Cost-effectiveness of staging laparoscopy with peritoneal cytology in pancreatic adenocarcinoma
胰腺腺癌分期腹腔镜检查和腹腔细胞学检查的成本效益

Maya Jodidio, BA $^{a}$ , Neal S. Panse, MPH $^{a}$ , Vishnu Prasath, MS $^{b,c}$ , Ronak Trivedi, BS $^{b}$ , Simran Arjani, MD $^{b}$ , Ravi J. Chokshi, MD, MPH, FACS $^{a,*}$

Introduction 导言

Pancreatic cancer has the tenth highest annual incidence among malignancies in the United States, with 62,210 new cases in

2022 .^{1}

Treatment of this condition represents a significant healthcare expenditure, with total cost over

$ 4

billion annually.

^{2}

Despite improvements in surgical techniques and chemotherapy regimens, pancreatic cancer remains a malignancy with a poor 5 -year survival rate of approximately

10 %^{1}

The high cost of care for therapies which may only offer short survival benefits necessitates cost-effectiveness analysis of available treatment strategies.

2022 .^{1}

在美国，胰腺癌的年发病率在恶性肿瘤中高居第十位，每年新增病例62210例

2022 .^{1}

治疗胰腺癌的医疗开支巨大，每年的总费用超过

$ 4

十亿美元。

^{2}

尽管手术技术和化疗方案有所改进，但胰腺癌仍然是一种5年生存率很低的恶性肿瘤，大约只有

10 %^{1}

高昂的治疗费用只能带来短暂的生存益处，因此有必要对现有的治疗策略进行成本效益分析。

Treatment regimens in pancreatic cancer depend on the stage at diagnosis, and the detection of any metastatic disease drastically changes treatment course. Use of CT alone for initial staging without further diagnostic workup can fail to detect metastases in up to

41 %

of cases.

^{3}

Failure to detect metastases increases for smaller and/or isoattenuating tumors as well as asymptomatic cases. Other imaging techniques, including positron emission tomography (PET) may also fail to accurately detect small metastatic lesions.

^{4}

Historically, since patients with metastatic disease are not candidates for curative resection, finding occult metastases during a planned resection subjects them to morbidity associated with nontherapeutic exploratory laparotomy while delay-
胰腺癌的治疗方案取决于诊断时的分期，任何转移性疾病的发现都会大大改变治疗方案。在

41 %

的病例中，仅使用CT进行初步分期而不做进一步诊断可能无法检测到转移灶。

^{3}

对于较小和/或等衰减肿瘤以及无症状病例，检测不到转移灶的情况会增加。包括正电子发射断层扫描（PET）在内的其他成像技术也可能无法准确检测到小的转移病灶。

^{4}

从历史上看，由于转移性疾病患者不适合进行根治性切除术，因此在计划的切除术中发现隐匿性转移灶会使患者承受非治疗性探查性开腹手术带来的发病率，同时延误治疗。

ing definitive systemic therapy. More thorough staging may reduce the rate of futile surgery.

^{5}

Staging laparoscopy prior to resection can aid in the visualization of metastases not appreciated on initial imaging and allow for time for cytopathology. In most hospital systems, intraoperative cytopathology is not routine. Performing laparoscopy prior to resection, as opposed to on the same-day, allows for the addition of other diagnostics such as peritoneal washings with cytology or peritoneal tumor markers, which can take several days to analyze and report and may help guide therapy.

^{6 - 8}

In addition, cytologic analysis of peritoneal fluid samples can detect micro-metastases, which may not be identifiable via CT or laparoscopy but indicate poor prognosis in resected patients.

^{9, 10}

Without adequate diagnostic work-up, patients with occult metastases may undergo resection and have low survival despite attempted curative surgery.

^{5}

Improved staging could reduce costs associated with over-treatment, increase survival in those who undergo resection, and improve quality of life ( QoL ) in all patients by determining optimal treatment.

^{5}

在进行明确的系统治疗时。更彻底的分期可减少无效手术率。

^{5}

在切除术前进行分期腹腔镜检查可帮助观察最初影像学检查未发现的转移灶，并为细胞病理学检查留出时间。在大多数医院系统中，术中细胞病理学检查并非常规。在切除术前进行腹腔镜检查，而不是在当天进行，可以增加其他诊断项目，如腹腔冲洗细胞学检查或腹膜肿瘤标记物检查，这些检查需要几天时间进行分析和报告，可能有助于指导治疗。

^{6 - 8}

此外，腹腔液样本的细胞学分析可检测出微小转移灶，CT或腹腔镜检查可能无法识别微小转移灶，但却预示着切除患者的不良预后。

^{9, 10}

如果没有充分的诊断检查，有隐匿性转移灶的患者可能会接受切除手术，尽管尝试了根治性手术，但生存率很低。

^{5}

改进分期可减少过度治疗带来的费用，提高接受切除术患者的生存率，并通过确定最佳治疗方法提高所有患者的生活质量（QoL）。

^{5}

Diagnostic laparoscopy may increase cost-effectiveness of treatment in patients with resectable and borderline resectable tumors, as the additional upfront costs improve QoL through avoidance of nontherapeutic surgery and allow for earlier initiation of definitive treatment.

^{11}

This study compares cost-effectiveness of CT alone and CT with laparoscopy and peritoneal cytology for initial staging of pancreatic adenocarcinoma prior to neoadjuvant therapy.
诊断性腹腔镜检查可提高可切除和边缘可切除肿瘤患者的治疗成本效益，因为额外的前期费用可避免非治疗性手术，从而改善患者的生活质量，并可更早开始明确治疗。

^{11}

本研究比较了单纯CT与CT联合腹腔镜检查和腹腔细胞学检查在新辅助治疗前对胰腺腺癌进行初始分期的成本效益。

Methods 方法

Theoretical cohort 理论队列

Our model represents a theoretical cohort of patients with biopsy-proven pancreatic adenocarcinoma. All stages of pancreatic cancer were included. Treatment regimens and their associated outcomes were obtained from peer-reviewed, published literature. Patients were included if they were staged with either CT or CT with laparoscopy and cytology and then received neoadjuvant therapy. We found that literature reporting on probabilities used in this analysis performed laparoscopy and cytology on patients prior to neoadjuvant therapy. PET scan was not considered given its unclear role in initial staging.

