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A.V. Shabunin

Russian Medical Academy of Continuous Professional Education;
Botkin Moscow City Clinical Hospital

A.A. Karpov

Botkin Clinical Hospital

V.V. Bedin

Botkin Moscow City Clinical Hospital;
Russian Medical Academy of Continuous Professional Education

M.M. Tavobilov

Botkin Moscow City Clinical Hospital;
Russian Medical Academy of Continuous Professional Education

S.S. Lebedev

Russian Medical Academy for Continuous Professional Education;
Botkin City Clinical Hospital

D.S. Ozerova

Botkin Moscow, City Clinical Hospital;
Russian Medical Academy of Continuous Professional Education

M.N. Aladin

Russian Medical Academy of Continuous Postgraduate Education

F.F. Alieva

Russian Medical Academy for Continuous Professional Education

Preoperative radiation navigation in determining surgical strategy for liver echinococcosis

Authors:

A.V. Shabunin, A.A. Karpov, V.V. Bedin, M.M. Tavobilov, S.S. Lebedev, D.S. Ozerova, M.N. Aladin, F.F. Alieva

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To cite this article:

Shabunin AV, Karpov AA, Bedin VV, Tavobilov MM, Lebedev SS, Ozerova DS, Aladin MN, Alieva FF. Preoperative radiation navigation in determining surgical strategy for liver echinococcosis. Pirogov Russian Journal of Surgery = Khirurgiya. Zurnal im. N.I. Pirogova. 2023;(3):5‑13. (In Russ., In Engl.)
https://doi.org/10.17116/hirurgia20230315

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Introduction

According the World Health Organization (WHO) declarations, echinococcosis is among the diseases that should be eliminated by 2050. Nevertheless, prevalence of echinococcosis is up to 10% in some regions [1, 2]. This trend is largely due to population migration waves, transition of rural population to larger cities and metropolitan areas. According to the Moscow Department of Health, incidence of liver echinococcosis is being also increased in the capital [3].

Etiology of echinococcosis is well studied. The helminth E. granulosus leads to development of one or many hydatid cysts, and liver is the most common localization [4, 5].

Currently, there are no clear guidelines in the world literature regarding surgical intervention in a particular clinical situation.

There are various surgical techniques including partial resections associated, on the one hand, with high risk of postoperative morbidity and mortality and, on the other hand, with unsatisfactory long-term results. Therefore, surgeons need to understand features of hydatid cyst growth, correct interpret diagnostic data and choose adequate surgical procedure. This problem is the subject of our study.

Material and methods

In the Botkin Clinical Hospital, we developed a theory of diagnostic modeling of liver echinococcosis. We analyzed 264 patients between 2007 and 2021. Age patients varied from 18 to 90 years (mean 45±3.4). Men-to-women ratio was 1:1. Age-adjusted distribution of patients was almost normal (Fig. 1). In 180 (68.1%) patients, asymptomatic hydatid cysts were incidental findings.

Fig. 1. Distribution of patients by age, sex and echinococcosis WHO stage.

Young and middle-aged patients prevailed that could by associated with features of disease, more thorough screening and elements of labor migration waves (Fig. 1). We divided patients depending on the WHO stage of parasitic process. Patients with active hydatid cysts WHO stage II and III prevailed [6].

Patients were divided into 2 groups (2007-2016, 2017-2021). This distribution is due to changes in paradigm and approaches to the treatment of liver echinococcosis, i.e. the use of diagnostic modeling technology in the 2nd group.

The main inclusion criterion was patients over 18 years old hospitalized with liver echinococcosis.

Symptoms included feeling of heaviness and pain in the right hypochondrium (47 (17.8%) patients). Moreover, 10 (3.6%) patients complained of nausea. Obstructive jaundice was found in 3 (1.1%) patients.

All patients underwent preoperative examination including analysis of IgG antibodies to echinococcus. To analyze localization, number and dimensions of focal liver lesions, as well as anatomical relationship of cysts with liver vessels, we performed Doppler ultrasound and CT of the abdomen and retroperitoneal space (in native mode until 2011).

In the 2nd group, preoperative contrast-enhanced CT of the abdomen became obligatory in patients with liver echinococcosis.

To exclude involvement of bile ducts, we used magnetic resonance cholangiopancreatography (MRCP). Differential diagnosis with other cystic liver lesions required contrast-enhanced MRI of the abdomen.

When planning extended liver resections, we analyzed functional liver remnant using single photon emission computed tomography (SPECT/CT).

Distribution of patients into subgroups in the 1st group was related to the treatment of parasitic cysts. Subgroup 1.1 included 23 patients who underwent conservative therapy. Subgroup 1.2 included 22 patients who underwent open echinococcectomy for some reasons. Subgroup 1.3 included 44 patients who underwent pericystectomy. Subgroup 1.4 enrolled 58 patients who underwent liver resections (right-sided hemihepatectomy).

