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Breast Conservative Surgery for Breast Cancer: Indian Surgeon’s Preferences and Factors Influencing Them

Breast Conservative Surgery for Breast Cancer: Indian Surgeon’s Preferences and Factors... Background It is well established that disease-free survival and overall survival after breast conservation surgery (BCS) followed by radiotherapy are equivalent to that after mastectomy. However, in Asian countries, the rate of BCS continues to remain low. The cause may be multifactorial including the patient’s choice, availability and accessibility of infrastructure, and surgeon’s choice. We aimed to elucidate the Indian surgeons’ perspective while choosing between BCS and mastectomy, in women oncologically eligible for BCS. Methods We conducted a survey-based cross-sectional study in January–February 2021. Indian surgeons with general surgical or specialised oncosurgical training, who consented to participate were included in the study. Multinomial logistic regression was performed to assess the effect of study variables on offering mastectomy or BCS. Results A total of 347 responses were included. The mean age of the participants was 43 ± 11 years. Sixty-three of the sur- geons were in the 25–44 years age group with the majority (80%) being males. 66.4% of surgeons ‘almost always’ offered BCS to oncologically eligible patients. Surgeons who had undergone specialised training in oncosurgery or breast conser- vation surgery were 35 times more likely to offer BCS (p < 0.01). Surgeons working in hospitals with in-house radiation oncology facilities were 9 times more likely to offer BCS (p < 0.05). Surgeons’ years of practice, age, sex and hospital setting did not influence the surgery offered. Conclusion Two-thirds of Indian surgeons preferred BCS over mastectomy. Lack of radiotherapy facilities and specialised surgical training were deterrents to offering BCS to eligible women. Keywords Breast conservative surgery · Mastectomy · Breast cancer · Cancer surgery · India Introduction breast cancer in India [2]. By 2025, breast cancer is projected to make up 15% of the nation’s total cancer burden [3, 4]. Breast cancer is the most common malignancy among Over decades, the standard surgical procedure to treat breast women in India and around the world [1, 2]. In the year 2020, malignancy has been modified radical mastectomy (MRM). 178,361 new cases and 90,408 fatalities were attributed to More recently, breast conservative surgery (BCS) with * Nobhojit Roy Dayanand Medical College and Hospital, Ludhiana, Punjab, nobhojit.roy@ki.se India Maulana Azad Medical College, New Delhi, India World Health Organisation Collaborating Centre for Research in Surgical Care Delivery in Low-Middle- Institute of Post-Graduate Medical Education & Research, Income Countries, Mumbai, India Seth Sukhlal Karnani Memorial Hospital, Kolkata, India 2 8 Christian Medical College and Hospital, Ludhiana, Punjab, Department of Public Health Systems, Karolinska Institute, India 171 77 Stockholm, Sweden 3 9 Government Medical College Amritsar, Punjab, India The George Institute for Global Health, New Delhi, India Sri Guru Ram Das Institute of Health and Science, Amritsar, Punjab, India Vol.:(0123456789) 1 3 Indian Journal of Surgical Oncology radiotherapy has gained widespread acceptance in the treat- initiated by the WHO Collaborating Centre for Research ment of breast cancer all over the world. With advancements in Surgical Care Delivery in LMICs, Mumbai, India. The in surgical techniques, oncoplastic procedures and radiation survey was designed in the English language and questions therapy technology, survival rates after BCS followed by were tested through a series of pilot surveys for unbiased radiotherapy have been found to be equivalent to mastectomy, intents and ambiguity. Data variables were chosen to include making breast cancer treatment less mutilating and cosmeti- factors addressed in the literature and were objective, eas- cally more acceptable for women [3, 4]. Despite this, the rate ily standardised and relevant to minimise missing data and of BCS has been relatively low in Asian countries [5]. While maximise data quality. The survey was strictly anonymised the USA reported 64.5% of women with early-stage breast and no identifying data were collected. cancer undergoing BCS, 31% of breast carcinoma patients in The survey had three sections (supplementary file). Vari- Singapore underwent BCS [6, 7]. In India, only 11.3% of the ables such as details of surgical training, volume of breast patients who were offered BCS, underwent the procedure [8 ]. cancer surgeries performed and area of practice listed in The strikingly low rates of BCS in low-and-middle- the survey were re-grouped during analysis as seen in the income countries (LMICs), including India, is because ‘Results’ section. The first section included questions about the majority of breast carcinoma cases are being detected surgeons’ demographics, educational qualifications, area of at advanced stages as compared to high-income countries expertise, training in oncosurgery and whether they prac- (HICs) [9–12]. Several infrastructure-related factors (avail- tised in public (free service) or private (fee for service) ability and accessibility and affordability), shortage of sur - hospitals [18, 19]. The second section enquired about the geons with specialised BCS training, patient concerns about breast cancer work volumes, whether they offer BCS or recurrence and radiation have also been documented to con- MRM in women who are oncologically eligible to receive tribute to the preference of mastectomy over BCS [8, 13, breast conservation surgery and their expertise and comfort 14]. Adjuvant radiotherapy facilities and multidisciplinary in performing BCS [20]. The third section included reasons, teams predominantly are concentrated in urban areas leading if any, for choosing MRM over BCS, in patients who are to resource mismatch [14]. Furthermore, 75% of cancer costs eligible for breast conservation. This