Standardized diagnosis of gastrointestinal tumors: an update regarding the situation in Germany

Abstract

Purpose

To evaluate the current status of the diagnosis of gastrointestinal tumors in Germany by means of a survey of the oncological imaging working group of the German Radiological Society (DRG) with a focus on the CT protocols being used.

Materials and Method

Radiologists working in outpatient or inpatient care in Germany were invited. The survey was conducted between 10/2022 and 06/2023 using the SurveyMonkey web tool. Questions related to gastrointestinal cancer were asked with regard to the commonly used imaging modalities, body coverage, and contrast agent phases in CT as well as the use of oral or rectal contrast. The results of the survey were analyzed using descriptive statistics.

Results

Clear differences were identified regarding the acquired contrast phases in relation to the place of work – outpatient care, smaller hospitals, maximum care hospitals, or university hospitals. Variances were also recognized regarding oral and rectal contrast. Based on the results and international guidelines, proposals for CT protocols were derived.

Conclusion

CT protocols in Germany show a heterogeneous picture regarding acquired contrast phases, as well as oral and rectal contrast for the staging of gastrointestinal cancer. Clear recommendations in the respective guidelines would aid in quality assurance and comparability between different centers.

Key Points

• The examination protocols for the staging of gastrointestinal tumors are heterogeneous in Germany.

• The application of oral and rectal contrast is handled differently at the various radiological centers.

• Standardization of imaging should be targeted.

Citation Format

• Gerwing M, Ristow I, Afat S et al. Standardized diagnosis of gastrointestinal tumors: an update regarding the situation in Germany. Rofo 2025; 197: 657–668

Keywords

Esophageal cancer - Gastric cancer - Colorectal cancer - contrast agents - CT protocol

Introduction

The incidence and gender distribution of tumors of the gastrointestinal tract (GI tract) differ depending on the anatomical location, but they are fundamental diseases with an average age of onset of about 70 years and a predominance among men. The incidence is 2.2/100 000 women and 9/100 000 men for esophageal cancer, 6.7/100 000 women and 13.8/100 000 men for gastric cancer, and 30/100 000 women and 46/100 000 men for colorectal cancer (CRC) [1]. GI tract tumors are some of the most common tumor entities. Important risk factors include alcohol and tobacco consumption and obesity. There are other specific risk factors for individual entities, e.g., an infection of the gastric mucosa with helicobacter pylori or the Epstein-Barr virus in the case of gastric cancer, or a low-fiber diet in colorectal cancer [1].

The radiologist’s responsibilities include noninvasive imaging for initial clinical staging (cTNM) and subsequent follow-up during treatment. In the case of colorectal cancer, early detection with radiological imaging is possible. If colonoscopy cannot be completed due to technical difficulties like adhesions, CT colonography should be performed for early detection [2].

Some of the recommendations in the German and European guidelines and of the German Commission on Radiological Protection differ. [Table 1] provides an overview of the recommendations in the German S3 guidelines [3] [4] [5], the recommendations of the European Society for Medical Oncology (ESMO) [6] [7], and those of the German Commission on Radiological Protection [8].

Table 1 Overview over current recommendations regarding imaging of esophageal, gastric, and colorectal cancer – comparison of the current S3 guidelines from Germany and the recommendations of ESMO as well as the German Commission on Radiation Protection (IV: intravenous, CM: contrast medium, MRI: magnetic resonance imaging, (FDG)-PET/CT: fluorodeoxyglucose-positron emission tomography, NA: not applicable).

