# Surgical patterns of care of pancreatic cancer. A French population-based study

Guillaume Goebel, Valérie Jooste, Florence Molinié, Pascale Grosclaude, Anne-sophie Woronoff, Arnaud Alvès, Véronique Bouvier, Jean-Baptiste Nousbaum, Sandrine Plouvier, Leïla Bengrine Lefevre, et al.

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## To cite this version:

Guillaume Goebel, Valérie Jooste, Florence Molinié, Pascale Grosclaude, Anne-sophie Woronoff, et al. Surgical patterns of care of pancreatic cancer. A French population-based study. EJSO - European Journal of Surgical Oncology, 2025, 51 (8), pp.108748. 10.1016/j.ejso.2024.108748. hal-04951172

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# Surgical patterns of care of pancreatic cancer. A French population-based study

Guillaume Goebel<sup>a,1</sup>, Valérie Jooste<sup>b,c,d,e,f,g,h</sup>, Florence Molinie<sup>c,g,h</sup>, Pascale Grosclaude<sup>c,h,i</sup>, Anne-Sophie Woronoff<sup>c,j,k</sup>, Arnaud Alves<sup>c,l,m</sup>, Véronique Bouvier<sup>c,l,m</sup>, Jean-Baptiste Nousbaum<sup>c,n,o,p</sup>, Sandrine Plouvier<sup>c,q</sup>, Leila Bengrine-Lefevre<sup>r</sup>, Thomas Rabel<sup>a,1</sup>, Anne-Marie Bouvier<sup>b,c,d,e,f,g</sup>, FRANCIM Network

## ABSTRACT

**Introduction:** Surgical resection is the standard recommended treatment in localized pancreatic cancer. The benefit of neoadjuvant chemotherapy is still debated. The aim of this population-based study was to describe the pancreatic cancer surgical management.

**Material and methods:** An observational real-world study from the French Network of Cancer Registries sampled 638 pancreatic adenocarcinomas diagnosed in 2019. Characteristics of patients, tumours and recommended and administered treatments were collected. Operability of the patients and resectability of the tumours were described. A multivariate logistic regression was used to identify factors associated with the probability of having surgical resection.

**Results:** Among the 263 (41 %) patients with M0 pancreatic adenocarcinomas, 202 patients (77 %) were considered operable and 157 (60 %) also had a tumour considered resectable. Upfront resection was recommended for 68 % and resection after neoadjuvant chemotherapy for 32 % of these patients. Among operable patients with resectable tumour, 36 % underwent upfront R0 resection, and 15 % achieved R0 resection following neoadjuvant chemotherapy. Eventually, among M0 pancreatic adenocarcinomas, age over 80 years (OR≥80 years vs < 65 years: 0.16 [0.06–0.39], p < 0.001) and WHO performance status over 0 (OR1.2 vs 0: 0.43 [0.24–0.79], p = 0.013) decreased the odds of having resection. R0 surgical resection was achieved in 61 % of patients selected for upfront surgical recommendation, and 29 % of those selected for a prior neoadjuvant chemotherapy.

**Conclusion:** In a non-selected population, one-third of patients with localized pancreatic cancer had a complete R0 surgical resection. Neoadjuvant chemotherapy did not achieve a resection rate similar to that of patients selected for upfront surgical indication.

<footnote><sup>a</sup> Surgical Oncology Department, Centre Georges François Leclerc, Dijon, France</footnote>

<footnote><sup>b</sup> Digestive Cancer Registry of Burgundy, Dijon, France</footnote>

<footnote><sup>c</sup> French Network of Cancer Registries (FRANCIM), France</footnote>

<footnote><sup>d</sup> Dijon University Hospital, Dijon, France</footnote>

<footnote><sup>e</sup> INSERM UMR 1231, EPICAD, Dijon, France</footnote>

<footnote><sup>f</sup> Université de Bourgogne, Dijon, France</footnote>

<footnote><sup>g</sup> Loire-Atlantique/Vendée Cancer Registry, SIRIC-ILIAD, Nantes, France</footnote>