Analyzing diagnostic data and treatment outcomes in the 1st group, we have formulated diagnostic modeling technology. The last one made it possible to determine the method and extent of surgical intervention at the preoperative stage.

Depending on treatment method, patients of the 2nd group were divided into the following subgroups: 71 patients after pericystectomy, 13 patients after hemihepatectomy, 33 patients who underwent PAIR, RFA or mi crowave ablation.

Results

Analysis of diagnostic data and treatment outcomes in the retrospective group

The first stage of retrospective clinical study was evaluation of results of various diagnostic techniques to develop the criteria for diagnostic modeling of liver echinococcosis. In the retrospective group, highly informative diagnostic methods (sensitivity over 90%) were performed only in 44.9% of patients who underwent preoperative contrast-enhanced CT or MRI of the abdomen. These data made it possible to determine the indications for surgical interventions in these patients (Table 1).

Table 1. Indications for treatment methods in the 1st group

Variable

Subgroup 1.1 (n=23, 15.6%)

Subgroup 1.2 (n=22, 15%)

Subgroup 1.3 (n=44, 29.9%)

Subgroup 1.4 (n=58, 39.5%)

Total (n=147)

WHO classification

CE1

22 (95.7%)

1 (4.5%)

3 (6.8%)

3 (5.2%)

29 (19.7%)

CE2

1 (4.3%)

2 (9%)

7 (15.9%)

11 (18.9%)

22 (15%)

CE3

11 (50%)

31 (70.5%)

32 (55.2%)

78 (53%)

CE4

8 (36.4%)

2 (4.5%)

3 (5.2%)

15 (10.2%)

CE5

1 (2.3%)

2 (3.4%)

3 (2%)

Number of cyst per a patient

1

16 (69.6%)

24 (54.5%)

7 (12.1%)

73 (49.7%)

2

4 (17.4%)

20 (91%)

17 (38.6%)

12 (20.7%)

36 (24.4%)

≥ 3

3 (13%)

2 (9%)

3 (6.8%)

32 (55.2%)

38 (25.6%)

Infection

2 (9%)

9 (6.1%)

Cyst dimension

<5 cm

9 (20.5%)

4 (6.9%)

39 (26.5%)

5-10

cm

3 (13.6%)

27 (61.4%)

31 (53.4%)

65 (44.2%)

>10 cm

1 (4.3%)

19 (86.4%)

8 (18.2%)

16 (27.6%)

43 (29.3%)

Attachment to vascular structures:

hepatic veins

17 (77.2%)

7 (15.9%)

21 (36.2%)

45 (30.6%)

portal vein

5 (22.7%)

5 (11.4%)

20 (34.5%)

30 (20.4%)

In subgroup 1.1, the indications for conservative therapy were single cysts (69.6%) up to 5 cm (95.7%) without signs of infection (100%). WHO class CE1 was the most common (95.7%).

Analysis of subgroup 1.2 (open echinococcectomy) revealed that the indication for open echinococcectomy was a single cyst over 10 cm (91 and 86.4%, respectively) adjacent to hepatic veins (77.2%). CE3 type was found in 11 (50%) cases.

In subgroup 1.3 (pericystectomy), the indications for surgery were 1 or 2 cysts 5-10 cm (54.4 and 61.4%) with predominant WHO type CE3 (70.5%).

Subgroup 1.4 (hemihepatectomy) was characterized by multiple cysts (55.2%) with a dimeter of 5-10 cm (53.4%) adjacent to great veins (>36.2%). Apparently, this did not allow parenchyma-sparing intervention.

These data made it possible to formulate the concept of diagnostic modeling of surgical treatment of cystic liver echinococcosis.

Immediate and long-term results of open surgical treatment of liver echinococcosis

We analyzed the immediate and long-term results of open surgical treatment (Table 2). Open echinococcectomy was followed by high incidence of general surgical complications grade III and higher (77.2%). Incidence of such events after pericystectomy and hemihepatectomy was 27.2 and 51%, respectively.

Table 2. Early and long-term postoperative results in retrospective group

Variable

Subgroup 1.2 (n=22)

Subgroup 1.3 (n=44)

Subgroup 1.4 (n=58)

p-value

Surgery time, min

187±31

234±17

317±61

<0.001*

p1.3—1.2<0.001

p1.4—1.2<0.001

Blood loss, ml

74±30

313±59

415±112

<0.001*

p1.3—1.2<0.001

p1.4—1.2<0.001

p1.4—1.3=0.014

Clavien —Dindo grade

p1.3—1.2<0.001

p1.4—1.2<0.001

I

17

5

7

II

14

7

9

III

14

10

17

IV

2

2

4

V

1 (4.5%)

0

5 (8.6%)

Total

48

24

41

ISGLS*

<0.001*

p1.4—1.3=0.003

A

1

1

14

B

0

0

19

C

0

0

5

Total

1

1

28

Postoperative hospital-stay, days

18±9

14±6.3

15±3.7

>0.05

Recurrence within 3 years

12/21 (57.1%)

7/44 (15.9%)

1/46 (2.2%)

p1.3—1.2<0.001

p1.4—1.2<0.001

Note. ISGLS* — ISGLS classification of post-resection liver failure.

