Usefulness of selective arterial calcium injection tests for functional pancreatic neuroendocrine tumors

ABSTRACT The selective arterial calcium injection (SACI) test is useful for patients with functional pancreatic neuroendocrine tumors (F-PNETs). This study evaluated which patients with

F-PNETs would benefit from the SACI test. We retrospectively analyzed the preoperative findings of patients on computed tomography (CT), magnetic resonance imaging (MRI), CT angiography

(CTA), and the SACI test. Fourteen patients who underwent pancreatectomy between January 1997 and September 2016 for F-PNETs were evaluated. We classified these patients into groups A, B,

and C; group A, one tumor detected by either CT or MRI; group B, multiple tumors detected; and group C, the tumor location was accordant on CT, MRI, and CTA, but the SACI test revealed

another tumor. In group A, the tumor was also detected by CTA and the SACI test was positive on calcium injection. In group B, the focus tumor among the multiple tumors was detected by the

SACI test. In group C, another tumor was identified by the SACI test, whose location was different from that detected using CT and MRI. The SACI test is more useful for multiple F-PNETs on

CT or MRI. If CT or MRI detects a single tumor, the SACI test or CTA may be unnecessary. SIMILAR CONTENT BEING VIEWED BY OTHERS USEFULNESS OF ENDOSCOPIC ULTRASONOGRAPHY FOR DIFFERENTIATING

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Article Open access 16 September 2022 INTRODUCTION The use of the selective arterial calcium injection (SACI) test has resulted in the increased performance of curative resection surgery for

patients with functional pancreatic neuroendocrine tumors (F-PNETs), such as insulinomas and gastrinomas1,2. In 1991, Doppman et al.2 reported a method of localizing insulinomas using 0.025

 mEq/kg calcium gluconate as the secretagogue. Moreover, the SACI test has a high diagnostic performance for the accurate localization of F-PNETs for curative resection when F-PNETs such as

insulinomas and gastrinomas are usually small, solitary, and intrapancreatic3,4,5. Other imaging studies, such as computed tomography (CT), magnetic resonance imaging (MRI), and CT

angiography (CTA), can also be used to visualize endocrine tumors as hypervascular tumors surrounding pancreatoduodenal lesions. Although the specificity and sensitivity of these methods are

both less than 70–80% for pancreatic tumors6, CT is the initial modality of choice to evaluate pancreatic lesions while MRI has a major role in pancreatic tumor characterization7. In

contrast, compared to CT or MRI, the SACI test and CTA are relatively invasive examinations for patients with F-PNETs; therefore, these invasive examinations should not be performed if

possible. Moreover, it is unclear which patients with F-PNETs would benefit from the SACI test, and only a few studies have determined the value of the SACI test compared to preoperative

findings of CT, MRI, and CTA5,8. Therefore, in this study, we aimed to investigate the preoperative findings of the SACI test, CT, MRI, and CTA, and to determine the type of patients with

F-PNETs in whom the SACI test would be very effective. PATIENTS AND METHODS PATIENTS Patients who underwent the SACI test and curative pancreatectomy for F-PNETs at our institution between

January 1997 and September 2016 were retrospectively reviewed. All patients were histologically confirmed as having F-PNETs such as insulinomas or gastrinomas. Along with the SACI test, all

patients underwent other preoperative tumor localization procedures such as dynamic CT, dynamic MRI, and CTA. The results of the SACI test were compared with the findings on these

procedures, as well as the surgical and pathological results. We conducted this retrospective study using the “opt-out” method of our hospital. The study was approved by the Ethics Committee

of Keio University School of Medicine, which waived the need of informed consent for our study, and conducted in accordance with the Helsinki Declaration of 1975. THE SACI TEST Before

angiography, a 5-Fr shepherd hook catheter (Hanako Medical, Terumo, Japan) was placed in the right or middle hepatic vein through the right femoral vein. In addition, a 5-Fr catheter was

placed in the celiac artery and superior mesenteric artery [SMA] through the right femoral artery followed by insertion of a microcatheter (Progreat ∑, Terumo, Japan) into an artery feeding

the pancreas (e.g., the common hepatic artery [CHA], gastroduodenal artery [GDA], splenic artery [SPA], distal pancreatic artery [DPA], or inferior pancreaticoduodenal artery [IPDA]).

