TITRE: Viability predictive factors of the daughter vesicles in hepatic hydatid cyst

doi:10.21203/rs.3.rs-3250170/v1

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TITRE: Viability predictive factors of the daughter vesicles in hepatic hydatid cyst

https://doi.org/10.21203/rs.3.rs-3250170/v1

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published 03 Jan, 2024

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Introduction: Management of hepatic hydatidosis requires knowledge of certain aspects related to the survival of Echinococcus granulosus. The viability of daughter vesicles (DV) is a determining factor in guiding therapeutic indications, particularly for transiently active Cysts type CE3b.

Purpose: To determine the predictive factors of DV viability and its impact on the therapeutic management of CE3b type.

Materials and Methods: This is a prospective pilot study with analytical aim on patients with hydatid cysts of the liver type CE2 and CE3b, operated in the General Surgery Department of Habib-Bourguiba Academic Hospital, Sfax-Tunisia during 22 months from March 2018 until December 2019. The unit of the study is the DV. A parasitological study of the DV was done in the parasitology laboratory.

Results: During the study period, 27 (40.9%) of 66 operated Cystic Hydatid Disease from 21 patients containing 248 DV were explored. The median viability of DV protoscoleces was 16.7%. In bivariate analysis, factors for viability of DV protoscoleces were: fever, acute cholangitis, hyperbilirubinemia, left liver location, rock water and bilious hydatid fluid (HF), cyst size ≥ 43mm, intracystic pressure ≥ 35 mmHg, DV size ≥ 6.5mm, volume, number of DV/cyst ≥ 5, and opaque wall (p < 0.05). Predictive factors for Non-viability of DV were: CE3b type, purulent HF and gelatinous HF. In multivariate analysis, only CE2 type, cyst size ≥ 43 mm, number of DV/cyst ≥ 5 and DV size ≥ 6.5 mm were factors significantly associated with the viability of DV protoscoleces.

Conclusion: CE3b cysts without the criteria of viability of DV protoscoleces may become candidates for 'Wait-and-Watch' procedure.

Echinococcus Infection

Hepatic

daughter vesicles

Hydatidosis or cystic echinococcosis is a parasitic anthropozoonosis due to the development of the larval form of a cestode, Echinococcus granulosus in humans. Proper management of hydatidosis requires knowledge of certain aspects related to the survival of the parasitic agent, particularly protoscolex. In the literature, the study of the fertility of hydatid cysts and the viability of protoscoleces has always been performed on hydatid fluid (HF) [1, 2]. However, no study concerning the lesional aspects of daughter vesicles (DV) is available at present. Therefore, a better knowledge of these aspects as well as of the predictive factors of hydatid dissemination allows us to guide our future practices in order to guide the therapeutic indications. Indeed, while therapeutic indications are increasingly codified for active cysts (I/ II/ II Gharbi and CE1/CE2/CE3a WHO) and inactive cysts (IV/V Gharbi and CE4/CE5 WHO) [3, 8], cysts of transient activity, especially CE3b (CE3b WHO) are not codified. This type has long been considered as a CE4 cyst that contains DV. With this in mind, in the present study we addressed the parasite content of daughter vesicles in viable protoscolex (Viability of DV protoscoleces) from human liver hydatid cysts (HCL) operated on in our Department and the aim of this study was to search for an association with data from patients operated on for HCL, the characteristics of the cysts and DV, and the impact of these parameters on the therapeutic management of HCL, and in particular transiently active cysts of the CE3b type.

We conducted a prospective analytical pilot study including patients with hydatid cysts of the liver type CE2 and CE3b according to the WHO classification, operated in the General Surgery Department of the Habib Bourguiba Academic Hospital of Sfax-Tunisia, during a 22-month period from March 1, 2018 until December 31, 2019. We performed a microscopic study of the cyst contents and daughter vesicles.

We included multivesicular hydatid cysts of the liver type CE2 and CE3b of the WHO classification (9). We did not include patients with severe cholangitis or shock and excluded destroyed DV and DV not preserved at + 4°C. The unit of this study was the DV. The number of daughter vesicles required for this study was determined from data from a pre-investigation performed on 20 daughter vesicles from 5 different liver hydatid cysts. Thus, we found a viability of 20% and the necessary number of DV was estimated to be 246 with a precision of 5%. Before the initiation of our study, an agreement was authorized by the Committee for the Protection of Persons Suitable for Medical or Scientific Experimentation of Medicinal Products for Human Medicine “CPP” under the reference “CPP sud number 0021/2017”. The CPP is the only center for medical or scientific research on medicinal products of human medicine in our institution "University of Sfax", approved by the Ministry of Public Health. All patients, who participated in our prospective study, signed a consent agreement after being informed by our research protocol.