<footnote><sup>h</sup> CERPOP, UMR 1295, Université de Toulouse III, Toulouse, France</footnote>

<footnote><sup>i</sup> Tarn Cancers Registry, Claudius Regaud Institute, Toulouse University Cancer Institute (IUCT- O), Toulouse, France</footnote>

<footnote><sup>j</sup> Doubs Cancer Registry, Besançon University Hospital, Besançon, France</footnote>

<footnote><sup>k</sup> Research Unit EA3181, Franche-Comté University, Besançon, France</footnote>

<footnote><sup>l</sup> Calvados Digestive Cancer Registry, University Hospital Centre, Caen, France</footnote>

<footnote><sup>m</sup> ANTICIPE U1086 INSERM-UCN, Centre François Baclesse, Normandie UNICAEN University, Caen, France</footnote>

<footnote><sup>n</sup> Registre des Cancers Digestifs Du Finistère, 29609, Brest, France</footnote>

<footnote><sup>o</sup> EA7479 SPURBO, Université de Bretagne Occidentale, 29200, Brest, France</footnote>

<footnote><sup>p</sup> CHRU Brest, Service D'Hépato-gastro-entérologie, 29200, Brest, France</footnote>

<footnote><sup>q</sup> General Cancer Registry of Lille Area, C2RC, Lille, France</footnote>

<footnote><sup>r</sup> Medical Oncology Department, UCOG Bourgogne, Centre Georges François Leclerc, Dijon, France</footnote>

<footnote>* Corresponding author. Digestive cancer registry of Burgundy, INSERM CTM, UMR 1231, BP 87900, 21079, Dijon, Cedex, France.
E-mail address: anne-marie.bouvier@u-bourgogne.fr (A.-M. Bouvier).</footnote>

<footnote n="1">¹ Equal contribution.</footnote>
# 1. Introduction

Pancreatic cancer is the 7th most frequent cancer and the 4th leading cause of death by cancer in Europe [1]. In France, pancreatic cancer incidence increased by 2,7 % and 3,8 % per year for men and women respectively between 1990 and 2018 according to the latest estimates from the French Network of Cancer Registries (FRANCIM) [2,3]. In 2018, the number of new cases was estimated at about 14,000 and the number of deaths at more than 11,000. The 5-year net survival was less than 10 % [4]. Pancreatic cancer is one of the priorities in the fight against cancer.

Pancreatic ductal adenocarcinoma (PDAC) is the most frequent histological type. Prognosis is mainly determined by the patient's factors (WHO performance status, nutritional status, comorbidities), by metastatic spread and tumour resectability [5]. Pancreatic cancer surgery is major and complex and should be practiced by trained surgeons in expert center [6]. To date, surgical resection is the only curative treatment despite a heavy post-operative morbidity varying from 30 to 40 % and a 30-day mortality from 1 to 5 % [7-9]. Indication of surgical resection should be guided by the National Comprehensive Cancer Network (NCCN) resectability criteria of the tumour. Based on imaging, PDAC can be staged resectable, borderline-resectable, and locally advanced forms [10]. Surgical resection can thus only be considered after a strict assessment of the resectability criteria, and of the potential surgical contraindications (distant metastasis, patient's comorbidities ...) at diagnosis. In the literature, after a well-conducted pre-therapeutic evaluation, 15-20 % of patients seem candidates to a surgical resection [11]. For metastatic PDAC, the recommended treatment is chemotherapy. For locally advanced PDAC, chemotherapy is also recommended with reassessment of potential resectability in case of good response. For borderline-resectable PDAC, neoadjuvant chemotherapy followed by resection based on patient's overall condition and tumour characteristics is often preferred to upfront resection. For resectable PDAC, upfront surgery is recommended, followed by chemotherapy. The interest of a neoadjuvant therapy, despite wide administration, to borderline-resectable and resectable PDAC still remains debated [12-14].

The real-life surgical management of patients with PDAC is not well known. Data provided by specialized centers or clinical trials cannot be used to describe patterns of care because of unavoidable selection bias. Population-based studies that include all cases diagnosed in a well-defined area are the best way to picture the management of cancer in the real world. Such studies are rare because they require accurate and detailed data collection through dedicated surveys on representative samples of cases.

