Revisión histórico - narrativa del ALPPS

Oliver Guillén, José R.; Ramia Ángel, José M.; Serradilla Martín, Mario; Oliver Guillén, José R.; Ramia Ángel, José M.; Serradilla Martín, Mario

doi:10.25132/raac.v113.n1.1510.ei

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Revista argentina de cirugía

versión On-line ISSN 2250-639X

Rev. argent. cir. vol.113 no.1 Cap. Fed. abr. 2021

http://dx.doi.org/10.25132/raac.v113.n1.1510.ei

Articles

ALPPS: a historical review

José R. Oliver Guillén¹^*

José M. Ramia Ángel²

Mario Serradilla Martín¹

^¹ Instituto de Investiga ción Sanitaria Aragón, Servicio de Cirugía General y del Aparato Digestivo, Hospital Uni versitario Miguel Servet, Zaragoza, España.

^² Servicio de Cirugía General y del Aparato Digestivo, Hospital Universitario de Guadalajara, Guadalajara, España

Introduction

The current associating liver partition and portal vein ligation for staged hepatectomy (ALPPS) procedure has represented breakthrough in the field of hepato-pancreato-biliary (HPB) surgery¹^,².

Surgery remains the only curative option for malignant liver tumors. Large liver resections are commonly required to achieve clear surgical margins. Thus, an adequate volume and future liver remnant (FLR) is mandatory, as posthepatectomy liver failure (PHLF) is one the main causes of morbidity and mortality after extensive liver resections³^,⁴. Classically, at least two anatomically contiguous liver segments had to be preserved, representing a critical minimum FLR of 20-25%⁴^,⁵, and of 40% in the presence of chronic liver disease. ALPPS broke this paradigm⁴^,⁵.

Material and methods

We conducted a bibliographic search in PubMed using the term “ALPPS”, and a clustering approach selecting the articles by their relevance and historical influence on the technique.

Techniques for liver regeneration before ALPPS

Over the past decades, two methods have been developed to induce hypertrophy of the FLR: portal vein occlusion (PVO) through embolization (PVE) or ligation (PVL) and two-stage hepatectomy (TSH)⁶; both methods are usually used in association. PVE is currently the gold standard method. In the eighties, Makuuchi⁷ introduced this new concept: right PVE to induce hypertrophy of the left liver lobe to safely resect large or multiple tumors. However, hypertrophy of the FLR is not always sufficient resulting in PHLF. Even more, the disease may accelerate in some patients after PVE^4, ⁸. Up to 40% of the patients are not candidates for surgery for these reasons⁴^,⁹.

Two-stage hepatectomy was described by Adam et al.10 in 2000 to treat patients with bilobar involvement due colorectal liver metastases (CRLM) initially unresectable. During first-stage hepatectomy the greatest number of metastases are resected, and after a period of hypertrophy of the FLR and systemic chemotherapy, the second hepatectomy can be carried out as a curative intent procedure. Morbidity is between 49% and 59% and mortality ranges between 6.4% and 8.8%⁴. Complete resection is not achieved in about 25% of the patients¹¹.

First procedures of portal vein ligation and liver partition

In 2007, Hans Schlitt performed the technique that was later known as ALPPS for the first time in a patient with Bismuth type IV hilar cholangiocarcinoma. The first report was a case series of three patients presented by Lang at the 9th congress of the E-AHPBA (European-African Hepato-Pancreato-Biliary Association) in Cape Town, South Africa, in 2011, which generated significant excitement and controversy¹².

In 2011, Alvarez et al.¹³ published a new technique for liver regeneration performed on a patient with colorectal cancer and initially unresectable liver metastases: left hemicolectomy, cleaning of the metastases in the left liver and in situ liver split with right PVL. The procedure also included ligation of the right bile duct, a gesture that was later associated with increased risk of bile leak¹⁴. They described a 40% increase of the FLR on postoperative day 6 and completed the right liver resection on day 7; the patient was discharged 11 days later.

