals with cancer are often characterized as warriors or fighters, while therapeutic interventions are metaphorically framed as weapons. 9 The nuanced impact of these metaphors remains a subject of ongoing debate.

Globally, irrespective of the existence of a term for cancer in various cultures, the condition often carries stigma. In Western societies, such as Canada and the UK, cancer is frequently colloquially labeled as the “C-word” 11 or “the big C,” 12 reflecting its perceived ominous, intimidating, and sensitive nature. In India, cancer is euphemistically referred to as “a problem.” In the Netherlands, a prevalent insult involves telling someone to “get cancer.” 13 Some academic discourse suggests refraining from using the term cancer for cancers classified as low risk, such as slow-growing papillary thyroid cancers, aiming to alleviate potential patient anxiety that might influence decisions toward more invasive treatments. 14

In Africa, the absence of many scientific terms in the approximately 2000 languages spoken poses challenges in understanding medical terminology. 15 , 16 Local languages may lack adequate terminology for diseases and their treatment, exacerbating challenges in accessing timely diagnosis and treatment. The present study aimed to investigate the meaning of cancer terminology in African languages and how language might contribute to fear, stigma, and communication challenges for HCWs, potentially perpetuating misconceptions and myths about the disease.

In this survey study, we invited HCWs, community health workers, researchers, and scientists involved in cancer care and research as well as traditional healers to respond to an online questionnaire available in English, French, Portuguese, and Arabic (eAppendix in Supplement 2 ). The survey was developed by the International Agency for Research on Cancer (IARC) in partnership with Aga Khan University, Nairobi, and was disseminated by the African Organisation for Research and Training in Cancer, a collaborator with a vast network of HCWs and researchers in cancer care and research. The survey was also shared on the authors’ institutional platforms and networks after ethical approval was obtained by the IARC ethics committee. Written informed consent was sought from all participants at the beginning of the survey. The survey was open from February to April 2023 and received at least 1 response from most countries in Africa. The survey provided a list of cancer terms ( Table 1 ) used in cancer diagnosis and treatment to participants, who were asked to provide each term in their local language followed by a direct translation of its meaning into English, French, Arabic, or Portuguese. Detailed methods are available in the eMethods in Supplement 2 . The study followed the Consolidated Criteria for Reporting Qualitative Research ( COREQ ) and American Association for Public Opinion Research ( AAPOR ) reporting guidelines. Survey participants did not receive compensation.

We conducted thematic analysis of the English-translated terms to identify patterns of meaning that recurred across languages. The analysis followed a 6-step process of familiarization, coding, generating themes, reviewing themes, defining and naming themes, and writing and adaptation of the COREQ guideline. 17 , 18 This analysis identified 5 themes, into which the responses for all 16 terms ( cancer , tumor , malignant , radiotherapy , chemotherapy , benign , biopsy , chronic , metastasis , staging , surgery , trial , palliation , recur , survival , and remission ) were categorized: (1) neutral was used for translations that offered outcome-based or descriptive explanations of the term, maintaining a neutral and factual tone; (2) negative was used to describe translations with negative connotations, outcomes, or emotions that superseded the neutral description; (3) positive was used to describe translations with positive connotations, outcomes, or emotions that superseded the neutral description; (4) phonetic or borrowed was used to describe terms that had phonemic semblance to the original term or for terms that were borrowed from another language; and (5) unknown was used for unknown or nonexistent translations.

Descriptive statistical methods were used to analyze the survey data using Stata, version 17 (StataCorp LLC). Quantitative analysis involved calculating the frequency and percentage of responses within each theme as well as summary statistics for age, self-reported gender, and profession distribution. No advanced inferential statistics were used.

A total of 107 responses were received and were equally distributed between participants identifying as men (53 [49%]) and women (54 [50%]), with 32 (58%) of a total of 55 African countries represented (eTable in Supplement 1 ). The response rate was not calculated given the open and widespread distribution strategy. Most participants (63 [59%]) were aged 18 to 40 years followed by 38 (36%) aged 41 to 60 years and 6 (6%) aged 60 years or older. The study’s participants were predominantly HCWs (62 [58%]), with 32 (30%) specializing in oncology and 30 (28%) in other health care fields. Cancer researchers (n = 31) composed 29% of the sample, while researchers from other disciplines (n = 7) constituted 7%. Seven participants (7%) represented diverse professions, including students and religious leaders. The largest number of participants was from Nigeria (11 [10%]) followed by South Africa (9 [8%]). The geographic coverage of this survey is shown in Figure 1 . A total of 44 languages were reported, with the most reported languages being Arabic (11 [25%]), Swahili (7 [16%]), Afrikaans (6 [14%]), and Amharic (6 [14%]) (eFigure in Supplement 2 ). Many of these languages originated from multiple countries, such as Arabic (Algeria, Egypt, Libya, Morrocco, Sudan, Chad, and Tunisia), Swahili (Kenya, Uganda, and Tanzania), Tswana (South Africa and Botswana), and Afrikaans (Namibia and South Africa).

An overview of participants’ responses across all 16 terms revealed a consistent pattern, with 23 (22%) and 46 (43%) indicating that the terms survival and palliation , respectively, either did not exist in their language or that they were unsure of the translations; the remaining terms fell within this range ( Table 1 ). Some terms stood out with a higher percentage of negative connotations, such as cancer (19 respondents [18%]), with translations such as “evil spirit infliction,” “chronic illness that leads to death,” and “destroyer”; surgery (19 [18%]), with translations including “to be butchered”; and malignant (30 [28%]), with translations such as “malevolent or evil” and “angry or intending to do harm.” Another term with a relatively high percentage of translations coded as negative was radiotherapy (24 [22%]). Additionally, for the term chronic , a notable proportion of participants (10 [9%]) expressed negative perceptions through translations such as “incurable” and “bedridden.”

Seventy-seven participants (72%) recorded a term for cancer that existed in their local vernaculars. The themes established for these lexical translations encompassed distinct classifications: phonetic or borrowed (34 [32%]), neutral (24 [22%]), negative (19 [18%]), and an overarching category of unknown (30 [28%]) ( Table 1 ).

Participants from Tanzania, Kenya, Chad, Algeria, Sudan, and Morrocco reported that the term for cancer in their respective languages was saratane , saratani , or saratan . These terms are borrowed from the Arabic lexeme saratan , which means “cancer.” This etymological borrowing underpins the relationship between these linguistic expressions, as they share a common origin in their historical roots. Regarding the theme “phonetic or borrowed,” 10 terms that phonemically resemble the term cancer were reported, which included kankere (Botswana), maladi ya kansere (Democratic Republic of Congo), kanza (Kenya), khansa (Malawi), oria kansa or kansa (Nigeria), kansa (Tanzania), kanseri (Rwanda), kanker (South Africa), and kansevi (Togo). Within the thematic category “negative” were a series of translated terms that evoked fear or suggested the incurable nature of cancer and translations laden with malevolent spiritual connotations.

The term cancer in Luganda (language spoken in Uganda) was reported by participants to be kokolo or kookolo , and 1 participant elaborated,

The term kookolo has come to directly translate to cancer, although it is not known by everyone. Many members of the general public do not know names of diseases until they have directly been affected by them. Other terms used in place of cancer are descriptive terms such as “obulwadde bw’ebizimba,” which means “illness (characterized) of swellings,” or “obuladde bw’ebbwa eritawona,” which means “illness of a wound that does not heal.”

In Shona, a language spoken in Zimbabwe, the term is gomarara , which means a parasitic plant. A participant explained, “This is a plant that grows on top of another plant, in a parasitic way, usually killing or disabling the plant.”

For the term radiotherapy , 67 participants (63%) reported that the term existed in their local language. The themes established for these etymological translations were neutral (43 [40%]), negative (24 [22%]), and unknown (40 [37%]). The term radiotherapy yieled a high percentage of translations with negative connotations ( Table 1 ), with references to burning, roasting, or being burned with fire, heat, and electricity. Exemplifying this category, a participant from Uganda who speaks Luganda remarked,

The scientific words “radiation therapy” are translated in our local language as “roasting” or using “electricity.” In the actual sense, some of the radiotherapy side effects are the dry and moist skin desquamation, which physically appear like burns or partially roasted meat. So to a layperson or a patient who is already anxious, this is “Gospel truth.” During health education, some clients will ask, “Are we going to be put in the machine (direct English translation) and be roasted like meat?” The one roasting is the radiation therapist and the local oven is the Cobalt-60 machine. The stalks of meat are the parts on the patient’s body to be radiated.

Participants also shared perspectives on the overarching theme of translating cancer terms into local languages ( Figure 2 ) and cited reasons for communication challenges ( Box ).

Select Health Care Workers’ Responses to Whether They Experienced Challenges or Barriers Communicating With Patients Using the Local Language

“Yes, especially when dealing with [elderly patients] who have never been to school.” Botswana (seTswana)

“Sometimes. I navigate by explaining where the organ is located, its function, and then probing the understanding of the patient.” Botswana (seTswana)

“Principal barriers are illiteracy.” Guinea (Toma)

“Barriers or challenges are encountered when communicating cancer terms, but explaining in broader terms in the local language usually helps.” Malawi (Chichewa)

“Yes. I have downloaded applications to help me with translations; however, they are not always accurate.” South Africa (isiZulu)

“Easily understood, but the etiology and more info usually are needed as patients do not know more details about what exactly they suffer from.” Tanzania (Kiswahili)

“Since the whole cancer concept is new to many patients, and they are more familiar with infectious diseases, it can take time for patients/caregivers to grasp concepts. Repeated communication and giving illustrative examples is crucial.” Uganda (Luganda)

“Some words just don’t exist.” Zambia (Ngoni)

This study investigated the symbolic relevance and importance of cancer terminology in African populations and how these understandings impact communication efforts in care and practice in health care settings in Africa. Results for the 16 terms used in cancer care revealed a spectrum of diversity in terminology and translations. Participants’ local terms often contained linguistic references reflective of their cultural and social contexts. Our study highlighted the nonexistence or lack of knowledge of cancer terminology in African languages for approximately one-third of respondents for a given term. The revelation that certain terms may not exist or are not widely enfolded into lexicons of meaning in some African languages points to potential barriers in disseminating crucial information about cancer and its care. The results highlight the need for patient-centered communication strategies, HCW training, and engaging patients with cancer and cancer survivors to integrate their lived experiences.

In our study, the term cancer had translations with connotations of fear, tragedy, incurability, and fatality reported from several languages and countries. Certain terms and their translations incorporated malevolent spiritual undertones, indicating a connection between perceptions of illness and belief in spiritual causation. The weightiness associated with the term cancer often extends to its connotation of being overwhelming, unbeatable, and frequently final, contributing to a sense of cancer fatalism. This connotation was evident in our results from the terms used for cancer in several countries, underscoring the gravity and inevitability of fatality.

The term radiotherapy invoked ideas across several languages that referenced fire, heat, and electricity. A prevalent theme emerged wherein radiotherapy was referred to by HCWs and researchers as burning, roasting, or being burned. This recurrent motif emphasizes a widespread conceptualization of radiotherapy rooted in the elemental forces of fire and heat across diverse linguistic contexts. This raises concerns about the potential psychological effect on patients, as it may induce fear and apprehension and may be a deterrent to treatment initiation. While this characterization may initially evoke concerns, questions remain regarding whether radiotherapy can be reframed positively as a symbol of the transformative and healing nature of the treatment. Negative connotations for radiotherapy are not unique to African languages; in many European languages, the term radiotherapy is often similar to the term used in nuclear accidents.

