Comparison of Laparoscopic Splenectomy Outcomes for Benign and Malignant Hemopathies

Abstract

Background:

Laparoscopic splenectomy for malignant hemopathies has been associated with a higher morbidity than for benign hemopathies. Recent progress in medical and surgical treatment for malignant hemopathies may have improved the outcomes of laparoscopic splenectomy. The purpose of this study is to compare the outcomes of laparoscopic splenectomy for malignant hemopathies (SHM) and benign hemopathies (SHB).

Materials and Methods:

We retrospectively reviewed all patients with hematological diseases who underwent a non-post-traumatic laparoscopic splenectomy between 2008 and 2019. Patients who suffered splenectomy for a malignant and benign disease were divided into two groups and compared.

Results:

Fifty patients suffered a splenectomy for hematologic disorder, 19 patients for benign hemopathy, and 31 for malignant hemopathy. SHM group was significantly older, and had more history of abdominal surgery and significantly larger spleens (P < .05). There was no significant difference in terms of operative time (150 versus 146 minutes; P < .8) and blood loss (243 versus 402 mL; P < .26). Hospital stay for SHB and SHM groups was 5.4 and 7.6 days, respectively (P = .19). There was no significant difference in terms of early (10% versus 13%; P = 1) and late complications (0% versus 13%; P = .28). One conversion to open surgery and one perioperative death in each group (P = 1) were reported. Splenectomy effectiveness was 83% and 79% in benign hemopathy and malignant hemopathy groups (P = .91), respectively.

Conclusions:

Laparoscopic splenectomy for malignant hemopathy shows similar outcomes to laparoscopic splenectomy for benign hemopathy, despite older patients, larger spleens, and more important abdominal surgery history. Higher late morbidity rate after laparoscopic splenectomy for malignant hemopathy may justify a careful follow-up.

Introduction

Since it was first performed in 1991 by Delaitre and Maignien,¹ laparoscopic splenectomy has established itself as the gold standard for the treatment of hemopathies requiring surgical spleen ablation.

The minimally invasive approach has been widely described over the last 25 years, by laparoscopy in dorsal and lateral decubitus, and more recently, by single incision laparoscopy or robotic surgery. Several meta-analyses have shown that once past the learning curve, laparoscopy reduces morbidity, perioperative bleeding losses, and hospital stay compared to open surgery.^2,3

In literature, there is a consensus regarding the laparoscopic approach for normovolemic spleens and benign hemopathies, while the debate persists for major splenomegalies and malignant hemopathies. Although splenomegaly is no longer considered a contraindication to laparoscopy,⁴ perisplenitis, hilar adenopathies, and comorbidities of patients with malignant hemopathies can complicate laparoscopic surgery. The few studies comparing the results of laparoscopic splenectomy for malignant hematopathies (SHM) and benign hemopathies (SHB) show an increase in blood loss, operative time, conversion rate, and morbidity.^5–10

Some include hand-assisted laparoscopy^5,8,10 and others do not represent consecutive series, suggesting a selection of cases appropriate for laparoscopy.^6,9 Parallel to the evolution of these results, there has been an improvement in the medical treatment of malignant hemopathies in which splenectomy could be indicated. This is the case with splenomegaly associated with myeloproliferative syndromes that can currently be treated pharmacologically (interferon-α, hydroxyurea, and JAK inhibitors) or with hairycell leukemia, which may benefit from the arrival of new drugs such as the purine analogue and monoclonal antibodies.

The objective of this study is to compare the outcomes in SHM and SHB.

Materials and Methods

Patients

This is a retrospective study of a prospectively collected database of all patients who suffered a splenectomy between 2008 and 2019. Only splenectomies for traumatic causes were excluded. All patients were operated by laparoscopy.

The clinical report of each patient included a physical examination, a preoperative blood test, and an abdominal ultrasound or computed tomography (CT)-scanner to assess the volume of the spleen.

The diagnosis of malignant hemopathy was established in the preoperative or postoperative course with histopathological findings. All patients who benefited from elective splenectomy received vaccinations against Streptococcus pneumoniae, Haemophilus influenzae, and Meningococcus C, 2 weeks before surgery. Patients operated in emergency benefited from a 2-week postoperative antibiotic prophylaxis with vaccinations in the following days.

The splenic volume was calculated by multiplying the height by the width on the frontal plane and by the anteroposterior diameter. The result was then divided by two.