The unit of this study was the DV. The primary endpoint was the viability of the daughter vesicle. Viability was defined as the presence of viable protoscolex within the cyst. This viability is equal to the number of viable protoscolex in relation to the total number (or a sample of 150 if the fluid is very fertile) of protoscolex in the HF (2). A pre-established form was filled in with the data of the operated patient,

the cyst, the hydatid fluid (HF) and the daughter vesicles (DV) for which a macroscopic and microscopic study was performed.

The study protocol was standardized: A standard workup and systematic preoperative imaging such as ultrasound and abdominopelvic CT were performed. In the operating room, all patients had an intraoperative ultrasound followed by a systematic measurement of the intracystic pressure. Then, for each cyst, a hydatid fluid aspiration was performed with a graduated syringe before cystotomy, and the DV were collected with a sterile spoon and placed in a container. The hydatid material (HF + DV) was sent to the Parasitology-Mycology laboratory on the same day of the surgery or at the latest the next day after conservation at + 4°C. The daughter vesicles are treated in the laboratory with a standardized technique as well: a random sample is thus taken from a petri dish of 10 intact DV if the cyst contains a number ≥ 10 DV / cyst or all the DV if the number of the latter/cyst is < 10, different in size and appearance using a spoon to avoid selection bias. Then, these vesicles are washed with a sterile 0.9 sodium chloride solution, the volume of each DV is measured with a test tube or a graduated syringe, the liquid of each DV is collected with a sterile syringe and sedimented for 30 min and the blades are read under a light microscope after adding eosin.

For the macroscopic study of the hydatid material, a visual description of the HF and the DV was performed. We described the puncture fluid (rock water, bilious, purulent or gelatinous) and for the DV, we studied its consistency (tense or flaccid) and its transparency (opaque or transparent).

For the microscopic study, we performed a viability study of the protoscolex of hydatid material. Indeed, 100 microliters of the sedimentation pellet of the liquid, we added the same volume of eosin to 1‰ which was put between slide and cover glass and let it act for 2 minutes, and then we observed under the light microscope at magnification × 10. Unstained protoscolex were viable and unstained protoscolex were nonviable (Fig. 1). This examination allowed us to assess the presence of viable protoscolex within all protoscolex and to calculate their percentage.

Data entry and analysis were performed using SPSS 20.0 software. The quantitative variables were described using the means, standard deviation and limits for variables with a Gaussian distribution; and in the opposite case, the median and extremes. The normality of the distribution of quantitative variables was studied using the Kolmogorov-Smirnov test. The qualitative variables were described using the calculation of the observed numbers and relative frequencies (percentages). We used the Chi-square test for the comparison of two or more frequencies, the Spearman correlation test for the study of the correlation between the quantitative variables and the t-test for the comparison of two averages when the conditions of application were verified and the Mann Whitney test in the opposite case.

To determine the thresholds of the quantitative variables, we used the ROC curve (receiver operating characteristic). For the multivariate study, we used logistic regression using the 10% threshold for viability of hydatid material. The significance level was set with an α risk at 5%.

During the study period, 27 (41%) of 66 operated HCL from 21 patients containing 248 DV were investigated in the Parasitology-Mycology laboratory. The average age of patients was 41 years with extremes ranging from 14 to 76 years. The most affected age group was between 30 and 39 years. A surgical history of hydatid cyst was observed in only four patients (19%): two patients were operated for HCL, one patient for hydatid cyst of the lung and one patient for hydatid cyst of the heart. Four patients (19%) were asymptomatic at the time of diagnosis. Pain was the main symptom and was found in 15 patients (71%). The other clinical signs were: fever in seven patients (33%), cutaneous-mucosal jaundice in three patients (14%) and acute cholangitis in four patients (19%). Liver function tests were pathological in 10 patients (47%). Eight patients (38%) presented with hepatic cholestasis. Hyperbilirubinemia was noted in five patients (62%). Hepatic cytolysis was noted in four patients (19%). 18 cysts (67%) were located in the right liver and nine (33%) in the left liver.

The median cyst size was 10 mm with extremes ranging from 37 to 170 mm. A size greater than 10 cm was found in 14 cysts (52%). 15 cysts (56%) were CE2 and contained 161 DV and 12 cysts containing 87 DV were CE3b. 15 cysts (55.5%) corresponding to 10 patients (47%) had imaging complications. Opening of the HCL into the bile duct was observed in 11 cysts (71%) and suppuration in four cysts (27%). In addition, no cyst rupture into the peritoneum or thorax was observed.