Tumor entity		Esophageal cancer			Gastric cancer			Colorectal cancer
Guidelines		S3 guidelines	ESMO	German Commission on Radiation Protection	S3 guidelines	ESMO	German Commission on Radiation Protection	S3 guidelines	ESMO	German Commission on Radiation Protection
CT protocol	Contrast phases	IV CM			IV CM
	Oral and rectal contrast	Negative oral CM			Oral water or CM
Primary staging	Locally limited	CT of the neck, chest, abdomen	FDG-PET/CT or CT of the chest/abdomen	Ultrasound of the neck/abdomen, CT of the chest/abdomen	Ultrasound of the neck/abdomen, CT of the chest/abdomen	CT of the neck/chest/abdomen, possibly FDG-PET/CT	Ultrasound of the abdomen, CT of the abdomen, possibly of the chest	Ultrasound of the abdomen, chest X-ray MRI (rectum), in the case of suspicion of distant metastases, CT of the abdomen and/or chest	CT of the chest/abdomen, MRI (rectum, liver)	Ultrasound of the abdomen, MRI (rectum, liver, before surgery)
	Advanced	FDG-PET/CT	FDG-PET/CT	NA	NA	NA	NA	CT of the chest/abdomen	Possibly PET/CT	Possibly CT of the abdomen or PET/CT
Follow-up		Possibly CT	NA	NA	NA	CT of the chest/abdomen	CT, possibly FDG-PET/CT	Ultrasound	CT or MRI	Ultrasound of the abdomen, possibly CT or MRI

A comparison of the recommendations clearly shows that even in the case of a fundamentally comparable approach there is no consensus and no standardized recommendation at least regarding the concrete implementation of staging and follow-up examinations. Consequently, particularly the contrast phases that are acquired and the use of oral or rectal contrast vary in clinical routine.

The goal of this survey was to determine the status quo in Germany and to compare it with the current recommendations.

Materials and Methods

Development, validation, and implementation of the survey

The CT protocols used for the staging of certain tumor entities to be included in the online survey were determined based on a preparatory discussion among all participating members of the Oncological Imaging Working Group. This article exclusively addresses tumors of the gastrointestinal tract. Other tumor entities included in the survey were hepatocellular carcinoma, pancreatic cancer, breast cancer, ovarian cancer, bronchial cancer, renal cell cancer, transitional cell cancer, malignant melanoma, and head and neck tumors. The data on these tumor entities will be analyzed and published separately.

The survey was generated using a SurveyMonkey web tool (SurveyMonkey, San Mateo, California, USA) provided by the German Radiological Society and was then validated internally by 15 test people with respect to understandability and technical feasibility.

Structure of the survey

The sequence of questions per tumor entity was based on a fixed and repeating scheme. The survey began with a question about the frequency of staging for the particular tumor entity at the participant’s own facility. This was followed by six questions about the use of various imaging modalities, the use of oral, rectal, and intravenous (IV) contrast agent, areas of the body covered by CT, and the dedicated CT protocol for the abdomen including the acquired contrast phases.

The individual questions regarding esophageal and gastric cancer as well as colorectal cancer are provided in [Table 2].

Table 2 Questions and possible answers to the questionnaire.

Question	Possible responses
Frequency of initial staging (extent of metastatic disease/not local staging) for colorectal cancer, esophageal cancer, and gastric cancer at the different places of work.	1: Never 2: Rarely 3: Sometimes 4: Often 5: Very often
The imaging modality regularly used for advanced local staging and for indicated imaging to determine the extent of metastatic disease is: (Note: multiple answers possible)	1: CT 2: cMRI 3: MRI (chest + abdomen) 4: Ultrasound 5: X-ray 6: Hybrid (PET/CT or PET/MR)
The CT protocol is performed with/without contrast agent	1: Exclusively without contrast 2: With IV contrast administration 3: Without contrast + with IV contrast administration
Is oral contrast used?	1: Yes, a negative contrast agent (water) 2: Yes, a positive contrast agent (containing iodine) 3: No
Additional question regarding the use of rectal contrast in the case of colorectal cancer: Is rectal contrast used?	1: Yes, a negative contrast agent (water) 2: Yes, a positive contrast agent (containing iodine) 3: No
The CT protocol covers the following regions of the body: (Note: multiple answers possible)	1: Head 2: Neck 3: Chest 4: Abdomen (including the pelvis)
The CT protocol of the abdomen includes the following contrast phases: (Note: multiple answers possible)	1: Unenhanced 2: Virtual-unenhanced 3: Arterial (15–20 s) 4: Portal venous (60 s) 5: Venous (80–120 s) 6: Urographic 7: Split bolus

After completion of all questions about the tumor entities, the following demographic information was gathered on a voluntary basis: Gender, age, professional experience, professional position (resident, specialist, or management), type of workplace (university hospital, maximum care hospital, small/medium-size hospital, medical practice or health care center, or other). The survey also recorded whether the workplace specializes in oncological imaging.