In subgroup 1.4, resections were associated with significantly higher number of specific postoperative complications and mortality (48.3% and 8.6%), as well as low incidence of recurrent parasitic process (2.2% vs. 1% in the open echinococcectomy group). Thus, extensive liver resection increased postoperative morbidity and mortality due to acute post-resection liver failure in most cases.

Assessing the unsatisfactory treatment outcomes in the 1st group, we can conclude that morbidity, mortality and recurrence rates depended on surgical procedure. However, the absence of clear indications for certain treatment method depending on the stage and localization of parasitic process, as well as clinical and diagnostic data led to the choice of ineffective or overly traumatic surgery.

Clinical and diagnostic criteria for modeling liver echinococcosis. Characteristics of the "models" of hepatic echinococcosis

Considierng unfavorable immediate and long-term treatment outcomes in the retrospective group, we substantiated the technology of diagnostic modeling of liver echinococcosis. The last one considers not only WHO stage of parasitic process, surgeon’s opinion, tactical approaches in a particular hospital, but also the number of cysts, volume of damaged liver parenchyma, localization of lesion, adherence to great vessels and bile ducts.

We analyzed ultrasound, CT, MRI, SPECT/CT and intraoperative findings. These data were supplemented by the results of various treatment options in the retrospective group, since over 30% of patients underwent insufficiently radical intervention at the first stage. Thus, we developed the criteria for choosing the most effective surgical method:

1. WHO / ultrasound stage.

2. Number of cysts: single/multiple.

3. Localization: 1 / 2 liver lobes.

4. Localization: extraparenchymal / intraparenchymal.

5. Attachment to the portal and/or hepatic veins.

6. Attachment / connection with the bile ducts.

7. Substitution of liver lobe parenchyma with parasitic cysts (we analyzed anatomical and functional volume of each lobe in case of total replacement of one of the liver lobes with parasitic cysts or multiple cysts not allowing parenchyma-sparing intervention).

These criteria for assessing the parasitic process allowed us to formulate the principle of modeling the course of liver echinococcosis and determine the most effective treatment strategy. Scoring system for parasitic process spread allowed us to identify 4 models of cystic liver echinococcosis.

Model 1

WHO stage: CE1, CE2, CE3.

Number of cysts: single.

Localization: intraparenchymal.

Attachment to vascular structures: +/–.

Attachment / connection with bile ducts: no.

Substitution of liver lobe with parasitic cysts: no.

Cyst dimension: 0-10 cm.

These patients are candidates for minimally invasive percutaneous treatments (Fig. 2).

Fig. 2. Liver echinococcosis. Model 1.

Model 2

WHO stage: CE1-CE5.

Number of cysts: single (1-3).

Localization: extraparenchymal.

Attachment to vascular structures: +.

Attachment / connection with bile ducts: +/-.

Substitution of liver lobe with parasitic cysts: no.

Diagnosis: any cyst dimension.

For these patients, parenchyma-preserving methods of treatment are indicated (Fig. 3).

Fig. 3. Liver echinococcosis. Model 2.

Model 2a

WHO stage: CE1, CE2, CE3.

Number of cysts: single (1-3).

Localization: extraparenchymal.

Attachment to vascular structures: +/-.

Attachment / connection with bile ducts: +/-.

Substitution of liver lobe with parasitic cysts: no.

Diagnosis: dimension < 10 cm.

These patients require minimally invasive (laparoscopic and robot-assisted) parenchymal-preserving methods of treatment (Fig. 4).

Fig. 4. Liver echinococcosis. Model 2a.

Model 3

WHO stage: CE1, CE2, CE3.

Number of cysts: single/multiple.

Localization: extraparenchymal / intraparenchymal.

Attachment to vascular structures: +.

Attachment / connection with bile ducts: +/+.

Substitution of liver lobe with parasitic cysts: yes.

Diagnosis: any cyst dimension.

Anatomical volume of liver lobe remnant: > 30%.

Functional volume of liver lobe remnant: > 30%.

Resections are advisable for these patients (Fig. 5).

Fig. 5. Liver echinococcosis. Model 3.

If simultaneous liver resection is impossible, a two-stage surgical treatment with embolization of the right portal vein is performed.