The macroscopic study of the HF at cyst puncture was rock water in nine cysts (33%), bilious in 10 cysts (37%), gelatinous in four patients (15%) and purulent in four patients (15%). The median intracystic pressure was 43 mmHg (E: 9-152). The number of DV per cyst was variable. 15 cysts (57%) had a number of DV ≥ 10. The median size of the harvested DV was 1.56 (E: 0.1–4.24). The median DV volume was 2 mL (E: 0.1–40). For DV consistency, 173 DV (69.8%) were strained and 75 DV (30.2%) were flaccid. For wall transparency, 127 DV (51.2%) were opaque and 121 DV (48.8%) were translucent. Only one DV (0.4%) contained small daughter vesicles.

The viability rate of the protoscolex of the DV was 16.7% and that of the HF was 20%. The viability rate of HF from CE3b cysts was 9.2%, whereas that of CE2 cysts was 64%.

For the analytical study of the daughter vesicles, in a bivariate study at the end of ours, fever, acute cholangitis, hyperbilirubinemia, localization in the left liver, rock water and bilious hydatid fluid, the size of the cyst ≥ 43mm, intracystic pressure ≥ 35 mmHg, DV size ≥ 6.5mm, volume ≥ 0.15 ml, number of DV/cyst ≥ 5, and opaque wall were significantly associated with DV protoscolex viability. (Tables 1 and 2) The threshold for quantitative parameters (Table 3) being determined by the ROC curve (Fig. 2).

Table 1

Predictive factors for viability of DV protoscoleces in bivariate study (qualitative criteria)
Parameters	Correlation Coefficient, r	p
Area
Age	-0.111	0.081
Hepatic assessment
AST	-0.040	0.530
ALT	-0.118	0.063
ALP	-0.092	0.147
GGT	-0.025	0.7
Total Bilirubin	0.308	< 0.001
Cyst characteristics
Cyst size	0.254	< 0.001
Intra cystic pressure	0.167	0.008
Peri-cyst thickness	-0.023	0.713
Number of DV/Cysts	0.169	0.008
HF Viability	0.017	0.089
DV characteristics
DV Diameter	0.557	< 0.001
DV Volume	0.557	< 0.001
AST : aspartate aminotransferase ; ALT: alanine aminotransferase ; ALP: Alkaline phosphatase ; GGT: Gamma-glutamyl transferase ; DV: Daughter vesicle, HF : Hydatid fluid

Table 2

Predictive factors of DV fertility in bivariate study (qualitative criteria)
Parameters		Viability (%) Average (standard deviation)	p
Area
Gender	Male (N = 143)	31.8 (35.3)	0.225
Gender	Female (N = 105)	37.9 (40.8)	0.225
Recurrent HHC	No (N = 222)	35.3 (37.9)	0.281
Recurrent HHC	Yes (N = 26)	26.8 (36)	0.281
Clinical signs
Pain	No (N = 74)	36.8 (41)	0.508
Pain	Yes (N = 174)	33.3 (36.3)	0.508
Fever	No (N = 173)	28.6 (35.1)	< 0.001
Fever	Yes (N = 75)	47.8 (40)	< 0.001
Acute angiochilitis	No (N = 220)	32.1 (37.7)	0.007
Acute angiochilitis	Yes (N = 28)	52.3 (33)	0.007
Cyst chracteristics
WHO classification	CE2	45.0 (39.5)	< 0.001
WHO classification	CE3b	14.8 (24.5)	< 0.001
Located in liver	Left liver (N = 70)	43.2 (43.9)	0.038
Located in liver	Right Liver (N = 178)	30.9 (34.6)	0.038
HF aspect
Rock water HF	No (N = 150)	27.8 (32.9)	0.001
Rock water HF	Yes (N = 98)	44.5 (42.4)	0.001
Biliary HF	No (N = 163)	30.1 (39.5)	0.009
Biliary HF	Yes (N = 85)	42.6 (32.9)	0.009
Purulent HF	No (N = 213)	39.3 (38)	< 0.001
Purulent HF	Yes (N = 35)	4.3 (15.8)	< 0.001
Gelatinous HF	No (N = 218)	37.3 (38.4)	< 0.001
Gelatinous HF	Yes(N = 30)	13.3 (24.8)	< 0.001
Complications
Cystobiliary fistula	No (N = 125)	33.7 (37)	0.318
Cystobiliary fistula	Yes (N = 123)	35.1 (38.6)	0.318
Suppurations	No (N = 218)	37.5 (38.4)	0.001
Suppurations	Yes (N = 30)	11.8 (23.1)	0.001
DV characteristics
consistency	Strained (N = 173)	34.4 (36.6)	0.991
consistency	Flaccid (N = 75)	34.4 (40.6)	0.991
Transparence	Opaque(N = 127)	39.2 (36.7)	0.042
Transparence	Translucent (N = 121)	29.5 (38.4)	0.042
HHC : hepatic hydatid cyst ; HF: hydatid fluid ; DV: daughter vesicle