Distribution of the survey

The target group was defined as all radiologists working in outpatient and inpatient care. Invitations to participate in the anonymous survey were distributed by the following means: Newsletter of the German Radiological Society, newsletter of the Oncological Imaging Working Group of the German Radiological Society, newsletter of the Forum of Young Radiologists of the German Radiological Society. Additional means of communication included an ad in the journal Fortschr Röntgenstr and advertising on the digital career platform LinkedIn (LinkedIn Corporation, Dublin, Ireland). The online survey was able to be completed in the period between 10/2022 and 06/2023.

Statistics

Statistical analysis was performed with SAS, Version 9.4 (SAS Institute, Cary NC). Continuous variables are presented as mean and standard deviation. Box plots show the observed distributions. Categorical variables are provided as absolute and relative frequencies. Grouped and stacked bar charts were used to show the relative frequencies. The results are presented on a purely descriptive basis.

Results

Characteristics of the participants

The questions regarding esophageal and gastric cancer were answered by 100 participants, while 139 participants answered the questions about colorectal cancer. Insufficiently completed surveys were excluded resulting in a total of 97 and 99 online surveys, respectively, that could be used for the statistical analysis.

The characteristics of the participants differ only marginally between esophageal and gastric cancer ([Fig. 1]) and colorectal cancer ([Fig. 2]). In total, approximately half of participants were residents (52.6% and 52.5%, respectively) followed by specialists (32.0% and 32.3%, respectively), and radiologists with management positions (15.5% and 15.2%, respectively). The workplaces of the participants were also similar for the tumor entities, with just over one third of participants working in a small/medium-sized hospital (38.1% and 37.4%, respectively) or university hospital (35.1% and 34.3%, respectively), while only less than 15% of participants worked in a medical practice or health care center (12.4% and 14.1%, respectively) or a maximum care hospital (14.4% and 14.4%, respectively).

Fig. 1 Demographics of the participants of this survey regarding staging of esophageal and gastric cancer. Only those who reported performing initial staging at least “rarely” were included. N: answers not missing, n: number of answers, SD: standard deviation, (%): percentage based on N for category “overall” on n (overall) for all other categories.

Fig. 2 Demographics of the participants of this survey regarding staging of colorectal cancer. Only those who reported performing initial staging at least “rarely” were included. N: answers not missing, n: number of answers, SD: standard deviation, (%): percentage based on N for category “overall” on n (overall) for all other categories.

Examination frequency

In total, 13% of participants stated that they rarely perform initial staging in the case of esophageal and gastric cancer, while 33% perform staging sometimes, 38% often, and 16% very often (Supplementary Figure 1).

In the case of colorectal cancer, initial staging is performed rarely by 6.5% of survey participants, sometimes by 17.3%, often by 41.7%, and very often by 34.5% (Supplementary Figure 1). The two graphs in [Fig. 3] show the examination frequency at the different workplaces.

Fig. 3 Frequency of staging examinations in patients with esophageal and gastric or colorectal cancer at the different workplaces. n: number of answers in each category, percentages based on number of answers per workplace.

Regularly used imaging modalities

When staging esophageal and gastric cancer, CT is the most commonly used imaging modality (98.0% of cases), while MRI of the chest and abdomen or chest X-ray are used in 4.0% of cases and abdominal ultrasound in 8.1%. Additional MRI examination of the neurocranium (cMRI) is conducted by 3.0% of those surveyed. Hybrid imaging with 18F-FDG-PET/CT is performed by 14.1% of those surveyed (Supplementary Figure 2).

With respect to the areas of the body covered by CT examination, 100% of those surveyed examine the abdomen, 99.0% also examine the chest, 23.7% additionally examine the neck, and 1.0% examine the neurocranium (Supplementary Figure 3). The selected imaging modality for esophageal and gastric cancer varies in some cases depending on the workplace ([Fig. 4]).