Thus, this study aimed to describe the PDAC surgical management in a population-based cohort study from the French Network of Cancer Registries.

# 2. Material and methods

## 2.1. Study population

The French network of population-based cancer registries (FRANCIM), together with the Biostatistics Department of the Hospices Civils de Lyon, the French Institute for Public Health Surveillance, and the French National Cancer Institute manage a common database. Quality checks are carried out in accordance with the International Agency for Research on Cancer guidelines. The quality and exhaustiveness of these registries are certified every five years by an audit of the National Evaluation Committee. Each cancer registry involved in this study has received the approval of the French regulatory authorities for the collection and analysis of medical data: the Comité Consultatif sur le Traitement de l'Information en matière de Recherche dans le Domaine de la Santé (ethics approval) and the Commission Nationale Informationique et Libertés (legal framework and data protection). In agreement

with French legislation, there was no requirement for written informed consent for this observational non-interventional study.

Among all pancreatic ductal adenocarcinoma (code C25 in accordance with the International Classification of Diseases in Oncology, third revision) diagnosed in 2019 in residents of 16 French administrative areas covered by a registry ('département', Calvados, Côte d'Or, Doubs, Finistère, Gironde, Hérault, Isère, Lille, Manche, Bas-Rhin, Haut-Rhin, Saône et Loire, Haute-Vienne, Poitou-Charente, Somme, Tarn) which represent 18 % of the French population, a random sample of 40 cases per 'département' was constituted by considering days and months of birth. This process makes it possible to complete the sample with rare, but inherent to any population-based registry, cases that are registered late. Finally, 638 cases of PDAC were considered for analysis.

## 2.2. Data collection and study design

Through a dedicated survey in all concerned healthcare structures, information about age, sex, clinical morphological examination, geriatric clinical evaluation, metastatic status at diagnosis, treatment modalities (surgery and chemotherapy), and healthcare facilities at diagnosis (university hospital and cancer therapy center, general public hospital or private hospital) was collected. Age was categorized into "<65 years", "65-79 years" and "≥80 years" groups for all analyses and into "70-74 years", "75-79 years" and "≥80 years" for the description of geriatric evaluation description. The ECOG/WHO performance status at diagnosis (before any treatment) was categorized from best to worst ability into the following groups: "0", "1-2", and "3-4". Based on the content and conclusions of patients' medical and surgical records, the 'operability' of patients (assessed according to the presence or not of general contraindications to surgery), and the 'resectability' of the tumour (assessed according to the NCCN guidelines from the Computed Tomography scan (CT), the Magnetic Resonance Imaging (MRI), or the endoscopic UltraSound report) were registered. Metastatic status M0 or M1 was collected (unknown for 11 cases). Borderline-resectable and resectable M0 PDAC were not separated in the data collection and were designed as Localized pancreatic cancers. In the French clinical care process, patients' medical records are usually presented to a multidisciplinary team meeting to design the treatment plan. Information on the planned treatment (surgical resection, chemotherapy, palliative care ...) has been collected. Regarding the surgical data, the quality of resection was evaluated as either complete resection R0 or not. Data of attempts at resection with laparotomy alone without resection possibility were also collected. The Flow chart of the study design is presented in Fig. 1. The study population consisted of 627 PDAC patients with known metastatic status.

## 2.3. Statistical analysis

The association between categorical data was analyzed using the chi-square test (or Fisher's exact test if needed). Distributions of continuous variables were described as means. A non-conditional multivariate logistic regression was used to identify factors independently associated with the probability of having surgical resection using adjusted odds ratios (OR) and their 95 % confidence interval (CI). The significance of the covariates was tested by the likelihood ratio test. The analyses were performed using STATA software, version 18 (STATA Corp., College Station, Texas, USA).