In 2012, Schnitzbauer et al.⁵ published a retrospective review of 25 cases, mostly of CRLM, treated between 2007 and 2011 with a 2-step technique. In the first step, right portal vein ligation and in situ splitting of the liver parenchyma along the falciform ligament were performed. The right lobe was covered in a plastic bag to prevent adhesions. After a median interval of 9 days (range: 5-28 days), hypertrophy of about 75% of the left liver lobe was induced and volumetry was performed. In the second step, patients underwent right trisectorectomy (Fig. 1).

Figure 1 Initial ALPPS technique. Top, left (first stage): liver tumors mainly in the right liver. Right portal vein ligation. Top, right (first stage): in situ split of the right liver in plastic bag; a suture is placed to tag the right hilum. Bottom, left (second stage): li gation of the right hepatic hilum and right hepatic vien. Bottom, right (second stage): fi nal result, with hypertrophy of the FLR.

Sixty-four percent of the patients presented complications. Of the 50 complications documented, 22 (44%) were classified as grade III or IV of the Clavien- Dindo classification. Mortality rate was 12%.

The technique was initially described as “2-staged extended right hepatectomy with initial surgical exploration, right PVL, and in situ splitting”. In 2012, de Santibañes and Clavien⁵ proposed the acronym “ALPPS” to describe this novel approach (Table 1).

Table 1 Chronology of ALPPS

Expansion and international registry

The approach aroused considerable interest16, and an international registry created in 2012 recruited more than 1200 cases¹⁷. The registry contributed to monitoring the results, improving patient selection and analyzing complications and their possible solutions.

The first report published data of 202 patients retrieved from the registry until January 2014¹⁸. Overall survival (OS) at 1 and 2 years was 73% and 59%, respectively, and disease-free survival (DFS) was 60% and 42%, respectively, with mean survival rate of 24 months. Mortality at 90 days was 9%. Predictors for severe complications were primary liver tumors, age > 60 years, need for intraoperative red blood cell transfusions and operative time > 5 hours. Patients with cholangiocarcinoma and gallbladder cancer had worse outcomes¹⁸, probably due to the high rate of biliary complications⁴.

The registry was also useful to analyze the indications of ALPPS¹⁹. Records from 2012 to 2017 were screened, considering that patients with a remnant liver to body weight ratio ≥ 0.5% in healthy livers and ≥ 0.8% in case of liver damage could undergo one-stage hepatectomy, and thus, a right liver resection could have avoided such additional risk. The authors concluded that about one third of patients undergoing ALPPS did not fulfill the criteria. This article has reopened the debate that emerged from the beginning, since many authors consider that ALPPS has almost become a fashion that has increased its misuse and should be understood as another option available for surgeons²⁰.

Modifications of the original technique

Many technical variations of ALPPS have been described since the initial description:

▪▪Minimally invasive surgery (MIS) for ALPPS. In 2012, Machado et al.²¹ performed the first laparoscopic ALPPS, and Vivent at al.²² published the first robotic ALPPS in 2016 The systematic review by Melandro et al.²³ included 27 patients undergoing MIS-ALPPS using a laparoscopic or robotic approach; 15.4% of the patients presented grade III complications, and no deaths were reported. In their review, Michal et al.²⁴ compared 46 patients undergoing MIS-ALPPS versus 1088 treated with open surgery. Operative parameters (time and blood loss) did not differ between the two groups. Open ALPPS patients had a more diverse profile of underlying comorbidities, more right extended hepatectomies, and higher rate of severe complications and mortality. In conclusion, there is still limited evidence.

▪▪Tourniquet-ALPPS (ALTPS). The procedure, described by Roblesetal.²⁵ in 2012, consists of right portal vein ligation and applying a tourniquet on the transection line, accelerating hypertrophy, and achieving efficient regeneration with acceptable morbidity and mortality rates²⁶.

