Cancer care in South India: perspectives from visiting Canadian oncologists.

Cancer is recognized as an increasing threat to public health in lowand middle-income countries (lmics). In light of that epidemiologic transition, interest in the field of global oncology is growing. As medical oncologists (SRB, CMB) and trainees (SK, JCD) from Canada, we had the opportunity in early 2016 to visit a large academic cancer centre in South India for stays ranging from 2 weeks to 3 months. In this commentary, we offer our perspectives on the delivery of cancer care in Kerala. A disproportionate burden of cancer affects the lmics. The World Health Organization reports that, without immediate action, the global number of deaths from cancer will increase by approximately 80% by 2030, with most of those deaths occurring in the lmics1. Although more than half of new cancer cases and about two thirds of cancer deaths occur in the lmics, only 5% of global cancer resources are spent in those settings2. In 2012, 1 million new cancer cases were diagnosed in India, and approximately 700,000 deaths from cancer occurred. The most common cancers in India are oral cavity, lung, stomach, and colorectal cancers in men and breast, cervical, oral cavity, and colorectal cancers in women3. The state of Kerala (population approximately 33 million), located on the southwest coast of India, has the highest Human Development Index of all states in India4. Kerala also has the highest literacy rate, greatest life expectancy, and lowest infant mortality rate4. Representing 1% of India’s land mass and 3% of its population, Kerala is one of the more densely populated states in India. Cancer care in Kerala is delivered at 2 governmentfunded multimodality comprehensive cancer centres and 5 government medical colleges. Smaller cancer programs also exist at a number of private hospitals. The largest and oldest cancer centre is located in the capital city of Trivandrum (population 1 million). The Trivandrum Regional Cancer Centre (rcc) was established in 1981 and currently sees 16,000 new cancer cases annually, representing approximately one third of all cancer cases in Kerala. Oncology training in Kerala is modelled after the British system. Graduates earn an mbbs (Bachelor of Medicine, Bachelor of Surgery) after 5.5 years of medical school. Most oncologists complete 3 years of general medical training before beginning a 3-year rotation in clinical oncology. That education can be followed by optional site-specific fellowship training. In that training scheme, oncologists are equipped to deliver both radiation and chemotherapy. In more recent years, dedicated programs in medical oncology have been introduced; they involve 3 years of internal medicine training after medical school followed by 3 years of dedicated medical oncology. At the rcc, medical oncologists provide care for patients with hematologic and connective-tissue malignancies. Our first (and perhaps most striking) observation upon arriving at the rcc was the sheer volume of patients. Given that Kerala’s population approaches that of Canada and that the state has only 2 comprehensive cancer centres, we should not have been surprised to arrive on our first day to a waiting room overflowing with a sea of patients and their family members. The clinic area was much the same, with hundreds of patients patiently waiting outside the clinic doors for their name to be called. The number of sick patients was at times overwhelming. Each day, the oncologists worked diligently and effectively; it was not uncommon for 1 oncologist to see 80 patients in a single day. Physicians in India typically work 6 days per week. The oncologists at the rcc run large outpatient clinics 3 days and have 3 days per week for radiation planning and treatment review. The high clinical volumes limit the amount of time that can be spent with each patient. Understandably, they are left with little opportunity to initiate important conversations about prognosis and goals of care. Despite the recognized time pressures, the oncologists are deeply motivated and committed to providing excellent patient care. Evidence-based treatment decisions

also exist at a number of private hospitals. The largest and oldest cancer centre is located in the capital city of Trivandrum (population 1 million). The Trivandrum Regional Cancer Centre (rcc) was established in 1981 and currently sees 16,000 new cancer cases annually, representing approximately one third of all cancer cases in Kerala. Oncology training in Kerala is modelled after the British system. Graduates earn an mbbs (Bachelor of Medicine, Bachelor of Surgery) after 5.5 years of medical school. Most oncologists complete 3 years of general medical training before beginning a 3-year rotation in clinical oncology. That education can be followed by optional site-specific fellowship training. In that training scheme, oncologists are equipped to deliver both radiation and chemotherapy. In more recent years, dedicated programs in medical oncology have been introduced; they involve 3 years of internal medicine training after medical school followed by 3 years of dedicated medical oncology. At the rcc, medical oncologists provide care for patients with hematologic and connective-tissue malignancies.