The translations provided for the term chronic revealed a concerning divergence from its true definition. This discrepancy highlights the need for accuracy and clarity when conveying the concept of chronicity. Of note is the 9% of translations with negative connotations, with expressions such as “incurable,” “bedridden,” and “noncurative.” These translations present a notable departure from the medical connotation of chronic conditions, which generally denote long-term persistence 19 rather than an inherent lack of cure or immobility. These translations emphasize a critical need for medical-linguistic precision to accurately convey the medical concept of chronic conditions.

The findings of our study showed that some participants reported the nonexistence of various cancer-related terms in their languages or expressed uncertainty, ranging from 23 (22%) for terms like survival and recur to 46 (43%) for palliation . This highlights potential challenges in conveying essential cancer concepts. For instance, a participant noted the absence of the word prostate in Bantu languages, illustrating challenges in explaining a common cause of cancer mortality in African men.

The translation for the term metastasis provided by a Ugandan participant, “ekiziba kyasindika obwana bwayo ahare,” meaning “the mother mass has sent seedlings into another site,” is particularly noteworthy as it exemplifies a unique linguistic expression deeply rooted in idioms and proverbs within the Luganda language. This intricate metaphorical construction, likening metastasis to the dispersal of seedlings from a mother mass, underscores the richness of cultural idioms embedded in African languages to describe complex medical concepts. It reveals an interplay between traditional linguistic expressions and the articulation of scientific terms, emphasizing the need to recognize and appreciate the diverse and metaphorical nature of cancer terminology within African linguistic and cultural contexts.

In terms of idioms of distress 20 used, exemplified in instances where cancer was referred to as the “wound with which we will be buried” (translated from Wolof), these embedded meanings signify psychological and emotional markers of distress related to the participants’ culturally located experiences and perceptions of cancer. Other linguistic expressions, like “forest disease” (translated from Djerma) and “parasitic plant” (translated from Shona), highlight the wider symbolic import of where and how cancer is understood differently across geographies and cultures.

The interpretations of survival and remission in translations carried positive undertones, suggesting notions of healing, cure, and recovery. In certain translations for survival , metaphors related to warfare surfaced, such as “to defeat a life-threatening situation” and “to conquer.” For the term remission , a handful of translations incorporated the term forgive , potentially indicating a perspective that views cancer as a form of punishment.

Work done in South Africa with patients with cancer highlighted that the term cancer exists in only 3 of 11 official languages: isiZulu, siSwati, and isiXhosa (Umdlavuza, U’mdlopha, and Umlaza, respectively). 21 Evidence from a 2016 Kenyan study suggests that language problems may hinder patients and family members from comprehending cancer diagnoses and seeking out appropriate interventions. 5 A South African study analyzing perspectives on cancer, chemotherapy, and radiotherapy among 9 Xhosa-speaking patients with cancer revealed an overall lack of knowledge about cancer and cancer treatment. 22 An added complexity in the African setting is that patient-centered communication and treatment decision-making may not be directly communicated to the persons with cancer themselves, especially for older persons. 5 , 23 The challenge of effective communication in cancer care is not unique to Africa. A report from the US emphasized that inadequate patient-practitioner communication was a significant factor contributing to the suboptimal state of cancer care delivery. 24 , 25

The challenges linked with health communication extend beyond cancer to other medical conditions such as tuberculosis, HIV infection and AIDS, and mental illness. 26 , 27 Tuberculosis is frequently labeled as the “disease of poverty,” which stigmatizes those affected. 26 In tuberculosis care and research, certain terms, shared with the context of cancer, contribute to stigmatization by embodying “metaphors of transgression and punishment.” 26 Noteworthy examples include treatment defaulter , implying a judgment akin to nonpayment of a loan; tuberculosis suspect , suggesting criminal behavior; and noncompliant , assigning blame and patient labeling without acknowledging systemic and structural barriers to treatment adherence. 26 In the context of cancer, terms such as delayed presentation or loss to follow-up may erroneously suggest patient fault, overlooking the repeated engagements individuals experiencing delays in diagnosis have with the health system, which are common in low- and middle-income countries. 28 , 29 Work done during the early years of the HIV epidemic in Africa to overcome stigmatizing language also serves as a blueprint for cancer communication. 30 - 32 Initiatives such as the Stop TB Partnership’s Tuberculosis Language Guide have been instrumental in outlining nonstigmatizing alternatives for tuberculosis care and research, which may lend lessons to the oncology setting. 26 The American Cancer Society’s initiatives for patient and caregiver education and the International Atomic Energy Agency’s Rays of Hope radiotherapy program show the potential for translations 33 and positive terminology alternatives 34 in Africa.

This study has limitations. While the insights from this study offer valuable contributions to our understanding of the linguistic nuances associated with cancer treatments, caution must be exercised in generalizing the findings. The study’s small sample size based on convenience sampling poses limitations, and the use of an online survey as the primary data collection tool may not have captured the depth required for a comprehensive analysis but provided initial insightful information. Another limitation is the lack of patient perspectives in our study. Our focus on HCWs and researchers trained in the language of Western medicine may not have fully captured the linguistic nuances experienced by patients. Recommendations for future work are detailed in Table 2 .

The findings of this survey study showed that oncology terminology in African languages may contribute to fear, health disparities, and barriers to care and create communication difficulties for health professionals. There is a pressing need for the development of alternatives to cancer terms that invoke fear or stigma or disempower patients in local languages. Multisectoral approaches between clinicians, anthropologists, and communities may help to develop an emerging lexicon that offers neutrality or at least hope of treatment and/or cure. This study highlights the need for culturally sensitive approaches to cancer communication in health care settings across African populations.

Accepted for Publication: June 27, 2024.

Published: August 30, 2024. doi:10.1001/jamanetworkopen.2024.31128

Corresponding Author: Hannah Simba, PhD, Environment and Lifestyle Epidemiology Branch, International Agency for Research on Cancer, 69366 Lyon Cedex 07, France ( [email protected] ).

Author Contributions: Drs Simba and McCormack had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Simba, Mutebi, Galukande, Addissie, Abebe, Onwuka, Chimera, Prah, McCormack.

Acquisition, analysis, or interpretation of data: Simba, Mutebi, Galukande, Mahamat-Saleh, Aglago, Addissie, Onwuka, Odongo, Onyije, Motlhale, de Paula Silva, Malope, Narh, Msoka, Schüz, McCormack.

Drafting of the manuscript: Simba, Mutebi, Msoka.

Critical review of the manuscript for important intellectual content: All authors.

Statistical analysis: Simba, Mahamat-Saleh, Onwuka, Odongo, Malope.

Administrative, technical, or material support: Simba, Mutebi, Galukande, Mahamat-Saleh, Aglago, Addissie, Abebe, Onyije, Chimera, Motlhale, de Paula Silva, Narh.

Supervision: Mutebi, Addissie, McCormack.

Conflict of Interest Disclosures: None reported.

Funding/Support: This work was funded by the World Health Organization (WHO) International Agency for Research on Cancer (IARC) fellowship fund (Dr Simba).

Role of the Funder/Sponsor: The funding provided supported Dr Simba during the design and conduct of the study, data collection, management, analysis, and interpretation of the data, as well as in the preparation, review, and approval of the manuscript.

Disclaimer: Where authors are identified as personnel of the WHO IARC, the authors alone are responsible for the views expressed in this article, which do not necessarily represent the decisions, policy, or views of these organizations.

Data Sharing Statement: See Supplement 3 .

Additional Contributions: Asmaa El Hamdouchi, PhD, of the Unité Mixte de Recherche en Nutrition et Alimentation (CNESTEN-UIT, Morocco), assisted with the Arabic translation of the survey without compensation. We acknowledge all the participants who took part in the survey. No compensation was given.

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Open Access

Peer-reviewed

Research Article

Religious beliefs and practices toward HPV vaccine acceptance in Islamic countries: A scoping review

Contributed equally to this work with: Sezer Kisa, Adnan Kisa

Roles Conceptualization, Data curation, Methodology, Writing – original draft, Writing – review & editing

* E-mail: [email protected]

Affiliation Faculty of Health Sciences, Department of Nursing and Health Promotion, Oslo Metropolitan University, Oslo, Norway

Affiliations School of Health Sciences, Kristiania University College, Oslo, Norway, Department of International Health and Sustainable Development, Tulane University, New Orleans, United States of America

Sezer Kisa,

Published: August 29, 2024
https://doi.org/10.1371/journal.pone.0309597
Reader Comments

Despite the availability of effective HPV vaccines, their acceptance in Islamic countries is often influenced by religious beliefs, practices, and misconceptions.

This review aimed to identify the current literature on the religious beliefs and any misconceptions toward HPV vaccine acceptance within the Organisation of Islamic Cooperation (OIC) countries.

Using key terms, a systematic search in MEDLINE/PubMed, Embase, and CINAHL yielded 23 studies that met the inclusion and exclusion criteria. The scope of this review included all research articles published in English until October 31, 2023. A form based on the aim of the study was developed and used to extract the data.

The review highlights the complexity of the relationship between religious beliefs and HPV vaccine uptake. The findings reveal significant objections among a number of Muslims. Some of them believe vaccines lead to infertility and sexual promiscuity, defy religious norms, are a sneaky way to inject good Muslims with haram ingredients, and are an abandonment of righteous principles in general.

Conclusions

Vaccine hesitancy is a result of doubts regarding the vaccine’s safety, necessity, and compatibility with religious beliefs. It is recommended to encourage HPV vaccine uptake in Islamic countries by using public health strategies that adopt a holistic approach that incorporates religious, cultural, and social aspects.

Citation: Kisa S, Kisa A (2024) Religious beliefs and practices toward HPV vaccine acceptance in Islamic countries: A scoping review. PLoS ONE 19(8): e0309597. https://doi.org/10.1371/journal.pone.0309597

Editor: Emmanuel Timmy Donkoh, University of Energy and Natural Resources, GHANA

Received: February 12, 2024; Accepted: August 11, 2024; Published: August 29, 2024

Copyright: © 2024 Kisa, Kisa. 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 author and source are credited.

Data Availability: All relevant data are within the manuscript and its Supporting Information files.

Funding: The author(s) received no specific funding for this work.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Human papillomavirus (HPV) is a sexually transmitted infection commonly seen in low- and middle-income countries [ 1 , 2 ]. The global spread of HPV remains a significant public health challenge. It is the leading cause of cervical cancer, which is the fourth most significant cause of cancer-related death among women around the world. It is also responsible for cancers in the anus, vulva, vagina, penis, head, and neck [ 1 , 3 ]. Studies indicate a rising trend of HPV infection in young women who engage in early sexual activities [ 3 – 5 ]. The underlying risk factors for HPV infection include low socioeconomic status, other sexually transmitted agents, multiple sexual partners, early marriage, early onset of sexual activity, immunosuppression, more permissive sexual attitudes among the younger population, and unprotected sex [ 2 , 4 ].

Preventive public health strategies, including cervical screening and vaccination, protect against the most harmful types of the virus (types 16 and 18) [ 5 ]. The World Health Organization recommends vaccinating girls aged 9–14 who have not yet initiated sexual activity and those up to age 25 who have not been previously vaccinated [ 5 ]. The HPV vaccine is widely recognized for its efficacy in preventing cervical cancer, which is primarily caused by high-risk HPV types such as HPV-16 and HPV-18 [ 3 , 6 , 7 ]. It also reduces the incidence of genital warts, which are caused by low-risk HPV types such as HPV-6 and HPV-11 [ 8 , 9 ]. These benefits can influence acceptance and attitudes towards the vaccine, as some individuals may view it as a cancer prevention tool, while others may value its ability to reduce the morbidity associated with sexually transmitted infections. The global adoption of these vaccines faces challenges, such as: lack of recommendation from a physician [ 10 , 11 ]; family acceptance or parental opposition/ignorance [ 11 , 12 ]; fear of side effects; fearing being too young for the vaccine [ 13 ]; lack of knowledge about HPV transmission, cervical cancer, and vaccines [ 14 , 15 ]; skepticism about the vaccine’s content, safety, and effectiveness [ 13 ]; and concerns about the costs of vaccination [ 5 , 15 – 17 ].