^{12}

Patients were not considered if they underwent a surgery-first approach without neoadjuvant therapy, or if they received diagnostic laparoscopy without cytology. Patients were also excluded if they were diagnosed with pancreatic endocrine tumors, received neoadjuvant therapy prior to laparoscopy with cytology, or underwent repeat laparoscopy with cytology prior to resection.
我们的模型代表了经活检证实的胰腺腺癌患者的理论队列。所有分期的胰腺癌都包括在内。治疗方案及其相关结果均来自同行评议的已发表文献。如果患者通过 CT 或 CT 结合腹腔镜和细胞学检查进行了分期，然后接受了新辅助治疗，则被纳入研究范围。我们发现，报告本分析所用概率的文献均在新辅助治疗前对患者进行了腹腔镜检查和细胞学检查。鉴于PET扫描在初始分期中的作用尚不明确，因此未将其考虑在内。

^{12}

如果患者先接受手术而未接受新辅助治疗，或接受腹腔镜诊断而未进行细胞学检查，则不在考虑之列。如果患者被诊断为胰腺内分泌肿瘤，在接受腹腔镜细胞学检查前接受了新辅助治疗，或在切除术前接受了重复腹腔镜细胞学检查，也不在考虑之列。

Decision tree model 决策树模型

A decision tree is a model which compares the effectiveness of competing clinical strategies. The design of the decision tree was similar to prior works by our group.

^{13 - 17}

TreeAge (TreeAge Software, Williamstown, MA) was the software we used to create a decision tree comparing diagnostic methods for initial pancreatic cancer staging. The model diverged into two main branches based on the staging techniques being compared in this study: CT alone and CT with laparoscopy and cytology for suspected pancreatic cancer (Fig 1). Patients undergoing diagnostic laparoscopy with cytology had no evidence of metastasis on CT and underwent this procedure prior to initiation of neoadjuvant therapy. After diagnostic staging, all patients were classified as resectable, locoregional, or metastatic in both the CT alone and CT with laparoscopy and cytology arms. The locoregional group included patients meeting NCCN criteria for either borderline resectable or locally advanced disease.

^{12}

All patients without identified metastases at staging were started on neoadjuvant therapy. Those who were metastatic at diagnosis received definitive chemotherapy. Following completion of neoadjuvant therapy, patients with potentially resectable
决策树是一种比较不同临床策略有效性的模型。决策树的设计与我们小组之前的工作类似。

^{13 - 17}

我们使用TreeAge（TreeAge Software, Williamstown, MA）软件创建了一个决策树，用于比较胰腺癌初步分期的诊断方法。根据本研究比较的分期技术，该模型分为两个主要分支：单纯 CT 和 CT 与腹腔镜检查和疑似胰腺癌细胞学检查（图 1）。接受腹腔镜诊断和细胞学检查的患者在 CT 上无转移证据，且在开始新辅助治疗前接受了该检查。在诊断分期后，所有患者都被分为可切除组、局部组和转移组。局部区域组包括符合NCCN标准的边缘可切除或局部晚期疾病患者。

^{12}

所有在分期时未发现转移灶的患者均开始接受新辅助治疗。诊断时已发现转移灶的患者则接受明确的化疗。完成新辅助治疗后，有可能切除肿瘤的患者将接受化疗。

Fig. 1. Decision tree comparing outcomes in pancreatic cancer following CT alone and CT with laparoscopy and cytology for staging. Each branch and endpoint represent clinical scenarios and outcomes which could occur during treatment. Costs are represented in USD($) and quality of life is represented in quality-adjusted life-years (QALYs). Abbreviations: PDAC, pancreatic ductal adenocarcinoma.
图 1.比较胰腺癌单纯 CT 分期和 CT 联合腹腔镜检查和细胞学检查分期结果的决策树。每个分支和终点代表治疗过程中可能出现的临床情况和结果。成本以美元表示，生活质量以质量调整生命年（QALYs）表示。缩写：PDAC：胰腺导管腺癌。
disease were re-evaluated for surgical candidacy by restaging CT. Patients were deemed nonsurgical candidates if they had disease progression, lesions not amenable to surgical resection, or poor performance status, and these individuals then received definitive therapy. The remaining surgical candidates underwent attempted resection. Upon laparotomy incision, occult metastases or unresectable disease not detected by restaging CT were discovered in some patients. In these cases, the procedure was halted and they instead received definitive therapy. Those undergoing resection subsequently received adjuvant chemotherapy.
通过 CT 重新分期，重新评估患者是否适合手术治疗。如果患者出现疾病进展、病变不适合手术切除或表现不佳，则被视为非手术候选者，这些患者随后将接受明确的治疗。其余的手术候选者则接受尝试性切除。一些患者在开腹手术中发现了隐性转移灶或 CT 重分期未发现的无法切除的病灶。在这些病例中，手术被中止，转而接受确定性治疗。接受切除术的患者随后接受了辅助化疗。

Table 1 表 1
Costs of interventions. 干预成本。

Intervention 干预措施	Cost (USD$) 费用（美元）
CT scan CT 扫描	457.00
Laparoscopy with peritoneal cytology 腹腔镜腹膜细胞学检查	8666.34
Base neoadjuvant therapy (resectable) 基础新辅助治疗（可切除）	6439.32
Base neoadjuvant therapy (borderline resectable) 基础新辅助治疗（边缘可切除）	6296.30
Base neoadjuvant therapy (locally advanced) 基础新辅助治疗（局部晚期）	9540.76
Exploratory laparotomy 剖腹探查术	$26, 940.71$
Standard Whipple 标准惠普	$37, 788.49$
Definitive chemotherapy (cost per month) 最终化疗（每月费用）	4626.82

Abbreviations: CT, computed tomography.
缩写：CT：计算机断层扫描。

Parameters studied 研究参数

The endpoint for both arms of the tree was death. Restaging following neoadjuvant chemoradiation was performed on a per-protocol basis; therefore, patients who dropped out of the included studies or deferred surgery were considered nonsurgical candidates. Successful resection was defined as margin-negative (R0) resection. The resection of a macroscopic tumor with positive microscopic margins (R1) was included as a separate branch. Patients were considered to undergo nontherapeutic laparotomy if they underwent exploratory laparotomy without intervention, resection with residual macroscopic disease (R2), or margin-indeterminate resection. Average survival among patients with nontherapeutic laparotomy was calculated using a weighted average based on the procedure performed.
两组研究的终点均为死亡。新辅助化疗后的重新分期按方案进行；因此，退出纳入研究或推迟手术的患者被视为非手术候选者。成功切除的定义是边缘阴性（R0）切除。显微镜下边缘阳性（R1）的大肿瘤切除术被列为一个单独的分支。如果患者接受了未干预的探查性开腹手术、大体病灶残留（R2）的切除术或边缘不确定的切除术，则被视为接受了非治疗性开腹手术。非治疗性开腹手术患者的平均生存率是根据所实施的手术进行加权平均计算得出的。