Fig. 4 Regularly used diagnostic modality for patients with esophageal or gastric cancer, as well as colorectal cancer, categorized according to the workplace. N: number of participants, n: number of answers; percentages based on N. Multiple answers possible.

A comparison of the imaging modalities being used for the staging of colorectal cancer shows that CT is the clearly upfront with 96.2%. An MRI examination of the chest and abdomen is additionally performed by 16.5% of respondents and cMRI by 16.5%. 8.3% of those surveyed use abdominal ultrasound and 3.0% conduct chest X-ray examinations or hybrid imaging with 18F-FDG-PET/CT (Supplementary Figure 4).

Supplementary cMRI is regularly performed by 16.5% of those surveyed.

With respect to the areas of the body covered by CT examination, 97.0% of those surveyed report performing supplementary examination of the abdomen (100%) with simultaneous examination of the chest, 1.0% report additionally performing examination of the neck, and 2.0% additionally examine the neurocranium (Supplementary Figure 5). Which modalities are used in addition to CT for CRC staging differs slightly between the workplaces of the survey participants.

Contrast phases

The extent to which contrast phases in addition to the portal venous phase are regularly acquired differs between university hospitals and other small hospitals or medical practices. The arterial contrast phase apparently plays a secondary role in the staging of GI tumors at university hospitals compared to other places of work ([Fig. 5]). In contrast, university hospitals have started using virtual unenhanced phases instead of acquired unenhanced CT examinations on modern dual-energy CT (DECT) scanners.

Fig. 5 Scanned contrast phases when staging esophageal and gastric or colorectal cancer per workplace. n: number of answers; percentages based on answers per workplace.

Contrast agent administration

Those surveyed perform IV contrast agent administration in all cases for the staging of esophageal and gastric cancer and colorectal cancer. However, there are significant differences regarding the administration of oral (Supplementary Figure 6) and rectal (Supplementary Figure 7) contrast between the places of work. Thus, positive contrast agent is used significantly less frequently at university hospitals and maximum care hospitals (20.6% and 23.1%) compared to medical practices and small hospitals (58.3% and 48.6%). Larger hospitals were also more likely to not use rectal contrast in the case of colorectal cancer (69.7% and 50.0%) compared to medical practices and small hospitals (8.3% and 5.4%).

Discussion

The results of the survey show that all survey participants regularly perform staging examinations for both esophageal and gastric cancer (combined in the survey) as well as colorectal cancer. A comparison of workplaces shows that the majority of participants who indicated that they “rarely” perform staging examinations for both tumor entities work in a medical practice or health care center. However, some survey participants at these places of work indicated that they perform staging “often” or “very often”. Therefore, staging examinations could primarily be carried out by specialized practices or health care centers in the daily routine. Current literature from Germany regarding patients with colorectal cancer shows that these patients have a higher chance of survival when treated at a certified center [9]. However, whether radiological imaging plays a role here was not explicitly analyzed.

For the entities analyzed here, CT was specified as the imaging modality regularly used for staging in almost all cases. While MRI is additionally used to a limited extent for colorectal cancer, hybrid imaging with PET/CT or PET/MRI is used in some cases of gastric and esophageal cancer. X-ray and ultrasound both play a secondary role here. The participants’ responses regarding esophageal and gastric cancer coincide with the recommendations of the German S3 guidelines [3] [4] and the ESMO guidelines [6] [10]. It can be speculated that the cases involving hybrid imaging primarily relate to adenocarcinomas in the esophagogastric junction (AEG types 1–3). Both guidelines provide recommendations for this tumor entity based on the current data [11]. However, the studies on the role of PET/CT in the staging of gastric cancer also show positive results so that this imaging modality could play a greater role here in the future [12].