It is well-established in the literature that religious beliefs have a profound impact on an individual’s decision-making and health-related behaviors, including sexual health [ 18 – 20 ]. Mouallif et al. (2014) note that leaving health outcomes to God’s will is a common belief [ 21 ], while another study highlights the preference for faith healing and traditional medicine over orthodox methods [ 22 ]. Additionally, adherence to religious principles, such as abstaining from premarital sex or believing that religiously-based circumcision reduces HPV prevalence, play a role in shaping one’s health-related choices [ 17 , 23 ]. Religious beliefs, derived from religious teachings, guide moral and ethical decisions and influence behavior. Dietary rules that distinguish what is permissible from what is forbidden also play a role in guiding behavior. Religious beliefs may encompass traditional healing practices and interpretations from religious authorities, who set community standards and shape ethical decisions [ 24 – 27 ]. The influence of religion goes beyond personal beliefs. It shapes attitudes toward preventive health measures such as vaccination [ 12 , 17 , 22 ]. It has been proven that there is a strong relationship between religious beliefs and vaccine acceptance, including vaccine decision-making for sexually transmitted infections such as HPV [ 12 , 21 , 28 , 29 ]. A study in Saudi Arabia found that religious objections accounted for 30% of opposition to the vaccine [ 28 ]. Another study noted the role of religious leaders in shaping vaccine uptake within African communities [ 30 ]. Some people may perceive vaccines as consistent with their religious principles and view vaccines as a means of preserving health in line with divine will [ 31 ]. Conversely, some religious perspectives may lead to hesitancy or resistance due to concerns about the vaccine’s content (e.g., claims that a vaccine was processed from pig’s blood), moral implications, or perceived conflicts with sacred teachings [ 12 , 32 ].

Islamic countries exhibit unique socio-cultural dynamics in which religious beliefs and practices play an important role in shaping social norms. It is commanded in Islam to abstain from sex until after marriage. Since HPV is sexually transmitted, some parents may believe that vaccinating their daughters is unnecessary and immoral because it may encourage sexual activity at an early age [ 12 ]. Pelčić and colleagues (2016) found that, despite the absence of any taboo against vaccination and a general alignment of religion with vaccines and public health, there has been a rise in vaccine refusal attributed to religious objections [ 33 ]. Furthermore, recent events in Indonesia have highlighted the impact of religious rulings on immunization rates, as Islamic clerics declared a measles-rubella vaccine containing pork components as impure, leading to a significant decline in vaccine coverage [ 34 ]. Additionally, a multi-country analysis conducted in sub-Saharan African countries found that in several nations, including those with significant Muslim populations, there were lower levels of vaccine coverage among Muslim communities compared to Christian ones [ 35 ]. This trend is frequently linked to individual parents or religious leaders opposing vaccination and providing questionable interpretations of religious teachings. Despite the abundance of studies on the safety of the HPV vaccine, there is little research on how religious practices influence vaccine acceptance in these communities. Understanding the full spectrum of the vaccine’s benefits is crucial in shaping public perception and acceptance [ 9 , 36 ] and is particularly relevant in the context of Islamic countries, where cultural and religious beliefs significantly influence health behaviors. This lack of understanding hinders the development of targeted interventions to address barriers arising from religious attitudes. Research has focused on knowledge about HPV vaccines themselves, leaving a gap in understanding religious beliefs about vaccines and their acceptance. Therefore, this review is guided by the following research questions:

Does religion influence HPV vaccine acceptance in the Organisation of Islamic Cooperation (OIC) countries?
What religious beliefs and practices potentially forbid the HPV vaccine in the OIC countries?
What objections and misconceptions against the HPV vaccine are found in the OIC countries?

This study was designed as a scoping review, following the methodology described by the Joanna Briggs Institute, to systematically map the existing literature on religious beliefs, practices, and misconceptions regarding HPV vaccine acceptability, and to identify any research gaps. This method is particularly effective for investigating emerging research domains and generating practical evidence [ 37 ]. Our methodology was guided by the principles developed by Arksey and O’Malley (2005) [ 38 ]. The inclusive nature of the scoping review allowed for an examination of a wide range of literature, including but not limited to primary research studies, systematic reviews, meta-analyses, correspondence, guidelines, and various online resources. We started by enlisting the aid of a librarian to identify the aim and research questions and to develop the research strategy.

Following JBI’s guidelines, a three-stage search strategy was formulated. The first stage entailed searching Google Scholar. In the second stage, key terms from titles, abstracts, and index lists of articles were identified by one of the reviewers (AK), and the MEDLINE/PubMed, Embase, and CINAHL databases were searched. Database-specific vocabulary focused on “HPV vaccine” OR “HPV Vaccination” in conjunction with the names of the countries within the OIC [ 39 ]. These countries are Algeria, Benin, Burkina Faso, Cameroon, Chad, Comoros, Djibouti, Egypt, Gabon, Gambia, Guinea, Guinea-Bissau, Ivory Coast, Libya, Mali, Mauritania, Morocco, Mozambique, Niger, Nigeria, Senegal, Sierra Leone, Somalia, Sudan, Togo, Tunisia, Uganda, Afghanistan, Azerbaijan, Bahrain, Bangladesh, Brunei, Indonesia, Iran, Iraq, Jordan, Kazakhstan, Kuwait, Kyrgyzstan, Lebanon, Malaysia, Maldives, Oman, Pakistan, Palestine, Qatar, Saudi Arabia, Syria, Tajikistan, Turkey, Turkmenistan, United Arab Emirates (UAE), Uzbekistan, and Yemen ( Table 1 ). The last stage of the research was expanded to include tracing references from relevant studies and examining gray literature to identify additional studies.

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https://doi.org/10.1371/journal.pone.0309597.t001

Following a systematic search based on predefined inclusion and exclusion criteria, relevant studies were identified and imported into EndNote (version 21). We did not conduct a quality assessment since it’s not recommended in scoping reviews [ 38 ]. The scope of this review included all research articles published in English until October 31, 2023. Sources for this review were carefully selected, focusing on databases rich in medical and public health literature. The initial phase involved database searches conducted by one reviewer (AK), with subsequent removal of duplicate records. Two reviewers (AK and SK) independently assessed titles and abstracts, followed by full-text reviews and data extraction. Discrepancies between the reviewers were resolved through discussion. Articles that did not meet the eligibility criteria to address the research questions were excluded. Excluded studies were those that focused on vaccine acceptance barriers beyond religious beliefs, practices, and misconceptions; were published as dissertations, reviews, conference abstracts, editorials, opinion pieces, or came from non-peer-reviewed sources; were published in languages other than English; or which primarily investigated HPV knowledge and awareness. The PRISMA flow chart in Fig 1 presents detailed information on the exclusion process.

https://doi.org/10.1371/journal.pone.0309597.g001

Data were extracted into an extraction form designed by a single reviewer (SK) in alignment with the research questions. The form included data pertinent to the characteristics of the studies (author(s), publication year, journal, study aims, research question, population, method, sample size, outcomes, and contextual details) and information related to the religious aspects of HPV vaccine acceptance. Both reviewers endorsed the extraction form, deliberated on each element to be captured, and resolved any conflicts. The findings were organized into two primary categories that addressed the research questions regarding religious beliefs and practices, and objections and misconceptions.

Study characteristics

For this scoping review, a comprehensive examination of 595 studies was conducted. From these, 282 studies were selected through their abstracts, and 23 articles were found eligible for review to answer the study’s research questions. These eligible studies represented a wide geographic range, with their distribution as follows: Gambia (1), Indonesia (4), Malaysia (2), Morocco (1), Nigeria (7), Pakistan (1), Uganda (2), Saudi Arabia (3), and the United Arab Emirates (2). Notably, all these countries are predominantly Sunni, which is the largest branch of Islam. Among the included articles, most were designed as cross-sectional studies and published in 2023 (six studies), followed by six studies in 2022 and three in 2021. The diverse sample populations provided a comprehensive overview of the issue across different demographics, enhancing the generalizability of the findings. The variety in settings, from urban centers to rural communities, allowed for a complete understanding of how different environments influence religious beliefs and practices.

The studies examined various levels of awareness and acceptance of the HPV vaccine. A school-based HPV immunization program in Malaysia was found to be effective in a multicultural and religious society [ 40 ]. In Nigeria, healthcare professionals showed high awareness of HPV (91%) and the vaccine (44%), with male professionals significantly more likely than their female counterparts to approve the vaccine for their teenage daughters [ 41 ]. In Morocco, awareness and acceptability of the HPV vaccine were low, and were influenced by education, income, and religious beliefs, with mothers being less likely than fathers to accept the vaccine [ 21 ]. Among male university students in the UAE, knowledge of HPV was low (32%), with religious objections and concerns about vaccine safety being common [ 42 ]. In Nigeria, females demonstrated higher awareness of cervical cancer and were generally more receptive to HPV vaccination compared to males [ 22 ].

In Indonesia, a high willingness to receive the HPV vaccine was observed among university students, particularly females [ 43 ]. Knowledge levels about HPV and vaccine acceptability in Saudi Arabia showed no significant gender differences [ 28 ]. Cultural and safety concerns influenced vaccine acceptance among Emirati men [ 44 ]. Despite these insights, it is important to note that 13 out of the 23 reviewed studies did not include any gender-specific analyses. This indicates a gap in the literature regarding the differential impact of religious beliefs on HPV vaccine acceptance between males and females. However, exploring gender differences was not the primary aim of this review [ 40 , 42 , 44 – 54 ].

The results are summarized in Table 2 .

https://doi.org/10.1371/journal.pone.0309597.t002

Religious beliefs and practices on HPV vaccine acceptance

The findings of this review highlight the complex interplay between religious beliefs and HPV vaccine acceptance among various populations. Some studies have indicated that religious beliefs did not influence vaccine uptake [ 40 , 41 , 43 , 44 , 49 ], while others found that religious beliefs had the opposite effect [ 21 , 28 , 45 , 47 , 51 , 55 – 57 ]. This influence stemmed from various beliefs, including “health outcomes being determined by God’s will” [ 21 ], faith healing and traditional medicine over orthodox methods [ 22 ], religious beliefs influencing health-related decisions [ 16 , 47 , 48 ], trust in religious bodies [ 30 , 50 ], parents with religious beliefs [ 53 ], or need for their husbands’ approval for vaccination [ 54 ]. Elebiyo (2023) showed that Nigerian parents’ religious beliefs significantly influenced their decision to vaccinate their children [ 46 ]. Concerns about the HPV vaccine being seen as a license for sexual promiscuity reflected cultural and religious expectations around chastity before marriage in Nigeria [ 22 ]. Conversely, Ling et al. (2012) [ 40 ] found a high acceptance of HPV vaccination among teachers in a predominantly Islamic country, challenging the notion that religion is inherently anti-vaccination.

