ABSTRACT
The study evaluates the outcome after surgery for pancreatic and periampullary tumors in Greenlandic Inuit with overall survival (OS) of pancreatic ductal adenocarcinoma (PDAC) as secondary outcome. Results were compared with Danish patients with an identical tumor stage and age operated at the same hospital during the same period from 31. January 1999 to 31. January 2021. Follow up was minimum one year. Preoperative health data shoved a higher rate of smoking among Greenlandic patients, but a lower preoperative comorbidity than in Danish patients. Patients from Greenland had a lower resection rate and a higher rate of palliative operations. Postoperative complications and in-hospital mortality were not significantly different. Adjuvant oncologic treatment was well accepted by Greenlandic patients but less common in a palliative setting than in Danish patients. The one, two, and five-year survival in Greenlandic and Danish patients after radical operation for PDAC was 54.4% vs. 74.6%, 23.4% vs. 48.6%, and 0.0% vs. 23.4%, respectively. The overall survival with non-resectable PDAC was 5.9 and 8.8 months, respectively. It is concluded that although patients from Greenland have the same access to specialized treatment, the outcome after treatment for pancreatic and periampullary cancer is less favorable than in Danish patients.
Introduction
Worldwide, pancreatic and periampullary cancer is the seventh leading cause of cancer-related mortality but with continental variations [Citation1,Citation2]. Since the Second World War the Inuit (Indigenous population in the Arctic) have gone through a Westernization, which has improved the health conditions but also changed the disease panorama with an increasing incidence of cancer [Citation3–5]. The incidence of pancreatic and periampullary cancer has been reported to be the same among Inuit but with a higher incidence than among the Caucasian population in Canada, the United States and Denmark [Citation6].
Greenland is part of the Kingdom of Denmark. The population is estimated to 56,000 (year 2020) of which 90% is of Inuit descent, the remaining is Caucasian (mostly Danish). Like the Danish, the Inuit population has free access to health care in Greenland and in Denmark.
There are only five hospitals in Greenland. In remote settlements, there are health stations with limited services and educated staff. Queen Ingrid’s Hospital in the capital, Nuuk, is the main hospital and has units within general medicine, surgery, and gynaecology/obstetrics. Most patients, who need oncologic surgery, are referred to Copenhagen from the main hospital, but adjuvant and palliative chemotherapy is offered for selected diagnoses in Greenland. Surgical treatment of hepato-pancreato-biliary (HPB) tumours in the Greenlandic population is undertaken at Rigshospitalet, Copenhagen University Hospital. The hospital is a tertiary centre for HPB surgery affiliated with Copenhagen University and has a catchment area of around 2.5 million people.
The aim of the study was to investigate the results of pancreatic surgery for pancreatic and periampullary tumours in Greenland Inuit patients, and the secondary outcome was to compare the overall survival (OS) of PDAC with Danish patients.
Material and methods
Study population
The study includes all Inuit patients living in Greenland, who had pancreatic surgery for pancreatic and periampullary tumours at Copenhagen University Hospital from 31 January 1999 to 31 January 2021. Periampullary tumours define a heterogeneous group of neoplasms arising from the head of the pancreas, the distal common bile duct, and the duodenum.
Patients from Greenland (last patient operated 11 January 2021) were compared with a corresponding group of Danish patients with the same age distribution, 41–79 years, operated at the hospital for pancreatic and periampullary tumours in the same period. Patients’ survival was recorded until 31. January 2022. Cancer cases were classified by site in accordance with the International Classification of Diseases (ICD-10), 19th edition. All diagnoses were validated and histologically verified by the Department of Pathology at Rigshospitalet. Due to the small number of patients from Greenland, long-term survival was only analysed for patients with pancreatic ductal adenocarcinoma (PDAC).
Data
Data were collected from our prospectively maintained database of pancreatic operations, from patients’ electronic hospital records in Greenland (Cosmic) and in Denmark (Orbit and Epic), from the Danish National Pathology Data Registry and from the national Cause of Death Register in Denmark and in Greenland. The latter is administered by the Danish Health Data Agency and contains data from 1970 and onwards about gender, age, and causes, place and time of death. All Nationals in Greenland and Denmark have a Central Person Registration number that enables the search of health data [Citation7].