Once the decision tree was constructed, published studies were reviewed to assign probabilities and QoL data to each branch. Because the model was constructed without identifiable patient data, our study was exempt from obtaining approval from the Rutgers Institutional Review Board.
构建决策树后，我们对已发表的研究进行了回顾，以便为每个分支分配概率和 QoL 数据。由于模型的构建不涉及可识别的患者数据，因此我们的研究无需获得罗格斯大学机构审查委员会的批准。

Cost and effectiveness 成本和效益

Procedural costs, measured in USD($), were obtained using the 2021 Medicare Inpatient Prospective Payment System, Medicare Physician Fee Schedule 2021, and the 2021 Medicare Procedure Price Lookup for procedures. Due to variations in hospital charges by location, Medicare data was used to standardize results and allow for generalizability across different regions and hospital systems. Procedural costs accounted for complication and reoperation rates, which increased reimbursement (Table 1).

^{18, 19}

Cost of initial biopsy was not included, as this was equivalent in all patients. The cost of treatments for symptom improvement was also not considered. Reimbursement for distal pancreatectomy was not calculated separately from pancreaticoduodenectomy given the similarity in major complication rates and identical reimbursement coding for the two procedures.

^{20}

使用 2021 年医疗保险住院病人预付费系统、2021 年医疗保险医生收费表和 2021 年医疗保险手术价格查询获得了以美元为单位的手术成本。由于不同地区的医院收费存在差异，因此使用了医疗保险数据来统一结果，以便在不同地区和医院系统之间进行推广。手术费用包括并发症和再手术率，这增加了报销额度（表1）。

^{18, 19}

初始活检费用未包括在内，因为所有患者的费用相同。改善症状的治疗费用也未考虑在内。鉴于胰十二指肠切除术和远端胰腺切除术的主要并发症发生率相似，且两种手术的报销编码完全相同，因此远端胰腺切除术的报销费用未与胰十二指肠切除术分开计算。

^{20}

Chemotherapy costs were calculated using corresponding medication codes from the Healthcare Common Procedure Coding System and prices from the 2021 Average Sales Price Drug Pricing File from the Centers for Medicare and Medicaid Services (Table 1). Infusion cost and cost associated with adverse events of included chemotherapy regimens were obtained from literature using Medicare data.

^{21, 22}

Neoadjuvant chemoradiation regimens differed in the studies examining borderline resectable and locally advanced, thus a weighted average was used to determine chemotherapy cost for the locoregional group.

^{23 - 25}

Prices for intensity-modulated radiotherapy were identified in the outpatient Medicare Procedure Price Lookup. Cost of definitive therapy was calculated until death. Discounts were applied to costs accrued after the initial 12 months.

^{26}

化疗成本的计算采用了医疗保健通用程序编码系统（Healthcare Common Procedure Coding System）中的相应药物编码以及美国医疗保险和医疗补助服务中心（Centers for Medicare and Medicaid Services）2021 年平均销售价格药物定价文件中的价格（表 1）。纳入化疗方案的输液成本和不良事件相关成本是利用医疗保险数据从文献中获得的。

^{21, 22}

新辅助化疗方案在边缘可切除和局部晚期的研究中有所不同，因此采用加权平均值来确定局部晚期组的化疗成本。

^{23 - 25}

在门诊医疗保险程序价格查询中确定了调强放疗的价格。确定性治疗的成本计算至患者死亡。最初12个月后的费用适用折扣。

^{26}

QoL was measured using quality-adjusted life-years (QALYs), which represent the product of aggregate QoL score and survival time for each respective endpoint within the model. One QALY equates to one year of perfect health, while zero QALYs equates to death. QoL is determined using utility weights, values that represent QoL associated with various health states. Specifically, QALY is calculated by multiplying the change in utility value, or disutility, induced by the treatment by the duration of the treatment effect

^{11, 27 - 30}

Disutility associated with procedures lasted for 6 months postprocedure, including post-pancreatectomy, which is consistent with the methodology of similar studies.

^{11}

Disutility related to chemoradiation was assumed to end when therapy ended. Survival data was obtained from published studies.

^{24, 25, 31}

Literature suggests significantly worse survival among resected patients with occult metastases than those without metastases; the CT alone group would include a higher percentage with occult metastases than the laparoscopy with cytology group.

^{5}

To account for reduced rate of noncurative resection and early distant metastasis following invasive staging, survival after R0 resection in the laparoscopy with cytology arm was adjusted based on the percentage found to be metastatic after staging. This resulted in longer survival with R0 resection in those following laparoscopy with cytology, which would be expected if fewer patients with occult metastases underwent presumed R0 resection. An adjustment using the declining exponential approximation of life expectancy (DEALE) method was then performed to account for average life expectancy of patients with similar age and sex, in this case a 70 year-old male.

^{32, 33}

Final QALYs for each branch after listed within Figure 1.
QoL 采用质量调整生命年（QALYs）来衡量，QALYs 表示模型中每个终点的 QoL 总分与生存时间的乘积。一个 QALY 相当于一年的完全健康，而零 QALY 相当于死亡。QoL 使用效用权重来确定，效用权重值代表与各种健康状况相关的 QoL。具体来说，计算 QALY 的方法是将治疗引起的效用值变化（或称效用缺失）乘以治疗效果的持续时间

^{11, 27 - 30}

与手术相关的效用缺失在术后持续 6 个月，包括胰腺切除术后，这与类似研究的方法一致。

^{11}

与化疗相关的效用假定在治疗结束时终止。生存数据来自已发表的研究。

^{24, 25, 31}

文献表明，有隐匿转移灶的切除患者的生存率明显低于无转移灶的患者；单纯CT组中有隐匿转移灶的比例高于腹腔镜加细胞学组。

^{5}

考虑到侵入性分期后非根治性切除率降低和早期远处转移，根据分期后发现转移的比例调整了腹腔镜联合细胞学检查组R0切除后的生存率。结果显示，接受腹腔镜和细胞学检查的患者R0切除术后的存活期更长，如果有较少的隐匿性转移患者接受假定的R0切除术，存活期就会更长。然后使用预期寿命指数递减近似法（DEALE）进行调整，以考虑年龄和性别相似的患者（本例中为 70 岁男性）的平均预期寿命。

^{32, 33}

图 1 中列出了每个分支的最终 QALY。

Incremental cost-effectiveness ratio (ICER) was the primary outcome measure for this study. A threshold for willingness-to-pay was set at

$ 100, 000 /

QALY.