Religious objections and misconceptions

This review identified several misconceptions and objections about HPV vaccination that are rooted in religious beliefs. These misconceptions include the belief that the vaccine causes diseases, is unnecessary in certain situations, or is still experimental, as well as religious skepticism about modern medicine [ 52 ]. In addition, there is a perception that the vaccine may serve as a license for unbridled sex, reflecting religious expectations about chastity before marriage [ 48 , 51 ]. Some hold beliefs about vaccines containing haram substances and being unnatural [ 43 ]. There is also a perception that the vaccine is unnecessary for married couples who enjoy a proper religious upbringing [ 54 ]. There are also worries about the vaccine causing infertility [ 52 , 57 ]. Additionally, there are questions about the vaccine’s compatibility with religious beliefs and lack of religious endorsement [ 51 ], while some see the HPV vaccine as a surreptitious form of birth control [ 57 ]. Objections from religious authorities were reported in various studies [ 22 , 28 , 42 ]. In contrast, one study using a community-based survey among girls reported no religious misconceptions about the HPV vaccine [ 49 ].

Suggestions for public health interventions

Some of the studies also suggested public health strategies to increase uptake by increasing awareness among people refusing the HPV vaccine about religious beliefs and misconceptions about HPV vaccination. Some studies recommended public health campaigns that address religious concerns via scientific information [ 21 , 28 , 41 , 44 , 46 , 49 , 53 – 56 ]. Other studies suggested collaborating with religious leaders and institutions to influence community attitudes on health-related decisions [ 16 , 22 , 40 ] and develop culturally and religiously sensitive educational materials to bridge the gap between scientific knowledge and religious understanding, or utilize religious platforms for health education [ 42 , 43 , 52 , 57 ]. Public health officials need to be sensitive to religious objections, addressing them respectfully and informally [ 48 , 50 ].

By relying on the relevant literature, this review aimed to understand the religious factors that play a role in HPV vaccine acceptance and decision-making in Islamic countriesThe review incorporated studies from various cultural and religious settings. The explored concepts centered on the interplay of religious beliefs, health, and vaccine acceptance. Most of the studies focused on awareness, attitudes, and acceptance of the vaccine among groups such as university students, parents, healthcare providers, and school nurses. The studies investigated the factors that influence vaccination decisions but did not explore how religious beliefs play a role in the decision to vaccinate. Thus, this review included only those studies that presented variations in religious beliefs related to HPV vaccination and its acceptability in Islamic countries.

During the COVID-19 pandemic, an important issue that emerged was the public’s trust in vaccination programs in general. While this review focused on studies published up to October 2023, it is notable that not one of them addressed the intersection of COVID-19 with HPV vaccine perceptions. The global health crisis has undeniably influenced public attitudes towards vaccines. For instance, increased vaccine hesitancy or, conversely, a heightened trust in the power of vaccines due to the rapid development of COVID-19 vaccines could influence public perception of other remedies, including those for HPV [ 58 ]. This intersection presents a unique opportunity to examine how crises impact long-term vaccine strategies and acceptance, particularly in contexts where vaccine hesitancy is already influenced by complex factors such as religious beliefs and cultural practices [ 21 , 41 , 58 ]. Future research could include comparative analyses of HPV vaccine acceptance pre- and post-COVID to better understand the pandemic’s impact on public trust and vaccination behavior. Public health campaigns promoting the HPV vaccine should consider incorporating lessons learned from the COVID vaccination efforts. This includes addressing misinformation, leveraging trusted community and religious leaders, and ensuring transparent communication about vaccine safety and efficacy [ 16 , 48 ].

The review also found that the degree of religious influence on health decisions varies not only between countries but also within different regions of the same country, reflecting the diversity in religious denominations and sects [ 28 , 45 ]. These findings are consistent with previous studies in non-Islamic countries [ 18 , 23 , 59 ]. Religious affiliation influenced acceptability, showing fewer acceptors among Hindus and Muslims than those without religious affiliation [ 60 ]. However, more recently, Coleman and colleagues (2024) reported that religiosity had little effect on HPV vaccine decisions for urban, Black, and Hispanic parents [ 61 ].

Best and colleagues (2019) proved with further analysis that the relationship between religious beliefs and HPV vaccination was fully mediated by sexual activity [ 18 ]. This finding may clarify the link between religious beliefs and vaccine acceptance because strong religious or spiritual beliefs are often associated with abstaining from premarital sex. Given that sexually active individuals are at higher risk for HPV infection, the decision to get vaccinated is tied to one’s faith and lifestyle [ 23 ]. This also explains the doubts about the vaccine’s necessity, another finding of the present review.

Studies showed that a common question within Islamic countries is why a pious family with sexually inactive children needs to be immunized against sexually transmissible diseases at all. Commitment to religious principles, such as abstaining from premarital sex, was frequently indicated in the included studies. This finding is important because it aligns with the belief that having sex outside of marriage is a sin and that adhering to religious principles obviates the need for HPV vaccination [ 62 , 63 ]. This finding resonates with studies conducted in various religious contexts. For instance, a survey of 1557 Christian college students in the USA identified that following the injunction against premarital sex is the greatest predictor of HPV vaccine uptake [ 59 ]. Another study on Christian teachings about sexual relationships among parents found that religious propriety had a negative impact on the intention to vaccinate children [ 64 ]. A qualitative study of Jewish mothers stated that the religious laws governing family purity and abstinence until marriage are the reasons for their daughters’ low HPV vaccine uptake [ 29 ].

One noteworthy finding in this review was the belief that the HPV vaccine would encourage wanton sexual behavior. This sentiment was particularly pronounced in regions where conservative religious beliefs strongly influence societal norms [ 60 ]. Other studies on HPV-related beliefs and vaccine acceptability in the USA and Kenya revealed that parents were concerned that vaccination might encourage sexual activity at a younger age, elevate risky behaviors, and contribute to increased promiscuity [ 65 , 66 ]. There are contradictory studies in the literature about whether these fears are justified. Some studies found no connection between HPV vaccination status and age of sexual onset or number of sexual partners [ 67 , 68 ]. On the other hand, Brabin and colleagues (2009) reported that HPV-vaccinated girls aged 12–13 years stated that they might engage in more risky sex after vaccination [ 69 ]. These findings underscore the complex interplay between cultural beliefs and public health interventions, highlighting the need for culturally sensitive education and communication strategies to address misconceptions about the HPV vaccine.

Some individuals perceive health as beyond their control, surrendering themselves to luck, fate, or a higher power [ 70 ]. In this review, parents’ religious beliefs were found to influence HPV vaccine acceptance. This result is consistent with previous studies [ 11 , 12 , 32 ]. Parents who strongly adhere to religious or cultural views are less likely to accept HPV vaccination [ 60 ]. A qualitative study involving parents of adolescents from Arabic backgrounds in Western Sydney revealed the role of parents’ religion in forming attitudes about HPV vaccination [ 63 ]. Children born to Muslim mothers were found to have a higher likelihood of being under- or unvaccinated compared to their Hindu counterparts [ 33 ]. Many female students in the French-speaking part of Switzerland often cited parental opposition as one of the primary reasons for declining HPV vaccination [ 11 ].

Moreover, the review identified misconceptions about the vaccine’s composition. This finding is consistent with those of a study that some Muslim students believe the vaccine contains pig protein, which is why Muslim families may avoid using it [ 59 ]. Many mothers indicated that they would not permit their teenage children to have the HPV vaccine if it was non-halal [ 63 ]. This result also explains why some religious leaders are against vaccination. A study revealed that some imams have forbidden the use of vaccines due to their alleged porcine components [ 71 ]. Islamic law prohibits using medicines or ingredients derived from haram sources, specifically those containing pig and its derivatives [ 72 ].

Despite considerable evidence showing little connection between the HPV vaccine and infertility, rumors about the vaccines serving some genocidal purpose continue in the Islamic community. This review highlighted the paucity of qualitative studies addressing the association between the HPV vaccine and infertility in Islamic countries. Studies in Islamic countries have mainly focused on concerns about vaccines in general. For example, in a study by Sheikh and colleagues (2013) [ 71 ], participants stated that “Vaccination is a conspiracy of the Zionists. Vaccinating our children will inevitably make them sterile.” Schuler and colleagues (2014) [ 73 ] reported that mothers with concerns about vaccine-associated infertility had less intention to vaccinate their sons than other parents. And yet, a self-reported survey of women aged 20 to 33 showed that those who had been married and had received an HPV vaccine were less likely to report infertility [ 74 ]. A recent systematic review and meta-analysis study shed light on the need for high-quality prospective studies to confirm the relationship between the HPV vaccine and infertility [ 75 ].

Objections were observed in the studies that examined the role of religious authorities in shaping attitudes towards HPV vaccination. These objections may have arisen from concerns about the vaccine’s compatibility with religious principles or broader ethical considerations, emphasizing the need for a nuanced engagement with religious leaders to promote informed decision-making regarding vaccination. A study from South Dakota found that religious leaders’ messages were more effective than statements from political or medical figures in shaping a positive perception of the COVID-19 vaccine [ 76 ]. Conflicts between religious practices and medical recommendations can lead to misunderstandings and poor treatment adherence [ 70 ]. This finding emphasizes the impact of religious leaders on health-related behaviors within their communities. The role played by religious leaders or institutions suggests that collaborating with them could enhance health education for HPV vaccine acceptance. Therefore, recognizing the importance of diversity is vital for understanding specific religious dynamics and ensuring that public health strategies remain culturally and religiously sensitive.

Limitations

This scoping review has several limitations. First, its geographical focus is primarily on the OIC countries. This may limit the findings’ applicability to other regions with different religious and cultural backgrounds. Second, the literature search was limited to three databases: MEDLINE/PubMed, Embase, and CINAHL. This selection might exclude relevant studies published in local journals or languages other than English. Third, the methodological diversity among the included studies, encompassing various research designs and sample sizes, complicates data comparison and synthesis, potentially impacting the conclusion’s strengths. Fourth, focusing on religious factors might lead to underestimating other important determinants such as socioeconomic status, education, and healthcare access, which can also influence health decisions and vaccine uptake. Fifth, the review did not find any articles that specifically compared HPV vaccine acceptance between the Sunni and Shia branches of Islam. Although most of the countries in this review are predominantly Sunni, the lack of explicit comparisons limits our understanding of potential differences in religious influence on vaccine acceptance. The primary aim of this study was to explore the broader impact of religious beliefs on HPV vaccine acceptance within the OIC countries. The existing literature did not provide explicit comparisons between these branches. Future research should explore these potential differences to provide a more nuanced understanding of the impact of religious beliefs on HPV vaccination. Sixth, the majority of the included studies did not conduct gender-specific analyses, which limits our ability to fully understand gender differences in HPV vaccine acceptance across different cultural contexts. Seventh, none of the included studies explicitly addressed the impact of COVID-19 on HPV vaccine perceptions. The pandemic has significantly influenced public perceptions of vaccines, highlighting issues of vaccine hesitancy, misinformation, and public trust. Future research should include comparative analyses of HPV vaccine acceptance pre- and post-COVID to understand the pandemic’s impact on vaccination behavior and public trust. Lastly, despite a systematic approach, the restriction to English language studies and Muslim countries could lead to favoring certain types of studies, possibly overlooking useful research that does not fit the predefined parameters. Future research should employ multilingual searches to ensure a more comprehensive inclusion of relevant literature.

Several findings from this study contribute to understanding the religious factors that influence the acceptance of HPV vaccines. The review showed that religious beliefs did not always affect overall vaccine uptake, but they did influence vaccine acceptability. The study identified a range of misconceptions and beliefs related to HPV vaccination. Some of these misconceptions included seeing the vaccine as a form of ethnic cleansing, a license for wanton behavior, a defiance of religious norms, a sneaky way to inject good Muslims with haram ingredients, and an abandonment of righteous principles in general.