Calcium gluconate at a dose of 0.025 mEq/kg was diluted to a 4 mL bolus, and injected rapidly into each artery. Blood samples for insulin or gastrin were obtained from the right hepatic vein

at 30, 60, 90, 120, and 150 or 180 s after the calcium injection. The results were considered positive for an insulinoma if the maximum increase in serum levels of immunoreactive insulin

(IRI) was twice at 30–60 s compared to the basal serum IRI level2. In contrast, for gastrinomas, the results were considered positive when serum levels of immunoreactive gastrin (IRG) were 

> 80 pg/ml at 40 s after the calcium injection9, and IRG was > 20% above the basal serum IRG at 40 s after the calcium injection9. When a positive response was observed in the SPA and

DPA, the tumor was considered to be localized to the body or tail of the pancreas; when it was identified in the CHA, SMA, GDA, and IPDA, the tumor was considered localized to the pancreatic

head (Fig. 1). SURGICAL RESECTION AND PATHOLOGY Surgical procedures included enucleation, partial pancreatectomy, laparoscopic or open distal pancreatectomy, and pancreaticoduodenectomy.

Pathological staging was performed according to the Union for International Cancer Control Tumor-Node-Metastasis (UICC-TNM) Classification of Malignant Tumors (8th edition), and tumors were

classified as PanNET G1, PanNET G2, PanNET G3, and PanNEC (G3) according to the 4th edition of the WHO Classification of Tumors of Endocrine Organs. Immunostaining was performed for

chromogranin A, synaptophysin, CD56, insulin, gastrin, somatostatin, glucagon, and pancreatic polypeptide. Moreover, pancreatic neuroendocrine microadenomas, which are benign non-functioning

 neuroendocrine tumors < 0.5 cm with a low proliferation rate, were also counted. POSTOPERATIVE ASSESSMENT AND FOLLOW-UP We evaluated the postoperative symptoms and the IRI or IRG levels,

and all the patients were followed-up at 1, 3, 6, and 12 months after surgery. Patients also underwent semiannual reviews. In addition, clinical examinations, laboratory investigations, and

abdominal computed tomography (to detect tumor recurrence) were performed. INFORMED CONSENT STATEMENT Patients were not required to give informed consent to the study because the analysis

used anonymous clinical data that were obtained after each patient agreed to treatment by written consent. This statement was approved by the Human Experimentation Committee of Keio

University School of Medicine. RESULTS DEMOGRAPHIC AND PERIOPERATIVE CHARACTERISTICS A total of 14 patients underwent the SACI test and curative resection for F-PNETs between January 1997

and September 2016. The patient characteristics are summarized in Table 1. There were 7 men and 7 women, with a median age of 55 years (range, 18–75 years). The most common clinical

presentations were hypoglycemia (n = 11, 78.6%), followed by melena (n = 1, 7.1%) and elevation in glycated hemoglobin levels (n = 1, 7.1%); 1 patient (7.1%) was asymptomatic. The diagnosis

was insulinoma in 11 patients (78.6%) and gastrinoma in 3 (21.4%). Five patients (35.7%) underwent open or laparoscopic distal pancreatectomy, 4 (35.7%) underwent partial pancreatectomy, 4

(35.7%) underwent open or laparoscopic enucleation, and 1 (7.1%) underwent pancreaticoduodenectomy. Three patients (no. 3, 4, and 7; 21.4%) were diagnosed with multiple endocrine neoplasia

type 1 (MEN-I). After surgery, all patients showed no symptoms, and the levels of IRI and IRG improved. Patient no. 4 had bone metastasis as well as metastases in the lymph nodes of the

aorta; the patient died approximately 5 years after surgery. The results of preoperative imaging studies in 14 patients (dynamic CT, MRI, CTA, and the SACI test) are shown in Table 2. The

detection rate of F-PNET was 78.6% for CT, 91.7% for MRI, 100% for CT and MRI, and 100% for CTA. We classified these patients into groups A, B, and C; group A, one tumor detected by either

