Oncofertility – integrating cancer care with fertility preservation (FP) – is expected to be an essential part of the standard care for patients, ¹ with international guidelines recommending fertility preservation counselling as routine for reproductive-age cancer patients and for prepubertal children undergoing gonadotoxic therapies. ² However, successful implementation of oncofertility care requires a coordinated referral system among healthcare providers. ³ While it is established that the role of oncologists and reproductive specialists is key for successful oncofertility, ^{3 , 4} it is also believed that primary care physicians (PCPs) can play an important role in ensuring successful fertility preservation referrals. ⁵

PCPs inclusive of general physicians (GPs) and paediatricians (PEDs), are considered as gatekeepers of the healthcare system who provide comprehensive, individual-centric and coordinated continuous care. ⁶ It has been reported that about two thirds of patients with long-term or complex health issues prefer interpersonal continuity with a PCP whom they know, trust and who also knows their medical history. ^{7 , 8} PCPs not only coordinate referrals to oncology or other specialty services, but are also involved in providing general medical care, emotional support and overall decision making for the patient during cancer care. ⁹ Post-treatment physical and psychosocial surveillance by primary care clinicians is recommended by the American Society of Clinical Oncology breast cancer survivorship guidelines, which also recommend that PCPs expedite referrals to reproductive endocrinologists in survivors experiencing infertility. ¹⁰

It is therefore important for PCPs dealing with cancer patients or patients with non-malignant conditions requiring gonadotoxic therapies, to be adequately knowledgeable both of the adverse gonadotoxic effects of chemo- and radiotherapy as well as the options available to mitigate them. The awareness of PCPs of international fertility preservation guidelines and on the available fertility preservation options are expected to strengthen the likelihood of fertility preservation referrals. ¹¹ Therefore, this study was aimed to assess the awareness, knowledge and perceptions of PCPs towards fertility preservation, along with exploring the existing barriers to oncofertility establishment in India.

The study was approved by the Institutional Ethics Committee, Kasturba Medical College & Kasturba Hospital, Manipal, India (IEC No: 880/2017), and is in continuation of a previously published study. ⁴ The earlier work included the use of an eighteen-item survey, which was given to oncologists and gynaecologists to explore their attitudes towards fertility preservation. The survey was designed in collaboration with the Oncofertility Consortium, USA. Content validation for the survey was done by experts in the field ¹² and a pilot study was conducted on a small group of healthcare providers to validate the comprehensibility of the survey questions (unpublished). In our new study, the survey was administered randomly to GPs and PEDs of the country at various national conferences and virtual platforms from May 2019 to September 2020. Written informed consent was taken from all the subjects participating in the survey.

In brief, the survey contained a total of eighteen questions, of which ten were aimed at understanding the participants’ knowledge, attitudes, and practice trends in oncofertility, including their familiarity with existing oncofertility barriers in India, and sought the respondent’s suggestions, if any, for effective use of fertility preservation. The remaining eight questions covered the demographics of the survey respondents and contextual details such as the number of new cancer patients treated in a month and the patient age groups. The questions were of different complexities, including those of a dichotomous nature, assessment tools with grading scales, multiple choice items where only one response could be selected, multiple response items where more than one answer could be selected, and even open-ended questions. During the analysis, the survey responses were assigned numerical values (Yes=1, No=0), and the data was analysed using descriptive statistics calculated with Microsoft Excel. In questions containing grading scales or multiple choice, options such as ‘not aware’, ‘aware but inadequate knowledge’, ‘knowledgeable’, ‘very knowledgeable’, were clubbed as two categories – ‘inadequate knowledge’ and ‘knowledgeable’. For open-ended questions such as suggestions for oncofertility practice, all the responses were considered and grouped based on similarity of the suggestions made. Questions that showed a high variation in responses, such as more than half of the participants not answering, were not included in the analysis.

Out of 105 survey forms distributed, 23 responses each from general physicians (GPs) and pediatricians (PEDs) were received, with an average response rate of 43.8%. The demographics of the PCPs are shown in Table 1.

This study showed, for the first time, the perceptions and attitudes towards oncofertility among PCPs in India. Lack of knowledge about the current international FP guidelines and of the available FP options were key observations made in this survey.