The results of the survey in relation to colorectal cancer show that the clinical routine is ahead of the currently valid S3 guidelines (from 2019), which recommend a preoperative ultrasound examination of the abdomen and conventional X-ray of the chest in two planes [5]. CT examination of the chest and/or abdomen (depending on the suspected location of the metastasis) is only recommended here in the case of an advanced local finding or suspicion of a distant metastasis. Local staging of rectal cancer using MRI was not specifically addressed in this survey. However, its relevance has already been discussed in detail in Fortschr Röntgenstr. In an interdisciplinary recommendation, Attenberger et al. concluded that this is a valuable evaluation method for the further treatment stratification of rectal cancer and therefore standardized image quality is essential [13]. In contrast, the ESMO guidelines recommend contrast-enhanced CT of the chest and abdomen to rule out distant metastases, MRI of the rectum to determine the local extent, and optionally MRI of the liver in the case of suspicion of liver metastases [7]. However, 18F-FDG-PET/CT, which is recommended in the case of elevated tumor markers without detectable metastases or to define the extent of metastatic disease in the case of potentially resectable metastases seems to barely be used in the clinical routine [7]. More recent studies show that PET/MRI combined with CT of the chest provides optimal initial staging and could be advisable particularly in high-risk tumors [14] [15].

While all participants administer IV contrast agent when staging gastric and esophageal cancer, there is a lack of agreement regarding the acquired phase. An arterial phase is acquired in more than 60% of cases at workplaces outside university hospitals, while this is only performed in 32% of cases at university hospitals. Studies on this topic show that two-phase CT with arterial and venous contrast phases can increase the accuracy of T-staging. However, the diagnostic significance of CT is generally limited with respect to T-staging [11] [16]. The acquisition of an additional arterial phase for the detection of hepatic metastases in esophageal and gastric cancer, similar to colorectal tumors, is a topic of controversy in the literature.

The majority of participants also used IV contrast agent for the staging of colorectal cancer. There are only small differences between workplaces. While in general scanning is performed in the portal venous phase in the majority of cases, examinations in the arterial phase are performed in more than 50% of cases at the various workplaces with the exception of university hospitals where they are only performed in 24% of cases. A concrete recommendation regarding the CT imaging protocol is not provided in the guidelines. However, IV contrast administration is assumed. Some studies recommend performing biphasic CT, with the arterial phase scan including the liver for optimized detection of hepatic metastases [17] [18]. A further advantage is greater diagnostic reliability due to the additional arterial phase in order to be able to reliably differentiate benign hepatic findings from metastases [19]. Other studies did not find any advantage with respect to the acquisition of an additional arterial phase for detecting liver metastases [20] [21]. There is a lack of consensus in the literature regarding the additional acquisition of the arterial phase when screening for hepatic metastases. Since metastases of gastrointestinal tumors are usually hypovascularized, this is typically not necessary in the clinical routine [22]. International recommendations also agree with this and only recommend the acquisition of a venous contrast phase [23].

While approximately one fourth of participants did not use oral contrast for the staging of gastric and esophageal cancer, oral contrast is used in the majority of cases, with negative contrast being used in half of cases and positive in the other half. There are also differences here depending on the workplace: positive or negative oral contrast is used in the majority of examinations in medical practices and health care centers or small/medium hospitals, while oral contrast with water or no contrast is used at university hospitals and maximum care hospitals. This is not specified in the corresponding guidelines. Only the basic administration of oral contrast is recommended. The use of oral contrast has been increasingly eliminated in Germany in recent years. In the last survey on this topic in 2016, 62% of participants still used oral contrast [24].

There is a similar divergence regarding the administration of oral contrast for the staging of colorectal cancer. A significant difference in relation to workplace is also seen here. While oral contrast is not used in the majority of cases (70%) at university hospitals and in 50% of cases at maximum care hospitals, survey participants working at medical practices/health care centers and small/medium-size hospitals prefer the administration of positive, iodine-containing contrast agent in 50% and 60% of cases, respectively.

The indications for the administration of positive oral contrast agent are the subject of debate in the literature. In a review article from 2020 on current indications, contraindications, and controversial indications for oral contrast administration, it was concluded that the administration of oral, water-soluble, non-ionic contrast agents is generally indicated for oncological examinations [25]. A comparison between abdominal CT examinations using negative and positive contrast agents showed comparable diagnostic performance. Negative oral contrast was sufficient in most cases [26]. With respect to distension of the bowel and the ability to evaluate contrast enhancement and the bowel wall, mannitol was shown to provide optimal contrast compared to water and positive contrast agent in one study. However, this is currently primarily established for diagnosing chronic inflammatory bowel diseases [27]. The need for optimization to ensure clear, data-based protocol recommendations has already been identified, particularly with regard to oral contrast administration. Such clear recommendations would standardize protocols resulting in improved comparability between centers. However, the current survey results show that since the last survey in this regard by the Abdominal and Gastrointestinal Imaging Working Group in 2016 there has not really been an increase in standardization in Germany and concrete definitions of the recommended CT imaging protocols in the guidelines are needed [24].