^{34}

ICER values greater than

$ 100, 000 / QALY

exceeded the willingness-to-pay threshold and were thus not cost-effective. Oneway and two-way sensitivity analyses were performed on all branch-point probabilities based over their

95 %

confidence interval, which was determined based on sample size of included studies. A probabilistic sensitivity analysis with 100,000 random sampling simulations was also conducted.
增量成本效益比（ICER）是本研究的主要结果指标。支付意愿阈值设定为

$ 100, 000 /

QALY。

^{34}

ICER值大于

$ 100, 000 / QALY

，超过了支付意愿阈值，因此不具有成本效益。根据纳入研究的样本量确定的

95 %

置信区间，对所有分支点概率进行单向和双向敏感性分析。此外，还进行了 100,000 次随机抽样模拟的概率敏感性分析。

Data selection 数据选择

All data within our model was obtained from published peer-reviewed studies. PubMed and Scopus were queried for studies reporting probabilities which could be used to populate the decision tree. We sought to include studies examining resectable and locoregional disease with similar neoadjuvant regimens after laparoscopy with cytology to maximize comparability of results. Recent meta-analyses, randomized controlled trials, and prospective cohort studies were preferred over case reports and older studies. Meta-analyses and citations from included studies were examined to identify studies which may not have been found through our original search.
我们模型中的所有数据均来自已发表的同行评审研究。我们在 PubMed 和 Scopus 上查询了报告概率的研究，这些概率可用于填充决策树。我们试图纳入对腹腔镜细胞学检查后采用类似新辅助治疗方案的可切除性和局部区域性疾病的研究，以最大限度地提高结果的可比性。与病例报告和较早的研究相比，最新的荟萃分析、随机对照试验和前瞻性队列研究更受青睐。我们还检查了纳入研究的荟萃分析和引文，以找出我们最初搜索时可能没有发现的研究。

Rates of NCCN resectability status by initial CT, surgical outcomes following CT alone, and positivity of laparoscopy with cytology were identified (Table 2).

^{9, 23 - 25, 31, 35, 36}

While invasive staging may increase rates of surgical candidacy and R0 resection rate, surgical outcome probabilities following laparoscopy with cytology were assumed to be equivalent to those following CT alone due to limitations in the literature.

^{5}

Neoadjuvant therapy in included studies consisted of gemcitabine and radiation.

^{24, 25, 31}

Although this is not a preferred neoadjuvant regimen by current guidelines, it was chosen due to lack of available high-quality, comparable studies using FOLFIRINOX (5-fluorouracil, irinotecan, oxaliplatin, and leucovorin) or other preferred regimens after invasive staging.

^{12}

Definitive chemotherapy consisted primarily of gemcitabine, with some receiving FOLFOX (5-fluorouracil, oxaliplatin, and leucovorin).

^{9}

All included studies report life expectancy of patients without surgical excision but did not differentiate survival between patients deemed to be nonsurgical candidates after neoadjuvant therapy and those who underwent exploratory laparotomy without resection.

^{24, 25, 31}

Therefore, survival of these 2 endpoints in the tree were assumed to be equivalent to the survival of patients with unresectable disease. One study reported survival following R2 and margin-indeterminate resection.

^{25}

A weighted average survival for these patients and those undergoing only exploratory laparotomy was used
通过初始CT确定了NCCN可切除性状态的比率、单纯CT后的手术结果以及腹腔镜细胞学检查的阳性率（表2）。

^{9, 23 - 25, 31, 35, 36}

虽然侵入性分期可能会提高手术候选率和R0切除率，但由于文献的局限性，腹腔镜和细胞学检查后的手术结果概率被假定为等同于单纯CT检查后的手术结果概率。

^{5}

纳入研究的新辅助治疗包括吉西他滨和放射治疗。

^{24, 25, 31}

虽然这并不是目前指南中首选的新辅助治疗方案，但由于缺乏使用FOLFIRINOX（5-氟尿嘧啶、伊立替康、奥沙利铂和白求恩）或其他侵入性分期后首选方案的高质量可比研究，因此选择了这一方案。

^{12}

最终化疗主要包括吉西他滨，部分患者接受FOLFOX（5-氟尿嘧啶、奥沙利铂和白血病素）。

^{9}

所有纳入的研究都报告了未进行手术切除的患者的预期寿命，但没有区分新辅助治疗后被认为不适合手术的患者和接受探查性开腹手术但未切除的患者的生存率。

^{24, 25, 31}

因此，树中这2个终点的生存率被假定为等同于不可切除疾病患者的生存率。一项研究报告了R2和边缘不确定切除术后的生存率。

^{25}

采用了这些患者和仅接受探查性开腹手术患者的加权平均生存率

Table 2 表 2
Branch-point probabilities with

95 %

confidence interval.
带

95 %

置信区间的分支点概率。

Parameter 参数	Best Estimate 最佳估计	Low Value 低价值	High Value 高价值	Citation 引用
CT alone 仅 CT
Resectable 可切除	0.391	0.3534	0.4303	$[1]$
Surgical candidate 手术候选人	0.896	0.8509	0.9284	$[2]$
R0 resection R0 切除术	0.825	0.7405	0.8865	$[2]$
R1 resection R1 切除术	0	0	0.1103	$[3]$
Locoregional 地区	0.406	0.3677	0.4450	$[1]$
Surgical candidate 手术候选人	0.306	0.2503	0.3681	$[4, 5]$
R0 resection R0 切除术	0.507	0.3934	0.6199	$[4, 5]$
R1 resection R1 切除术	0.4118	0.2876	0.5484	$[4, 5]$
Metastatic 转移性	0.203	0.1730	0.2365	$[1]$
CT with laparoscopy and cytology CT 与腹腔镜检查和细胞学检查	0.284
Resectable 可切除	0.273	0.1832	0.3737	$[1, 6]$
Laparoscopy/cytology positivity 腹腔镜检查/细胞学检查阳性	0.896	0.1315	0.4816	$[6, 7]$
Surgical candidate 手术候选人	0.825	0.7409	0.9284	$[2]$
R0 Resection R0 切除	0	0	0.8865	$[2]$
R1 Resection R1 切除	0.240	0.187	0.1103	$[3]$
Locoregional 地区	0.4085	0.3311	0.298	$[1]$
Laparoscopy/cytology positivity 腹腔镜检查/细胞学检查阳性	0.306	0.4907	$[8, 9]$
Surgical candidate 手术候选人	0.507	0.2503	0.3681	$[4, 5, 8, 9]$
R0 resection R0 切除术	0.4118	0.3934	0.6199	$[4, 5, 8, 9]$
R1 resection R1 切除术	0.476	0.3876	0.5484	$[4, 5]$
Metastatic 转移性			0.6295	$[1, 6, 8, 9]$

