Current state of surgical treatment of gastric cancer in Austria—results of a multicentric retrospective online survey

Gastric cancer represents 4.9% of the worldwide cancer burden and has the fifth highest incidence rate of all cancers according to global cancer statistics (Globocan) [1]. In Austria, the incidence of gastric cancer is the 11th highest of all cancer entities. However, its incidence has been decreasing worldwide for decades, and this trend can also be observed in Austria. Despite the decrease in incidence in total, overall survival remains poor [2].

Gastric cancer rates fifth in cancer-related mortality, representing 6.8% of the total cancer deaths worldwide [1].

The EUROCARE project, a population-based dataset in Europe, has monitored cancer survival since 1989. Over time, survival has increased from 23.3% in 1999–2001 up to 25.1% in the 2005–2007 period Europe-wide. In Austria, the 5‑year survival rate was 30.7% in 1999–2001 and 33.6% in 2005–2007, showing an absolute difference of 2.9% (p = 0.009) [3].

Late diagnosis in advanced tumor stages contributes to this low 5‑year survival rate. Therefore, endeavors are being made to promote the early diagnosis of gastric cancer and to improve treatment modalities.

Central and Eastern Europe are high-incidence countries, following East Asia. In the white population, the presence of Helicobacter pylori infection was identified as the most relevant risk factor. It is held responsible for about 75% of noncardia adenocarcinoma by introducing a precancerous process. Further risk factors are a history of smoking, current smoking, diet, and genetic factors. At present, no reliable biomarkers are available for early detection of gastric cancer. Population-wide screening is considered unlikely to improve outcomes in gastric cancer, but screening in at-risk patients, e.g., in current smokers, is discussed, and certain countries like Japan perform screening programs [4, 5]. Enormous medical advances have been made in the diagnosis and treatment of gastric cancer in recent decades. Improvements and innovations in endoscopy have changed the diagnostic pathway.

In Austria, the last published evaluation of the standard of care of gastric cancer is from 1997. Rabl et al. aimed to evaluate and document diagnostics, surgical therapy, and postoperative outcomes of 1994. A questionnaire containing 26 queries was created and sent to 54 surgical centers which were also members of the Austrian Society of Surgical Oncology (ACO-ASSO). The authors concluded that surgical treatment of gastric cancer in Austria met the international standards of surgical oncology [6].

Since diagnostic and therapeutic modalities have changed significantly since 1994, there is a need for a renewed analysis of gastric cancer treatment in Austria to generate knowledge of current modalities and possible shortcomings.

The main objective of this study was to document the current surgical standard of care of gastric cancer in Austria. Furthermore, we wanted to detect changes in diagnostics and treatment during the past three decades and compare the collected data with epidemiological data.

In order to assess the clinical practice all over Austria, this study was executed in consultation with the Austrian Society for Surgery (ÖGCH) and the Austrian Society of Surgical Oncology (ACO-ASSO). Contact information of all national surgical departments was obtained by the ÖGCH. Data collection was retrospective and anonymous; the observation period was defined from January 2022 to December 2022.

We created an online survey using the online platform SurveyMonkey (SurveyMonkey Inc., San Mateo, CA, USA; www.surveymonkey.de). The survey was generated based on the questionnaire of Rabl et al. [6]. Questions or answers that were no longer up to date due to changes in diagnostic or treatment patterns were adjusted. The survey from 1994 contained 26 questions, of which 22 were incorporated without adjustments [6]. Adjustments to the questionnaire were made by K.O.O. and W.E., and the questionnaire was then reviewed by E.K. Final approval was given by E.K. as ACO-ASSO president and by T. A. as president of the ÖGCH in 2023.

In Table 1, the 32 questions and their answer options are displayed.

The SurveyMonkey platform provides a link to the survey which can be passed on as preferred. In order to address the departments directly, we sent an invitation in name of the ÖGCH via email to all 133 departments of general and visceral surgery in Austria. The invitation explained the aim of our study and its conduction. Via email, a link with direct access to the questionnaire was provided. The first email invitation was sent in February 2023, and the questionnaire was accessible until January 2024. Additionally, the ÖGCH sent an invitation via email to all his members and mentioned the running survey in their newsletter. Throughout the ongoing poll, we emitted personally addressed reminders via email to several heads of clinics. This was carried out twice to increase response rate.

All surgical departments could be contacted and received an invitation via email to participate in our survey; 18 of the 133 departments contacted (13.5%) took part. The results are displayed in Table 2 for the individual questions.