CT or MRI; group B, multiple tumors detected; and group C, the tumor location was accordant on CT, MRI, and CTA, but the SACI test revealed another tumor. In group A consisting of patient

no. 1, 2, 5, 6, 8, 9, 10, 11, 12, and 13, the tumor was also detected by CTA and the SACI test was positive on calcium injection. In group B consisting of patient no. 3, 4, and 7, the focus

tumor among the multiple tumors was detected by the SACI test. Moreover, all patients in group B had MEN-I. In group C consisting of patient no. 14, another tumor was identified by the SACI

test, whose location was different from that detected using CT, MRI, and CTA. PATHOLOGICAL FINDINGS The pathological findings of the tumors are shown in Table 3. The UICC stage was 1A in 10

patients (71.4%) and 1B in 4 (28.6%), and PanNET G1 was detected in 9 patients (64.3%) and PanNET G2 in 5 (35.7%). Patients in group B had a tendency of having pancreatic neuroendocrine

microadenomas. DISCUSSION The study findings demonstrated that the SACI test should be performed when multiple tumors are detected on CT or MRI with inheritable characteristics such as

MEN-I; this will help in localizing the causative tumor among multiple tumors as well as in deciding the indications for the extent of surgery to resect the tumors in the pancreas. However,

the SACI test or CTA should not be performed if a single tumor is detected via CT and MRI because the SACI test is relatively invasive compared to CT or MRI. Nevertheless, we need to be

careful about false-positive results or occult tumors, such as those observed in no. 14 in which the tumor location revealed on the SACI test differed from that detected on CT and MRI.

According to international guidelines such as the European Neuroendocrine Tumor Society (ENETS)10, the North American Neuroendocrine Tumor Society (NANETS)11 and the National Comprehensive

Cancer Network (NCCN)12, the SACI tests should be considered in patients with F-PNETs when other imaging tests, such as CT or MRI, are equivocal or negative. Furthermore, most experts

recommend this test only for patients with persistent or recurrent insulin-mediated hypoglycemia. According to the ENETS guideline10, the SACI tests should be performed in patients with

multiple lesions or MEN-I, and excision should be performed based on the results of the SACI tests. Our results were consistent with the ENETS guideline, but not other guidelines. Therefore,

this study supported the adaptation of the SACI tests mentioned in the ENETS consensus guidelines. The SACI test is a method for the identification and differentiation of insulinomas or

gastrinomas among multiple NETs that are essentially impossible to identify on imaging techniques alone, and it is useful for planning the surgical strategy preoperatively3,4,5. In patient

no. 3 and 7 in group B, the SACI test revealed accurate localization among multiple NETs, and we performed the surgical procedure according to the result of the SACI test. However, in no. 4

in group B, although the SACI test revealed the tumor in the pancreatic head, we performed distal pancreatectomy and not pancreaticoduodenectomy. Although we planned pancreaticoduodenectomy

and enucleation for the tumor in the pancreatic body in no. 4 preoperatively, there was a main pancreatic duct injury while performing enucleation. We could not perform total pancreatectomy

per the patient’s wishes, so we had no choice but to perform distal pancreatectomy. However, fortunately, the symptoms of hypercalcemia and postoperative IRI improved after surgery;

therefore, we suspected that the tumor in patient no. 4 was in the pancreatic body, and that the SACI test did not always reveal the correct localization. In fact, Doppman et al.2 found that

elevated hepatic venous insulin levels were not always correlated with the correct localization: unequivocal localization was reported in only 5 of 9 patients (56%) but a gradient in venous

insulin levels was observed in all 9 patients. EUS plays a specific role in PNETs, but the necessity of EUS is a little different according to the international guidelines from ENETS10,