Collected information included demographic data, operators, splenectomy indication, preoperative and postoperative laboratory results, histopathological findings, early (defined as occurring within 30 days from the intervention) or late (after 30 days) postoperative complications, and overall survival. Splenectomy was considered effective at >6 months, depending on surgical indication: correction of hypersplenism, anemia, or definitive therapy. Splenectomies for diagnostic purpose were excluded while comparing effectiveness.

The follow-up included daily blood tests, a physical examination, and, in the case of malignant hemopathies, diagnostic imaging tests. In case of surgery failure, an imaging test was performed with the aim of searching for an accessory spleen.

Laparoscopic procedure

The surgical technique consisted in approaching the patient in dorsal decubitus, in right rotation, and in anti-Trendelenburg position. Five trocars were needed for a classical laparoscopic surgery. In 3 cases, we performed a laparoscopic approach with a single incision. The spleen was placed in a bag in the abdominal cavity and cut into pieces of maximum 3 cm. The extraction was performed either through Pfannenstiel or after enlargement of the orifice of the trocar in the left hypochondrium.

Statistical analysis

Data are expressed in mean ± standard deviation. Continuous data were compared with the Student's t-test and the proportions with the Chi-squared test or with the Fischer test. A P value <.05 was considered statistically significant.

Results

Patients' characteristics

Between February 2008 and January 2019, 50 patients suffered a laparoscopic splenectomy for benign or malignant hemopathy. Among these, 19 were in the SHB group and 31 in the SHM group. Hematologic pathologies and surgical indications are listed in Table 1. In the SHB group, the most frequent pathology was idiopathic thrombocytopenic purpura (ITP) (58%) and the main indication for splenectomy was thrombocytopenia (74%). In the SHM group, the most frequent diseases were non-Hodgkin's lymphoma (39%), myelofibrosis (32%), and chronic lymphoid leukemia (23%). The majority of surgical indications were for hypersplenism (55%), anemia (26%), and symptomatic splenomegaly (10%). In 2 cases, the splenomegaly compromised chemotherapy, and in a third, it induced major gastric compression. One patient in the SHM group received a curative splenectomy for a case of splenic lymphoma.

Table 1.

Pathologies and Indications of Laparoscopic Splenectomy

Pathologies	n
SHB	19
Idiopathic thrombocytopenic purpura	11
Thrombocytopenia related to HIV	3
Spherocytosis	1
Beta thalassemia	1
Congenital dyserythropoiesis	1
Epithelial cyst	1
Splenic mycotic abscess	1
SHM	31
Non-Hodgkin lymphoma	12
Myelofibrosis	10
Chronic lymphocytic leukemia	7
Hairy cell leukemia	1
Hodgkin lymphoma	1
Indications
SHB
Thrombocytopenia	14
Anemia	3
Diagnostic purpose	1
Infectious	1
SHM
Hypersplenism	17
Anemia	8
Disabling splenomegaly	3
Diagnostic purpose	2
Curative purpose (splenic lymphoma)	1

SHB, splenectomy for benign hemopathies; SHM, splenectomy for malignant hemopathies.

Table 2 displays patients' clinical data. Patients in the SHM group were older than those in the SHB group (67.2 versus 38.8 years old; P < .05), had more frequently suffered abdominal surgery (18/31 versus 5/19; P < .05), and had a larger splenic volume (1515 versus 422 mL; P < .05).

Table 2.

Patients' Clinical Data

	SHB (n = 19)	SHM (n = 31)	P
Age (years)	38.8 ± 17	67.2 ± 12	<.05
Sex ratio, M/F	10/9	19/12	.54
Body mass index	22.7 ± 5.4	23.5 ± 3.2	.64
Diabetes	3/19	3/31	.67
History of abdominal surgery	5/19	18/31	<.05
Preoperative corticotherapy	8/19	4/31	.1
Preoperative platelets ( × 10³/mL)	161 ± 113	156 ± 108	.89
Preoperative white blood cell count (/mL)	9938 ± 9042	15,696 ± 18,950	.17
Preoperative hemoglobin (g/dL)	11.4 ± 2.1	10.1 ± 1.6	.06
Spleen volume (mL)	422 ± 439	1515 ± 662	<.05

SHB, splenectomy for benign hemopathies; SHM, splenectomy for malignant hemopathies.