Treatment
All surgical procedures were standardised and included pancreato-duodenectomy (Whipple’s operation: resection of the pancreatic head, duodenum, antral part of the stomach, gall bladder and the common bile duct), total pancreatectomy as Whipple’s procedure including splenectomy, and distal pancreatectomy with resection of the body and tail of the gland including splenectomy. Palliative operations included gastrojejunostomy and hepaticojejunostomy.
Indication for stenting of the biliary duct by endoscopic retrograde cholangiopancreatography (ERCP) or percutaneous transhepatic cholangiography (PTC) was severe jaundice (>6 mg/dL), when operation could not be performed within one week or palliation of non-resectable tumours This procedure was performed, if possible, at the main hospital in Nuuk (only ERCP) or at Copenhagen University Hospital.
Before operation, a pancreatic surgeon and an anaesthetist evaluated the patient’s operability in the out-patient clinic, and a dedicated counselling providing the patient with information about operation and goals for recovery was given. The hospital has a staff of Greenlandic interpreters who were present during the information and at doctor’s round, if necessary.
Neither patients from Greenland nor Denmark received neoadjuvant oncologic therapy, which we define as a preoperative treatment for patients with up-front resectable tumours. Since 2008, adjuvant chemotherapy with gemcitabine became an offer to all patients with PDAC in Denmark and Greenland [Citation8] and from August 2016 the ESPAC-4 protocol with gemcitabine and capecitabine was implemented [Citation9]. From July 2018, combination therapy with FOLFIRINOX (folic acid, fluorouracil, irinotecan and oxaliplatin) was included in the adjuvant therapy for fit patients [Citation10]. Due to lack of evidence, patients with duodenal carcinoma were only offered adjuvant therapy in cases of regional lymph node metastases and/or low tumour differentiation, in which cases most patients were treated with FOLFOX (folic acid, fluorouracil, and oxaliplatin).
During the study period, there was no follow-up program for patients living in Greenland, but patients contacted their general practitioner or local health station, if needed. Danish patients with adenocarcinomas were followed until two years after the operation or until recurrence, in case of which they were referred to oncologic treatment. Follow-up with clinical assessment and clinical chemistry including serum cancer-associated antigen CA 19–9 was undertaken every three months the first postoperative year and every six months the second year or on demand. Since there is no present evidence that routine thoracoabdominal CT scan has an impact on survival this examination was only performed if recurrence was suspected, but on wide indications.
Definitions
Waiting time for operation was counted from the time of presentation of patient’s case at the MDT and until surgery. Relevant postoperative complications were recorded and included leakage from the pancreatic, bile or gastrojejunal anastomosis, intraabdominal haemorrhage and abscess formation, and other complications with severe or fatal outcome. In-hospital mortality was defined as all deaths from time of admission until discharge. Outcomes were described as postoperative complications, 30-days mortality, and OS. OS was defined as the time from operation to death from any cause at the time of the last follow-up. Contrary to OS, postoperative outcome was regarded as independent of pathology. All patients were followed for a minimum of one year.
Statistical analysis
The study was reported according to the STROCSS guidelines [Citation11] (www.strocssguideline.com). Data are presented as median, 25 and 75%iles (interquartile range, IQR). Categorical data are presented as numbers or percentages and were analysed with Fisher's exact test when appropriate. The Kaplan–Meier method was used to estimate OS and the log-rank test (Mantel-Cox) and Gehan’s test to examine the differences between curves. A p < 0.05 was considered significant. Statistical analysis was performed with GraphPad Prism version 6.05 (GraphPad®, La Jolla, CA).
Ethical approval
The study is an observational, retrospective quality assurance project according to the guidelines of the Danish Health Data Authority (http://Sundhedsdatastyrelsen.dk). The study was conducted following the principles stated in the Declaration of Helsinki. Patients’ written consent for using health data was obtained before operation. The use of registered data followed the General Data Protection Regulation of the European Union and the Danish Data Protection Agency. The study and the use of data were consented by the hospital ethical committee (Rigshospitalet), the Danish Data Protection Agency (RH −2015-07, nr. 03616) and the local ethical committee in Greenland.