There is also a lack of agreement with respect to rectal contrast administration for the staging of colorectal cancer. While 10% of participants use negative contrast agent, 25% administer an iodine-based contrast agent and 65% don’t use any rectal contrast at all. Also in this case, it is primarily university hospitals and maximum care hospitals that dispense with the use of rectal contrast, while positive contrast is used at 25% of medical practices/health care centers and in 38% of cases at small and medium-size hospitals. Although studies show improved ability to evaluate tumors in some cases, general use is not recommended [28]. This is in light of the fact that a dedicated MRI examination of the rectum is typically additionally performed at a certified colon cancer center for the evaluation of local tumor extent. Compared to the status in 2016, rectal contrast is increasingly no longer used: At that time almost 60% of participants stated that they use rectal contrast administration [24]. The guidelines do not include any recommendations regarding the administration of oral or rectal contrast agent for the staging of colorectal cancer on CT. Therefore, clear recommendations would also be desirable here.

Protocol recommendation

Based on the current data, contrast-enhanced CT of the chest and abdomen should be regularly performed for the staging of gastrointestinal tumors, with a CT scan in the portal-venous phase (approx. 60–80 s post-injection) typically being sufficient. Administration of negative oral contrast agent causes distension of the gastrointestinal tract and should be performed as preparation for the planned examination whenever possible ([Table 3]). Local staging via MRI in the case of rectal cancer is obligatory and should be performed regardless of CT imaging performed to determine the extent of metastatic disease.

Table 3 Recommendations for the staging of tumor entities with CT.

Tumor entity	Indication	Body region	Slice thickness	IV CM	Oral CM	Rectal CM
p. i. = post injection
Esophageal cancer	Staging	Neck Chest Abdomen	Max. 5 mm, preferably 2–3 mm	Venous Abdomen portal venous (60–80 s p.i.)	Water	No
	Follow-up	Chest Abdomen	Max. 5 mm, preferably 2–3 mm	Venous Abdomen portal venous (60–80 s p.i.)	Water	No
Gastric cancer	Staging	Chest Abdomen	Max. 5 mm, preferably 2–3 mm	Venous Abdomen portal venous (60–80 s p.i.)	Water	No
	Follow-up	Chest Abdomen	Max. 5 mm, preferably 2–3 mm	Venous Abdomen portal venous (60–80 s p.i.)	Water	No
Colorectal cancer	Staging	Chest Abdomen	Max. 5 mm, preferably 2–3 mm	Venous Abdomen portal venous (60–80 s p.i.)	Water	No
	Follow-up	Chest Abdomen	Max. 5 mm, preferably 2–3 mm	Venous Abdomen portal venous (60–80 s p.i.)	Water	No

Conclusion

All survey participants report that they regularly perform staging examinations in esophageal and gastric cancer and in colorectal cancer. However, in relation to the CT protocols being used, there are some significant differences between the various workplaces with respect to both the scanned contrast phases and the administration of oral or rectal contrast. Guidelines with clearly formulated protocol recommendations would allow uniformity and standardization for optimized comparability of examinations, radiation protection for patients, and for multi-center research. Therefore, such recommendations should be targeted in the future.

Clinical relevance of the study

• This study evaluates the status quo of diagnostic imaging currently performed for the staging of gastrointestinal tumors in Germany.

• The study shows that there is significant heterogeneity in Germany, particularly in relation to oral/rectal contrast administration.

• Standardization is necessary and should be targeted in the future.

Conflict of Interest

The authors declare that they have no conflict of interest.

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Publikationsverlauf

Eingereicht: 22. Mai 2024

Angenommen nach Revision: 16. Juli 2024

Artikel online veröffentlicht:
16. Oktober 2024