This study also investigated public health interventions that responded to these misconceptions. To encourage HPV vaccine uptake in Islamic countries, public health strategies must adopt a holistic approach that incorporates religious, cultural, and social aspects. A key strategy mentioned in the studies is engagement with religious leaders and communities. Leveraging the influence of religious leaders can shift community attitudes toward vaccine acceptance, especially when the messages are aligned with religious teachings and values. Educational materials should present the facts about HPV vaccines in a manner that respects religious beliefs. The adaptability of public health campaigns to regional variations in faith and practices can ensure that the interventions are relevant to different cultural contexts. Training health professionals in religious literacy and cultural competence is also essential,because it can equip them to better understand and address the concerns of the communities they serve. Future research should focus on deepening our understanding of the dynamic relationship between religious beliefs and health behaviors. Comparative studies across different contexts are essential for understanding the different ways that religion influences health decisions. Qualitative studies are critical as they can provide a deeper understanding of religious beliefs on vaccine acceptance and other religious-related health behaviors.

Supporting information

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PMC11329594

Neuroendocrine neoplasms of the breast: a review of literature

Federica vegni.

Division of Anatomic Pathology and Histology-Fondazione, Policlinico Universitario “Agostino Gemelli”-IRCCS, Università Cattolica del Sacro Cuore, Largo Francesco Vito, 1, 00168 Rome, Italy

Ilenia Sara De Stefano

Federica policardo, pietro tralongo, angela feraco, angela carlino, giulia ferraro, qianqian zhang, giulia scaglione, nicoletta d’alessandris, elena navarra, gianfranco zannoni, angela santoro, antonino mule, esther diana rossi, associated data.

There is a word file including the details of our cases.

Primary neuroendocrine neoplasms (NENs) of the breast are characterized by neuroendocrine architectural and cytological features, which must be supported by immunohistochemical positivity for neuroendocrine markers (such as Chromogranin and Synaptophysin). According to the literature, making a diagnosis of primary neuroendocrine breast cancer always needs to rule out a possible primary neuroendocrine neoplasm from another site. Currently, the latest 2022 version of the WHO of endocrine and neuroendocrine neoplasms has classified breast NENs as well-differentiated neuroendocrine tumours (NETs) and aggressive neuroendocrine carcinomas (NECs), differentiating them from invasive breast cancers of no special type (IBCs-NST). with neuroendocrine features. The current review article describes six cases from our series and a comprehensive review of the literature in the field of NENs of the breast.

Introduction

Primary neuroendocrine neoplasms (NENs) of the breast are characterized by neuroendocrine architectural and cytological features, which must be supported by immunohistochemistry positivity for neuroendocrine markers (such as Chromogranin and Synaptophysin) [ 1 ]. Making a diagnosis of primary neuroendocrine breast cancer needs to rule out metastasis from another anatomical site [ 2 ]. The Br-NEN classification has undergone substantial changes over the years and in the various editions of the WHO that have followed (2003, 2012). Currently, according to the latest 2019 classification of the WHO of breast tumours, NENs of the breast are classified as well-differentiated neuroendocrine tumours (NETs), aggressive neuroendocrine carcinomas (NECs) and invasive breast cancers of no special type (IBCs-NST) with neuroendocrine features. A similar diagnostic approach is recommended in the WHO blue book (2022) on endocrine and neuroendocrine tumours, in the chapter on neuroendocrine neoplasms in non-endocrine organs [ 3 ]. Because of their rarity (< 1% of breast cancers), the literature is not so extensive, and despite continued advances in research, especially in the molecular biology, to date, there are still no specific guidelines regarding their treatment [ 3 ].

The true incidence and clinical features of Br-NENs (breast-NENs) are difficult to define, since neuroendocrine (NE) markers are not routinely used in breast cancer diagnosis and, to date, studies have not established a definitive value for immunohistochemistry (IHC) positivity in order to establish a NE differentiation [ 2 ]. Incidence is highly variable, from < 0.1 to 5.4%, probably due to the completely different data collection procedures [ 4 , 5 ].

Specifically, the third version of the WHO classification, published in 2003, was the first one to classify Br-NENs as a distinct pathological entity. They were divided into three categories: solid NECs, small cell/oat cell carcinomas, and large cell carcinomas [ 6 ]. They were distinguished by NE morphologic characteristics comparable to those of GI/lung NETs and expression of NE markers in more than 50% of cell populations. The 2012 WHO Working Group included NENs under the category “carcinomas with NE features” (exhibiting morphological features similar to those of NE tumour of GI tract and lung and expressing NE markers, i.e., chromogranin (CgA) and synaptophysin (Syn) [ 7 , 8 ]. Thus, in the 4th edition (2012), the definition of NE breast cancers was changed to “cancers with NE features” and the threshold of 50% NE markers was removed. Invasive breast carcinomas with NE differentiation, well-differentiated neuroendocrine tumours (WD-NETs), and poorly differentiated small cell carcinomas were recognized as three subtypes of carcinomas with NE features . Well-differentiated NETs, despite their morphological similarities with carcinoid tumours of other sites, often lacked the classical nuclear features. NECs exhibited common features of small cell carcinoma (SmCC), rather than large cell NEC (LCNEC). Moreover, invasive BCs with NE differentiation exhibited distinct subtypes, including MC of type B and SPC, as well as IBCs-NST. Additionally, lobular invasive carcinomas with NE differentiation were observed, though this occurred less commonly.

In the most recent WHO classification (5th ed. 2019)), the term NEN is used for all neoplasms with predominately NE differentiation, which is separated into well- and poorly differentiated neoplasms based on the presence of NE histological /immunohistochemical characteristics in more than 90% of the neoplasm. A well-differentiated NEN corresponds to NET, whereas a poorly differentiated NEN corresponds to NEC. Both categories have low/intermediate or high Nottingham histologic grade NE morphology, as well as extensive NE markers expression [ 5 ]. In this way, according to the Nottingham grading system, Br-NENs are graded as well-differentiated tumour (G1), intermediate differentiated tumour (G2), or poorly differentiated (G3) carcinoma. Special-type breast carcinomas (BCs) expressing NE markers, such as SPCs and MCs, were removed from the NEN category.

Two authors independently conducted the online literature search via PubMed, within the last 10 years. This search started on June 1, 2013, and was continued every day before the last search on July 31, 2023. The terms and free text words were combined using Boolean operators (AND, OR). The following search string was used and inserted into the search bars of the previously reported databases: “breast” AND (“neuroendocrine carcinoma” OR “neuroendocrine tumours” OR “neuroendocrine differentiation”). We considered only studies written and published in English. Abstracts, duplicates, incorrectly entered population, and publications without complete data were excluded. The last search was conducted on 07/31/2023, reporting a total of 7152 records on the PubMed database. These records were screened by title and abstract only, and a total number of 2215 articles passed the first screening process. The resulting records were subjected to full-text reading to meet the exclusion criteria. After this last step, a total of 109 articles met the criteria and were included in the quality and summary. To supplement the literature, we report 6 case reports from the Agostino Gemelli IRCCS University Policlinic Foundation.

Case reports

Cases are all summarized in Table 1 . Herein is the detailed description for each of them.

The table details the cases analyzed in the manuscript

Case n	Age	Diameter (mm)	Localization	Presence of in situ carcinoma	ER/PR/Her2	Ki-67	GATA3	Other immmunohistochemical markers	Histological diagnosis
1*	54	7	UOQ-LB	LIN 1/2	-/-/0	3%	-	/	Metastasis from thyroid medullary carcinoma
		4	UOQ-RB	LIN2	10%/10%/0	5%	-	CrA + Syn +	Metastasis from thyroid medullary carcinoma
2	67	/	UOQ-LB	no	-/-/0	90%	-	AE1/AE3 + CrA + Syn + CK20 + CK7-HMWCK TIF-1-CDX2-p63-p40-Mammoglobin-	Metastasis from Merkel cell carcinoma of the skin
3	46	23	UOQ-LB	no	95%/90%/0	80%	+	SSTR2A +	PD-NEC from the breast
4	40	22	IOQ-LB	DCIS	100%/60%/2 + (NA)	35%	+	CrA + Syn +	IC-N G3 from the breast
5	36	95	UOQ-LB	DCIS-N	-/-/0	70%	+	CrA + Syn + CK7 + TTF-1	PD-NEC from the breast
6	47	3	IOQ-LB	no	95%/95%/2 + (NA)	30%	+	CrA + Syn +	IC-N G2 from the breast

LB ; left breast, RB ; right breast, UOQ ; upper quadrant, IOQ ; inferior quadrant

A 54-year-old woman, with no available clinical information, presented with a 7-mm nodule in the upper outer quadrant of the left breast. Histological diagnosis was multiple foci of small cell carcinoma with NE differentiation associated with foci of lobular intraepithelial neoplasm (LIN) 1/2 and a triple-negative immunohistochemical profile (Fig. 1 ). Eight years after, a new 4 mm nodule was diagnosed as invasive carcinoma with LIN-2 foci (Figs. (Figs.2, 2 , ,3, 3 , and and4), 4 ), showing positivity for CgA and Syn, and a Ki-67 of 5%. Sentinel lymph nodes were negative (Figs. (Figs.5 5 and and6) 6 ) (Table 1 ). Surprisingly, it was only after this second surgery that it became known that the patient had been under follow-up and treatment (with somatostatin analogues—SSAs and periodic monitoring of serum calcitonin and CEA levels) for multi-metastatic medullary thyroid carcinoma since 1994. The recognition of this finding, although late, allowed both lesions to be classified as secondary to the original medullary thyroid carcinoma. Given the rarity of this type of neoplasm, careful anatomic-clinical integration is therefore essential to complement the histologic examination (in particular calcitonin immunohistochemical analysis and Congo Red histochemical evaluation have been performed).

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Multiple foci of carcinoma with small cells and neuroendocrine differentiation in breast tissue with numerous foci of LIN1-2 (H&E 200X)

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Details of invasive carcinoma with some foci of LIN2 (H&E 400X)

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Sheets and nests of round or slightly spindle or plasmacytoid cells with round to oval, regular hyperchromatic nuclei with occasional nucleoli, salt and pepper chromatin in a fibrous tissue. Mitoses were scant (H&E 200X)

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Routine mammography: multiple bilateral calcifications and 4 mm hypo-echoic, homogeneous, roundish nodule at EUQ (RIGHT BREAST), with pale margins, with lobular appearance and not-well defined borders

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Foci of neoplastic cells with expression of Chromogranin A (AB, 200X)

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Foci of neoplastic cells with expression of Synaptophysin (AB 400X)

A 67-year-old woman presented with a nodule of the superior-external quadrant of the left breast, which histologically showed solid architecture and small, hyperchromic cells, giving the neoplasm a “blue appearance” (Table 1 ). The conclusive diagnosis was poorly differentiated carcinoma with small cells and neuroendocrine differentiation with Merkel-like features. Metastasis could not be excluded; in fact, medical history revealed that several years earlier the patient had removed a skin CK20 + nodule, diagnosed as Merkel cell carcinoma. Therefore, the final diagnosis was Merkel cell carcinoma, being metastatic to the breast.

Metastases to the breast affected two patients aged respectively 54 and 67 years. Metastases originated from thyroid medullary carcinoma (case 1, two nodules) and Merkel cell carcinoma of the skin. In both cases, clinical history was of crucial importance for the diagnosis. In case 1, it is of note that lobular in situ neoplasia of classic type was present in the breast parenchyma surrounding the neoplastic nodules. In both cases, ER/PR/Her2 and GATA3 stained negative in the neoplastic cells.