NANETS11, and NCCN12. These guidelines recommended that EUS can be used as appropriate if there are equivocal CT or MRI findings, or if the tumors were not detected by them. Furthermore, EUS

is recommended if pancreatic resection is considered for assessing and localizing tumors preoperatively. The NANETS guideline11 suggested that EUS should be performed when there is a

question of multifocality, such as in patients with MEN1, and EUS can be useful when some F-PNETs are too small to be imaged with CT or MRI. EUS-FNA can also be considered to confirm the

diagnosis and tumor grade, although tumor heterogeneity may preclude accurate assessment; thus, EUS or EUS-FNA can also be considered as additional imaging tools instead of CT or MRI in the

above specific situations11. Recently various studies10,11,12,13,14 have reported that positron emission tomography with CT (PET/CT) with 68 Ga-labeled somatostatin analogues (68 Ga-PET/CT)

has the highest sensitivity for localizing not also NF-PNETs but also FP-NETs, and is also a cornerstone tool for both diagnosis and staging for PNETs. The sensitivity varies from 86–100%,

and the specificity from 79–100% for all p-NETs. Thus, the SACI test, which is relatively invasive, could be omitted in patients with F-PNETs, especially those with gastrinomas. Furthermore,

international guidelines10,11,12 have recommended 68 Ga-PET/CT as the first-line diagnostic imaging method for staging in patients with gastrinoma. However, 68 Ga-PET/CT is not useful for

insulinoma. Shorma P et al. revealed that its sensitivity is only 25%11. Although the adaptation and usefulness of the SACI test has been limited because other non-invasive functional

imaging techniques, such as 68 Ga-PET/CT, are being used instead to determine surgical planning, staging, and medical management, the SACI tests for insulinoma may still useful under special

conditions for patients with FP-NETs (especially insulinoma) with multiple lesions or patients with MEN-I where CT or MRI are equivocal or negative. If F-PNETs are not detected on

preoperative imaging studies, i.e. if they are “occult tumors,” blind distal, subtotal, or total pancreatectomy is now obsolete. These blind pancreatic resections are no longer indicated and

should not be performed because of their short-term (e.g., pancreatitis, pancreatic fistula, and pancreatic abscess) and long-term morbidities (e.g., exocrine pancreatic insufficiency and

diabetes mellitus)6,15. Indications for occult insulinomas and gastrinomas have been reported in ENTES or NCCN guidelines10,12. First, for occult insulinoma, observation and surgical

exploration are options for occult tumors. Few studies have advocate intraoperative localization through palpation, and the addition of intraoperative ultrasound may be more sensitive than

invasive preoperative methods1,16,17. Second, for gastrinomas, exploratory surgery including duodenotomy or local resection/enucleation of tumors, periduodenal node dissection, and

intraoperative ultrasound have been considered in a previous report12. In patient no. 14 in group C, the tumor location revealed on the SACI test was different from the location observed on

CT, MRI, and CTA. Based on the result of the SACI test, the tumor might have been located in the pancreatic head although the tumor was not detected on CT, MRI, and CTA; therefore, the tumor

might have been an occult tumor. Another alternative could be that the result of the SACI test might have been a false-positive result and that there was no tumor there. After we informed

the patient of these two possibilities, we performed distal pancreatectomy, instead of blind pancreaticoduodenectomy, considering the postoperative surgical complications. Although we

performed intraoperative ultrasonography for the pancreatic head, a tumor was not detected. In addition, during the semiannual clinical examinations, laboratory investigations, and abdominal

computed tomography, a new tumor was not detected in the remnant pancreas and the IRG level decrease to 170 pg/ml. Therefore, in this case, we suspect that the result of the SACI test might

be a false-positive result and that there was no tumor at that location. According to the NCCN guidelines12, we may consider exploratory surgery including intraoperative ultrasound in the

future for patient #14 in our study if the patient’s IRG level continue to increase. We suggest that the SACI test and CTA do not need to be performed if a single tumor is detected on CT and

MRI. The preoperative detection rates of CT and MRI for PNETs depended on the patient age and type of study7,18,19, although the development in the technology of scanners has resulted in a

marked improvement in the sensitivity of CT and MRI6,7. In this study, the detection rate of F-PNETs was 100% for a combination of dynamic CT and MRI, and if a single tumor was observed, the