section included factors in India are out-of-pocket expenditures which contribute to that would influence the surgeons’ decisions based on patient delayed diagnosis and treatment [13]. Mandatory addition of population, radiotherapy facilities available in the area of adjuvant radiotherapy to BCS adds to this burden. practice and their training and ability to perform BCS. In Asia, although treatment options are discussed with patients, it is seen that the treatment decision is signifi- cantly based on the surgeon’s recommendations [15]. Even Data Collection in tertiary care centres, the surgeon is documented as an independent determinant for mastectomy [16]. Therefore, This was an open (open access to anybody with the survey understanding the factors that influence the treating sur - link) self-administered survey administered via ‘Google geon’s choice of surgery is very important. There is a pau- Forms’ that automatically captured the data. The survey link city of data on the factors that affect providers’ decisions in was circulated in various surgical groups on social media India. Thus, we conducted this study to elucidate the Indian and email lists of professional associations and societies of surgeons’ choice of surgical treatment between BCS and surgeons and surgical oncologists. Survey link responses mastectomy in oncologically eligible women [17]. were active for 3 weeks between January 2021 and February 2021. Participation in the survey was voluntary after agree- ing to consent to participate. No reminder emails and mes- Methodology sages were sent to the participants. Surgeons who had either completed a masters degree in general surgery or underwent Study Design oncosurgical training during or following their masters in general surgery, and were practising in India were included We conducted a cross-sectional survey among surgeons in the study. Surgeons who did not consent to participate or practising in India, to assess their perception about choos- are not performing any breast cancer surgery were excluded ing BCS and MRM in treating patients with breast cancer from the study. Participation in the survey was voluntary, for 3 weeks between January and February 2021. without any incentive for participation. Development and Pretesting Statistical Analysis The survey was developed by a research consortium ‘Ind- Data were analysed using SPSS Version 24 and Micro- Surg’ constituting practising surgeons and medical students, soft Excel 2019. Descriptive statistics for overall study 1 3 Indian Journal of Surgical Oncology participants were presented as absolute numbers and per- Table 1 Participant characteristics centages of the group. Multinomial logistic regression was Variable N = 347 % performed to assess the effect of study variables on offering Age, years: mean ± SD (range) 43 ± 11 (25–83) BCS to an eligible patient. A p-value of less than 0.05 was Age group (years) considered statistically significant.    25–34 90 25.9%    35–44 129 37.2%    45–54 71 20.5% Results    55–64 41 11.8%    ≥ 65 16 4.6% A total of 351 responses were received at the end of the Sex of participant study period. Four surgeons did not perform breast surgery    Male 276 80.5% as a part of their clinical practice, so were excluded from    Female 67 19.5% further analyses yielding a final sample of 347 respondents. Details of surgical training Since the survey was circulated through multiple platforms,    Surgeons with oncosurgery training 207 59.8% we were unable to calculate a response rate.    Masters in general surgery 139 40.2% Setting of practice Participant Characteristics    Private 194 56.1%    Public 152 43.9% The mean age of the study participants was 43 ± 11 years Level of institution with 63.1% of the participants in the 25–44 years age group.    Tertiary hospital 303 88.1% The majority of participants (80.5%) was males. 59.8%    Secondary hospital 41 11.9% had received specialised oncosurgical training. A quarter Duration of surgical practice (years) (25.6%) of the study participants reported that they were    < 10 150 43.5% practising breast surgery for the last 20 years or more and    10–20 106 30.7% 137 (42.2%) surgeons mentioned that they perform more    > 20 89 25.8% than ten breast cancer surgeries in a month as a lead surgeon The volume of breast cancer surgeries in your practice per month as (Table 1). Of the 207 participants with oncosurgical training, a lead surgeon 191 had done a fellowship or masters course in oncosurgery    < 10 surgeries 188 57.8% and 16 had BCS training as a part of their masters/residency    ≥ 10 surgeries 137 42.2% training in general surgery. Distance of radiation oncology facility from your institute/place of practice Surgeons’ Choice Between BCS and Mastectomy    Same institute 209 60.8%    Not in the same institute but in the same city 128 36.8% Two-thirds (66.4%) of the surgeons almost always offered How likely are you to offer BCS to an eligible woman? BCS to every eligible woman (Table 1). Various reasons for    Almost always 229 66.4% not offering BCS were expressed by the surgeons, even if    Occasionally 91 26.4% the woman was oncologically eligible for BCS (Table 2).    