to represent survival of nontherapeutic laparotomy for these patients. Survival in patients with metastatic disease was a weighted average of survival in resectable and locoregional patients without resection.
代表这些患者非治疗性开腹手术的存活率。转移性疾病患者的生存率是可切除患者和未切除的局部区域患者生存率的加权平均值。

Results 成果

Invasive staging identified occult metastatic disease in

27.3 %

of patients with resectable disease and

40.9 %

of patients with locoregional disease.

^{9, 35, 36}

Positive cytology in the absence of gross metastasis was noted in

0 %

of cases with resectable disease and

13.8 %

of cases with locoregional disease.

^{9, 35, 36}

CT with laparoscopy and cytology yielded 1.304 QALYs at
在

27.3 %

例可切除疾病患者和

40.9 %

例局部疾病患者中，侵入性分期发现了隐匿性转移疾病。

^{9, 35, 36}

在

0 %

例可切除病例和

13.8 %

例局部病例中发现细胞学阳性，但无大面积转移。

^{9, 35, 36}

CT与腹腔镜检查和细胞学检查可产生1.304 QALYs（以QALY值计）。

Table 3 表 3
Cost-effectiveness of CT alone and CT with laparoscopy and cytology.
单纯 CT 和 CT 与腹腔镜检查和细胞学检查的成本效益。

Base Case 基本情况	Cost $($)$ 费用 $($)$	QALYs	Cost $($) /$ QALY 成本 $($) /$ QALY	ICER
CT with laparoscopy and cytology CT 与腹腔镜检查和细胞学检查	$55, 314.11$	1.304	$42, 418.80$	-
CT alone 仅 CT	$42, 620.43$	1.315	$32, 410.97$	$1, 117, 169.54$

Abbreviations: ICER, incremental cost-effectiveness ratio (change in cost ($)/change in QALYs); QALY, quality-adjusted life-year.
缩写：ICER：增量成本效益比（成本变化（美元）/ QALYs 变化）；QALY：质量调整生命年。

Fig. 2. Scatterplot of a probabilistic sensitivity analysis (Monte Carlo). A total of 1000 simulations are shown for optimal visualization. Costs are represented in

USD ($)

and quality of life is represented in quality-adjusted life-years (QALYs).
图 2.概率敏感性分析（蒙特卡罗）的散点图。为达到最佳可视化效果，共显示了 1000 次模拟。成本以

USD ($)

表示，生活质量以质量调整生命年（QALYs）表示。

$ 55, 314.11

, while CT alone yielded 1.315 QALYs at

$ 42, 620.43

(Table 3). This resulted in an ICER of

$ 1, 117, 169.54 /

QALY with CT alone, which therefore was the preferred strategy. Twelve oneway sensitivity analyses were performed. Within the

95 %

confidence intervals of each parameter, there were no values where laparoscopy and cytology was preferred within the

$ 100, 000

threshold. Outside of the confidence interval, addition of laparoscopy with cytology in all nonmetastatic patients would be favored when the percentage of resectable and locoregional patients were high. Laparoscopy and cytology would also be favored when the percentage of metastatic patients was low, also outside the

95 %

confidence interval. Two-way sensitivity analyses found that laparoscopy and cytology would be preferred when the percentage of resectable and locoregional patients were high,

38 %

and

48 %

, respectively, and R0/R1 resection rates were high, approaching

100 %

. However, the percentages required for these values were lower than in the one-way sensitivity analyses. A probabilistic sensitivity analysis favored CT alone in

99.9 %

of simulations (Fig 2).

$ 55, 314.11

，而单用 CT 在

$ 42, 620.43

时可获得 1.315 QALY（表 3）。因此，单用 CT 的 ICER 为

$ 1, 117, 169.54 /

QALY，是首选策略。共进行了 12 项单向敏感性分析。在每个参数的

95 %

置信区间内，在

$ 100, 000

阈值内没有腹腔镜检查和细胞学检查为首选的值。在置信区间外，如果可切除和局部区域患者的比例较高，则所有非转移性患者都应首选腹腔镜和细胞学检查。当转移性患者比例较低时，同样在

95 %

置信区间外，腹腔镜和细胞学检查也会受到青睐。双向敏感性分析发现，当可切除患者和局部区域性患者的比例较高，分别为

38 %

和

48 %

，且R0/R1切除率较高，接近

100 %

时，腹腔镜检查和细胞学检查将成为首选。然而，这些值所需的百分比低于单向敏感性分析。在

99.9 %

的模拟中，概率敏感性分析倾向于单纯 CT（图 2）。

Discussion 讨论

This study was designed to compare the cost-effectiveness of CT alone and CT with laparoscopy and cytology in the staging of pancreatic adenocarcinoma. Adding laparoscopy with cytology resulted in a higher percentage of patients with identified metastases at staging (47.6%)
本研究旨在比较在胰腺腺癌分期中单纯 CT 与 CT 加腹腔镜检查和细胞学检查的成本效益。增加腹腔镜检查和细胞学检查后，分期时发现转移灶的患者比例更高（47.6%）。
as compared to CT alone (20.3%).