SACI test was not necessary for checking the localization of the single tumor to administer the calcium injection because we should not perform blind pancreatectomy for occult PNETs. CTA,

an invasive localization modality, is considered the “gold standard” for tumor detection, and the detection rates varied from 29 to 100% depending on the experience of the operator and the

center6,9,20,21. In our institution, CTA has often been performed for not only F-PNETs but also NF-PNETs, and as shown in Table 2, CTA may be useful to detect multiple small tumors with

hereditary disease, such as MEN-I. This study has a few limitations. First, this was a retrospective study conducted at a single institution with a relatively small number of patients.

However, as the number of patients with F-PNETs is small and most previous studies were case series22,23,24, a multi-center study with many patients is needed to further evaluate the

usefulness of the SACI test. Second, the time span of this study (from 1997 and 2016) is very long considering the technical improvements of both CT and MRI. In this study, two patients

underwent surgery in 1997 and 1999, and 12 patients had undergone pancreatic surgery since 2007, in which multi-detector row CT or dynamic MRI had a mechanical efficacy similar to the recent

CT or MRI technology. Although we considered excluding these two patients, there are only a few patients that undergo the SACI tests and this study already had a small number of patients;

thus, we included these two patients and the time span became long. Finally, among 14 patients, 8 patients (57.1%) underwent EUS10,11,12,25, 4 (28.6%) underwent 18F-FDG PET/CT26, and 2

(14.3%) underwent somatostatin receptor scintigraphy (SRS)27. We have been performing EUS on patients with pancreatic neuroendocrine tumors (PNETs) since 2007, and now we perform EUS more

actively in most patients with PNETs, future prospective research studies are needed to confirm and evaluate these preliminary findings, by including EUS, 18F-FDG PET/CT, and 68 Ga-PET/CT,

all of which are useful to evaluate the location of PNETs. In conclusion, the SACI test should be performed for F-PNETS with multiple tumors detected on CT or MRI, especially for those with

inheritable characteristics such as MEN-I. This will help in determining the tumor localization among multiple tumors and deciding the appropriate surgical method for the treatment of the

multiple tumors in the pancreas. Moreover, the SACI test or CTA should not be performed if a single tumor is detected via CT and MRI, because we should not perform blind pancreatectomy

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13–20 (2017). Article  CAS  Google Scholar  Download references ACKNOWLEDGEMENTS We wish like to thank Editage (www.editage.jp) for English language editing. FUNDING The authors declare no

source of funding. AUTHOR INFORMATION AUTHORS AND AFFILIATIONS * Department of Surgery, Keio University School of Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo, 160-8582, Japan Yutaka

Nakano, Minoru Kitago, Masahiro Shinoda, Hiroshi Yagi, Yuta Abe, Go Oshima, Shutaro Hori, Takahiro Yokose & Yuko Kitagawa * Department of Diagnostic Radiology, Keio University School of

Medicine, 35 Shinanomachi, Shinjuku-ku, Tokyo, 160-8582, Japan Seishi Nakatsuka * Department of Nephrology, Endocrinology and Metabolism, Keio University School of Medicine, 35 Shinanomachi,

Shinjuku-ku, Tokyo, 160-8582, Japan Isao Kurihara Authors * Yutaka Nakano View author publications You can also search for this author inPubMed Google Scholar * Minoru Kitago View author

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for this author inPubMed Google Scholar CONTRIBUTIONS All authors helped conduct the research; N.Y. manuscript writing and data analysis; K.M., S.M., Y.H., A.Y., O.G. and H.S. data analysis;

N.S., K.I., Y.T. and K.Y. data analysis, drafting conception, and design; All authors read and approved the final manuscript. CORRESPONDING AUTHOR Correspondence to Minoru Kitago. ETHICS

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calcium injection tests for functional pancreatic neuroendocrine tumors. _Sci Rep_ 11, 235 (2021). https://doi.org/10.1038/s41598-020-80538-0 Download citation * Received: 03 May 2020 *

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