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Our study highlights numerous changes in the surgical treatment of gastric cancer in Austria over the past three decades. The survey observed significant advancements driven by improvements in diagnostic techniques, surgical methods, and a multidisciplinary approach to cancer care. Due to these changes, extended resections are rarely necessary, and postoperative mortality is significantly reduced. Furthermore, efforts in organ preservation are seen through the changing proportion of proximal gastrectomies in comparison to total and subtotal resections.

Major improvements have been achieved in diagnostic techniques. In 1994, only 81.4% of patients underwent preoperative esophagogastroduodenoscopy. A contrast-enhanced X‑ray was performed in 18.6%, and only 25% of patients underwent both examinations. Nowadays, an esophagogastroduodenoscopy is gold standard in diagnostics, supplemented by EUS which was introduced in 1980 and is recommended by S3 guidelines in every curative treatment approach [2]. However, two clinics of our cohort lack this standard and do not perform EUS. During evaluation for endoscopic resection, EUS is considered mandatory [9]. It can be assumed that there is a high staging standard in the participating departments, but we do not know what the quality looks like in the departments that did not take part in the survey.

The majority of departments follow the S3 recommendation, as they perform PET-CT subject to tumor stage. Furthermore, exploratory laparoscopy improves staging in advanced stages of gastric cancer (≥ cT3) and is therefore recommended prior to neoadjuvant therapy. Accordingly, 72.2% of the departments perform an exploratory laparoscopy depending on tumor stage.

The TNM and Laurén classifications are prevalent and used in all clinics. However, the WHO and TCGA classifications are noticeably underrepresented, despite both of these classifications being recommended by S3 guidelines. The TCGA classification was included in the guidelines in 2018. In summary, the survey observed that real-life practice in diagnostics is only partially in accordance with the current S3 guideline. This fact should be discussed with the country’s pathology institutes.

There are endeavors in promoting organ-preserving treatment strategies. Endoscopic resection techniques aim to resect precancerous lesions and early-stage gastric cancer while preserving the organ. These less-invasive procedures contribute to better quality of life in patients. In advanced disease, endoscopic palliative procedures provide quality of life by treating symptoms like tumor bleeding and stenosis, and they enable palliative surgical interventions to be avoided [10]. According to Statistics Austria, endoscopic stent placement is an increasing intervention in gastric cancer patients, and 38 stents were placed in 2022. It is striking that in all 18 departments, endoscopies are performed by surgeons. In 16 departments, endoscopies are also performed by gastroenterologists.

Furthermore, we see a significant increase in proximal gastrectomies as an organ-preserving surgical technique over time, whereas total gastrectomy experienced a decline. Proximal gastrectomy shows better quality of life while maintaining nutritional requirements [11, 12].

A single institution reported 43 exploratory laparotomies. We believe that this must have been an error when filling out the questionnaire. They rather performed a relevant number of diagnostic laparoscopies, and, therefore, the significant increase in comparison to 1994 (21.0% vs. 5.0%) is considered to be biased.

One of the most significant advancements is the adoption of minimally invasive surgical techniques, particularly laparoscopic and robot-assisted surgeries. In various studies, the feasibility of minimally invasive gastrectomy has been shown. Both early and locally advanced tumors can be treated safely, while there is non-inferiority of oncological features such as lymph node dissection and resection margins. Postoperative recovery and morbidity showed improvements compared to open surgery for minimally invasive techniques when performed by experienced surgeons [13‐15].

However, minimally invasive surgery in gastric cancer is still to be implemented routinely in Austria. Only 44.4% of departments perform minimally invasive procedures. Robot-assisted gastrectomies are carried out even more restrictedly: they take place in only three departments (16.6%). The numbers of minimally invasive surgeries in gastric cancer are reasonable in the survey, but similar to the case with EUS, it can be assumed that less minimally invasive surgery is carried out in the departments that did not take part in the survey.

The number of extended resections decreased over time. Improvements in neoadjuvant cancer treatment can result in downstaging of the tumor, which leads to less radical resections and fewer multivisceral resections. Rabl et al. reported a high number of splenectomies in 1994. In proximal gastric cancer, the metastasis rate of splenic hilar lymph nodes, lymph node station 10, ranges in the literature from 8% to 27.9% [16]. Therefore, splenectomy was routinely performed for complete lymph node dissection, also including distal pancreatectomy. Over time, surgical techniques developed, and organ-preserving lymph node dissection was established. It was especially aimed at preservation of the pancreas in order to reduce postoperative morbidity and mortality. Nowadays, D2 lymphadenectomy is fulfilled with a total number of 25 resected lymph nodes [2, 17]. In the case of suspicious splenic hilar lymph nodes, lymphadenectomy, and—only if necessary—splenectomy while preserving the pancreas is recommended.