Therapeutic outcomes

The preoperative and postoperative data are summarized in Table 3. There was no significant difference in terms of operative time (150 versus 146 minutes; P < .8) and blood loss (243 versus 402 mL; P < .26).

Table 3.

Preoperative and Postoperative Outcomes

	SHB (n = 19)	SHM (n = 31)	P
Operative time (minutes)	150 ± 50	146 ± 54	.8
Blood loss (mL)	243 ± 375	402 ± 550	.26
Associated surgical procedure	3/19	5/31	.1
Conversion to laparotomy	1/19	1/31	.1
Hospital stay (days)	5.4 ± 3.5	7.6 ± 8	.19
Early complications	2/19	4/31	1
Late complications	0/19	4/31	.28
Perioperative mortality	1/19	1/31	1
Follow-up (months)	68 ± 42	37 ± 39	<.05

SHB, splenectomy for benign hemopathies; SHM, splenectomy for malignant hemopathies.

Eight patients benefited from associated procedures, 3 in the SHB group (2 cholecystectomies and 1 cure for umbilical hernia) and 5 in the SHM group (2 cholecystectomies, 1 intestinal closure, 1 caudal pancreatectomy for bleeding, and 1 cure for eventration). There was one conversion to laparotomy in both groups (P = 1): in the SHB group, it was a patient with a splenic mycotic abscess converted due to excessive bleeding, while in the SHM group, it was a 65-year-old patient presenting a splenic abscess and moderate monocytopenia with a final diagnosis of diffuse B cell lymphoma (the conversion was made because of a hilar adenopathy difficult to dry up).

The hospital stay for the SHB and SHM group was 5.4 and 7.6 days, respectively (P = .19).

There was no significant difference in terms of early (10% versus 13%; P = 1) and late complications (0% versus 13%; P = .28) between SHB and SHM groups. In the SHB group, two early complications were described (10%): a case of bronchopneumonia that required specific antimicrobial treatment and a colic perforation due to a Veress needle reoperated on day 6 for an intestinal closure and peritoneal toilet.

Four patients presented an early complication in the SHM group (13%): 2 cases of hemoperitoneum, 1 subphrenic abscess that justified a laparoscopic drainage, and 1 bacteremia treated with antibiotics.

Four patients presented late complications in the SHM group (13%): 1 pneumococcal sepsis (4 months after splenectomy in a patient who had been previously vaccinated), 1 septic shock (3 months postsurgery after chemotherapy in a neutropenic patient), 1 pulmonary embolism (2 years later), and 1 portal thrombosis (1 year later). No late complication was reported in the SHB group.

One perioperative death in each group (P = 1) was reported. In the SHB group, it was a case of a mycotic abscess of the spleen, which extended to the meninges leading to death of the subject on the 19th postoperative day. In the SHM group, it was a 78-year-old patient with a diffuse B lymphoma, who developed a septic shock with death on the 30th postoperative day.

Median follow-up was significantly shorter in the SHM group (37 versus 68 months; P < .05).

Splenectomy efficacy was 83% and 79% in SHB and SHM groups (P = .91), respectively: in the SHB group, two failures concerned patients with ITP and were attributed to the persistence of an accessory spleen (confirmed by imaging). In patients splenectomized for hypersplenism in the SHM group, the mean platelet rate 1 month after surgery for patients operated successfully (n = 13) and unsuccessfully (n = 4) were, respectively, 387 ± 125 versus 138 ± 90 × 10³/mL (P < .05).

Discussion

Several studies have demonstrated the usefulness of laparoscopic splenectomy for certain benign hemopathies.^11,12 These encouraging results have imposed laparoscopic splenectomy as a first-choice technique for elective splenectomy in patients with a normovolemic spleen.¹³

Our results suggest that this approach is equally safe and effective for suspected or confirmed malignant hemopathies; despite an older population, presenting frequently with more history of abdominal surgery and larger spleen, the SHM group did not present significantly higher operative times, blood losses, or conversions to laparotomy.

To describe spleen size, we used the spleen volume rather than weight or length; as pointed out by Knauer et al.,⁵ the weight has the disadvantage of being assessable exclusively after the removal and is also affected by possible aspiration of intraorganic blood.

The splenic length, indeed, does not always reflect the actual size of the spleen, given that a short and wide spleen could be more difficult to extract than a long and narrow spleen.