Almost never 25 7.2% Factors Associated with Surgeons’ Decision on Treatment Table 2 Reason for choosing mastectomy over BCS Choosing MRM over BCS reason N = 261 % Multinomial logistic regression was used to predict the independent factors that would decide the type of surgery My patients may not follow up for radiation after 109 31.4% from the surgeon’s perspective (Table 3). The relationship surgery between dependent variables (offering BCS to an eligible My patients cannot afford BCS and adjuvant radia- 61 17.6% tion woman) was probed by considering the ‘almost never offer - ing BCS’ as a reference category. Surgeons with special- Believe mastectomy is an oncologically safer 42 12.1% option ised oncosurgical training had significantly higher chances No radiotherapy facilities where I practice 24 6.9% of offering BCS than general surgeons (occasionally offer - I lack the training or expertise to perform BCS 20 5.7% ing BCS OR 8.27, p = 0.059 and almost always offering No mammography facility where I practice 5 1.4% BCS OR 35.24, p = 0.001). There was no association of the surgeons’ demographic details (age, sex) and years of prac- *Numbers and percentages may not add up due to multiple reasons tice on their preference of surgical procedure. Surgeons given by many surgeons 1 3 Indian Journal of Surgical Oncology 1 3 Table 3 Multinomial logistic regression—how likely are surgeons to offer BCS to an eligible woman Narration Almost never (referent Occasional Almost always category) n n Odds ratio (95% CI) p-value n Odds ratio (95% CI) p-value Age group (years) (N = 345)    25–34 9 26 0.314 (0.006–15.232) 0.559 54 0.211 (0.004–10.605) 0.436    35–44 5 34 0.5 (0.013–19.143) 0.709 89 0.218 (0.005–8.694) 0.418    45–54 5 19 0.539 (0.029–9.903) 0.677 47 0.303 (0.016–5.746) 0.427    55–64 4 8 0.436 (0.03–6.332) 0.543 29 0.641 (0.045–9.134) 0.743    > 65 2 4 Referent category 10 Referent category Sex of participant (N = 341)    Female 5 17 1.558 (0.351–6.917) 0.56 45 1.615 (0.36–7.243) 0.531    Male 20 72 Referent category 182 Referent category Details of surgical training (N = 344)    Surgeons with oncosurgery training 1 32 8.273 (0.927–73.845) 0.059 173 35.236 (4.059–305.862) 0.001    Masters in general surgery 24 59 Referent category 55 Referent category Practice centre (N = 344)    Public 14 53 1.033 (0.328–3.252) 0.955 83 0.49 (0.153–1.564) 0.228    Private 11 38 Referent category 145 Referent category Centre level (N = 342)    Tertiary hospital 19 80 0.814 (0.177–3.739) 0.791 202 0.993 (0.209–4.724) 0.993    Secondary hospital 6 11 Referent category 24 Referent category Duration of practising surgery (N = 343)    < 10 years 10 43 3.69 (0.212–64.352) 0.371 95 3.213 (0.182–56.684) 0.425    10–20 years 6 26 1.039 (0.134–8.035) 0.971 74 0.873 (0.111–6.866) 0.897    > 20 years 8 21 Referent category 60 Referent category The volume of breast cancer surgeries performed in a month as a lead surgeon (N = 323)    < 10 surgeries 19 66 0.961 (0.174–5.321) 0.964 103 0.443 (0.083–2.366) 0.34    ≥ 10 surgeries 2 21 Referent category 112 Referent category Distance to the radiation oncology facility from institute/place of practice (N = 337)    Same institute 5 49 7.488 (1.059–52.936) 0.044 153 9.655 (1.325–70.374) 0.025    Not in the same institute but in same 14 31 1.637 (0.33–8.135) 0.547 64 1.724 (0.329–9.043) 0.52 city < 2 h    In same city > 2 h 5 7 Referent category 9 Referent category *Two participants have not responded to the offering of BCS question, those were not considered in the multinomial logistic regression analysis Indian Journal of Surgical Oncology demonstrated seven and nine times higher odds of ‘occa- breast cancer [26]. However, our study did not show any sionally’ and ‘almost always’ offering BCS respectively if variation in the outlook towards BCS according to sur- the radiation oncology facility was available in the same geons’ sex or age. This was similar to another study from institute (OR = 7.488, p = 0.044, OR = 9.655, p = 0.025). India done by Bothra et al. [19]. We did not find a statisti- cally significant association between surgeons’ years of experience with their decision to offer BCS. Conversely, Discussion Bothra et al. highlighted that Indian surgeons during the early part of their career (age group of 20–30 years) pre- Our study explored the Indian surgeons’ perspective ferred to perform mastectomy over BCS due to the per- while offering BCS to oncologically eligible women. It ceived fear of tarnishing reputation in case of failure of was seen that 66.4% of surgeons almost always offered treatment. Senior surgeons (age > 50 years) preferred to BCS to oncologically eligible women. Specialised surgi- perform mastectomy due to their lack of training in BCS cal training and distance of the radiation oncology facil- [19]. Arnaud et  al. also found that patients treated by ity from the surgeon’s institute were the independent older surgeons underwent mastectomy more often [27]. determinants for choosing BCS over mastectomy. Our study has a large sample size and a good represen- Our study highlighted that surgeons with oncosurgi- tation of participating surgeons across age and years in cal training almost always offered BCS to oncologically practice. However, it has several limitations. A majority eligible patients. This was similar to studies from India of participants (81%) included in our study practised in (p < 0.01) and China (p = 0.003) which found that surgeons tertiary care centres, whereas the majority of the breast with super speciality surgical training were performing cancer surgeries is performed by the general surgeons at BCS more frequently compared to general surgeons and secondary-level hospitals or private hospitals, in India. were independent predictors of BCS [8, 21]. In contrast, a Similarly, rural areas where 70% of India’s population study from the USA reports that surgical oncologists were resides may not have surgeons trained in BCS or access more likely to perform mastectomy over BCS. However, it to radiotherapy. This survey thus may underrepresent was also reported that this could be a reflection of the fact the surgeons of rural areas, private hospitals and smaller that they treat more complicated patients [22]. setups where significant volumes of breast surgeries are The perceived inability of patients to follow up for performed [14]. It provides insight into why surgeons adjuvant radiotherapy was cited as one of the most com- may hesitate to offer BCS to eligible women, but does mon reasons for not offering BCS in our study. Surgeons not take into account violations from standard practice, were nine times more likely to almost always offer BCS such as the number of times surgeons did not offer BCS to patients if radiotherapy facilities were available in the to eligible patients, as our survey focussed primarily on same institute compared to if the radiation facility was the surgeons’ perspective and relies