# 3. Results

Table 1 shows patients' characteristics according to their metastatic status. Overall, 263 (42 %) patients had a localized non-metastatic (M0) pancreatic cancer. Sex and age were not associated with metastatic status. Patients' healthcare facility at diagnosis was associated with metastatic status (p = 0.040). Patients diagnosed in public healthcare facilities (university or not) had more distant metastasis (61 %) than
<figure><img src="image_4.png" /><figcaption>Fig. 1. Study population and patterns of care of pancreatic adenocarcinoma patients.</figcaption></figure>
<table><caption>**Table 1**

Description of the pancreatic adenocarcinoma population according to metastatic status at diagnosis.</caption><thead><tr><th></th><th>N</th><th>M0<br>N (%)</th><th>M1<br>N (%)</th><th>p<sup>a</sup></th></tr></thead><tbody><tr><td>Overall</td><td>627</td><td>263 (42)</td><td>364 (58)</td><td></td></tr><tr><td>Sex</td><td></td><td></td><td></td><td></td></tr><tr><td>Men</td><td>336</td><td>132 (39)</td><td>204 (61)</td><td></td></tr><tr><td>Women</td><td>291</td><td>131 (45)</td><td>160 (55)</td><td>0.147</td></tr><tr><td>Age</td><td></td><td></td><td></td><td></td></tr><tr><td>&lt;65 years</td><td>147</td><td>61 (42)</td><td>86 (58)</td><td></td></tr><tr><td>65-79 years</td><td>301</td><td>123 (41)</td><td>178 (59)</td><td></td></tr><tr><td>≥80 years</td><td>179</td><td>79 (44)</td><td>100 (56)</td><td>0.775</td></tr><tr><td>WHO Performance Status</td><td></td><td></td><td></td><td></td></tr><tr><td>0</td><td>181</td><td>103 (57)</td><td>78 (43)</td><td></td></tr><tr><td>1-2</td><td>320</td><td>125 (39)</td><td>195 (61)</td><td></td></tr><tr><td>3-4</td><td>75</td><td>12 (16)</td><td>63 (84)</td><td>&lt;0.001</td></tr><tr><td>Healthcare facility</td><td></td><td></td><td></td><td></td></tr><tr><td>Public university</td><td>228</td><td>96 (42)</td><td>132 (58)</td><td></td></tr><tr><td>Public non-university</td><td>234</td><td>85 (36)</td><td>149 (64)</td><td></td></tr><tr><td>Private</td><td>163</td><td>80 (49)</td><td>83 (51)</td><td>0.040</td></tr></tbody></table>

M0: no metastasis at diagnosis, M1: metastasis at diagnosis.

Missing information: WHO performance status N = 28 in M1 and N = 23 in M0; Healthcare facility N = 2 in M0.

a Chi2 test.

those diagnosed in private institutions (51 %). Moreover, patients diagnosed in private institutions had better WHO performance status (37 % in the group “0”, 8 % in the group “3-4”) than those diagnosed in public university healthcare facilities (34 % in the group “0”, 14 % in the group “3-4”) and in public non-university healthcare facilities (25 % in the group “0”, 16 % in the group “3-4”) (p = 0.029). Additionally, geriatric clinical evaluation was performed in respectively 6 % (3/48), 9 % (3/33) and 30 % (21/71) of the ‘70-74 years’, ‘75-79 years’ and ‘≥80 years’ groups.

Two hundred and two patients (77 % of M0 patients) were considered operable (Fig. 1), mainly males (87 % vs 67 % for females, p < 0.001), patients aged under 80 years old, or with a WHO performance status under 3. Among them, 45 % had both MRI and endoscopic US at diagnosis, 43 % had either MRI or endoscopic US, and 12 % had none of the two morphological examinations and 157 (78 %) had a tumour considered surgically resectable (Fig. 1, Table 2). The proportion of patients with tumour considered resectable decreased with increasing age at diagnosis. Sex, WHO performance status and healthcare facility at diagnosis were not associated with the tumour resectability proportion.