▪▪Modified ALTPS²⁷. The technique was designed for perihilar tumors requiring a “non-touch” technique to avoid left portal ligation; right PVE is performed on postoperative day 4.

▪▪Monosegment ALPPS. In 2015, Montalvá Oron et al.²⁸ and Schadde et al.⁶ published a case series of monosegment ALPPS in 8 and 12 patients, respectively. In the first case series, morbidity was 50%, mortality 25% and disease recurrence was 100%, with median DFS of 155 days ²⁸. In the second series, there were no deaths and 33.3% of the patients presented grade III complications, while disease recurrence was 50% after 14-month follow-up⁶.

▪▪RALPP (radiofrequency-assisted ALPPS). The approach published by Gall et al.29 in 2015 is through laparoscopic ALPPS with the use of radiofrequency ablation (RFA) to create a line of necrosis through the future transection line. This technique stops blood flow from the FLR to the contralateral liver while inducing hypertrophy of the FLR without a physical partition of the parenchyma.

▪▪LAPS (laparoscopic microwave ablation and portal vein ligation for staged hepatectomy). Gringeri et al.³⁰ described this technique in 2015, which is similar to RFA but uses microwave ablation for liver partition.

▪▪Mini-ALPPS. In 2016, de Santibañes et al.¹ suggested that partial parenchymal transection combined with intraoperative portal vein embolization (up to the middle hepatic vein) minimized the impact of the first stage and improved recovery compared with complete liver partition (up to the inferior vena cava). There were no serious complications and an adequate FLR was achieved⁴.

▪▪PALPP (percutaneous microwave ablation liver partition and portal vein embolization). De Hong et al.³¹ published the use of percutaneous liver partition using microwave ablation in 2016.

▪▪Hybrid-ALPPS32: Li. et al.³² described this technique in 2016 for tumors with infiltration to the right portal vein in which portal vein ligation is not feasible. They performed a “non-touch” technique with in-situ split using anterior approach, right PVE through interventional radiology (even through the ileocolic vein) without touching the hepatoduodenal ligament and the right liver, and finally completing 2-stage hepatectomy with transection of the portal bifurcation.

▪▪TIPE_ALPPS (transileocecal portal embolization): Sakamoto et al.³³ documented this technique in 2016. Portal vein embolization is performed via the ileocecal vein avoiding the hepatoduodenal ligament with partial partition of the liver along the Rex-Cantlie line.

▪▪PRALPPS (percutaneous radiofrequency-assisted liver partition): this technique was described in a case-control study by Melekhina et al.³⁴ in 2020 in patients with perihilar cholangiocarcinoma. The first stage of PRALPPS included percutaneous embolization of the right portal vein guided by ultrasonography and RFA along the right side of the middle hepatic vein under general anesthesia. Thermal ablation involved around 50% of the future transection plane, retaining a minimum distance of 2 cm from the hilar plate to avoid injury.

Because many variants of the ALPPS procedure emerged, Linecker et al.² proposed the development of a consensus terminology: Rescue-ALPPS (ALPPS after failure of PVE to induce hypertrophy), laparoscopic ALPPS (use of laparoscopy in any stage), PVE-ALPPS (use of PVE as part of the first stage), partial ALPPS (used for incomplete transection: ALTPS, RALPP and LAPS) or monosegment ALPPS.

Expert meetings

First International Expert Meeting

The first expert meeting on ALPPS was held in Hamburg, Germany, in 2015¹⁶. The meeting produced eight recommendations:

▪▪Knowledge of individual hepatic anatomy is crucial. All efforts should be made to preserve arterial inflow and venous drainage of the “deportalized” part of the liver. Every unnecessary manipulation of the hilum should be strictly avoided.

▪▪No technical variation of the transection technique can currently be recommended as superior.

▪▪A cholangiogram can simplify visualizing biliary tree anatomy and possible bile leaks. Tagging anatomical structures can be performed to facilitate stage 2.