Results
A timeline of operations is shown in . The number of operations of Greenlandic patients was almost uniform over time in contrast to Danish patients, where an increasing number of operations were seen during the study period. During this period, 46 Inuit patients were operated (). The distribution of patients followed the inhabited areas in Greenland with weight on the West coast and the capital Nuuk (). All patients were operated due to either verified malignancy or suspicion of malignant neoplasms. There were 42 (91.3%) patients with malignant neoplasms, which included 39 (84.8%) cases of pancreatic and periampullary adenocarcinoma. Other cases included one patient with a neuroendocrine tumour of the papilla, one patient with a gastric cancer in the antrum with growth into the pancreas, and one patient with a metastasis from a gastric cancer to the pancreatic tail. Four patients (8.7%) had benign pathology of whom one patient had a premalignant mucinous pancreatic cyst and three patients had pancreatitis.
Figure 1. Admissions over time of patients from Greenland and Denmark. Each value is the percentage of the total number of operations for each population during the whole study period.
Figure 2. Place of residence of 46 patients from Greenland operated on for pancreatic and periampullary tumours.
Table 1. Characteristics and operations of patients with pancreatic and periampullary tumours.
Pancreatic resection was performed in 30 patients (65.2%). This included 23 patients (76.7%) with pancreatic and periampullary adenocarcinoma, one patient with a neuroendocrine tumour, two patients with gastric adenocarcinoma involving the pancreas and four patients with benign tumours. The remaining 16 patients had non-resectable tumours of whom 12 patients (75.0%) had a palliative operation, either gastro-jejunostomy and/or hepatico-jejunostomy, while four patients (25.0%) only had an explorative laparotomy.
In the same period, 2264 Danish patients were operated, of whom 1887 patients (83.4%) had malignant tumours including 1538 patients (67.9%) with pancreatic or periampullary adenocarcinoma. The incidence of pancreatic and periampullary adenocarcinoma in the two groups is listed in . The median occurrence of adenocarcinomas was in the fifth decade in the Greenlandic and the sixth decade in the Danish patients ().
Table 2. Localization and stage of pancreatic and periampullary adenocarcinomas (%).
Table 3. Age distribution (males/females) with pancreatic ductal and periampullary adenocarcinoma. IQR inter quartile range.
Tobacco smoking was more prevalent among Greenlandic patients while diabetes and heart conditions were more prevalent in Danish patients ().
Table 4. Preoperative health data.
Time from first contact with the treating hospital (MDT conference) to the operation was 29 (IQR 20;43) days in Greenlandic patients and 33 (IQR 24;42) days in Danish patients.
The resection rate of malignant tumours in Greenlandic and Danish patients was 61.9% and 77.7%, respectively (p = 0.043). Preoperative stenting of the bile duct in jaundiced patients was performed in 13 out of 28 Greenlandic patients (46.4%) compared to 771 out of 935 Danish patients (82.5%) (p < 0.001). Extensive resection such as total pancreatectomy was performed in three Greenlandic patients (6.5%) and one patient (2.2%) had porto-mesenteric resection. In the Danish group, 330 patients (14.6%) had total pancreatectomy and 300 (13.3%) had porto-mesenteric resection.
The incidence of major surgical complications or death after pancreatic resection was independent of pathology and is listed in .
Table 5. Complications and 30-days mortality in patients after surgery for pancreatic and periampullary tumours.
Fourteen patients (60.9%) from Greenland with pancreatic and periampullary adenocarcinoma received adjuvant oncologic treatment compared to 772 (67.8%) Danish patients. But only four of 16 Greenlandic patients (25.0%) with non-resectable tumours had palliative oncologic treatment compared to 158 out of 300 (52.6%) Danish patients. Gemcitabine was the preferred treatment of PDAC in Greenland. Only two patients had combination therapy with FOLFIRINOX and one patient had gemcitabine and cabecitabine. Of 18 Greenlandic patients, who had adjuvant or palliative chemotherapy, seven patients were treated at the minor local hospitals (only gemcitabine), the remaining patients were treated at the main hospital in Nuuk.