<table><caption>**Table 2**

Characteristics associated with resectability of the tumour in operable patients with M0 pancreatic adenocarcinoma.</caption><thead><tr><th></th><th>N</th><th>Resectable<br>N (%)</th><th>p<sup>a</sup></th></tr></thead><tbody><tr><td>Total</td><td>202</td><td>157 (78)</td><td></td></tr><tr><td>Sex</td><td></td><td></td><td></td></tr><tr><td>Men</td><td>115</td><td>92 (80)</td><td></td></tr><tr><td>Women</td><td>87</td><td>65 (75)</td><td>0.371</td></tr><tr><td>Age at diagnosis</td><td></td><td></td><td></td></tr><tr><td>&lt;65 years</td><td>60</td><td>52 (87)</td><td></td></tr><tr><td>65-79 years</td><td>110</td><td>86 (78)</td><td></td></tr><tr><td>≥80 years</td><td>32</td><td>19 (59)</td><td>0.011</td></tr><tr><td>WHO Performance Status</td><td></td><td></td><td></td></tr><tr><td>0</td><td>92</td><td>73 (79)</td><td></td></tr><tr><td>1-2</td><td>84</td><td>65 (77)</td><td></td></tr><tr><td>3-4</td><td>4</td><td>2 (50)</td><td>0.379</td></tr><tr><td>Healthcare facility</td><td></td><td></td><td></td></tr><tr><td>Public university</td><td>77</td><td>61 (79)</td><td></td></tr><tr><td>Public non-university</td><td>60</td><td>45 (75)</td><td></td></tr><tr><td>Private</td><td>65</td><td>51 (78)</td><td>0.828</td></tr></tbody></table>

Missing information: WHO performance status N = 22.

a Chi2 test.

The multidisciplinary team meeting recommended upfront resection for 106 of these patients (68 %) and resection after neoadjuvant chemotherapy for 51 (32 %).

Eventually, 42 patients (27 %) did not undergo recommended resection due to patient refusal (N = 7), rapid general deterioration (N = 25), failure of neoadjuvant chemotherapy (N = 9) or unknown reason (N = 1) and 115 patients (73 %) were surgically operated on. Among them, 104 patients were resected and 11 had a laparotomy alone without the planned tumour resection due to intra-operative findings (Supplementary Table 1).

Eighty percent (85/106) of the patients with upfront resection recommendation did receive a surgical resection, of which 9 received it after neoadjuvant chemotherapy. Among the patients with neoadjuvant chemotherapy recommendation, 37 % (19/51) received both, 25 had chemotherapy not followed by resection and 7 had neither. Accounting for age, sex and WHO performance status, patients for whom upfront resection was recommended were nearly 10 times more likely to receive resection than patients for whom recommendation was neoadjuvant chemotherapy (OR<sub>upfront resection vs neoadjuvant therapy</sub>: 9.67 [4.13–22.6], p < 0.001, multivariate logistic regression, data not shown). Among the 27 aged patients who had a geriatric evaluation, 15 were considered operable, 9 resectable and 4 did undergo surgical resection.

Eighty patients (30 %) had an R0 resection out of the whole 263 patients with M0 pancreatic cancer. In multivariate analysis, age over 80 years (OR ≥80 years vs < 65 years: 0.16 [0.06–0.39], p < 0.001) and WHO performance status over 0 (OR 1-2 vs 0: 0.43 [0.24–0.79], p = 0.013) decreased the odds of receiving resection (Table 3).

Among the 157 operable patients with resectable tumour, 57 (36 %) had upfront R0 resection and 23 (15 %) had R0 resection after neoadjuvant chemotherapy. Sixty one percent (65/106) of the patients with upfront resection recommendation had a R0 surgical resection, of which 8 received it after neoadjuvant chemotherapy. Among the patients with neoadjuvant chemotherapy recommendation, 29 % (15/51) had a R0 resection.