In India, the established fertility preservation options include sperm, oocyte and embryo banking for post-pubertal and adult cancer patients while prepubertal options that are available include ovarian or immature testicular tissue cryopreservation, which are still considered experimental. Other options such as gonadal shielding, GnRH analogs are also offered to cancer-diagnosed patients. ¹³ However, the majority of PCPs participating in our study reported inadequate knowledge of even the established fertility preservation options along with a reduced awareness of the American Society of Clinical Oncology Fertility Preservation (ASCO-FP) guidelines. This is in line with a cross-sectional study in India on female cancer patients of reproductive age revealing that 68% reported a lack of information received from primary physicians about fertility risks and FP options. ¹⁴ There could be several contributing factors to the above finding in our study, one of which could be the lack of knowledge about FP in India, since more than 90% of healthcare workers in other parts of the country reported the need for continued medical education programs or seminars in oncofertility. ¹⁵ Secondly, the ASCO-FP guidelines are mainly targeted to oncologists and other cancer-care providers, ² and not to primary care physicians, though organizations such as the American Academy of Pediatrics have recommended fertility preservation counselling for pediatric and adolescent patients. ¹¹ While ASCO has released primary care focused cancer survivorship guidelines for a few cancers, ^{10 , 16} there is a need for fertility preservation guidelines before the onset of cancer treatment in pediatric and reproductive-age patients, that can be applicable to primary care settings. Also, PCPs’ depth of knowledge pertaining to long-term effects of cancer treatment could be limited due to their lack of exposure to relevant literature pertaining to the field, ¹⁷ therefore, conducting educational programs for PCPs to increase awareness and knowledge of the various fertility preservation options could aid PCPs in their discussions with patients. In an online survey conducted by Nahata et al., it was seen that the majority of pediatricians felt inadequately trained in fertility risks and sexual function, which was reflective in their comfort level when discussing such issues. ¹⁸ Though our study reported a higher comfort level among PEDs in discussing most FP options, a majority of them have suggested the need for fertility preservation awareness programs.

In India, the burden of cancer is steadily increasing, with the Globocan project predicting 1.7 million new cases by 2035. ¹⁹ However, the ratio of new cancer cases per clinical oncologist is 677:1 and it has been reported that medical oncologists from low- and middle-income countries such as India have a substantial workload compared to high-income countries. ^{20 – 22} While the onus of FP counselling is placed on oncologists and gynecologists, ² in the given situation, an integrated care model would be more appropriate. As PCPs have a continual relationship with the patients and are more familiar with their wishes, PCPs can be a part of the FP referrals or discussions, to enable patients to think through their decisions, rather than these discussions taking place only with the oncologists or surgeons. ^{23 – 25} For this to succeed however, knowledge dissemination and awareness building of fertility preservation among PCPs in developing countries like India is essential, as emphasized by the findings of the present study. Our earlier study specifically looked at oncologists and gynaecologists’ attitude towards fertility preservation, who also emphasized the need for oncofertility awareness. ⁴ A shared care model will not only promote oncofertility referrals but will also enable patients to take informed decisions towards preserving their fertility.

The scope of oncofertility has started to include fertility preservation in patients with non-oncological conditions who are at high risk of infertility due to gonadotoxic treatments, or individuals with sexual development or auto-immune disorders, and also, in the gender-diverse population. ²⁶ The successful establishment of fertility preservation in (non)-oncological conditions therefore requires physicians, both primary care and specialists, to have adequate knowledge of fertility preservation and its related guidelines.

Our pilot study highlights the dearth of oncofertility awareness among PCPs. With more information, this group could play a crucial role in patient decision-making, thereby helping in the successful establishment of oncofertility as part of standard cancer care. The involvement of PCPs whom the patients know and trust and who are also familiar with the patient’s wishes or life goals, in fertility preservation discussions could prove beneficial to the cancer-diagnosed patients and subsequently improve their quality-of-life post cancer care. This study should contribute to what is currently only limited literature in this area. Limitations of this study include a small sample size and selection bias due to random recruitment of survey participants at conferences.

PT: Collected and analyzed the data, wrote paper; SU, RKJ, KSU, GK, NS, TKW: Revised the manuscript critically for important intellectual content; SKA: Conceived and designed the study, wrote paper. PT is the guarantor of this work and as such, had full access to all the data and takes responsibility for the integrity of the data and the accuracy of the data analysis. All authors have given final approval for publication.