^{9, 23 - 25, 31, 35, 36}

Early exclusion of patients with occult metastases decreased the overall number of patients undergoing attempted resection while increasing the R0 resection rate. CT alone was the favored strategy, though addition of laparoscopy with cytology in all nonmetastatic patients became cost-effective when the percentage of resectable and locoregional patients were high and R0/R1 resection rates were high. While this occurred outside the confidence interval, it is possible that these values are real in certain healthcare systems. Overall, this indicates cost-effectiveness of laparoscopy with cytology is dependent on improved selection of candidates for treatment with curative intent.
与单纯 CT（20.3%）相比。

^{9, 23 - 25, 31, 35, 36}

早期排除隐匿转移灶患者减少了尝试切除的患者总数，同时提高了R0切除率。尽管在所有非转移患者中增加腹腔镜检查和细胞学检查在可切除和局部转移患者比例较高且R0/R1切除率较高时具有成本效益，但仅靠CT检查仍是首选策略。虽然这种情况发生在置信区间之外，但在某些医疗系统中，这些数值有可能是真实的。总体而言，这表明腹腔镜联合细胞学检查的成本效益取决于是否能更好地选择治疗对象。

Due to limitations in the literature, the effect of laparoscopy with cytology on surgical outcomes following neoadjuvant therapy is unclear. However, accurately identifying those with occult metastases during initial staging may increase the rate of R0 resection among patients undergoing surgical exploration.

^{37}

One meta-analysis found diagnostic laparoscopy in a surgeryfirst approach can reduce nontherapeutic laparotomy by

21 % .^{3}

This could potentially be reduced further through examination of peritoneal cytology and administration of neoadjuvant therapy.

^{3, 38, 39}

In contrast, a study by Peng et al.

^{9}

comparing CT alone and CT with laparoscopy and cytology for staging prior to neoadjuvant therapy found comparable rates of surgical candidacy and resection between the 2 groups. This study found survival to be similar as well. No other similar studies were identified. In our study, sensitivity analyses demonstrated a cost benefit with universal laparoscopy and cytology when the percentage of resectable and locoregional patients were high and R0/R1 resection rates were high. The percentage of resectable and locoregional patients was obtained from trials examining treatment outcomes following CT alone for staging due to lack of similar studies involving invasive staging.

^{24, 25, 31}

This increased comparability of the two arms of our analysis, but failed to capture any possible changes in outcomes following invasive staging. While some evidence suggests invasive staging could potentially increase rate of curative resection, there are few studies employing direct comparison with staging CT alone. A higher percentage of resectable and locoregional patients with invasive staging improved its cost-effectiveness, making it cost-effective at

38 %

and

48 %

, respectively.
由于文献资料的局限性，腹腔镜细胞学检查对新辅助治疗后手术效果的影响尚不明确。不过，在初始分期时准确识别隐匿性转移灶可能会提高接受手术探查患者的R0切除率。

^{37}

一项荟萃分析发现，诊断性腹腔镜检查在 "手术为先 "的方法中可减少

21 % .^{3}

非治疗性开腹手术，而通过腹膜细胞学检查和新辅助疗法的实施，可进一步减少非治疗性开腹手术。

^{3, 38, 39}

与此相反，Peng 等人的一项研究

^{9}

比较了单纯 CT 和 CT 与腹腔镜检查和细胞学检查在新辅助治疗前进行分期的情况，发现两组的手术候选率和切除率相当。该研究发现生存率也相似。没有发现其他类似的研究。在我们的研究中，敏感性分析表明，如果可切除和局部区域患者的比例较高，R0/R1切除率较高，则普及腹腔镜检查和细胞学检查具有成本效益。由于缺乏涉及侵入性分期的类似研究，可切除和局部区域性患者的比例是通过研究仅用CT进行分期后的治疗效果得出的。

^{24, 25, 31}

这增加了我们分析的两臂的可比性，但未能捕捉到有创分期后治疗结果的任何可能变化。虽然有证据表明有创分期有可能提高根治性切除率，但很少有研究将有创分期与单纯分期 CT 进行直接比较。可切除患者和局部区域患者的侵入性分期比例越高，其成本效益就越高，成本效益分别为

38 %

和

48 %

。

Use of invasive staging may offer an improvement in median survival time of resected patients. Without thorough staging, patients with occult metastases may undergo resection and endure surgical morbidity despite no significant survival benefit.

^{5}

In a study by Oba et al.,

^{5}

patients staged with CT alone were followed after resection; those with metastases identified within 6 months of resection had significantly lower survival ( 10.1 months) than those without early disease recurrence ( 35.3 months). The authors propose rapid recurrence occurred due to the presence of radiologically undetectable metastases at resection. They suggest enhanced staging could help avoid surgery in those with occult metastases, thereby increasing average survival following resection.

^{5}

Removing individuals with occult metastases from surgical consideration also has the potential to reduce the overall cost of care by avoiding high-cost neoadjuvant therapy and surgery in patients unlikely to benefit. Earlier detection of metastases via laparoscopy with cytology may therefore increase the cost-effectiveness of care through better optimization of treatment.
采用侵入性分期可延长切除患者的中位生存时间。如果不进行彻底的分期，隐匿性转移灶患者可能会接受切除手术，尽管对生存无明显益处，但仍要忍受手术发病率。

^{5}

在Oba等人的一项研究中，

^{5}

仅用CT分期的患者在切除术后接受了随访；在切除术后6个月内发现转移灶的患者的生存期（10.1个月）明显低于没有早期疾病复发的患者（35.3个月）。作者认为，由于切除时存在放射学上无法检测到的转移灶，导致疾病迅速复发。他们认为，加强分期有助于避免对有隐匿性转移灶的患者进行手术，从而提高切除术后的平均生存率。

^{5}

将隐匿性转移灶患者从手术考虑中剔除也有可能通过避免高成本的新辅助治疗和不太可能获益的患者的手术来降低总体治疗成本。因此，通过腹腔镜和细胞学检查及早发现转移灶，可以更好地优化治疗，从而提高医疗成本效益。

Even when accounting for improved survival with R0 resection after invasive staging, our analysis found CT alone to be the preferred strategy. This could suggest a survival benefit in attempting curative therapy in patients with metastases at staging. Though NCCN guidelines suggest positive cytology is not amenable to treatment with curative intent, there may be response to chemotherapy in patients with positive cytology or disseminated peritoneal disease.

^{12, 40}

Around

24 %

of these patients could even become candidates for resection, with about

18 %

achieving an R 0 resection.

^{40}

R0 resection is unlikely in most of these patients, but even margin-positive resection may offer a survival benefit over chemotherapy alone.