<table><caption>**Table 3**

Characteristics associated with tumour resection in the 263 non-metastatic patients.</caption><thead><tr><th rowspan="2"></th><th rowspan="2">N</th><th colspan="2">Resection</th><th colspan="3">Multivariate</th></tr><tr><th>Univariate<br>N (%)</th><th>p<sup>a</sup></th><th>Odds Ratio</th><th>IC 95 %</th><th>p<sup>b</sup></th></tr></thead><tbody><tr><td>Sex</td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Men</td><td>132</td><td>57<br>(43)</td><td></td><td>1</td><td></td><td></td></tr><tr><td>Women</td><td>131</td><td>47<br>(36)</td><td>0.226</td><td>1.02</td><td>[0.57–1.80]</td><td>0.960</td></tr><tr><td>Age</td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>&lt;65 years</td><td>61</td><td>35<br>(57)</td><td></td><td>1</td><td></td><td></td></tr><tr><td>65-79 years</td><td>123</td><td>59<br>(48)</td><td></td><td>0.75</td><td>[0.38–1.46]</td><td></td></tr><tr><td>≥80 years</td><td>79</td><td>10<br>(13)</td><td>0.000</td><td>0.16</td><td>[0.06–0.39]</td><td>&lt;0.001</td></tr><tr><td>WHO Performance Status</td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>0</td><td>103</td><td>53<br>(51)</td><td></td><td>1</td><td></td><td></td></tr><tr><td>1-2</td><td>125</td><td>37<br>(30)</td><td></td><td>0.43</td><td>[0.24–0.79]</td><td></td></tr><tr><td>3-4</td><td>12</td><td>1 (8)</td><td>0.000<sup>c</sup></td><td>0.13</td><td>[0.01–1.23]</td><td>0.013</td></tr><tr><td>Healthcare facility</td><td></td><td></td><td></td><td></td><td></td><td></td></tr><tr><td>Public university</td><td>96</td><td>42<br>(44)</td><td></td><td></td><td></td><td></td></tr><tr><td>Public non-university</td><td>85</td><td>29<br>(34)</td><td></td><td></td><td></td><td></td></tr><tr><td>Private</td><td>80</td><td>33<br>(41)</td><td>0.399</td><td></td><td></td><td></td></tr></tbody></table>

a Chi2 test.

b Likelihood ratio.

c Fisher's exact test.
surgical resection.

## 4. Discussion

This article reports a national French population-based management study for pancreatic cancers. To our knowledge, it is the first population-based study to detail surgical management according to the operability of the patients and resectability of the tumour. Our results showed that in the general population more than half of the cases had distant metastasis at diagnosis, in accordance with previously published rates [15], and 16% had a localized PDAC considered unresectable, witnessing a late diagnosis. One-quarter of the cases were considered operable and had a resectable tumour. Despite the current standard-of-care approach consisting of upfront surgery and adjuvant chemotherapy, neoadjuvant chemotherapy is recommended by multidisciplinary team evaluation in one-third of these cases. Although this observational study showed that tumour resection rate was higher when upfront resection was recommended than when neoadjuvant chemotherapy was recommended, a lot of patients develop early metastases during upfront chemotherapy. Such undetected micro-metastatic disease at diagnosis prevents responding the key question of whether upfront surgery provides better disease-free and overall survival compared to upfront chemotherapy. This complex issue remains under investigation in randomized controlled trials. The model proposed by Crippa et al. to determine the risk of futile pancreatectomy might help in selecting patients for upfront surgery or neoadjuvant therapy [16]. Increasing age and WHO performance status were associated with a decrease in resection whereas healthcare facility was not. In the end, only 16% of the population had a surgical resection of PDAC, and 30% of those with localized PDAC at diagnosis benefited from a complete R0 surgical resection.

Despite low 5-year survival for patients who can undergo surgical resection, varying from 10 to 25% in the literature, surgical resection is the only treatment that offers the possibility of curative treatment [15]. Tumours located in the pancreatic head are resected by pancreateoduodenectomy while tumours located in the pancreatic body or tail are resected by distal pancreatectomy often associated with splenectomy. Both surgeries present high morbidity and mortality, and thus can only be proposed to patients in good general condition. Although patients diagnosed in private structures had better WHO performance status than in public university and non-university facilities, the proportion of patients considered operable and of tumours considered resectable did not differ among healthcare facilities. It has been established that the clinical and surgical expertise for ensuring optimal patient care and outcomes varied among care centers. An inverse relationship between operative volume and mortality has been reported in a French population-based study. Ninety-day post-operative mortality was higher in low- and medium-volume centers than in high-volume centers (12.5% and 7.5% vs. 2.2%) [6].