▪▪The first liver volumetry should be done on days 8 to 10 and repeated weekly for 4 weeks if FLR is insufficient.

▪▪CRLM is the main indication. Caution is called to use ALPPS for hepatocellular carcinoma (HCC) and cholangiocarcinoma, in view of the associated higher morbidity and mortality.

▪▪ALPPS is a viable option in cases with very small FLR or bilobar lesions, as drop-out rates seem to be lower compared with PVE or TSH. A ‘‘rescue’’ ALPPS procedure can be feasible in these cases.

▪▪With MELD score >10, step 2 should be postponed. Age > 60 years is associated with higher risk of poor outcomes and may justify longer intervals between both stages.

▪▪ALPPS in CRLM should only be performed after neoadjuvant systemic therapy. Tumor progression on chemotherapy is a contraindication for ALPPS. In case of synchronous colorectal liver tumors, the liver-first approach can be a good option. Caution is given to balance performing simultaneous procedures in liver and bowel.

The “10th anniversary of ALPPS” expert meeting

The 10th anniversary of ALPPS was celebrated during the 12th congress of the E-AHPBA (Mainz, Germany, 2017) at an expert meeting to advance in establishing clear indications, selection of patients and standardization of the surgical technique³⁵. The main conclusions of the meeting are:

▪▪New technical modifications, minimizing the extensiveness of the first-stage procedure, are associated with significant improvements in safety.

▪▪The degree of FLR hypertrophy in fibrotic/cirrhotic livers appears somewhat less substantial than in noncirrhotic livers.

▪▪Resection rates are higher with ALPPS compared with TSH, with similar perioperative morbidity and mortality.

▪▪ALPPS is effective after failure of portal vein embolization.

Current situation of ALPPS

This procedure has demonstrated to offer an opportunity for cure to patients who, initially, have no surgical option¹¹^,¹⁵^,²³^,³⁶. In the meta-analysis by Moris et al.¹¹, complete resection was achieved in 90.9% of the patients undergoing ALPPS compared with 74.6% in those undergoing TSH. Some studies did not find differences in OS and DFS between both techniques¹¹^,³⁷^,³⁸. However, the results of the LIGRO trial³⁹^,⁴⁹ demonstrated that ALPPS improved survival in patients with CRLM compared with TSH, with higher resection and survival rates.

The rate of complications and mortality associated with the technique is a matter of concern. Linecher at al.⁴¹ validated two risk models for predicting 90-day mortality, and Raptis et al.⁴² established the benchmark values for ALPPS.

There are no data demonstrating that liver volume increase runs parallel to liver function⁴³. Most deaths due to PHLF occur after the second stage. Thus, a dilemma emerges about the optimal timing for the second procedure. The meeting in Hamburg determined that minimum values for proceeding to stage 2 were FLR > 30% or a FLR/body weight ratio (FLR/BW) > 0.5%, and FLR > 40% or FLR/BW > 0.8%, depending on parenchymal quality⁴^,¹⁶. The first CT scan should be done on days 8 to 10 after stage 1 and repeated weekly for 4 weeks, if FLR is insufficient⁴⁴. Functional tests such as scintigraphy or indocyanine green test should become routine before completing the second stage. They can be especially useful in patients with a borderline FLR to decide the best timing for the intervention and to prevent PHLF. Serenari et al.⁴⁵ performed hepatobiliary iminodiacetic acid (HIDA) scintigraphy combined with single photon emission-computed tomography (SPECT) before ALPPS stage 2 and developed the HIBA index (HIBA-i), which represents the proportion of radionuclide accumulated in the FLR. None of the patients with a cut-off value of 15% or greater developed PHLF.

