When Do Patients with Breast Cancer Seek Help from Psycho-oncology Services? A 3-Year Retrospective Study from India

Abstract Introduction  Breast cancer is the most frequent cancer among women. In the last few decades, the outcome of breast cancer has improved significantly in terms of survivorship and quality of life. However, it is crucial that alongside managing the disease, breast cancer services address and manage associated or co-occurring psychiatric illnesses such as acute stress reactions, procedural anxieties, adjustment issues, depression, and fear of recurrence, which leads to an overall better experience of the patient. Objective  There is a paucity of data on the patterns of psychiatric morbidity in patients with breast cancer who access psycho-oncology services in a naturalistic setup outside research studies from India. The current study focused on exploring this alongside reporting the common treatment methods adopted for this group of patients. Materials and Methods  Real-life data from electronic patient records were retrospectively reviewed for all patients with breast cancer accessing integrated psycho-oncology services in a tertiary care hospital in India over three 3 years (2018–2020). The various psychiatric morbidities were reported, along with associated cancer demographic data, disease characteristics, and treatment details. Results  Of all the breast cancer patients ( n  = 338) in the calendar years 2018 to 2020 reviewed by psycho-oncology services, the most common psychiatric diagnosis was depressive illness ( n  = 100, 29.6%), followed by adjustment disorders ( n  = 68, 20.1%) and anxiety ( n  = 66, 19.5%). There was a significant minority with serious enduring mental illnesses such as schizophrenia ( n  = 11, 3.3%) and bipolar disorders ( n  = 14, 4.1%). On the other hand, 14.2% ( n  = 48) of the patients with breast cancer who attended Psycho-oncology outpatient department did not have any psychiatric syndrome. Around 16.3% of patients could be managed without a prescription for any medications and almost half of the patients needed only one psychotropic medicine. Psychological interventions were used for 45.6% of patients. Conclusion  Integrated psycho-oncology services in a cancer hospital catering to patients with breast cancer help in psychiatric assessment, diagnosis, and addressing the mental health needs of patients. The treatment offered needs to be nuanced and individualized and may require a combination of psychotropic medications and psychological techniques.


Introduction
Breast cancer is presently the most diagnosed cancer and the fifth leading cause of death worldwide. 1In India, it is the most frequent cancer among women. 2In the past three decades, remarkable advancements have been made in breast cancer treatments, especially in the areas of surgery, radiotherapy, targeted systemic therapies, genomics, and molecular biology that in turn has not only improved overall survival (including disease-free survival) but has also resulted in better management of the axilla, more acceptable cosmetic outcomes, and reduced treatment time and hospital visits. 3Due to enhanced survivorship and better cosmesis, patients often face minimization of the subjective distress associated with the diagnosis.They often face comments as "it's only breast cancer" and that "there is nothing much to worry about." 4 However, objective data show, despite the medical advances, rates of psychological morbidities is highest among patients with breast cancer as compared to all other cancers. 5Breast cancer treatments, although ensuring longer survivorship, affect nearly all the key aspects of femininity including sexuality, physical identity, fertility, and the ability to breastfeed. 4 The diagnosed person or the survivor deals with a plethora of issues including a constant preoccupation about the relapse of cancer, body-image issues related to mastectomy, lymphoedema and hair loss, anticipated problems in companionship, sexual intimacy, reproduction, and parenting abilities, and even worries about passing the "cancer gene" to their grown-up children. 3,6,7Many of these concerns can be chronic and patients may continue to have anxiety and depressive symptoms for years. 8,9These symptoms are often colored by the patient's perception of the disease, their illness experience, and the coping resources of the person.Interestingly studies showed that the psychological symptoms are not associated with any biological prognostic factors like tumor size, histology, number of axillary lymph nodes involved, or other treatmentrelated factors, except for adjuvant chemotherapy which has been found to increase the risk for either or both anxiety and depression. 8The patient's concerns have a significant impact on the family members.The prevalence of anxiety and depression in family/caregivers is similar to that of breast cancer patients. 10In India, caregiving is mostly performed by family members (both physical and psychological) and in most cases, family members do not feel the need or have the means to seek professional help. 11Family caregivers of cancer patients often report significant anxiety or depressive symptoms and these symptoms persist during the initial months and years following the cancer diagnosis. 12There-fore, there has been an increasing emphasis on the psychosocial care of breast cancer patients, survivors, and caregivers.A recent study conducted in India points out that both the patient and the caregiver seek structured counselling services for patient-caregiver dyads, improved doctor-caregiver communication, and routine practice of disclosure of cancer diagnosis. 13sycho-oncology is a relatively recent area of specialization in India and not many cancer centers in India have a psycho-oncology service accessible to patients, although this is changing rapidly.One paper cites the lack of routine integration of psychosocial care in cancer settings. 14Most psycho-oncology studies conducted in India usually point to the need for the development of psychosocial approaches for cancer that are suitable and acceptable to patients.In this article, we report the types of mental health issues faced by patients with breast cancer who were assessed by the psycho-oncology unit in a tertiary cancer hospital in eastern India over 3 years starting from January 2018 and ending in December 2020.The article also discusses a service delivery model that is suited to low-and middle-income country settings.