As far as benign hemopathies are concerned, we find essentially ITP (58%) and thrombopenia (74%) as main indications, similar to data reported in literature.¹⁴

Due to the predominant diagnosis of ITP, we find more patients under corticotherapy in the SHB group than in the SHM group (P = .1), which may contribute to a similar early morbidity rate in both groups.

In the SHM group, we find very heterogeneous disorders with extremely different prognosis: for this reason, an analysis of the overall survival would not have made sense, considering that we would have had to take into account the natural evolution of each disease separately.

Surgical times in both groups were similar (P = .8) and even lower than the most recently published series^7,15; this means that, although spleen fragmentation requires additional time, the laparoscopic approach can be efficiently adapted to splenomegaly without a great waste of time. These positive results are equally explained by the fact that this analysis started after completion of the learning curve and by the optimal cooperation with the local hematologic service, which presents a high level of expertise.

Blood losses seemed more important in the SHM group, but were not significantly different (P = .26) and were not related to differences in postoperative transfusional rates. One of the explanations apart from the larger volume of the spleen is that the intervention starts with splenic hilum control; therefore, the blood lost at the time of spleen dissection is already seized in the organ. This can potentially confuse the calculation of blood loss to the disadvantage of the SHM group.

Patients in the SHM group were hospitalized for a longer time (P = .19), but these data were not statistically significant, in accordance with the literature.¹³ Splenectomies with diagnostic purpose that needed to be confirmed during the same hospital stay and the early complication rate (13%) leading to reintervention are responsible for the longer hospitalization time.

The two conversions of the SHB group (n = 1) and the SHM group (n = 1) had a splenic abscess; Carbonell et al.¹⁶ demonstrated that laparoscopic splenectomy in case of splenic abscess is feasible, but technically complicated.

The early morbidity for SHB and SHM groups was 10% and 13% (P = 1), respectively. One patient (5%) from the SHB group required a reintervention for 1 colonic perforation and 3 patients (10%) in the SHM group, 2 for hemoperitoneum and 1 for subphrenic abscess.

In the SHM group, early complications are attributable to the difficulty represented by a splenomegaly on malignant hematopathy¹³; the colonic perforation is to be attributed rather to a technical error. This underlines the importance of good hemostatic control, which led some authors^5,8 to suggest a “hand-assisted” approach for malignant hemopathies with large spleen.

In splenectomy by laparoscopy, the enlargement of the portal system and the decreased flow in the portal vein are major risk factors for thromboembolic events.^17,18 In our series, we report 1 portal thrombosis after 1 year and 1 pulmonary embolism after 2 years, in both cases in the SHM group. Although comparable to the rates of thromboembolic complications (2%–10%) reported by others,^17,19 these complications occurred later in our series. This could be related to the already existing pathology rather than the surgery. Silecchia et al.⁷ systematically performed a Doppler ultrasound of the portal system, showing a 9% incidence of portal thrombosis in asymptomatic patients. This demonstrates the difficulty of assessing the risk and incidence of postsplenectomy thromboembolic incident. However, early diagnosis remains important to promptly initiate an effective anticoagulation.²⁰

Two SHB splenectomies performed for thrombopenia have failed: at the time of control by postoperative scintigraphy, the presence of an accessory spleen was confirmed in both cases.

In 2008, Habermalz et al.¹³ concluded that a preoperative CT scan and a conscientious examination of the preoperative abdominal cavity were indicated, but did not confer 100% sensitivity for the detection of accessory spleens. Laparoscopy does not give a less important detection rate of accessory spleens than open surgery.¹³

The follow-up of the SHM group was significantly lower than the SHB group (37 versus 68 months), and this is probably related to a more limited life expectancy for the first group.

However, the follow-up seems long enough to allow us to interpret the long-term results of laparoscopic splenectomy.

With regard to the effectiveness of laparoscopic splenectomy for hypersplenism in malignant hematopathies, it can be seen that there is a significant difference in terms of platelet count after 1 month for patients who have been operated successfully compared to those in whom the intervention has failed (387 ± 125 versus 138 ± 90 × 10³ mL; P < .05). This observation suggests that a platelet rate that remains low 1 month after surgery is predictive of long-term failure of the intervention.

In our study, laparoscopic splenectomy for malignant hemopathies has similar outcomes to laparoscopic splenectomy for benign hematopathies, despite older patients, larger spleens, and more important abdominal surgery history. Higher late morbidity rate after laparoscopic splenectomy for malignant hemopathy may justify a careful follow-up.

Footnotes

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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