A 46-year-old woman presented with a 2.3 cm lump in the superior external quadrant of the left breast. Histologically, the lesion showed an insular architectural pattern consisting of cells with increased nucleus/cytoplasm ratio, pleomorphism, and salt-and-pepper nuclei, with intense mitotic activity (Figs. (Figs.7 7 and and8). 8 ). The cells were positive for CgA and Syn, SSTR2A, ER (95%), PR (90%), HER2 score 0, and ki-67% of 80%, with a definitive diagnosis of breast poorly differentiated-NEC (Figs. (Figs.9 9 and and10) 10 ) (Table 1 ).

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Foci of neoplastic cells with insular pattern (H&E 400X)

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Details about the mitotic activity in the neoplastic foci (H&E 400X)

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a and b Details of the expression of SSTR2A with different intensity (strong in a , moderate in b ) (AB 400X)

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Neoplastic areas with cribriform and papillary architecture (H&E 200X)

A 40-year-old woman showed a 2.2 cm nodule at the inferior-outer quadrant of the left breast. Histologically, a cribriform and papillary architecture were detected, with also solid nests and pseudo-rosettes, associated with a perilesional ductal carcinoma in situ (Table 1 ), with a final diagnosis of ductal invasive carcinoma G3, with neuroendocrine differentiation (Fig. 11 ).

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Neoplastic areas with pseudorosette and solid nests (H&E 400X)

A 36-year-old woman exhibited a 9.5 cm nodule at the superior external quadrant of the left breast. Histologically, it presented with a trabecular, cordonal, and insular pattern, consisting of cells with high nuclear and cytologic pleomorphism, increased nucleus/cytoplasm ratio, numerous mitotic figures, and foci of necrosis. Foci of cribriform and solid ductal carcinoma in situ were observed at the periphery of the lesion (Table 1 ). In light of morphological and immunohistochemical features, the differential diagnosis for this lesion included a NEN with pulmonary primitivity. However, literature cases [ 5 – 7 ] reported that these immunophenotypic features, if also present in the associated intraductal component, were suggestive of a mammary primary. Thus, the definitive diagnosis was breast poorly differentiated-NEC.

A 47-year-old woman came to our attention with a 3 cm mass-like area in the inferior outer quadrant of the left breast. Histologic examination showed a lesion with papillary/cribriform ductal invasive NST, and MC type B architecture, consisting of cells characterized by “salt and pepper” chromatin, high nuclear and cytologic pleomorphism, and some mitotic figures (Table 1 ). The definitive diagnosis was invasive ductal carcinoma G2, with neuroendocrine differentiation.

Four cases presented primary Br-NEN. Patients were all females, aged 36 to 47 years (mean 42).

ER/PR and GATA3 were positive in all cases. HER2 was 2 + in two cases.

Clinical features

Patients with Br-NEN present clinically in a similar way to patients with IBC-NST. Women of postmenopausal age or elderly are more likely to be affected [ 9 ]. No clinical data exist describing how Br-NEN manifests with clinical disorders linked to ectopic hormonal production, including carcinoid syndrome. A considerable proportion of patients diagnosed with NEN present with the disease at stage 2, and they are at a greater risk of developing local lymph node metastases [ 10 – 13 ].

Most cases of Br-NENs in postmenopausal white women in their last seventh decade of life have been reported, 10 years later than the usual types of BC; few cases in males have been described. In contrast to those who have invasive ductal carcinoma not otherwise specified (IDC-NOS) [ 14 , 15 ].

Radiological features do not substantially differ from those of primary breast cancers, being more similar to those of triple-negative breast carcinomas [ 16 – 18 ]. Somatostatin receptor (SSTR) scintigraphy or positron emission tomography (PET) with somatostatin analogues marked with gallium-68 is useful for predictive purposes if therapy with somatostatin analogues is indicated Care should be taken as SSTR scintigraphy with Indium-111 cannot detect small (< 1 cm) tumours, tumours SSTR negative, or with low affinity for the SSA octreotide [ 18 ].

Patients with highly differentiated tumours or advanced cancers may undergo PET-CT with 18-fluorodeossiglucose [ 19 ].

Macroscopic features

At gross examination Br-NENs are nodules with dimension variable from 0.8 to 13.5 cm (mean size of 2.7 cm); they can appear yellowish-coloured, with infiltrative margins or roundish/multilobulated with expansive margins; they can have firm consistency or they can be soft and gelatinous at cut surface, in particular, when if associated with a mucinous component [ 20 , 21 ].

Histological features of Br-NECs, Br-NETs, and of invasive carcinomas of no special type with neuroendocrine features

In the 5th WHO classification edition, NEC is defined as a high-grade malignant neoplasm [ 21 ], with histological characteristics resembling those of lung SCNEC and LCNEC, respectively. Despite being rare cancer, it exhibits distinctive morphological characteristics: densely packed hyperchromatic cells (cellular streaming) with scant cytoplasm, streaming, and crush artefacts in SCNEC (nuclear moulding is not a prominent feature); large cell with pleomorphic vesicular or hyperchromatic nuclei with irregular membranes and prominent nucleoli in LCNEC.

The precise morphological traits of Br-NETs remain uncertain. The identification of neurosecretory granules and extensive, homogeneous positivity for NE markers is employed to categorise NETs as low- to intermediate-grade invasive tumours with NE differentiation. INSM1 is reported to be a new marker and may aid in the diagnosis of NEN in addition to conventional NE markers [ 22 ]. Histologically, fusiform/plasmacytoid/polygonal/spindled cells with abundant eosinophilic and granular/vacuolated cytoplasm to large clear cells, with smooth nuclear borders, inconspicuous nucleoli, and salt and pepper chromatin are arranged in trabeculae and solid, densely packed nests, within a delicate/thin fibrovascular stroma. Ribbons, cords, and rosettes, which are typical characteristics of carcinoid tumours of the lung or NETs in the gastro-entero-pancreatic system, are not always present in Br-NETs. Extracellular mucin deposits or signet ring cells can also be detected. From a clinic-pathological point of view, a diagnosis of Br-NET, although the term tumour, implies an identical treatment to any BC of comparable grade, stage, and hormonal profile, being most Br-NETs hormonal receptors positive.

There is still a lack of clear-cut standardized diagnostic criteria to differentiate real Br-NENs from BCs having some degree of neuroendocrine differentiation. An effective differential diagnosis requires validated and reproducible morphological criteria, and well-defined qualitative and quantitative thresholds for neuroendocrine marker assessment. A previous study demonstrated that breast cancers with neuroendocrine differentiation are frequently misdiagnosed, making their identification challenging. They often lack specific morphological features. In addition, invasive ductal carcinoma and invasive lobular carcinoma (alveolar variant) can mimic some breast cancers with NE differentiation. Furthermore, the impact of NE differentiation in BC on prognosis is unclear, with studies reporting conflicting results [ 23 , 24 ]. The authors conclude that the correct classification of breast cancers with NE differentiation requires thorough observation of cytologic and structural characteristics and confirmation by IHC. Researchers have also explored the morphological characteristics of breast cancers with NE differentiation [ 22 , 25 , 26 ]. One study compared the characteristics of cancers in which more than 50% of the cells were positive IHC for NE markers with neoplasms of comparable morphology but negative IHC for NE markers. The presence of large, solid, cohesive nests, intermediate nuclear and histological grades, plasmacytoid tumour cells with spindle or columnar shapes, eosinophilic granular cytoplasm, and round nuclei were all identified by the authors as indicators of breast cancer with an NE component [ 27 ].

Diagnostic characteristics of NE-differentiated breast cancers in needle biopsy specimens

Apart from the known challenges in diagnosing NE-differentiated breast cancers by needle biopsy, there is very little literature describing in detail the diagnostic characteristics of NE-differentiated breast cancers in needle biopsy specimens. NETs are distinguished by loosely coherent sheets of orderly cells with plasmacytoid, eccentric granular cytoplasm, spherical nuclei with spotted “salt and pepper” chromatin, and discrete nucleoli, among other cytologic characteristics. The NEC resembles NECs developing at other places as well as the SCNEC of the lung. Further research is therefore required to accurately characterize and categorize breast cancers with NE differentiation [ 28 ].

Pure and mixed forms

Finally, in the breast parenchyma generally, the diagnosis of pure Br-NENs can be applied in a small subset of cases, whereas mixed forms, in which NEN component co-exists with an NST or special type BC, are more common. However, although mixed neoplasms (mixed neuroendocrine/non-neuroendocrine neoplasms, MiNENs) are considered an integral part of NENs in the digestive tract and other organs, the 2019 WHO classification of breast tumours does not consider this entity as a NEN.

Immunohistochemistry and molecular subtype

Immunohistochemical analysis of NE biomarkers represents the gold standard in the diagnosis of NENs. Together with the most sensitive and specific markers, namely CgA and Syn, recently, a novel biomarker, INSM1, has been proposed as an accurate indicator of NE differentiation to support NEN diagnosis, in particular, in poorly differentiated neoplasms [ 29 ]. However, these immunomarkers are not routinely assessed, whilst they are reserved only when a well-trained / expert pathologist identify or suspect a NE morphology in H&E-stained routinary slides.

We must remember that none of the above-mentioned NE markers proved to be useful in clearly distinguishing pure Br-NENs from other breast carcinomas with NE differentiation [ 30 ]. As a result, the diagnostic criteria, the proposed cut-off for NE immunomarkers, and the terminology of Br-NEN have varied in recent studies [ 23 ] creating limitations for the correlation of data. Well-differentiated NETs and poorly differentiated NECs are more likely to show diffuse NE marker positivity than IBC-NEDs.

ER/PR/AR markers show positivity in most well-differentiated NETs and in greater than 50% of poorly differentiated NECs (most NETs fall into the luminal B molecular subtype and molecularly cluster together with mucinous A-B tumors) . Poorly differentiated NECs of the breast often show expression of TTF1 (generally well known as a lineage marker of lung origin) and up to 45% of them also show expression of AR, often co-expressed with GCDFP15. Negativity for basal markers (CK5/6, CK14, p63) as well as the EGFR protein has been observed. CDX2 consistently shows negativity in primary breast NETs, so it could be useful to differentiate it from a gastro-intestinal primary. Other markers such as Calcitonin, CEA, PAX8 (variable and weak) [ 31 ], and the Congo red for amyloid, together with a triple-negative phenotype (ER-, PR-, HER2 score 0) can aid in diagnosing a breast metastasis from a medullary thyroid cancer,

SSTR expression in breast NENs, similarly to extra-mammary NENs, is a well long-known phenomenon, potentially allowing SSTR-based tumour imaging (octreoscan or 68 Ga-DOTATOC PET/CT) and SSTR-targeted tumour treatment (octreotide or lanreotide) [ 30 ]. Specifically, SSTR1-5 are G-protein-coupled plasma membrane receptors with 7 trans membrane regions; among them, SSTR 2A is a subtype overexpressed in the majority of NE tumours and also most commonly expressed in BC (6, being able to mediate the antiproliferative effect of molecular-targeted therapy with SSA in the strongest manner [ 32 ].

However, the SSTR 2A positivity rate in BC-NENs has only been analysed in two studies [ 23 , 33 ]. These recently published retrospective analyses of selected NENs reported a SSTR 2A positivity rate of 71% and 50%, respectively [ 23 , 33 ]. SSTR 2A, when overexpressed, can be a good candidate for the targeted therapy with SSA such as octreotide or lanreotide (antisecretory treatment and antiproliferative activity in functional NENs). In extra-mammary NENs, this therapy is mainly being considered in well-differentiated NETs (G1/2, Ki-67 < 10%) [ 34 , 35 ]. Current recommendations for Br-NENs therapy rely on general guidelines for breast cancer. Only SCNEC has specific therapeutical recommendations (i.e., platinum/etoposide-based chemotherapy similar to small cell lung cancer). SSA therapy has been evaluated in BC-NST and seemed to show response rates of up to 40% in a metastatic setting in phase I – II trials [ 36 ]. However, a phase III study comparing endocrine therapy with or without octreotide in primary ER + BC did not show a real clinical benefit of SSA treatment in this setting [ 37 ]. Thus, outside of the context of the exceedingly rare SCC of the breast, NE differentiation in breast neoplasms seems to be not regarded to have therapeutic significance.