Data on recurrence and causes of death were insufficiently recorded in the Greenlandic medical records, but 21 out of 23 patients, who had radical surgery for adenocarcinoma, had died at the end of the survey. Three patients developed other malignant tumours after pancreatic resection: one patient with pancreatitis developed a brain tumour with fatal outcome, one patient with periampullary adenocarcinoma a penis cancer, and one patient with adenocarcinoma of the common bile duct with parotid gland cancer. At the end of the study period, only seven patients (15.2%) from Greenland were alive. This included two patients with periampullary adenocarcinoma, one patient with metastasis to the pancreatic tail from a gastric cancer, one patient with a neuroendocrine tumour, one patient with a mucinous cyst and two patients with pancreatitis.
The median OS after radical surgery in patients from Greenland and Denmark with PDAC, which accounted for the largest group of malignancy, was 15.5 and 23.3 months, respectively () (p = 0.009). In non-resectable cases, the OS after explorative or palliative surgery was 5.9 and 9.5 months, respectively () (p = 0.026).
Figure 3. (a). Survival of patients operated on for pancreatic ductal adenocarcinoma. The median overall survival of Greenlandic and Danish patients was 15.5 months vs. 23.3 months (p = 0.009). (b) Survival of patients after surgery for non-resectable pancreatic ductal adenocarcinoma. The median overall survival of Greenlandic and Danish patients was 5.9 months vs. 9.5 months (p = 0.018).
Discussion
This is the first published study on the results of pancreatic surgery and survival among Inuit in Greenland. Although the number of patients was few and ranged over more than 20 years, it was possible to evaluate the outcome after surgery with the corresponding Danish patients. However, in some of the chosen parameters, a small number of patients did not have the power to rule out a real difference and avoid a type two error.
Since the Cause of Death Register is complete, neither patients in Greenland nor in Denmark were lost to follow-up regarding survival statistics. Reporting of cancer in Greenland to the Danish Cancer Registry is mandatory, but the real incidence of pancreatic and periampullary adenocarcinoma is unknown, as patients in sparsely populated areas may die without a diagnosis. In two studies from 1969 to 1988 and 2000 to 2010 [Citation12,Citation13], the crude rates and standardised incidence ratios of pancreatic and periampullary carcinoma were higher in Greenland compared to Denmark. This is in keeping with a higher incidence of gastrointestinal cancer among Inuit in the whole circumpolar area [Citation14,Citation15]. According to the NORDCAN, which is a database on cancer statistics of the Nordic countries [Citation16], the incidence of pancreatic cancer in males and females in Greenland is 12.0 and 11.6/100,000 inhabitants, respectively, compared to 8.6 and 6.8/100,000, respectively, in Denmark. During the study period, the number of Greenlandic patients who were operated for pancreatic and periampullary tumours was relatively stable in contrast to the increasing number of operations among Danish patients.
In addition to smoking [Citation17,Citation18], cancer risk factors, such as heavy alcohol use, dietary transition, obesity, and physical inactivity, have a high prevalence among Indigenous people in the Arctic, and this also applies to the population in Greenland [Citation19–22]. Other health risks like diabetes and hypertension are also increasing [Citation23–25]. However, we found that apart from a higher incidence of smokers among patients from Greenland, the incidence of diabetes and hypertension was still lower than among the Danish patients.
Patients from Greenland have the same access to specialised surgical treatment in Denmark as Danish patients [Citation26]. Time from diagnosis and referral after MDT conference was not significantly different between the two groups of patients. This is noteworthy in view of the difficult geographic conditions in Greenland and the meteorologic challenges that may prevent domestic air transport for days or even weeks. But despite this, there were differences in surgical pathology and the treatment of the two groups of patients. The rate of preoperative stenting of the bile duct in jaundiced patients, the resectability of tumours and the number of palliative operations among patients from Greenland were different from the Danish patients. The lower preoperative stenting was, at least in the beginning of the study, due to the lack of ERCP expertise in Greenland. The lower resectability in patients from Greenland was primarily due to locally advanced tumours while metastases were more prevalent in Danish patients. As the diagnosis of locally advanced tumours is less clear from radiological imaging compared to the diagnosis of metastases, more patients with locally advanced tumours are offered surgical exploration.