on their honesty in within the same city more than 2 h away (p = 0.01). A answering. Additionally, the knowledge gap of surgeons similar trend was seen in a study from the USA where was ascertained based on their level of education and the likelihood of BCS increased when a radiation facility training as per the participants’ responses. However, a was available in the same hospital [23]. The study also nuanced approach to look into factors determining these demonstrated that women who underwent BCS were less reasons should be explored in future studies. compliant to the use of adjuvant radiation therapy if they A surgeons’ intent to impart appropriate quality of lived greater distances (≥ 40 miles) from a centre with treatment and improved quality of life for the patient is a radiation facility. This is also in concordance with a essential for performing BCS in an eligible patient [8]. study from Iran where the non-availability of adjuvant Therefore, general surgeons with less exposure to BCS radiotherapy facilities was cited as one of the reasons training need to be trained in performing BCS and in for surgeons not recommending BCS to their patients counselling patients. This can occur through the incul- [24]. This highlights that access to adjuvant radiotherapy cation of training in BCS as a part of general surgical services is a major determinant of BCS and warrants training. Higher fellowships or specialised oncosurgical prioritisation of investment in radiotherapy facilities to training after completion of masters in general surgery increase its access and affordability. will always remain an option for a section of surgeons. In North America, female surgeons were found more Previous studies from Hong Kong and Malaysia have likely to offer BCS, as they were supposedly able to alle- found that most patients follow their surgeon’s recom- viate patients’ concerns regarding BCS better in compari- mendations in deciding between mastectomy and BCS son to their male counterparts [25]. Female surgeons were [28, 29]. This makes it essential for patients with breast twice more likely to offer BCS than males as shown in an cancer to be informed of all their treatment options by analysis by Hershman et al. in patients with early-stage the surgeons, to make an informed surgical decision. 1 3 Indian Journal of Surgical Oncology Competing Interests The authors declare no competing interests. This can be supported through the implementation of shared decision-making tools, which have been shown to increase the rate of BCS [30, 31]. Open Access This article is licensed under a Creative Commons Attri- bution 4.0 International License, which permits use, sharing, adapta- The data from our study shows that the majority of surgeons tion, distribution and reproduction in any medium or format, as long oe ff rs BCS to eligible patients. However, it is observed that a as you give appropriate credit to the original author(s) and the source, significant number of women who could be candidates for BCS provide a link to the Creative Commons licence, and indicate if changes still decide to undergo mastectomy [14]. Hence, larger-scale were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated studies analysing and documenting the effect of multiple factors otherwise in a credit line to the material. If material is not included in must be conducted to understand surgical care for breast cancer the article's Creative Commons licence and your intended use is not in India. Future work should focus on identifying intricate barri- permitted by statutory regulation or exceeds the permitted use, you will ers pertaining to access and availability of radiation treatments need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . that may influence patients’ choice of BCS [8 , 24]. Conclusion References We found that two-thirds of Indian surgeons prefers BCS 1. Cancer. (2021) World Health Organization. https://www .who. int/ over mastectomy. This is consistent with global trends. news- room/ fact- sheets/ detail/ cancer. Accessed August 2021. 2. The global cancer observatory. (2021). India Globocan 2020 [Fact Lack of surgeons trained in performing BCS was a common Sheet]. 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Surg 150(1):9 B., and N. R. conceptualised the study. R. D., P. P., G. B., B. S., M. K., 7. Teo SY, Chuwa E, Latha S, Lew YL, Tan YY (2014) Young A. M., L. B., and A. G. were involved in data collection and analysis. breast cancer in a specialised breast unit in Singapore: clinical, R. D., A. M., P. P., B. S., S. V., P. B., and A. G. were involved in the radiological and pathological factors. Ann Acad Med Singap literature review and writing of the manuscript. B. S., S. J., P. P., A. 43:79–85 M., M. K., L. B., G. B., S. C., P. B., N. R., and A. G. critically reviewed 8. Bothra S, Sabaretnam M, Chand G, Mishra A, Agarwal G, the manuscript. Agarwal A (2019) Indian surgeons’ perspective regarding breast-conserving surgery: a cohort study. Int J Mol Immuno Funding Open access funding provided by Karolinska Institute. Oncol 4:72–81 9. 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Bergh J et al (2013) Breast cancer survival and stage at diag- nosis in Australia, Canada, Denmark, Norway, Sweden and Consent for Publication Not applicable. 1 3 Indian Journal of Surgical Oncology the UK, 2000–2007: a population-based study. Br J Cancer 25. Gu J, Groot G, Boden C, Busch A, Holtslander L, Lim H (2018) 108(5):1195–1208 Review of factors influencing women’s choice of mastectomy 13. Pramesh C, Badwe R, Borthakur B, Chandra M, Raj E, Kannan versus breast conserving therapy in early stage breast cancer: a T et al (2014) Delivery of affordable and equitable cancer care in systematic review. Clin Breast Cancer 18(4) India. Lancet Oncol 15(6):e223–e233 26. Hershman DL, Buono D, Jacobson JS, McBride RB, Tsai WY, 14. Chatterjee S. (2020) Is India overdoing mastectomy?. Indian J Surg Joseph KA et al (2009) Surgeon characteristics and use of breast 15. 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Bellavance EC, Kesmodel SB (2016) Decision-making in the jurisdictional claims in published maps and institutional affiliations. surgical treatment of breast cancer: factors influencing women’s choices for mastectomy and breast conserving surgery. Front Springer Nature or its licensor holds exclusive rights to this article under Oncol 6 a publishing agreement with the author(s) or other rightsholder(s); 24. Najafi M, Ebrahimi M, Kaviani A, Hashemi E, Montazeri A author self-archiving of the accepted manuscript version of this article (2005) Breast conserving surgery versus mastectomy: cancer is solely governed by the terms of such publishing agreement and practice by general surgeons in Iran. BMC Cancer 5(1) applicable law. 1 3 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png Indian Journal of Surgical Oncology Springer Journals