Table 3

Threshold for quantitative parameters according to ROC curves
Parameters	Threshold	Se (%)	Sp (%)	VPN (%)
Size of the cyst (Fig. 2a)	43 mm	100	10	100
	95 mm	72	58	63
	125 mm	35	80	48
Intracystic pressure (Fig. 2b)	9.5 mmHg	95	1	14
	35 mmHg	68	55	59
	61 mmHg	25	84	45
Size of the DV (Fig. 2c)	6.5 mm	99	8	100
	12.7 mm	83	70	72
	16.2mm	60	89	66
Number of DV/cyst (Fig. 2d)	5	89	36	55
Number of DV/cyst (Fig. 2d)	7	71	40	51
Se: Sensitivity ; Sp: specificity ; VPN: negative predictive value ; DV: daughter vesicle

CE3b type as classified by the WHO, purulent HF, and gelatinous HF were factors significantly associated with non-viability of DV protoscoleces (Table 2).

However, other patient, cyst, and DV characteristics were not significantly associated with DV protoscolex viability.

In multivariate study, at the end of ours, CE2 type as classified by WHO, bilirubinemia > 9.5 µmol/L, number of DV/cyst ≥ 5, bilious hydatid fluid, intracystic pressure ≥ 35 mmHg, DV volume > 0.15 ml, and DV size ≥ 6.5 mm were significantly associated with DV protoscolex viability (Table 4). Age and purulent hydatid fluid were significantly associated with non-viability of DV protoscoleces. (Table 4).

Table 4

Predictive factors of DV fertility in multivariate study (all parameters included)
Predictive factors for the viability of DV protoscoleces	Odds Ratio	Confidence interval (95%)	p
Age (years)	0.8	0.5–1.1	0.001
WHO classification (CE2)	3.3	1.06–10.2	0.03
TB > 9.5 µmol/L	6.14	2.4–15.65	< 0.001
Number of DV /cyst ≥ 5	10.12	3.11–17.13	0.007
Biliary HF	5.63	2.44–13.29	< 0.001
Purulent HF purulent	0.13	0.02–0.66	0.014
Intracystic pressure ≥ 35 mmHg	8.5	3.3–21.37	< 0.001
DV volume ≥ 0.15 ml	11.31	5.14–24.9	< 0.001
DV size ≥ 6.5 mm	18.8	4.69–32.90	0.012
DV: daughter vesicle ; TB : Total bilirubin, ; HF: Hydatid fluid

Including only preoperative parameters, it was found that in multivariate analysis, CE2 type as classified by WHO, bilirubinemia > 9.5 µmol/L, cyst size ≥ 43mm, number of DV/cyst ≥ 5, and DV size > 6.5 mm were significantly associated factors with DV protoscolex viability. Age was a factor significantly associated with non-viability of DV protoscoleces. (Table 5)

Table 5

Predictive factors of DV fertility in multivariate study (preoperative parameters)
Predictive factors for the viability of DV protoscoleces preoperatively	Odds Ratio	Confidence interval (95%)	p
Age	0.5	0.2–0.7	0.003
WHO classification (CE2)	22	18–38	0.001
TB > 9.5 µmol/L	1.7	1.04–2.36	0.001
Cyst size ≥ 43mm	2.2	1.3–4.1	0.001
Number of DV /cyst ≥ 5	2.7	3.11–17.13	0.05
DV size ≥ 6.5mm	11.4	5.8–17.1	0.001
DV: Daughter Vesicle ;TB: Total Bilirubin

At the end of this study, we found that the viability of the DV is associated with the size of the cyst, the number of DV per cyst, the size of the DV. Added to that, the non-viability of the DV is associated with CE3b type as classified by the WHO. Could these findings help us in the therapeutic management of the CE3b cyst?

There is little works on the viability of protoscoleces. The results vary from one series to another due to the non-standardization of the methodologies applied to the study of parameters [1, 2, 4, 10–14]. These works are only interested in the study of hydatid fluid from cysts in humans and animals.