Recently, interest in neoadjuvant therapy for PDAC has increased to control early systemic spread and achieve microscopically tumour cell-free R0 resection margin despite potential deleterious disease progression during the period of neoadjuvant treatment [14]. This issue is still debated as recent studies showed different results for neoadjuvant chemotherapy in resectable and borderline-resectable PDAC on survival outcomes [12,13,17,18]. Currently, US National Comprehensive Cancer Network (NCCN) guidelines still recommend the use of adjuvant therapy after surgical resection as it lacks of high-level evidence in favor of the effectiveness of the neoadjuvant strategy.

Although this observational study does not allow for a direct comparison of effectiveness between the two groups, the R0 resection proportion was higher in patients with upfront surgery than in those receiving neoadjuvant chemotherapy, which is in line with the ESCAP-5 study [13]. Attempted tumour resection converted to laparotomy alone was mostly due to a rapid general condition degradation or failure of neoadjuvant chemotherapy, partly due to the well-established PDAC

resistance to chemotherapy [19].

This study has the advantage of including detailed descriptions of the management of patients with pancreatic cancer diagnosed in a population-based setting. It avoids the referral bias that often occurs in hospital-based series. The supply of healthcare in the studied geographic area had similar characteristics to those of other French areas (academic cancer centers, private and public university or non-university hospitals). Access to surgery or chemotherapy, in both private and public structures was unlimited, and the rules for authorizing the activities of healthcare facilities have been defined for the whole of France. French patients have the same access to national health insurance-funded care and to any place of treatment, whatever its geographic situation. The multi-institutional nature of the study population strengthens the reliability of the results.

However, the study was limited by its observational nature. One limit of the study was its relatively small size in some treatment categories and the lack of results about morbi-mortality after surgery and of type of chemotherapy administered. This study was constrained also in assessing tumour resectability, as it relied on medical and surgical records based on the multidisciplinary team meeting conclusions and radiological reports only classifying tumours as resectable or unresectable. Medical and surgical records lack detailed data for categorizing resectability into resectable, borderline-resectable, and locally advanced stages which is a crucial factor in determining the course of neoadjuvant strategy. This study did not differentiate resectable from borderline-resectable PDAC. A further enlarged high-resolution study should be set up throughout the French network of cancer registries to better understand the management of this cancer. In conclusion, these results highlight the difficulties involved in managing pancreatic cancer in the real world, whatever the healthcare facility and whatever the patient's characteristics.

## Funding statement

The French National Cancer Institute (INCa) provided financial support for the conduct of the research.

## Role of the funding source

The funding source had no role in the study nor in the writing of the manuscript.

## Availability of data and materials

The dataset used and analyzed within this study is available from the corresponding author on reasonable request.

## CRediT authorship contribution statement

**Guillaume Goebel:** Conceptualization, Methodology, Writing – original draft, Visualization. **Valérie Jooste:** Conceptualization, Methodology, Formal analysis, Data curation, Visualization. **Florence Molinie:** Validation, Writing – review & editing. **Pascale Grosclaude:** Resources, Writing, Validation, Writing – review & editing. **Anne-Sophie Woronoff:** Validation, Writing – review & editing. **Arnaud Alves:** Validation, Writing – review & editing. **Véronique Bouvier:** Validation, Writing – review & editing. **Jean-Baptiste Nousbaum:** Validation, Writing – review & editing. **Sandrine Plouvier:** Validation, Writing – review & editing. **Leila Bengrine-Lefevre:** Writing – review & editing. **Thomas Rabel:** Validation, Writing – review & editing. **Anne-Marie Bouvier:** Resources, Writing, Validation, Writing – original draft, editing, Supervision, Project administration.

## Declaration of competing interest

The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.

Acknowledgment

The authors thank the French Public Health Surveillance (Santé
Publique France) and the French National Cancer Institute (Institut
National du Cancer) for general support to the cancer registries.

**Appendix A. Supplementary data**

Supplementary data to this article can be found online at https://doi.
org/10.1016/j.ejso.2024.108748.

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