^{41}

In our model, invasive staging may have shifted some patients with occult metastases from curative to definitive regimens. This may have decreased survival in the laparoscopy with cytology branch and therefore was not cost-effective. Thus, aggressive management could prolong survival for some patients who would otherwise be excluded from attempted resection by invasive staging.
即使考虑到侵入性分期后进行 R0 切除术可提高生存率，我们的分析也发现仅 CT 是首选策略。这可能表明，对分期时有转移的患者尝试根治性治疗可提高生存率。尽管NCCN指南建议细胞学阳性的患者不能接受根治性治疗，但细胞学阳性或腹膜播散性疾病患者可能对化疗有反应。

^{12, 40}

这些患者中约有

24 %

甚至可能成为切除术的候选者，约有

18 %

达到R 0切除。

^{40}

R0切除对大多数患者来说不太可能，但即使是边缘阳性切除也可能比单纯化疗带来生存获益。

^{41}

在我们的模型中，侵入性分期可能使一些有隐匿性转移的患者从根治性治疗转向确定性治疗。这可能会降低腹腔镜与细胞学检查分部的生存率，因此不具成本效益。因此，积极的治疗可延长部分患者的生存期，否则这些患者会因侵入性分期而无法尝试切除。

As diagnostic modalities and presurgical treatment algorithms change, the role of laparoscopy with cytology will continue to evolve. Some practitioners advocate use of further diagnostic imaging alongside CT, such as MRI or PET, as this may improve accuracy of staging.

^{42, 43}

While additional imaging could lower risk of occult metastasis, one meta-analysis found MRI and PET did not have higher sensitivity or specificity than CT.

^{44}

These tests are also unlikely to detect small lesions or micro-metastases.

^{4, 45}

Laparoscopy with cytology can detect these lesions more accurately than imaging modalities, and advancements in analysis of DNA or RNA within peritoneal lavage samples may further increase the prognostic information offered by this procedure.

^{46, 47}

Regardless of staging technique, though, high-potency chemotherapy is increasingly being given to all adequate candidates due to evidence of increased R0 resection rate among surgical candidates and prolonged overall survival for all patients as compared to lowerpotency regimens.

^{48}

This survival benefit has been noted even among those with metastatic disease.

^{48}

Given the significant toxicity associated with these regimens, diagnostic laparoscopy with cytology may facilitate patient-centered treatment.

^{49}

Among those with low likelihood of resectability, some may have difficulty tolerating therapies with high morbidity, while others may prioritize quality of life over prolonging survival. If found to have metastatic disease, some could opt to avoid aggressive management. In these patients, the prognostic information offered by invasive staging could allow for treatment more in line with their individual goals of care. Features which may warrant invasive staging include locally advanced disease or borderline resectable disease with further risk factors given their high risk of occult metastasis.

^{50}

Despite the morbidity associated with an invasive procedure, the improved diagnostic value over imaging techniques can guide treatment strategy in patients likely to have undetected metastasis.
随着诊断方式和术前治疗算法的改变，腹腔镜和细胞学检查的作用也将继续发展。一些从业者主张在使用CT的同时使用进一步的诊断成像，如核磁共振成像或正电子发射计算机断层扫描，因为这可以提高分期的准确性。

^{42, 43}

虽然额外的影像学检查可以降低隐匿性转移的风险，但一项荟萃分析发现，MRI和PET的敏感性和特异性并不比CT高。

^{44}

这些检查也不太可能发现小病灶或微小转移。

^{4, 45}

腹腔镜和细胞学检查能比影像学检查更准确地检测出这些病灶，腹腔灌洗液样本中DNA或RNA分析的进步可能会进一步提高该检查提供的预后信息。

^{46, 47}

不过，无论采用哪种分期技术，有证据表明，与低效化疗方案相比，手术候选者的R0切除率提高了，所有患者的总生存期也延长了，因此，高效化疗正越来越多地用于所有合适的候选者。

^{48}

甚至在转移性疾病患者中也发现了这种生存获益。

^{48}

鉴于这些治疗方案具有明显的毒性，腹腔镜诊断和细胞学检查可促进以患者为中心的治疗。

^{49}

在切除可能性较低的患者中，有些人可能难以忍受高发病率的疗法，而另一些人则可能将生活质量置于延长生存期之上。如果发现有转移性疾病，有些人可能会选择避免积极治疗。对这些患者来说，有创分期提供的预后信息可以使治疗更符合他们的个人护理目标。需要进行有创分期的特征包括局部晚期疾病或边缘可切除疾病，由于其隐匿性转移的风险较高，有进一步的风险因素。

^{50}

尽管侵入性手术会带来发病率，但与影像学技术相比，侵入性手术的诊断价值更高，可为可能存在未发现转移的患者的治疗策略提供指导。

Limitations 局限性

Our study, like all theoretical models, has limitations. Our results may not be generalizable to all patient populations due to possible variations across different institutions and regions. In addition, due to limited published studies, our analysis could not account for changes in rates of surgical candidacy and R0/R1 resection with invasive staging. Improvement in these outcomes following invasive staging could shift results of this analysis in favor of laparoscopy with cytology. Our study also could not assess the impact of imaging modalities performed alongside CT, such as MRI, or other diagnostic techniques prior to invasive staging, as there are few published articles examining these treatment algorithms. The model included studies utilizing neoadjuvant therapy consisting of gemcitabine and radiation, which is not a preferred regimen based on current NCCN guidelines.

^{12}

This was due to a lack of studies in the published literature with long follow-up time utilizing FOLFIRINOX or gemcitabine with nab-paclitaxel after laparoscopy with cytology. Our model also did not utilize high-potency definitive therapy in patients with metastatic disease. Evidence suggests FOLFIRINOX may prolong overall survival and increase R0 resection rate as compared to gemcitabine-based therapy in those able to tolerate the higher rate of adverse effects.

^{49}

Improved tumor regression with newer regimens could improve surgical candidacy and reduce benefit from invasive staging. Also, we did not conduct assessments of pancreaticoduodenectomy and distal pancreatectomy separately due to lack of probability data in the literature. In addition, our analysis did not account for levels of carbohydrate antigen 19-9 (CA 19-9), a protein blood biomarker, which can potentially be elevated in patients with pancreatic cancer. The decision to not stratify by high or low CA 19-9 levels was two-fold: due to a lack of studies in the published literature and controversy over its use as a prognostic or diagnostic factor. CA 19-9 is falsely negative in the portion of the population with a Lewis negative (

a - b, b -

) phenotype, which is approximately

6 %

of the white population and

22 %

of the black population in the United States.