Breast Conservative Surgery for Breast Cancer: Indian Surgeon’s Preferences and Factors Influencing Them

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10.1007/s13193-022-01601-y
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Abstract

Background It is well established that disease-free survival and overall survival after breast conservation surgery (BCS) followed by radiotherapy are equivalent to that after mastectomy. However, in Asian countries, the rate of BCS continues to remain low. The cause may be multifactorial including the patient’s choice, availability and accessibility of infrastructure, and surgeon’s choice. We aimed to elucidate the Indian surgeons’ perspective while choosing between BCS and mastectomy, in women oncologically eligible for BCS. Methods We conducted a survey-based cross-sectional study in January–February 2021. Indian surgeons with general surgical or specialised oncosurgical training, who consented to participate were included in the study. Multinomial logistic regression was performed to assess the effect of study variables on offering mastectomy or BCS. Results A total of 347 responses were included. The mean age of the participants was 43 ± 11 years. Sixty-three of the sur- geons were in the 25–44 years age group with the majority (80%) being males. 66.4% of surgeons ‘almost always’ offered BCS to oncologically eligible patients. Surgeons who had undergone specialised training in oncosurgery or breast conser- vation surgery were 35 times more likely to offer BCS (p < 0.01). Surgeons working in hospitals with in-house radiation oncology facilities were 9 times more likely to offer BCS (p < 0.05). Surgeons’ years of practice, age, sex and hospital setting did not influence the surgery offered. Conclusion Two-thirds of Indian surgeons preferred BCS over mastectomy. Lack of radiotherapy facilities and specialised surgical training were deterrents to offering BCS to eligible women. Keywords Breast conservative surgery · Mastectomy · Breast cancer · Cancer surgery · India Introduction breast cancer in India [2]. By 2025, breast cancer is projected to make up 15% of the nation’s total cancer burden [3, 4]. Breast cancer is the most common malignancy among Over decades, the standard surgical procedure to treat breast women in India and around the world [1, 2]. In the year 2020, malignancy has been modified radical mastectomy (MRM). 178,361 new cases and 90,408 fatalities were attributed to More recently, breast conservative surgery (BCS) with * Nobhojit Roy Dayanand Medical College and Hospital, Ludhiana, Punjab, nobhojit.roy@ki.se India Maulana Azad Medical College, New Delhi, India World Health Organisation Collaborating Centre for Research in Surgical Care Delivery in Low-Middle- Institute of Post-Graduate Medical Education & Research, Income Countries, Mumbai, India Seth Sukhlal Karnani Memorial Hospital, Kolkata, India 2 8 Christian Medical College and Hospital, Ludhiana, Punjab, Department of Public Health Systems, Karolinska Institute, India 171 77 Stockholm, Sweden 3 9 Government Medical College Amritsar, Punjab, India The George Institute for Global Health, New Delhi, India Sri Guru Ram Das Institute of Health and Science, Amritsar, Punjab, India Vol.:(0123456789) 1 3 Indian Journal of Surgical Oncology radiotherapy has gained widespread acceptance in the treat- initiated by the WHO Collaborating Centre for Research ment of breast cancer all over the world. With advancements in Surgical Care Delivery in LMICs, Mumbai, India. The in surgical techniques, oncoplastic procedures and radiation survey was designed in the English language and questions therapy technology, survival rates after BCS followed by were tested through a series of pilot surveys for unbiased radiotherapy have been found to be equivalent to mastectomy, intents and ambiguity. Data variables were chosen to include making breast cancer treatment less mutilating and cosmeti- factors addressed in the literature and were objective, eas- cally more acceptable for women [3, 4]. Despite this, the rate ily standardised and relevant to minimise missing data and of BCS has been relatively low in Asian countries [5]. While maximise data quality. The survey was strictly anonymised the USA reported 64.5% of women with early-stage breast and no identifying data were collected. cancer undergoing BCS, 31% of breast carcinoma patients in The survey had three sections (supplementary file). Vari- Singapore underwent BCS [6, 7]. In India, only 11.3% of the ables such as details of surgical training, volume of breast patients who were offered BCS, underwent the procedure [8 ]. cancer surgeries performed and area of practice listed in The strikingly low rates of BCS in low-and-middle- the survey were re-grouped during analysis as seen in the income countries (LMICs), including India, is because ‘Results’ section. The first section included questions about the majority of breast carcinoma cases are being detected surgeons’ demographics, educational qualifications, area of at advanced stages as compared to high-income countries expertise, training in oncosurgery and whether they prac- (HICs) [9–12]. Several infrastructure-related factors (avail- tised in