Objectives
The main objective of the current study was to explore and describe the nature of psycho-oncological services accessed by patients with breast cancer in a specialist cancer center.

Study Design
The study follows a design of a retrospective case series for a period of 3 years based on a contemporaneous electronic medical record of psychiatric assessments documented for all the patients by the treating consultant psychiatrist after ethical clearance for the institutional review board.

Setting
This study was conducted in a tertiary, philanthropic cancer care center serving eastern Indian states and neighboring South Asian countries like Bangladesh, Nepal, and Bhutan.Currently, the hospital has a capacity of 431 beds and caters to a large catchment area.

Psycho-oncology Services
The study hospital has a well-functioning psycho-oncology service, developed since the very beginning of the hospital's Conclusion Integrated psycho-oncology services in a cancer hospital catering to patients with breast cancer help in psychiatric assessment, diagnosis, and addressing the mental health needs of patients.The treatment offered needs to be nuanced and individualized and may require a combination of psychotropic medications and psychological techniques.
inception and currently maintained by two consultant psychiatrists and clinical psychologists.The department has daily outpatient and in-patient services and works consistently and routinely for patients reaching out for psychological aid.The hospital's breast disease management protocol ensures optimal access for patients, who at times come with ailments in the context of their cancer diagnoses and at other times with a premorbid psychiatric illness that might affect cancer treatment itself.

Duration of Service Assessed
The duration of the study was for three calendar years, from January 1, 2018 to December 31, 2020.

Collection of Data
The study hospital maintains an electronic health record system and the department of psycho-oncology maintained contemporaneous health records electronically.Data were collected from the existing health records.The electronic hospital management system provided the demographic and clinical data for the patient and was supplemented by manual documents of the hospital.Institutional ethics approval was obtained (EC/WV/TMC/49/20) for the study.

Analysis of Data
All breast cancer patients who were assessed by the psychooncology department between 2018 to 2020 were included in the study.Simple descriptive statistics were used with frequencies to describe the patients accessing psycho-oncology services.The continuous variables (age and distance of the patient's home to the hospital) were checked for normality with the Shapiro-Wilk test and Q-Q plots and an appropriate measure of central tendency was used to describe the data.Since the results suggested that our data were not normally distributed, we proceeded to use the median and the interquartile range as descriptive parameters for the data.

Ethics
The present study was in accordance with the ethical standards of the institutional ethical committee, national guidance on research ethics, and the 1964 Helsinki Declaration and its later amendments. 15The study was approved by the institutional ethics committee of Tata Medical Center, Kolkata.In view of the retrospective nature of the study, a waiver of consent was obtained from the institutional ethics committee of Tata Medical Center, Kolkata.As per institutional policy (IEC Protocol Waiver No -EC/WV/TMC/49/20 on August 18, 2020).