Our first (and perhaps most striking) observation upon arriving at the rcc was the sheer volume of patients. Given that Kerala's population approaches that of Canada and that the state has only 2 comprehensive cancer centres, we should not have been surprised to arrive on our first day to a waiting room overflowing with a sea of patients and their family members. The clinic area was much the same, with hundreds of patients patiently waiting outside the clinic doors for their name to be called. The number of sick patients was at times overwhelming.
Each day, the oncologists worked diligently and effectively; it was not uncommon for 1 oncologist to see 80 patients in a single day. Physicians in India typically work 6 days per week. The oncologists at the rcc run large outpatient clinics 3 days and have 3 days per week for radiation planning and treatment review. The high clinical volumes limit the amount of time that can be spent with each patient. Understandably, they are left with little opportunity to initiate important conversations about prognosis and goals of care.
Despite the recognized time pressures, the oncologists are deeply motivated and committed to providing excellent patient care. Evidence-based treatment decisions mirror our practice in Canada, and their finely honed incisive clinical acumen allows them to make diagnoses and treatment decisions quickly and effectively. A vivid example was seen during ward rounds with a senior oncologist, who successfully reviewed 30 bone marrow transplant patients before morning clinic, but with an attention to detail that did not suffer from the necessary haste.
Because the rcc is the major referral centre for all of Kerala, it was not uncommon to see patients who had travelled up to 10 hours by overnight train to attend appointments. Although the need to travel vast distances undoubtedly put tremendous strain on the patients, delivery of care was organized to minimize the number of visits made to the rcc. It was not uncommon for us to see, in the radiation oncology clinic, a patient who required a surgical oncology consultation, palliative care consultation, or echocardiography. Those services could almost always be arranged within a few hours so that they took place on the same day. In that respect, the care at rcc was more "patient-centred" than at our centres, where patients return to clinic on numerous occasions to see each specialist separately.
To minimize the need for patients to travel a vast distance, the government of Kerala has recently established oncology units at various district hospitals across the region. However, the physicians who currently staff those units are general practitioners, many of whom have no formal training in oncology. Generally, only 1 physician is assigned to the oncology unit at those hospitals, requiring them to be always available for cancer patients. In addition, some of the district hospitals have limited facilities to diagnose and manage oncology complications. For instance, one of the smaller hospitals we visited had no on-site microbiology lab and was accordingly limited in providing care for patients with febrile neutropenia. Therefore, despite attempts to manage patients in the periphery, most patients were eventually sent to the rcc for further assessment, placing a further burden on the patients and the care team at the rcc.
A unique aspect of cancer care in Kerala is the level of family involvement. It was extremely rare to see a patient attend clinic alone. Family members are actively involved in all aspects of care, from symptom reporting to booking computed tomography imaging and hand-delivering chemotherapy orders. In some instances, a family member will request that the physician not tell the patient about the prognosis, for fear of how the patient would cope with the news. In other instances, the patient will simply relinquish disclosure and any decision-making about their cancer to a family member. In either instance, the oncologist will generally respect the family's request. Perhaps the most obvious display of family support is when a patient is admitted to hospital. At least 1 family member will remain at the bedside during the entire admission and will take responsibility for providing all meals for the patient.
During our time in Kerala, we saw a high proportion of advanced and incurable cancers. The cancer mortality rate in India is very high-estimated at 68% of the annual incidence 3 . The cause of such advanced disease is likely multifactorial, but can be partly attributed to a lack of health awareness and screening programs. Difficult social and economic conditions also contribute to the poor performance status of many patients seen at diagnosis. As a result, aggressive treatment and combination chemotherapy are delivered less commonly than oncologists in Canada are used to. In response to the limited performance status of many patients, one popular regimen that we saw used in head-and-neck cancers was metronomic methotrexate, a regimen that is very rarely used in North America 5 . Thus, the combination of advanced disease at presentation and poor functional status that limits aggressive treatment options likely both contribute to the high cancer mortality in India.