public (free service) or private (fee for service) ability and accessibility and affordability), shortage of sur - hospitals [18, 19]. The second section enquired about the geons with specialised BCS training, patient concerns about breast cancer work volumes, whether they offer BCS or recurrence and radiation have also been documented to con- MRM in women who are oncologically eligible to receive tribute to the preference of mastectomy over BCS [8, 13, breast conservation surgery and their expertise and comfort 14]. Adjuvant radiotherapy facilities and multidisciplinary in performing BCS [20]. The third section included reasons, teams predominantly are concentrated in urban areas leading if any, for choosing MRM over BCS, in patients who are to resource mismatch [14]. Furthermore, 75% of cancer costs eligible for breast conservation. This section included factors in India are out-of-pocket expenditures which contribute to that would influence the surgeons’ decisions based on patient delayed diagnosis and treatment [13]. Mandatory addition of population, radiotherapy facilities available in the area of adjuvant radiotherapy to BCS adds to this burden. practice and their training and ability to perform BCS. In Asia, although treatment options are discussed with patients, it is seen that the treatment decision is signifi- cantly based on the surgeon’s recommendations [15]. Even Data Collection in tertiary care centres, the surgeon is documented as an independent determinant for mastectomy [16]. Therefore, This was an open (open access to anybody with the survey understanding the factors that influence the treating sur - link) self-administered survey administered via ‘Google geon’s choice of surgery is very important. There is a pau- Forms’ that automatically captured the data. The survey link city of data on the factors that affect providers’ decisions in was circulated in various surgical groups on social media India. Thus, we conducted this study to elucidate the Indian and email lists of professional associations and societies of surgeons’ choice of surgical treatment between BCS and surgeons and surgical oncologists. Survey link responses mastectomy in oncologically eligible women [17]. were active for 3 weeks between January 2021 and February 2021. Participation in the survey was voluntary after agree- ing to consent to participate. No reminder emails and mes- Methodology sages were sent to the participants. Surgeons who had either completed a masters degree in general surgery or underwent Study Design oncosurgical training during or following their masters in general surgery, and were practising in India were included We conducted a cross-sectional survey among surgeons in the study. Surgeons who did not consent to participate or practising in India, to assess their perception about choos- are not performing any breast cancer surgery were excluded ing BCS and MRM in treating patients with breast cancer from the study. Participation in the survey was voluntary, for 3 weeks between January and February 2021. without any incentive for participation. Development and Pretesting Statistical Analysis The survey was developed by a research consortium ‘Ind- Data were analysed using SPSS Version 24 and Micro- Surg’ constituting practising surgeons and medical students, soft Excel 2019. Descriptive statistics for overall study 1 3 Indian Journal of Surgical Oncology participants were presented as absolute numbers and per- Table 1 Participant characteristics centages of the group. Multinomial logistic regression was Variable N = 347 % performed to assess the effect of study variables on offering Age, years: mean ± SD (range) 43 ± 11 (25–83) BCS to an eligible patient. A p-value of less than 0.05 was Age group (years) considered statistically significant.    25–34 90 25.9%    35–44 129 37.2%    45–54 71 20.5% Results    55–64 41 11.8%    ≥ 65 16 4.6% A total of 351 responses were received at the end of the Sex of participant study period. Four surgeons did not perform breast surgery    Male 276 80.5% as a part of their clinical practice, so were excluded from    Female 67 19.5% further analyses yielding a final sample of 347 respondents. Details of surgical training Since the survey was circulated through multiple platforms,    Surgeons with oncosurgery training 207 59.8% we were unable to calculate a response rate.    Masters in general surgery 139 40.2% Setting of practice Participant Characteristics    Private 194 56.1%    Public 152 43.9% The mean age of the study participants was 43 ± 11 years Level of institution with 63.1% of the participants in the 25–44 years age group.    Tertiary hospital 303 88.1% The majority of participants (80.5%) was males. 59.8%    Secondary hospital 41 11.9% had received specialised oncosurgical training. A quarter Duration of surgical practice (years) (25.6%) of the study participants reported that they were    < 10 150 43.5% practising breast surgery for the last 20 years or more and    10–20 106 30.7% 137 (42.2%) surgeons mentioned that they perform more    > 20 89 25.8% than ten breast cancer surgeries in a month as a lead surgeon The volume of breast cancer surgeries in your practice per month as (Table 1). Of the 207 participants with oncosurgical training, a lead surgeon 191 had done a fellowship or masters course in oncosurgery    < 10 surgeries 188 57.8% and 16 had BCS training as a part of their masters/residency    ≥ 10 surgeries 137 42.2% training in general surgery. Distance of radiation oncology facility from your institute/place of practice Surgeons’ Choice Between BCS and Mastectomy    Same institute 209 60.8%    Not in the same institute but in the same city 128 36.8% Two-thirds (66.4%) of the surgeons almost always offered How likely are you to offer BCS to an eligible woman? BCS to every eligible woman (Table 1). Various reasons for    Almost always 229 66.4% not offering BCS were expressed by the surgeons, even if    Occasionally 91 26.4% the woman was oncologically eligible for BCS (Table 2).    