Results
A total of 2,448 patients were treated by the breast oncosurgery team between the years 2018 and 2020, out of which 338 patients reached out for psycho-oncology services (►Table 1).Of 338 patients, 335 were females, while three of the patients were adult males with breast cancer.The age of the patient and the distance of the patient's home to the hospital were both continuous variables that were not normally distributed.The age of patients ranged from Of the 338 patients who accessed our service, 319 patients (94.4%) had a diagnosis of invasive ductal carcinoma, whereas 9 patients (2.7%) had invasive lobular carcinoma.Other carcinoma types (3% of all patients) included ductal carcinoma in situ, invasive mammary carcinoma, and carcinomas of no special type/mixed type (►Table 2).Among the patients who accessed psycho-oncology outpatient department, 171 (50.6%) patients were at stage 2 cancer, 110 (32.5%) patients had stage 3 cancer, and 45 (13.3%) patients were diagnosed to have stage 4 cancer.More than half of the patients (51.5%) patients underwent mastectomy, while 34.9% of patients underwent breast-conserving surgery.Among all the patients, 13.6% patients did not undergo any form of surgery as they had distant metastasis.Almost three-fourths of the patients (73.4%) did not have any distant metastasis.Most (88.8%) patients underwent some form of chemotherapy.More than three-fourths of all patients (83.1%) were given radiation therapy, while two-thirds of the patients (66.9%) received hormone therapy.More than half of all patients (190 or 56.20%) presented with some form of medical comorbidity; of them, 59 (17.45%) patients had at least two comorbidities and 26 (7.69%) had more than two comorbidities.Hypertension was the most common comorbidity reported in 123 (64.73%) patients, followed by diabetes in 68 (35.78%) patients and hypothyroidism/hyperthyroidism in 55 (28.94%) patients.Only 35 patients (10.35%) had both diabetes with hypertension.
Of all the breast cancer patients reviewed by psychooncology services, the most common psychiatric diagnosis was depressive illness (n ¼ 100, 29.6%), followed by adjustment disorders (n ¼ 68, 20.1%) and anxiety (n ¼ 66, 19.5%); next were major psychiatric disorders such as schizophrenia (n ¼ 11, 3.3%), bipolar disorders (n ¼ 14, 4.1%), organic mood or psychotic disorders (n ¼ 9, 2.7%), and neuro-cognitive disorders (n ¼ 3, 0.9%) (►Table 3).Amongst the patients who were referred, 14.2% (n ¼ 48) of the breast cancer patients did not have any psychiatric syndrome.There was no report of completed suicide amongst the patients diagnosed with breast cancer in the year for which the data were being analyzed.The number of treatment contacts with psycho-oncology services varied and ranged from a single contact to 24 separate contacts with mental health professionals, the median number of contacts being 2 (IQR ¼ 1-4).The number of contacts was more (median 3.50, IQR ¼ 1.75-9.25)for people with known severe enduring mental illness.Based on the median score, the entire sample of patients included in the study was divided into two groups (1-3 evaluations vs. >3 evaluations by psychooncology).The chi-square test was used for exploring the association of those with and without severe mental illnesses (e.g., schizophrenia, bipolar disorder, etc.), the total number of evaluations by psycho-oncology (1-3 evaluations vs. >3 eval-uations by psycho-oncology) was found to be statistically significant (p < 0.01).While some of the patients evaluated (16.3%) did not need any psychotropic medications, almost half of the patients (48.52%) were managed with only one medication for their symptoms.An almost equal percentage of patients (45.6%) also needed psychological interventions in the form of psychoeducation, psychological support, coping strategies, suggestion for lifestyle modifications including sleep hygiene techniques, or a combination of these.

Discussion
7][18] In the current article, around half of the patients who accessed psycho-oncology services presented in advanced stages (stage 3 or 4), while others presented in earlier stages.The majority of the patients received curative surgery, radiation therapy, and/or chemotherapy based on the weekly multidisciplinary group discussions.The common reasons for referral to psycho-oncology from the perspective of the oncologist were low mood, fragmented sleep, restlessness, and being agitated or expressing suicidal thoughts.It was rare that a syndromic psychiatric diagnosis was mentioned in the referral.Of the patients who were referred, most were diagnosed with depressive disorder (n ¼ 100, 29.6%), followed by adjustment disorders (n ¼ 68, 20.1%) and anxiety disorders (n ¼ 66, 19.5%).European and American guidelines stress the need for the incorporation of psychological interventions in breast cancer services. 19,20ven with significant improvement in the outcome of breast cancer over the last few decades, a survey conducted in 32 countries in Europe showed that only one-third of the countries had documented requirements and specific indicators for psychosocial interventions, resources they require, and educational requirements. 19The role of psychosocial support remains crucial in treatment."The SARS-CoV-2 pandemic had affected cancer care and service delivery around the world and we published the impact of the pandemic on psycho-oncology services separately." 21 recent review 22 covering several studies around the globe, including India, concluded the prevalence of depression in breast cancer to be around 32%.The higher rates of psychiatric morbidity reported in this audit were perhaps because we only evaluated patients who were referred.All patients are assessed by the breast surgery or medical oncology teams and referred to psycho-oncology as per accepted disease management guidelines when suspected to have psychological or psychiatric morbidity.Some patients diagnosed with syndromic psychiatric morbidity needed pharmacological management.Depression in breast cancer is associated with increased morbidity, suicidality, and longer hospital stays for treatment. 23Depression can result in poorer adherence to cancer-specific treatments 24 and that may indirectly increase the risk for mortality.Antidepressants including selective-serotonin reuptake inhibitors are recommended for managing syndromic depression and these are effective in this group of patients.The majority of patients treated by us were managed with a single psychotropic combined with psychological interventions.Only around one-third of the assessed patients needed more than one psychotropic medication.This was mostly due to the use of nonsedative antidepressants like Venlafaxine, with less propensity to interfere with the metabolism of Tamoxifen, 26 but occasionally requiring additional shortterm low-dose benzodiazepines for fragmented sleep.Overall, avoiding polypharmacy is recommended.Psychological interventions were initiated for almost half of the patients seeking help, which is often the preferred mode of intervention for the management of issues related to coping with a cancer diagnosis and related predicaments like proce-dural anxiety, body-image issues, fear of recurrence, and psychological distress at the end of life.Psycho-education about possible symptoms, treatment needed, and behavioral and lifestyle interventions such as sleep hygiene were used frequently.Lifestyle interventions empower the patient and their relatives to initiate simple changes that may help them navigate through complex treatment processes when the psychological distress is transient. 27,28Psycho-educational approaches, on the other hand, attempt to address realistic concerns by instilling a sense of control within transiently distressed patients; people with more serious psychological issues may need more specific psychological interventions. 29s evident from our data, psychological interventions are brief as many patients accessed the service for a few sessions only.The people who came for repeated consultations usually had a pre-existing mental illness.The study emphasizes the need for an integrated psycho-oncology service model.This can improve access to mental health care in resource-poor low and middle-income countries like India. 30,31he typical referrals of patients with breast cancer patients managed by psycho-oncology services are represented in ►Table 4.
Service delivery model for psycho-oncology services for women with breast cancer in low-and middle-income countries: Therefore, an integrated hospital-based psycho-oncology service for patients with cancer is proposed.It is necessary that clinicians treating women with breast cancer are initially sensitized about the magnitude of the problems and made aware of early warning signs of mental health difficulties that warrant a referral.The institutional breast cancer