Attached is a table of the different studies which were all retrospective. Only one prospective study on this subject was carried out by the team of El Saftawy A [14]. (Table 6) However, in the literature, no work has addressed the study of protoscolex viability within DV. Therefore, the management of hydatid cysts type CE3b (multivesicular cyst with mastic content) remains uncodified due to the lack of knowledge of the evolutionary process of DV. This is why this would be the first study which is interested in the content of the daughter vesicles of HCL which found that the DV can contain protoscolex which can be viable or non-viable.

Table 6

Summary table of the different studies analyzing the viability of protoscoleces for hydatid fluid
	Year	Type of study	Number	Location of cyst	Viability
Tsimoyiannis EC, ¹⁰	2000	Retrospective	28	Liver (Human)	60%
Dueger E, ¹¹	2001	Retrospective	212	Liver (animal)	73.2%
Monterola C, ¹²	2006	Retrospective	163	Liver ( human )	42%
Bygott JM, ⁴	2010	Retrospective	63	Liver Lung (human)	62%
Bygott JM, ⁴		Retrospective		Liver Lung (human)	70%
Zait H, ¹	2013	Retrospective	78	Liver and lungs (human)	74%
El Saftawy A, ¹⁴	2021	Prospective	40	Liver (Human)	Viability according to the therapeutic protocol

To this day, the therapeutic strategy for HCL remains non-consensual [15] and is based on the characteristics of the cyst, particularly its activity, surgical expertise, the technical platform available and the adherence of patients to long-term surveillance [16, 17].

While the therapeutic indications are increasingly codified for active cysts (I/II Gharbi and CE1/CE3a) candidate for aspiration or surgery and inactive cysts (IV/V Gharbi and CE4/CE5) [3–8] candidate for surveillance, those of cysts with transient activity, especially CE3b are not codified. Indeed, the 2 therapeutic modalities: surgery and surveillance: 'Wait and Watch' procedure, can be proposed [3, 18, 19]. The results are contradictory in the literature and are not very precise. Some authors are in favour of ‘Wait and Watch' procedure, considering that these cysts with gelatinous contents have the same characteristics as the CE4 cyst, while others are in favour of surgery, since they know nothing about the evolutionary process of the DV they contain.

In this study, we found that the predictive factors for non-viability of DV protoscoleces for the inherent preoperative parameters of the cyst and DV were CE3b type, cyst size < 4.3cm, DV size < 6.5 mm, and number of DV/cyst < 5 with a statistically significant association (p = 0.001; 0.001, 0.001, and 0.05, respectively). Thus, we could infer that gelatinous CE3b cysts with size < 4.3 cm with largest DV size < 6.5 mm and number of DV/cyst < 5 have inactive DV, and thus we could propose 'Wait and Watch' procedure for these patients. Otherwise, for CE3b cysts with DV that do not have the criteria for inactivity, we could propose surgery due to lack of knowledge of the activity of hydatid fluid of this type.

However, a prospective study of the viability of hydatid fluid from cysts essentially type CE3b with a calculation of the number of HF required is essential to complete our conclusions.

The management of liver hydatid cysts requires a better understanding of aspects related to the survival of the parasite, particularly protoscolex. Both daughter vesicles and hydatid fluid from cysts may be viable. The predictive factors for viability of daughter vesicles are: cyst size ≥ 43mm, DV size ≥ 6.5mm, number of DV per cyst ≥ 5, and WHO CE2 type. CE3b cysts with DV that do not meet these criteria may be candidates for a surveillance or 'Wait and Watch' procedure.

Availability of data and materials : Aymen Trigui ([email protected])

Competing interests : The authors declare that they have no ties of interest.

Funding : Not applicable

Authors' contributions :

Aymen Trigui : Management protocol, wrote the main manuscript text

Nahed Khmekhem : wrote the main manuscript text

Sami Fendri : wrote the main manuscript text

Rahma Daoud : wrote the table

Amira Akrout : data analysis

Jihene Trabelsi : data analysis

Rafik Mzali : Management protocol

Fatma Cheikhrouhou : data collection

Ali Ayadi : organization of the study

Chedli Dziri : manuscript review

Mohamed ben amar : data analysis, organization of the study

Saleh Boujelbene : organization of the study

Acknowledgement (optional) : Not applicable

Authors' information (optional) : Not applicable

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

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No competing interests reported.

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TITRE: Viability predictive factors of the daughter vesicles in hepatic hydatid cyst

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