Molecular features

From a molecular point of view, Br-NENs have been considered a distinct subtype of luminal (generally) breast carcinoma, occurring predominantly in post-menopausal women. They are ER (100%), PR (89%), GATA3 (98%), FOXA1 (96%), and CK8/18 (98%) positive. There was an almost equal distribution of luminal A (52%) and B (48%), with a low rate of PIK3CA and p53 mutations, lack of concurrent 1q gains/16q deletions, reported trisomy of chromosomes 7 and 12 and FGFR mutations, high frequency of GATA3 mutations and an aggressive clinical behaviour, representing a histologically and genomically entity related to MC, distinct from ER + /HER2- IBC-NST. There was no evidence of gene amplification in cMET, EGFR, or TOP2A. Targeted sequencing of 47 genes discovered variations in the TP53, PIK3CA, ERBB4, and APC genes. Gene expression data (including the somatostatin receptor gene family—SSTR1/2/3/4/5) were available for 5 patients, for which 3 out of 5 patients showed overexpression of at least one SSTR gene.

Differential diagnosis

Breast NENs have a wide range of potential diagnoses, including both benign and malignant conditions. Primary breast NEN can potentially be diagnosed as metastasis from other organs. Similarly, metastatic neuroendocrine neoplasm of extra-mammary location in the breast setting is the most significant differential diagnosis that must be ruled out [ 23 , 38 – 40 ]. Metastatic NENs from an extramammary site represent 1 to 2% of secondaries to the breast. In one review, 25 up to 44% (8 of 18) of metastatic NENs to the breast were misdiagnosed as primary breast cancers [ 40 ]. The distinction of primary from metastatic NEN is critical to avoid misdiagnosis and unnecessary surgical and medical therapy in the latter.

Primary Br-NEN are morphologically similar to NENs arising in other organs. Features indicating a primary breast origin are the positivity of site-specific lineage markers indicating breast origin as ER/PR/AR, GATA3, mammaglobin, GCDFP15; axillary N + ; lack of a history of an extramammary primary NEN; nuclear atypia or pleomorphism; the presence of a surrounding in situ component. However, in rare cases, similarly to Case 1 of our series, the detection of an in situ component seems to contradict this concept: specifically, in our case, an in situ lobular carcinoma was present around the metastatic thyroid medullary carcinoma. On this wave, careful clinical history and whole-body radiological imaging are of outmost important to correctly address the diagnosis. In doubtful cases, organ-specific markers can be of help [ 38 – 42 ].

Regarding the molecular subtype, most breast NENs are hormone receptor-positive and human epidermal growth factor receptor 2 (HER-2)-negative, presenting a luminal-like phenotype, so that ER might help to distinguish BR-NEN from possible metastasis. On the other hand, we have to consider that hormonal receptors may also be positive in metastatic neoplasms. Consequently, the diagnosis of BR-NENs is made on histology and IHC staining of neuroendocrine markers (Syn, CgA, INSM1), which should be always performed in the suspicion of a neuroendocrine differentiation, and supported by clinical and imaging data [ 38 – 40 ].

In routinary practice, breast carcinomas with neuroendocrine features are frequently underdiagnosed. This rate of misinterpretation is not surprising given the variable neuroendocrine features of primary breast NENs and the absence of standard testing for neuroendocrine markers. Misdiagnosis of neuroendocrine features in IDC-NOS or in lobular invasive carcinoma is unlikely to be significant, given the fact that there is no agreement on the clinical and prognostic implications of neuroendocrine differentiation [ 38 – 40 ].

Endocrine ductal carcinoma in situ (E-DCIS) and SPC share usual ductal hyperplasia (UDH) as a differential diagnosis. Both solid papillary carcinoma and E-DCIS have a solid growth pattern and cells that arrange themselves in a pattern like UDH. Because neuroendocrine marker positivity is not seen in benign breast lesions, it validates a diagnosis of E-DCIS or solid papillary cancer. UDH will also be ruled out if cytokeratin 5/6 is negative and ER is diffusely positive (clonal-type). Solid papillary carcinomas, unlike UDH, are negative for myoepithelial markers (smooth muscle myosin, actin, and p63) [ 23 , 38 – 41 ].

Some claimed that treating Br-NENs, particularly NETs, in the same manner as NENs originating in other organs, requires careful consideration because current Br-NETs lack a clear-cut morphology and rely on IHC for CgA and Syn, which can occasionally be expressed in other non-NENs as well. The authors also noted that breast NETs and non-NEN BCs exhibit similar clinical behaviours and therapeutic responses and that BrNETs and luminal type A breast cancer exhibit more similarities than NETs derived from other organs, according to molecular and genetic analyses.

NENs behave similarly to other invasive BCs so that the treatment plan is also based on prognostic and predictive factors, such as the TNM stage, ER and PgR receptor status, HER2 status, genotypes and nuclear grade, Ki67 index, age, menopausal status, and general health conditions, such as those that apply to another breast invasive tumours. One of the first distinct in treatment is between localized and metastatic disease. A minority of patients have a localized disease with no randomized trials to guide the management mostly due to the rarity. The management and therapeutic approach are mostly based on retrospective studies and/or case reports. However, surgery represents the first option for localized disease, similar to ductal and lobular cancers. Furthermore, adjuvant chemotherapy and chemoradiation are both used after surgery mostly depending on the tumour size, lymph nodal involvement, and metastases. In the next paragraphs, we briefly discuss some of these aspects in the management of these lesions.

According to the IBC-NST, both adjuvant and neoadjuvant chemotherapy are equally beneficial in reducing the risk of a distant recurrence and the mortality rate from brain cancer [ 40 ] In recent years, the practice of treating cases by escalation or de-escalation, in which postoperative care can be tailored based on the efficacy and responsiveness to neoadjuvant therapy, has also come to be accepted [ 42 – 45 ]. In cases of metastatic disease, palliative systemic chemotherapy is the main treatment.

According to the St Gallen guidelines, and regardless of the histotypes, women presenting with screen-detected or other early breast cancers are potential candidates for breast-conserving surgery [ 46 ] Nevertheless, several patients prefer a mastectomy including contralateral mastectomy mostly associated with the fears of recurrence, improvements in reconstruction techniques, more widespread use of MRI imaging during the diagnostic evaluation, genetic testing and lack of adequate physician/patient communication [ 47 ] Specifically, patients with resectable Br-NENs are advised to undergo surgery. To choose the best surgical strategy, it is crucial to distinguish between primary NENs and metastatic NENs from other organs [ 48 – 50 ].

Chemoradiotherapy

Adjuvant systemic therapy should be used based on each patient’s clinicopathological features and risk of recurrence. Data from literature are not sufficient to compare the benefit of adjuvant platinum-based versus taxane-based and/or anthracycline regimens [ 51 ]. The majority of studies, showing the long-term survival benefit of etoposide plus cisplatin or carboplatin have been derived from small-cell lung cancer studies [ 52 ]. Also, the number of cycles, six or four, is not well assessed and it is mostly based on patient tolerance [ 52 ]. Although the efficacy of adjuvant chemotherapy in patients with Br-NENs has not been reported in specific clinical trial reports, patients with high-risk disease should be treated with adjuvant or neoadjuvant chemotherapy on an individual basis. The key considerations when selecting whether to start adjuvant or neoadjuvant chemotherapy for patients with IBC-NSTs are tumour size, nodal status, nuclear grade, age, tumour subtype determined by IHC for ER, PgR, and HER2, and the Ki67 index. Tumour size and nodal status are also important predictors of recurrence in patients with Br-NENs [ 53 ].

Based on findings from GI NETs, breast NETs may be less sensitive to chemotherapy (CHT) than IBC-NSTs [ 54 – 58 ]. For the metastatic patients, the first line of chemotherapy has been derived from small-cell lung cancer, with etoposide plus platinum as the first standard approach [ 59 , 60 ]. More clinical trials are needed to determine whether the anthracycline plus taxane combination is a viable therapeutic option for people with high-risk Br-NENs.

Escalation therapy or response-guided treatment is being developed primarily in TN breast cancer. Adjuvant capecitabine treatment for 6 months enhanced disease-free survival in patients with remaining triple-negative breast cancer following conventional neoadjuvant chemotherapy [ 61 ].

Radiotherapy (RT) for the chest wall and regional lymph nodes should be given in the same way that it is for IBC-NSTs [ 45 , 62 , 63 ]. There have been no reports of clinical trials of radiation following surgery for Br-NEN patients. One case-controlled study found that RT improved survival in patients with NEC of the breast as defined by the WHO 2003 classification [ 45 ], whereas another population-based study found that adjuvant radiotherapy did not improve survival in patients with primary SCNEC of the breast [ 55 ].

In conclusion, basically, today, neuroendocrine neoplasms, except small cell type, do receive similar systemic treatments as stage and biomarkers matched NST carcinoma with or without neuroendocrine differentiation.

Hormonal and molecular therapy

According to case studies, Br-NENs are usually HR-positive, making hormone therapy a viable treatment option [ 11 , 64 , 65 ]. Breast NETs treated with hormonal therapy (HT) and RT had longer overall survival (OS) and disease-free survival (DFS) than those who did not receive, while patients who received CHT had lower OS and DFS than those who did not.

Adjuvant hormone therapy is recommended for 5–10 years for IBC and NST [ 65 ], and is also indicated for HR-positive Br-NEN. Combining an aromatase inhibitor or fulvestrant with a CDK4/6 inhibitor resulted in a significant improvement in progression-free survival and overall survival compared to hormonal therapy alone in important clinical studies in patients with HR-positive IBC-NSTs [ 66 – 72 ].

Recent molecular studies have found PIK3CA mutations in 7–33% of Br-NENs, which is lower than the prevalence reported in HR-positive HER2-negative IBC-NSTs [ 73 – 76 ]. A conventional therapy strategy for HR-positive, HER2-negative IBC-NSTs is to target the PI3K/AKT/mTOR pathway using a PI3K inhibitor (e.g., alpelisib) and a mTOR inhibitor (e.g., everolimus) in different studies [ 77 – 80 ] Interestingly, oncogenic, or possibly oncogenic PI3K pathway mutations were more prevalent in NETs than in NECs (50% vs. 18.2%). Targeting the PI3K/AKT/mTOR pathway may, therefore, be a realistic and promising method for treating HR-positive HER2-negative Br-NENs, particularly NETs.

Anti-HER2 therapy is appropriate for HER2-positive Br-NENs. Although there is minimal evidence that HER2 status predicts NENs, there is a case report in the literature of the success of trastuzumab treatment in a patient with NEC and HER2 amplification of the breast [ 81 ]. Another instance with well-differentiated NET of the breast with HR-positive HER2-positive status was treated with surgery, adjuvant CHT, trastuzumab, and HT, resulting in disease-free status after 9 years of follow-up [ 82 ]. Several other anti-HER2 agents and an antibody–drug conjugate have been established as standard treatments for HER2-positive IBC-NSCLC in both the adjuvant and metastatic settings [ 83 – 91 ].