In addition to providing patient care, oncologists at the rcc have led major research studies that have influenced practice globally. The rcc established a hospital-based cancer registry in 1982 and currently maintains a robust population-based cancer registry for the District of Trivandrum (population 3.3 million). Those datasets support a very active program in epidemiology at rcc 6 . The Trivandrum Oral Cancer Screening Study group published a pivotal cluster-randomized controlled trial in 2005 7 . Oral cavity cancer remains one of the most common causes of cancer death in the area. The study group evaluated whether a visual, inspection-based screening program would lead to a reduction in oral cancer mortality. Trained health workers performed oral visual inspections in 87,655 individuals, and the authors reported a substantial reduction in oral cancer mortality (hazard ratio: 0.66; 95% confidence interval: 0.45 to 0.95) among users of tobacco or alcohol 7 . Those data stimulated ongoing community-based oral cavity cancer screening camps throughout Kerala that target high-risk populations. The rcc oncologists are also leading a cluster-randomized trial of clinical breast exam in 115,652 women in Trivandrum district. Early results have been reported 8 , and final analyses are expected in the near future.
Lack of access to palliative care in the lmics is recognized as a global issue, with an urgent need for scale-up of services [9][10][11] . Unfortunately, in most lmics, opioids are not readily available, in large part because of strict government regulations and a lack of palliative care awareness 12 . In India, it is estimated that only 0.4% of cancer patients in need of opioids have access to them 13 . In that context, Kerala is widely recognized as a global leader in palliative care. One of India's first pain clinics was established at the rcc in 1986. The state government of Kerala adopted a palliative care policy in 2008, declaring that palliative care is an integral component of standard health care 14  Kerala is home to the world-renowned nongovernmental organization Pallium India. Pallium India provides clinical care to patients, educates health professionals from across India, and serves as a national advocate for palliative care. We had the opportunity to join the Pallium India care team for several home visits. During one memorable home visit to a boy with refractory bone metastases, we were able to witness the remarkable care that Pallium India provides. Despite several rounds of intensive chemotherapy, the boy was clearly suffering from uncontrolled pain, and his family was riddled with a deep sense of fear and anxiety. The palliative care physician spent time understanding the nature of the boy's pain and his current analgesic regimen. Through that assessment, the physician was able to discover that the boy's mother was weary of providing breakthrough medication for fear of side effects. He counselled the boy and his mother on better symptom control and management of side effects, and also addressed their underlying spiritual and existential suffering. Beyond holistic care, Pallium India also provides free medications, including opioids, to patients who would otherwise be unable to afford them. Although many challenges remain in accessing palliative care services, initiatives in Trivandrum are an encouraging step toward broad access across India.
Our collective time in Kerala had a significant impact on each of us as we consider our careers in oncology. We gained insight into the global burden of cancer and the challenges of delivering cancer care in a low-resource country. Some of the major barriers to quality cancer care in Kerala are the overwhelming number of patients (leading to an intense workload for oncologists and limited time for important conversations), inadequate care in the periphery outside the major cancer hospitals, and a higher prevalence of advanced disease leading to poor outcomes. Despite those challenges, we were inspired by the work ethic, dedication, and clinical acumen of the Indian physicians. Their commitment to their patients and to the improvement of cancer care in India was truly remarkable. Overall, the experience greatly enriched the practice of medical oncology for each of us. We returned home with a strong appreciation for the Canadian health care system, a renewed commitment to patient-centered care, and a growing passion to improve global cancer care. Although separated by great distances, we remain in frequent contact with our friends and colleagues in Kerala, having now established long-term partnerships in oncology medical education and cancer health services research.