The higher rate of palliative surgical procedures in patients from Greenland with non-resectable tumours was a result of the geographic conditions. A hepaticojejunostomy to relieve the bile duct from tumour obstruction was preferred to a biliary stent to avoid frequent long-distance travels for stent replacement. With the introduction of covered stents with long patency this procedure has changed.
A major problem in the present study was the retrieval of health data from Greenland, as the patient files were insufficiently kept. Therefore, we do not know time from the first symptoms until contact with the health system in Greenland and time from referral to the main hospital in Nuuk who conveys the contact with Copenhagen University Hospital. These data may explain differences in treatment and outcome but are not available, neither in other studies. However, a study of colorectal cancer found a median diagnostic interval of 55 days in patients from Nuuk and 95 days in patients outside Nuuk along the coastline [Citation27].
A database study of more than 200,000 Canadian Indigenous peoples including Inuit found an increased rate of postoperative adverse events and mortality after various surgical procedures compared to other Nationals [Citation28]. Despite small numbers, we did not find a difference between in-hospital mortality and the incidence of surgical complications in patients from Greenland and Denmark. This may be explained by centralisation of treatment because contrary to patients in the Canadian study all patients from Greenland were treated at the same hospital in a high-volume department for HPB surgery.
Adjuvant oncologic treatment could be administered in Greenland. Monotherapy with gemcitabine has fewer side effects and seven patients received this treatment at local hospitals. When combination chemotherapy became a common standard, this treatment was only possible in Nuuk. But this treatment also has more side-effects that limit its use.
Adjuvant oncologic treatment was generally accepted by the Greenlandic patients, but oncologic treatment in a palliative setting was only conducted in 25% of the patients compared to 52% of the Danish patients. This differs from a study of colorectal cancer, where palliative chemotherapy was equally frequent among Danish and Greenlandic patients [Citation29].
The OS after radical operation for PDAC differed significantly between the two groups. After the first postoperative year, there was an increasing deviation of the survival curves. After one, two and five years, survivors from Greenland amounted 54.4%, 23.4% and 0.0%, and from Denmark 74.6%, 48.6% and 23.4%. The results stand in contrast to the curative-intended treatment of colorectal cancer and lung cancer, where there is no difference in OS between patients from Greenland and the Nordic countries [Citation29,Citation30].
Greenlandic patients with non-resectable tumours also had a significantly lower remnant life compared to Danish patients. Here, the opt-out of palliative oncologic treatment may have influenced the numbers but also a lack of the best supportive care.
A Governmental report from 2013 recommended an improvement of palliative care in Greenland [Citation31], but the situation is complex as it also includes better support to relatives of patients with cancer [Citation32]. Another challenge is that an increasing number of the population is living alone [Citation33], which limits the social contact that is important in this group of patients.
Conclusion
Data show that patients from Greenland have the same access to treatment for pancreatic and periampullary tumours as the Danish population and tolerates operation well without a high incidence of complications. But the OS of PDAC after radical surgery as well as in a palliative setting is lower compared to Danish patients, and the geographical conditions put limits to follow-up and supportive care that are offered persons living in Denmark. Whether or not this can explain the difference in OS has to be investigated in studies with a larger population of patients with malignant diseases.
Limitations
The study of pancreatic surgery among Inuit in Greenland has limitations due to lack of patients’ data in the Greenlandic medical record system. A comparison between a Danish population operated at the same hospital during the same study period may at first seem to be a reasonable approach but implies both statistical difficulties due to the difference in numbers as well as a differences in culture including conditions of living. The results from Greenland are associated with a certain degree of uncertainty due to the small number of observations, thus making the Greenlandic rates vulnerable to even minor changes in the incidence of the chosen parameters.
Author contributions
CPH: Conceptualization, Methodology, Formal Analysis, Writing Original Draft, Writing Review and Editing; KA, JHS and SBA: Editing. All authors read and approved the final manuscript.
Disclosure statement
No potential conflict of interest was reported by the authors.
Data availability statement
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.
Additional information
Funding
References
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