Recent clinical studies have shown that novel antibody–drug conjugates aimed against HER2 offer considerable therapeutic advantages in the treatment of this kind of malignancy [ 92 , 93 ]. There are presently no clinical trials for the use of drug conjugates for neuroendocrine breast carcinomas with HER2 low immunophenotype. An interesting evidence from our cohort is that around 33% of our patients in our relatively small case series had a HER2 low immunophenotype.

Somatostatin analogues are an essential therapeutic option in the diagnosis and treatment of gastro-entero-pancreatic NETs. IHC has also revealed that breast NETs are positive for somatostatin receptor types 2, 2A, 2B, 3, and 5 [ 94 ]. While it can be a successful therapy option, somatostatin analogues have not yet shown clinical efficacy in the treatment of breast NETs [ 95 ]. SSTR2A can be assessed by immunohistochemistry, and it is given a score according to the following characteristics: Score 1 included pure cytoplasmic reactivity, either moderate/strong or weak; Score 2 was assigned when there was a membranous pattern of staining in less than 50% of tumour cells, either in scattered cells with complete membrane outlining or in most tumour cells with partial membrane staining; Score 3 was assigned when there was a membranous, usually intense, staining in more than 50% of tumour cells [ 96 ].

PRRT using radiolabelled somatostatin analogues for somatostatin receptor-targeted PET-CT has proven efficacy for NENs expressing somatostatin receptors and is predicted to be a promising therapeutic method as shown by two case reports [ 97 , 98 ].

Immune checkpoint inhibitors are being developed for breast cancer and have already established the standard of care for TNBC with PD-L1. Because single medications' efficacy has been insufficient, combination therapy with chemotherapy or other targeted therapies is now being researched [ 93 – 96 , 99 – 102 ]. For Br-NENs, there is no clinical data on immune checkpoint inhibitors.

Phase 1/2 trials were carried out to assess the role of immune checkpoint inhibitors in NENs, and the results revealed promising efficacy and controllable toxicity [ 97 , 103 ]. To explore the use of immune checkpoint inhibitors, it is reasonable to assess the PD-L1 status of HR-negative HER2-negative breast NEC.

Most studies published in the literature looked at NE breast neoplasms as a whole, without classification into various subtypes (as recommended by the WHO). As a result, data on the predictive significance of NE features in breast cancers is inadequate to be definitive. The question whether neuroendocrine differentiation affects the prognosis of BC patients remains a very much debated issue, with contrasting clinical results. The majority of published large series demonstrated an impaired prognosis for NENs and that neuroendocrine differentiation is an independent adverse prognostic factor for OS and DSS in BC, with a higher rate of local and distant recurrence although some smaller studies reported similar or even better outcomes for NEN compared to BC-NST patients (21) SCNEC had the worst outcome of any NE breast cancer [ 104 – 109 ]. The better prognosis of NETs in the breast compared to SCNECs is due in part to their lower histologic Nottingham grade. Although well-differentiated NETs had considerably better long-term results than non-NE tumours in other anatomic regions, there was no data to support comparable findings in the breast until today.

Histologic categorization and Nottingham staging are predictive factors in NEN, as they are in IBC. The Ki67 proliferation index, while beneficial in other NE tumours, is not predictive in NE breast cancers. The prognosis for IBC-NST with NE differentiation is less known. One explanation for this is that this subgroup is extremely diverse, with examples of varied NE marker expression and NE morphologic differentiation. Numerous studies that have indicated poorer outcomes in NE breast cancers (defined by NE marker expression) may have included numerous instances of IBC-NST with NE differentiation. [ 106 ].

It is debatable if the degree of expression of NE markers has any prognostic relevance. The presence of focused (as opposed to diffuse) NE markers, notably chromogranin (CG), was found to be a predictor of poor outcome [ 107 ]. Other studies that used a higher NE marker threshold or Tissue Microarray (TMA) analysis found no difference in survival, although their case selection may have underestimated instances with extremely low expression. Surprisingly, Cga/Syn pos breast tumours that also expressed other NE markers, such as DCLK1 and INSM1, had a better prognosis. Overall, a higher amount of NE differentiation appears to be associated with a better prognosis. Individual markers, but not other NE markers, were revealed to represent an independent negative prognostic predictor [ 108 ].

Because more thorough research is needed, these findings were preliminary yet intriguing. At this stage, it may be appropriate to advise that when diagnosing NEN, it is wise to distinguish between NET and NEC and to record the amount of expression of NE markers; the use of other markers (e.g., INSM1) may further stratify patients into various prognosis groups [ 109 , 110 ]. Future studies are more likely to show more solid prognostic information in Br-NENs with uniformity of diagnostic criteria and categorization [ 95 , 96 ]. Up to now, since neuroendocrine differentiation has been shown to be associated with impaired outcomes in several retrospective trials, further studies are needed to identify the most appropriate treatment strategy for this BC subtype [ 111 , 112 ].

Conclusions

Br-NENs are a special type of BCs with NE cytomorphological features and positivity for NE markers, mostly clustering with the luminal molecular profile. NENs are described in one specific chapter in the 2019 WHO classification of breast tumours. Br-NENs can occur in pure form or mixed forms. The real incidence of Br-NENs is difficult to define since NE markers are not routinely used in breast cancer diagnostic paths and due to the different data collection procedures. Thus, NENs of the breast are mis-diagnosed or under-recognized accounting for < 1% of BCs. According to the recent 2022 WHO classification of neuroendocrine neoplasms, Br-NENs can be distinguished into two families: well-differentiated forms (WD-NET) and poorly differentiated forms (NEC) according to morphology. We must keep in mind to be always careful to rule out metastatic nature from other origins (in particular excluding metastatic NEN from an extramammary site). The distinction of primary from metastatic NEN is critical to avoid misdiagnosis and unnecessary surgical and medical therapy. No consensus has been reached on the prognosis for Br-NENs and the efficacy of targeted therapies should be furtherly studied.

Abbreviations

BC	Breast carcinoma
Br-NENs	Breast neuroendocrine neoplasms
CHT	Chemotherapy
DFS	Disease-free survival
E-DCIS	Endocrine ductal carcinoma in situ
GI/NETs	Gastro-intestinal neuroendocrine tumours
HER-2	Human epidermal growth factor receptor 2
HT	Hormonal therapy
IBCs-NST	Invasive breast cancers of no special type
IDC-NOS	Invasive ductal carcinoma- no specific type
IHC	Immunohistochemistry
LCNEC	Large cell neuroendocrine carcinoma
LIN	Lobular intraepithelial neoplasm
MC	Mucinous carcinoma
MIBG	Meta-iodo-benzyl-guanidine
MiNEN	Mixed neuroendocrine/non-neuroendocrine neoplasm
NE	Neuroendocrine
NEN	Neuroendocrine neoplasm
NEC	Neuroendocrine carcinoma
OS	Overall survival
PRRT	Radionuclide therapy with peptide hormones
PET	Positron emission tomography
RT	Radiotherapy
SCNEC	Small cell neuroendocrine carcinoma
SPC	Solid papillary carcinoma
SSA	Somatostatin analogues
SSTR	Somatostatin receptor
TC	Computerized tomography
TMA	Tissue microarray
TN	Triple negative
UDH	Usual ductal hyperplasia
WD-NETs	Well differentiated – neuroendocrine tumours

Author contribution

FV, PT, FP, AF, ISDS wrote the first draft. AS, AM, EDR revised the first draft and the definitive version. EDR proposed the topic to the group. GS, NDA, QZ, AC, EN, GF contributed with the pictures.

Open access funding provided by Università Cattolica del Sacro Cuore within the CRUI-CARE Agreement.

Data availability

Declarations.

Ethical approval from the internal Committee Policlinico Gemelli 2023 n* 123.

The authors declare no competing interests.

Federica Vegni and Ilenia Sara De Stefano share first authorship.

Angela Santoro, Antonino Mule, and Esther Diana Rossi share the seniorship.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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A majority of pathology reports (83.5%) were produced after 2011, and two-thirds of the analysed reports originated from centres or laboratories within Lagos, Nigeria (67.7%). Many pathology reports were from private (55.2%) institutions or non-teaching hospitals (61.8%). Of the patients referred for breast cancer treatment, surgical and biopsy ...
Knowledge and Attitudes about Breast Cancer among Women: A Wake-Up Call
In a report by Siegel et al., it was indicated that deaths as a result of breast cancer in Nigeria reached 13,264 or 0.70% and the age adjusted Death Rate is 28.11 per 100,000 population, ranking Nigeria 4 th in the world. Adebamowo and Ajayi (1999) also stated that breast cancer is the most common cancer in Nigeria. ... Literature Review.
Cancer Care Terminology in African Languages
An estimated 801 000 incident cancer cases and 520 000 cancer deaths occurred in Africa in 2020. 1,2 The cancer burden in this region is increasing faster than in any other region of the world 3; thus, cancer surveillance, research, and control programs for prevention are major priorities. Effective communication between patients and care teams ...
Mammography and Breast Ultrasonography Services in Ghana, Availability
PURPOSE Breast cancer is the leading type of cancer diagnosed and the second leading cause of cancer-related death in Ghana. Mammography and ultrasound have proven benefits in the early detection of breast cancer. This study evaluates mammography, breast ultrasound, and radiology work force availability throughout Ghana. METHODS A survey was administered to all hospitals in Ghana from November ...
Breast Cancer Research to Support Evidence-Based Medicine in Nigeria: A
Results There were 1,651,326 breast cancer cases and 516,868 breast cancer deaths estimated in 2012. Approximately three quarters of all breast cancer cases and 60% of the breast cancer deaths ...
Breast Cancer Research to Support Evidence-Based Medicine in Nigeria: A
Europe PMC is an archive of life sciences journal literature. Breast Cancer Research to Support Evidence-Based Medicine in Nigeria: A Review of the Literature. Sign in | Create an account. https://orcid.org. Europe PMC. Menu. About ...
Religious beliefs and practices toward HPV vaccine acceptance in
Objective This review aimed to identify the current literature on the religious beliefs and any misconceptions toward HPV vaccine acceptance within the Organisation of Islamic Cooperation (OIC) countries. ... .Y., et al., Identifying Perceived Barriers to Human Papillomavirus Vaccination as a Preventative Strategy for Cervical Cancer in Nigeria ...
Neuroendocrine neoplasms of the breast: a review of literature
Making a diagnosis of primary neuroendocrine breast cancer needs to rule out metastasis from another anatomical site ... de Braud FGM, Di Cosimo S (2016) HER2-positive neuroendocrine breast cancer: case report and review of literature. Breast Care 11:424-426. 10.1159/000453572 10.1159/000453572 [PMC free article] [Google Scholar] 83. ...

Barriers to Early Presentation and Diagnosis of Breast Cancer in Nigerian Women

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Cancer Care Terminology in African Languages

Select Health Care Workers’ Responses to Whether They Experienced Challenges or Barriers Communicating With Patients Using the Local Language

Religious beliefs and practices toward HPV vaccine acceptance in Islamic countries: A scoping review

Conclusions

Introduction

Study characteristics

Religious beliefs and practices on HPV vaccine acceptance

Religious objections and misconceptions

Suggestions for public health interventions

Limitations

Supporting information

Neuroendocrine neoplasms of the breast: a review of literature

Ilenia Sara De Stefano

Introduction

Case reports

Clinical features

Macroscopic features

Histological features of Br-NECs, Br-NETs, and of invasive carcinomas of no special type with neuroendocrine features

Diagnostic characteristics of NE-differentiated breast cancers in needle biopsy specimens

Pure and mixed forms

Immunohistochemistry and molecular subtype

Molecular features

Differential diagnosis

Chemoradiotherapy

Hormonal and molecular therapy

Conclusions

Abbreviations

Author contribution

Data availability

IMAGES

COMMENTS