Almost never 25 7.2% Factors Associated with Surgeons’ Decision on Treatment Table 2 Reason for choosing mastectomy over BCS Choosing MRM over BCS reason N = 261 % Multinomial logistic regression was used to predict the independent factors that would decide the type of surgery My patients may not follow up for radiation after 109 31.4% from the surgeon’s perspective (Table 3). The relationship surgery between dependent variables (offering BCS to an eligible My patients cannot afford BCS and adjuvant radia- 61 17.6% tion woman) was probed by considering the ‘almost never offer - ing BCS’ as a reference category. Surgeons with special- Believe mastectomy is an oncologically safer 42 12.1% option ised oncosurgical training had significantly higher chances No radiotherapy facilities where I practice 24 6.9% of offering BCS than general surgeons (occasionally offer - I lack the training or expertise to perform BCS 20 5.7% ing BCS OR 8.27, p = 0.059 and almost always offering No mammography facility where I practice 5 1.4% BCS OR 35.24, p = 0.001). There was no association of the surgeons’ demographic details (age, sex) and years of prac- *Numbers and percentages may not add up due to multiple reasons tice on their preference of surgical procedure. Surgeons given by many surgeons 1 3 Indian Journal of Surgical Oncology 1 3 Table 3 Multinomial logistic regression—how likely are surgeons to offer BCS to an eligible woman Narration Almost never (referent Occasional Almost always category) n n Odds ratio (95% CI) p-value n Odds ratio (95% CI) p-value Age group (years) (N = 345)    25–34 9 26 0.314 (0.006–15.232) 0.559 54 0.211 (0.004–10.605) 0.436    35–44 5 34 0.5 (0.013–19.143) 0.709 89 0.218 (0.005–8.694) 0.418    45–54 5 19 0.539 (0.029–9.903) 0.677 47 0.303 (0.016–5.746) 0.427    55–64 4 8 0.436 (0.03–6.332) 0.543 29 0.641 (0.045–9.134) 0.743    > 65 2 4 Referent category 10 Referent category Sex of participant (N = 341)    Female 5 17 1.558 (0.351–6.917) 0.56 45 1.615 (0.36–7.243) 0.531    Male 20 72 Referent category 182 Referent category Details of surgical training (N = 344)    Surgeons with oncosurgery training 1 32 8.273 (0.927–73.845) 0.059 173 35.236 (4.059–305.862) 0.001    Masters in general surgery 24 59 Referent category 55 Referent category Practice centre (N = 344)    Public 14 53 1.033 (0.328–3.252) 0.955 83 0.49 (0.153–1.564) 0.228    Private 11 38 Referent category 145 Referent category Centre level (N = 342)    Tertiary hospital 19 80 0.814 (0.177–3.739) 0.791 202 0.993 (0.209–4.724) 0.993    Secondary hospital 6 11 Referent category 24 Referent category Duration of practising surgery (N = 343)    < 10 years 10 43 3.69 (0.212–64.352) 0.371 95 3.213 (0.182–56.684) 0.425    10–20 years 6 26 1.039 (0.134–8.035) 0.971 74 0.873 (0.111–6.866) 0.897    > 20 years 8 21 Referent category 60 Referent category The volume of breast cancer surgeries performed in a month as a lead surgeon (N = 323)    < 10 surgeries 19 66 0.961 (0.174–5.321) 0.964 103 0.443 (0.083–2.366) 0.34    ≥ 10 surgeries 2 21 Referent category 112 Referent category Distance to the radiation oncology facility from institute/place of practice (N = 337)    Same institute 5 49 7.488 (1.059–52.936) 0.044 153 9.655 (1.325–70.374) 0.025    Not in the same institute but in same 14 31 1.637 (0.33–8.135) 0.547 64 1.724 (0.329–9.043) 0.52 city < 2 h    In same city > 2 h 5 7 Referent category 9 Referent category *Two participants have not responded to the offering of BCS question, those were not considered in the multinomial logistic regression analysis Indian Journal of Surgical Oncology demonstrated seven and nine times higher odds of ‘occa- breast cancer [26]. However, our study did not show any sionally’ and ‘almost always’ offering BCS respectively if variation in the outlook towards BCS according to sur- the radiation oncology facility was available in the same geons’ sex or age. This was similar to another study from institute (OR = 7.488, p = 0.044, OR = 9.655, p = 0.025). India done by Bothra et al. [19]. We did not find a statisti- cally significant association between surgeons’ years of experience with their decision to offer BCS. Conversely, Discussion Bothra et al. highlighted that Indian surgeons during the early part of their career (age group of 20–30 years) pre- Our study explored the Indian surgeons’ perspective ferred to perform mastectomy over BCS due to the per- while offering BCS to oncologically eligible women. It ceived fear of tarnishing reputation in case of failure of was seen that 66.4% of surgeons almost always offered treatment. Senior surgeons (age > 50 years) preferred to BCS to oncologically eligible women. Specialised surgi- perform mastectomy due to their lack of training in BCS cal training and distance of the radiation oncology facil- [19]. Arnaud et  al. also found that patients treated by ity from the surgeon’s institute were the independent older surgeons underwent mastectomy more often [27]. determinants for choosing BCS over mastectomy. Our study has a large sample size and a good represen- Our study highlighted that surgeons with oncosurgi- tation of participating surgeons across age and years in cal training almost always offered BCS to oncologically practice. However, it has several limitations. A majority eligible patients. This was similar to studies from India of participants (81%) included in our study practised in (p < 0.01) and China (p = 0.003) which found that surgeons tertiary care centres, whereas the majority of the breast with super speciality surgical training were performing cancer surgeries is performed by the general surgeons at BCS more frequently compared to general surgeons and secondary-level hospitals or private hospitals, in India. were independent predictors of BCS [8, 21]. In contrast, a Similarly, rural areas where 70% of India’s population study from the USA reports that surgical oncologists were resides may not have surgeons trained in BCS or access more likely to perform mastectomy over BCS. However, it to radiotherapy. This survey thus may underrepresent was also reported that this