^{51}

Also, CA 19-9 is not specific to pancreatic cancer as it can be elevated in the presence of hyperbilirubinemia or extra-pancreatic malignancies. For these reasons, we chose not to stratify by CA 19-9 levels although rates of positive cytology or gross findings on
与所有理论模型一样，我们的研究也有局限性。由于不同机构和地区之间可能存在差异，我们的结果可能无法推广到所有患者群体。此外，由于已发表的研究有限，我们的分析无法考虑有创分期后手术候选率和R0/R1切除率的变化。有创分期后这些结果的改善可能会使本分析结果更倾向于腹腔镜和细胞学检查。我们的研究也无法评估与 CT 同时进行的成像模式（如 MRI）或有创分期前的其他诊断技术的影响，因为很少有已发表的文章对这些治疗算法进行研究。该模型包括使用吉西他滨和放射治疗的新辅助治疗研究，而根据目前的NCCN指南，这并不是首选方案。

^{12}

这是因为在已发表的文献中，缺乏在腹腔镜细胞学检查后使用FOLFIRINOX或吉西他滨联合纳布紫杉醇进行长时间随访的研究。我们的模型也没有在转移性疾病患者中使用高效力的确定性疗法。有证据表明，与吉西他滨为基础的疗法相比，FOLFIRINOX可延长总生存期并提高R0切除率，但前提是患者能够耐受较高的不良反应发生率。

^{49}

更新的治疗方案可改善肿瘤消退情况，从而提高手术治疗的可选性，并减少侵袭性分期的获益。此外，由于缺乏文献中的概率数据，我们没有对胰十二指肠切除术和胰腺远端切除术进行单独评估。此外，我们的分析没有考虑碳水化合物抗原 19-9（CA 19-9）的水平，这是一种蛋白质血液生物标志物，在胰腺癌患者中可能会升高。不按CA 19-9水平高低进行分层的决定有两个原因：一是已发表的文献中缺乏相关研究，二是将其作为预后或诊断因素存在争议。在美国，表型为Lewis阴性（

a - b, b -

）的人群中，CA 19-9为假阴性，这部分人群约占白人人口的

6 %

和黑人人口的

22 %

。

^{51}

此外，CA 19-9并非胰腺癌的特异性指标，因为它在高胆红素血症或胰腺外恶性肿瘤时也会升高。由于这些原因，尽管细胞学检查或大体检查结果阳性率较高，但我们选择不按CA 19-9水平进行分层。
laparoscopy may be higher in patients with elevated levels.

^{7}

Another analysis should be run to determine the efficacy of utilizing CA 19-9 levels to predict peritoneal metastases.

^{7}

CA 19-9水平升高的患者接受腹腔镜检查的风险可能更高。

^{7}

应进行另一项分析，以确定利用CA 19-9水平预测腹膜转移的效果。

Conclusions 结论

The addition of universal diagnostic laparoscopy with cytology for pancreatic cancer staging prior to neoadjuvant therapy can increase the detection of metastatic lesions but may not be cost-effective if done for all patients. However, patient populations with a high risk of occult metastasis may benefit. Individual goals of care may also guide the decision to perform invasive staging. Further study is required to assess changes in clinical outcomes associated with laparoscopy and cytology and the effect of preferred neoadjuvant chemotherapy regimens to determine which patients would most benefit from invasive staging.
在新辅助治疗前对胰腺癌分期增加腹腔镜细胞学诊断可提高转移病灶的检出率，但如果对所有患者都进行腹腔镜检查，可能并不划算。不过，隐匿性转移风险较高的患者群体可能会从中受益。个人的治疗目标也可指导是否进行有创分期。需要进一步研究评估与腹腔镜检查和细胞学检查相关的临床结果变化，以及首选新辅助化疗方案的效果，以确定哪些患者最受益于有创分期。

Presentation 介绍

Poster presented at the Pancreas Club Annual Meeting on May 20-21, 2022 in San Diego, CA.
在 2022 年 5 月 20-21 日于加利福尼亚州圣地亚哥举行的胰腺俱乐部年会上发表的海报。

Author Contributions 作者供稿

MJ, NSP, RT, VP, SA, and RJC contributed to the conception and design, acquisition of data, analysis, and interpretation of data, editing, and final approval. MJ, NSP, VP, and SA contributed to the drafting of the article. The revision of the article was performed by SA and RJC.
MJ、NSP、RT、VP、SA 和 RJC 参与了文章的构思和设计、数据采集、分析和解释、编辑以及最终审批。MJ、NSP、VP和SA参与了文章的起草。SA和RJC对文章进行了修改。

Declaration of Competing Interest
竞争利益声明

All authors (MJ, NSP, RT, VP, SA, RJC) have no conflicts of interest or financial ties to disclose.
所有作者（MJ、NSP、RT、VP、SA、RJC）均无利益冲突或经济关系需要披露。

Acknowledgments 致谢

We thank Dr. Patrick L Quinn for assistance in designing the conceptual framework of our model.
我们感谢 Patrick L Quinn 博士在设计模型概念框架时提供的帮助。

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From the $^{a}$ Division of Surgical Oncology, Department of Surgery, Rutgers New Jersey Medical School, Newark, NJ;
来自新泽西州纽瓦克市罗格斯新泽西医学院外科系肿瘤外科；
$^{b}$ Rutgers New Jersey Medical School, Newark, NJ; and $^{c}$ Department of Medicine, The Ohio State University College of Medicine, Columbus, OH
$^{b}$ 罗格斯新泽西医学院，新泽西州纽瓦克市； $^{c}$ 俄亥俄州立大学医学院医学系，俄亥俄州哥伦布市
Funding: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.
资金来源：本研究未从公共、商业或非营利部门的资助机构获得任何专项拨款。
- Address reprint requests to: Ravi J. Chokshi, MD, MPH, FACS, Division of Surgical Oncology, Department of Surgery, Rutgers New Jersey Medical School, 205 South Orange Ave, F1222, Newark, NJ 07103.
  转载请联系Ravi J. Chokshi, MD, MPH, FACS, Division of Surgical Oncology, Department of Surgery, Rutgers New Jersey Medical School, 205 South Orange Ave, F1222, Newark, NJ 07103.
E-mail address: chokshrj@njms.rutgers.edu (R.J. Chokshi).
电子邮件地址：chokshrj@njms.rutgers.edu (R.J. Chokshi)。
Abbreviations: CT, computed tomography. R0, margin-negative.
缩写：CT：计算机断层扫描。R0：边缘阴性。
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Cost-effectiveness of staging laparoscopy with peritoneal cytology in pancreatic adenocarcinoma 胰腺腺癌分期腹腔镜检查和腹腔细胞学检查的成本效益