There was no significant change in the number of postoperative complications observed in 1994 vs. 2022. However, there were numerous improvements realized in perioperative care. A multidisciplinary treatment approach is universal, and patients receive personalized and risk-adapted treatment strategies combining surgery, chemotherapy, and radiation therapy as needed [18, 19]. Also, postoperative care was further developed into a multidisciplinary task, as enhanced recovery after surgery (ERAS) protocols have been widely implemented to improve recovery times and outcomes for gastric cancer surgery patients. In the case of postoperative complications, the management of complex cases is carried out by radiologists, gastroenterologists, and surgeons on a multidisciplinary basis. In combination with advanced surgical standards, all these factors contribute to the significantly lower mortality rate of 0.4% vs. 8.4% in 1994 (p < 0.00001).

The main limitation of our study is the low response rate and its retrospective character.

In comparison to 1994, gathering contact information and communication is nowadays much faster. Rabl et al. only reached members of the ACO-ASSO organization by postal mail, reaching 54 surgical departments, whereas we obtained the contact information of all 133 departments in Austria easily. However, the response rate of the survey in 1994 via postal mail was higher than the response rate in our online survey (46% vs. 13.5%, respectively). Response rates are usually lower in online surveys. Furthermore, response rates are declining for all survey methods, possibly because of rising numbers of questionnaires in total. The limited number of replies we received carries a possible nonresponse bias [20].

Despite the low response rate, we document a relevant number of the performed surgical interventions when compared to the total numbers collected by Statistics Austria. With a response rate of 13.5%, we recorded 36.1% of all curative resections and 28.5% of diagnostic procedures. The majority of gastroenterostomies, 60.6%, are performed in departments that took part in the survey. From our point of view, there are two main reasons contributing to departments not taking part in the survey. First, in-house documentation is deficient and carrying out an analysis is time consuming and difficult. Without a proper and standardized documentation system, data analysis and quality management are impaired. We conclude that there is an urgent need for standardized documentation of preoperative diagnostic and postoperative outcomes. In this regard, health policy is called upon to act.

Second, case numbers are quite low, and there is no interest in reporting. Similar to the result in 1994, where all 25 departments performed gastrectomies themselves, all departments that took part in our survey carry out gastrectomies. Under the assumption that all of the other 115 surgical departments also perform gastrectomies, only 2.2 gastrectomies are carried out at each hospital per year. As we can see in our survey, only a couple of surgeons perform more than 10 gastrectomies per year. In the participating departments, 6 surgeons perform more than 10 gastrectomies per year.

There is an ongoing discussion regarding the minimum quantity of oncological resections performed per year and, in some countries, also per surgeon. In Austria, there are no regulations regarding oncological surgery of the stomach. Due to the high number of hospitals and the intention to provide easily accessible medical care, there are only a few operations regulated, and cut-off numbers are low in comparison to other European countries. Other countries, e.g., the Netherlands, assessed minimum numbers in oncological gastric surgery. National reports showed lower mortality, reduced length of hospital stay, and lower costs following the introduction of minimum numbers [21].

However, there are other optional possibilities to guarantee quality of care, e.g., receiving certification as an oncological center. Interdisciplinary patient care and patient-centered treatment are highly relevant. Oncology has developed into a multiprofessional field.

One main requirement is the availability of a multiprofessional tumor board. In 1994, 10 departments referred their patients to an oncologist, and 15 departments performed the oncological treatment, if necessary, themselves. In 2022, as our study showed, every patient case was discussed in a tumor board, and all surgical departments refer patients to the department of oncology. This is consistent with S3 guidelines.

As research and technology continue to advance, it is expected that surgical treatment for gastric cancer will continue to improve, thereby further benefiting patients.

The majority of participating departments met international standards for gastric surgical oncology. However, there is still an urgent need for improvements in the diagnostic pathway. Regarding histopathological findings, the WHO classification must be incorporated. Also, EUS must be available and carried out nationwide. The average number of procedures per department is too low to ensure adequate quality. Since the incidence decreases over time, it is to be feared that not all surgical departments will be able to meet international requirements. Uniform nationwide centralized documentation of procedures and complications as well as introduction of minimum case numbers of interventions should be considered in order to ensure cutting-edge oncological medicine in the future.