Strengths and Limitations
All patients were reviewed by consultant psychiatrists as per the International Classification of Diseases 10 Revision.The psycho-oncology services were provided in the same hospital, available every day of the week, and most patients are seen on the same day of the referral whenever possible.The nature of the services was comprehensive for both outpatients and inpatients.Despite being a single-center study, this center caters to a wide geographical region in India and surrounding countries, and thus provides a large catchment area.Additionally, the robust electronic hospital management system resulted in thorough and consistent patient records.This emphasizes the role of an integrated service model in low-and middle-income countries.
The article presented data on those women with breast cancer who accessed psycho-oncology services.This article cannot comment on the patients with breast cancer who did not attend psychiatry consultations or the overall prevalence of psychiatric morbidity in women with breast cancer.The data are presented using simple descriptive statistics and further associations were not presented as the study was originally not powered for multiple testing and there were no a hypotheses.Also, for some patients, the stage of cancer progressed over time.Hence testing for associations was avoided.

Conclusion
This study showed that a significant number of women with breast cancer access psycho-oncology services, of whom around half of the patients had anxiety or depressive illnesses, one-fifth had stress-related adjustment disorders and only a minority (10%) had major psychiatric disorders like schizophrenia or bipolar affective disorder.The availability of integrated psycho-oncology services in the cancer center improved the access to mental health care for patients who wanted to seek help.This article attempts to highlight the importance and need for a psycho-oncology service model managing common psychiatric comorbidities in the present health care milieu.
Statement: all authors have participated in the write up of the article and approved the submitted version of the manuscript.All the authors fulfil the authorship criteria and declare that the manuscript represents honest work.The contents of this manuscript have not been copyrighted or published previously and are not under consideration for publication elsewhere.In addition, this manuscript will not be copyrighted, submitted, or published elsewhere while acceptance by "Indian Journal of Medical and Paediatric Oncology" is under consideration.

Table 2
Breast Cancer Psycho-oncology Mukherjee et al. 213 Cancer disease characteristics of our sample group 25Indian Journal of Medical and Paediatric Oncology Vol. 45 No. 3/2024 © 2023.The Author(s).Abbreviations: COPD, chronic obstructive pulmonary disease; HER2, human epidermal growth factor receptor 2.

Table 4
Typical presentation and psycho-oncology management of patients with breast cancer protocol practiced included specific pointers for such a referral.The psycho-oncology services are offered for both out-patients and hospitalized patients and are almost always started on the day of referral.The psycho-oncology team used pharmacological and nonpharmacological methods of treatments delivered by consultant psychiatrists and clinical psychologists.The typical patient profiles and interventions offered are discussed in ►Table 4.