Model 4

Model 4 of liver echinococcosis implies diverse lesions of liver requiring combination of several methods, i.e. parenchyma-preserving procedures, resections and modern methods of physical impact (microwave ablation, RFA, cryodestruction) (Fig. 6).

Fig. 6. Liver echinococcosis. Model 4.

Thus, only ultrasound data describing the features of certain sonographic type of cyst cannot change surgical approach. Indeed, only combination of CT, MRI and, if necessary, SPECT/CT allows us to determine the most appropriate surgical intervention.

Immediate and long-term results of open surgical treatment of liver echinococcosis

Wwe analyzed the immediate and long-term results of open surgical treatment of liver echinococcosis (Table 3). Open echinococcectomy was followed by high incidnece of general surgical complications grade III and higher (77.2%). Pericystectomy and hemihepatectomy resulted complications in 27.2 and 51% of cases, respectively. In subgroup 1.4, resections were associated with significantly higher incidence of specific postoperative complications and mortality (48.3 and 8.6%, respectively), as well as low incidence of recurrent parasitic process (2.2 and 57.1 % in the open echinococcectomy group). Thus, extended surgery for liver echinococcosis increased postoperative morbidity and mortality due to acute post-resection liver failure. Assessing the unsatisfactory treatment outcomes in the 1st group, we can conclude that incidence of complications and recurrences, as well as mortality rate depended on surgical procedure. However, the absence of clear indications for certain treatment method depending on the stage and localization of parasitic process, as well as clinical and diagnostic data led to the choice of ineffective or overly traumatic surgery. In the second group, we abandoned from non-radical open echinococcectomy in favor of organ-preserving minimally invasive, traditional interventions and resections.

We observed less blood loss and shorter postoperative hospital-stay. Incidence of general postoperative complications was higher in the 1st group (77.6%; 114/147). In the 2nd (prospective) group, the number of general postoperative complications decreased to 36.8% (43/117). There were 28 (19%) and 10 (8.5%) specific complications in both groups, respectively (Table 3).

Table 3. Early and long-term postoperative results in retrospective and prospective groups

Variable

Group 1 (n=147)

Group 2 (n=117)

p-value

Surgery time, min

239.3±74.2

148.3±63.1

<0.001

Blood loss, ml

346±30

170±45

<0.001

Clavien-Dindo grade

<0.001

I

29

13

II

30

11

III

41

17

IV

8

1

V

6

1

Total

114

43

ISGLS*

<0.05

A

4

4

B

19

4

C

5

2

Total

28

10

Postoperative hospital-stay, days

17.5±9

9.2±1.9

<0.001

Recurrence

20/141 (14.2%)

7/117 (6%)

<0.05

Note. ISGLS* — ISGLS classification of post-resection liver failure.

Discussion

In our study, postoperative complications occurred after open echinococcectomy. Postoperative period was complicated in almost all patients afther this procedure, and biliary fistula was the nost common event (62.5%).

Recurrence of liver echinococcosis in long-term postoperative period occured in 57.1% of cases after open echinococcectomy. Thus, this non-radical procedure requires strict indications despite technical simplicity.

Anatomical liver resections were characterized by postoperative fluid accumulations, biliary fistulas and hemorrhagic complications in both subgroups. However, their number significantly decreased in the 2nd subgroup. Importantly, mortality from acute post-resection liver failure reduced from 8.6% to 0%.

Higher number of pericystectomies in the 2nd subgroup was characterized by lower postoperative morbidity (54.5 vs. 14.3%).

There were no recurrences of liver echinococcosis in long-term period after anatomical liver resections and pericystectomy in the 2nd group that confirms radical nature of these procedures. These data confirm the effectiveness and necessity of preoperative modeling. Five variants of echinococcal liver disease correlated with distribution of patients into the groups. Importantly, 9 patients had liver lesion model 4, and they underwent all surgical high-tech methods for preventing the recurrence of hydatid disease. This approach contributed not only to standardized choice of surgical interventions, but also reduction of postoperative morbidity and mortality, as well as significant decrease in the incidence of recurrences.

Conclusion

Significant improvement of postoperative outcomes in patients with liver echinococcosis is due not only and not so much to improvement of surgical techniques, but also changes of the principle of treating patients using a personalized approach. The last one is based on clinical and objective criteria including dimensions and localization of hydatid cysts (marginal or intraparenchymal), the number of echinococcal cysts, relationship with the bile ducts and vessels (hepatic artery, portal vein and hepatic veins), volume of the future liver remnant after resection.

Creating the models of echinococcal liver damage became possible due to correct interpretation of ultrasound and X-ray data, understanding and predicting complications. These models contributed to a differentiated approach to surgical treatment of liver echinococcosis.

The authors declare no conflicts of interest.

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