could be a reflection of the fact the surgeons of rural areas, private hospitals and smaller that they treat more complicated patients [22]. setups where significant volumes of breast surgeries are The perceived inability of patients to follow up for performed [14]. It provides insight into why surgeons adjuvant radiotherapy was cited as one of the most com- may hesitate to offer BCS to eligible women, but does mon reasons for not offering BCS in our study. Surgeons not take into account violations from standard practice, were nine times more likely to almost always offer BCS such as the number of times surgeons did not offer BCS to patients if radiotherapy facilities were available in the to eligible patients, as our survey focussed primarily on same institute compared to if the radiation facility was the surgeons’ perspective and relies on their honesty in within the same city more than 2 h away (p = 0.01). A answering. Additionally, the knowledge gap of surgeons similar trend was seen in a study from the USA where was ascertained based on their level of education and the likelihood of BCS increased when a radiation facility training as per the participants’ responses. However, a was available in the same hospital [23]. The study also nuanced approach to look into factors determining these demonstrated that women who underwent BCS were less reasons should be explored in future studies. compliant to the use of adjuvant radiation therapy if they A surgeons’ intent to impart appropriate quality of lived greater distances (≥ 40 miles) from a centre with treatment and improved quality of life for the patient is a radiation facility. This is also in concordance with a essential for performing BCS in an eligible patient [8]. study from Iran where the non-availability of adjuvant Therefore, general surgeons with less exposure to BCS radiotherapy facilities was cited as one of the reasons training need to be trained in performing BCS and in for surgeons not recommending BCS to their patients counselling patients. This can occur through the incul- [24]. This highlights that access to adjuvant radiotherapy cation of training in BCS as a part of general surgical services is a major determinant of BCS and warrants training. Higher fellowships or specialised oncosurgical prioritisation of investment in radiotherapy facilities to training after completion of masters in general surgery increase its access and affordability. will always remain an option for a section of surgeons. In North America, female surgeons were found more Previous studies from Hong Kong and Malaysia have likely to offer BCS, as they were supposedly able to alle- found that most patients follow their surgeon’s recom- viate patients’ concerns regarding BCS better in compari- mendations in deciding between mastectomy and BCS son to their male counterparts [25]. Female surgeons were [28, 29]. This makes it essential for patients with breast twice more likely to offer BCS than males as shown in an cancer to be informed of all their treatment options by analysis by Hershman et al. in patients with early-stage the surgeons, to make an informed surgical decision. 1 3 Indian Journal of Surgical Oncology Competing Interests The authors declare no competing interests. This can be supported through the implementation of shared decision-making tools, which have been shown to increase the rate of BCS [30, 31]. Open Access This article is licensed under a Creative Commons Attri- bution 4.0 International License, which permits use, sharing, adapta- The data from our study shows that the majority of surgeons tion, distribution and reproduction in any medium or format, as long oe ff rs BCS to eligible patients. However, it is observed that a as you give appropriate credit to the original author(s) and the source, significant number of women who could be candidates for BCS provide a link to the Creative Commons licence, and indicate if changes still decide to undergo mastectomy [14]. Hence, larger-scale were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated studies analysing and documenting the effect of multiple factors otherwise in a credit line to the material. If material is not included in must be conducted to understand surgical care for breast cancer the article's Creative Commons licence and your intended use is not in India. Future work should focus on identifying intricate barri- permitted by statutory regulation or exceeds the permitted use, you will ers pertaining to access and availability of radiation treatments need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://cr eativ ecommons. or g/licen ses/ b y/4.0/ . that may influence patients’ choice of BCS [8 , 24]. Conclusion References We found that two-thirds of Indian surgeons prefers BCS 1. Cancer. (2021) World Health Organization. https://www .who. int/ over mastectomy. This is consistent with global trends. news- room/ fact- sheets/ detail/ cancer. Accessed August 2021. 2. The global cancer observatory. (2021). India Globocan 2020 [Fact Lack of surgeons trained in performing BCS was a common Sheet]. 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Bellavance EC, Kesmodel SB (2016) Decision-making in the jurisdictional claims in published maps and institutional affiliations. surgical treatment of breast cancer: factors influencing women’s choices for mastectomy and breast conserving surgery. Front Springer Nature or its licensor holds exclusive rights to this article under Oncol 6 a publishing agreement with the author(s) or other rightsholder(s); 24. Najafi M, Ebrahimi M, Kaviani A, Hashemi E, Montazeri A author self-archiving of the accepted manuscript version of this article (2005) Breast conserving surgery versus mastectomy: cancer is solely governed by the terms of such publishing agreement and practice by general surgeons in Iran. BMC Cancer 5(1) applicable law. 1 3

Journal

Indian Journal of Surgical OncologySpringer Journals

Published: Aug 3, 2022

Keywords: Breast conservative surgery; Mastectomy; Breast cancer; Cancer surgery; India

References