The results obtained differ according to the disease that led to surgery:

CRLM

Colorectal liver metastasis is the main indication for ALPPS¹⁸^,³⁹^,^46-53 and has been described as independent predictor of lower rate of serious complications (Clavien-Dindo IIIa or greater) > 36%. Overall survival at 1 and 2 years is 76% and 62%, respectively, with DFS of 59% and 41%, respectively¹⁸. The LIGRO trial³⁹ is a multicenter, randomized control trial (RCT) that included 97 patients with CRLM randomized in a 1:1 manner to ALPPS or TSH. The resection rate for patients randomized to ALPPS was 92% versus 57% in those undergoing TSH (p < 0.0001). ALPPS induced greater hypertrophy of the FLR (ALPPS: 92% vs. TSH: 57%, p < 0.0001). There were no significant differences in the rate of serious complications (≥ IIIa) (ALPPS: 43% vs. TSH: 43%, p = 1) or 90-day mortality (ALPPS: 9,1% vs. TSH: 10.7%, p = 0.64). Time between stage 1 and stage 2 was longer in TSH (ALPPS: 11 ± 11 vs. TSH: 43 ± 15 days, p < 0.0001). Hasselgren et al.40 described median survival of 46 months for ALPPS vs. 26 months for TSH (p = 0.028).

HCC

Hypertrophy of the FLR develops less rapid and to a lesser extent (40-47% vs. 76-138%) in livers with HCC^54-56 according to the degree of fibrosis. Mortality ranges between 9%⁵⁶ and 31%⁵⁴, so ALPPS is recommended in HCC with low degree of fibrosis and with a longer interval between stage 1 and 2 to allow the development of sufficient hypertrophy⁹. In these patients, partial split does not seem to induce sufficient hypertrophy compared with complete split (17.5 mL/day vs. 31.2 mL/day, p = 0.022)⁵⁶. ALPPS presents better OS and DFS than transcatheter arterial chemoembolization (TACE)⁵⁷ and higher resection rate than PVE⁵⁸.

Cholangiocarcinoma

Patients operated on due to cholangiocarcinoma present high morbidity and mortality. The OS is higher with ALPPS compared with palliative chemotherapy⁵⁹ at 1, 2 and 3 years: 82.4%, 70.5% and 39.6%, respectively versus 51.2%, 21.4% and 11.3% (p < 0.01). This benefit is not observed in those patients with PHLF or multifocal intrahepatic cholangiocarcinoma. The rate of serious complications is 6.1% after stage 1, 41.1% after stage 2, and mortality is 21.2%.

The initial results reported for perihilar cholangiocarcinoma described mortality rate between 40%60 and 48% at 90 days and OS of 6 months⁶¹^,⁶². The use of TIPE-ALPPS⁶³ and PRALPPS³⁴ have been reported for these tumors. Olthof et al.⁶² reported the results of cases of perihilar cholangiocarcinoma included in the ALPPS registry; 90-day mortality was 48% and mean OS was 6 months. FLR hypertrophy induced by ALPPS was similar to the one produced by major hepatectomies, but mortality was higher, and OS was lower. Thus, the authors do not recommend ALPPS in perihilar cholangiocarcinoma and suggest PVE to increase the FLR.

ALPPS in pediatrics

The first indication of ALPPS in pediatrics was reported by Chan et al.⁶⁴ in 2014. In 2015, Wiederkehr et al.⁶⁵ published a series of 5 patients without serious complications or deaths.

Conclusions

The ALPPS procedure has generated considerable interest despite its significant morbidity and mortality. A better selection of patients has been possible, along with the definition of timing for the second stage and improved surgical techniques, which have led to acceptable rate of complications and mortality compared with standard liver resections. The technical modifications, have minimized the extensiveness of the first-stage procedure and are associated with significant improvements in safety, preserving a high rate of curative resection. The second stage must be delayed or even not performed in case of clinical impairment, complications or insufficient FLR. Recent data have confirmed higher resection rates achieved with ALPPS than with the standard procedures. ALPPS is an already established concept; nevertheless, several questions remain unanswered, particularly in terms of long-term oncological outcomes. ALPPS does not replace other technique but expands the therapeutic armament.

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Received: May 12, 2020; Accepted: September 22, 2020

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