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Role of portal color Doppler ultrasonography as noninvasive predictive tool for esophageal varices in cirrhotic patients

Role of portal color Doppler ultrasonography as noninvasive predictive tool for esophageal... Background: Esophageal varices (EV ) is the most common apprehensive complication of portal hypertension in patients with cirrhotic liver. Guidelines recommend Upper gastro‑intestinal endoscopic screening for EV in patients with newly diagnosed chronic cirrhosis (Imperiale et al. in Hepatology 45(4):870–878, 2007). Yet, it is invasive, time consuming and costly. To avoid unnecessary endoscopy, some studies have suggested Doppler ultrasound exami‑ nation as simple, and noninvasive tool in prediction and assessment of severity of EV (Agha et al. in Dig Dis Sci 54(3):654–660, 2009). Our study was to assess the role of different Doppler indices of portal vein, hepatic and splenic arteries as a noninvasive tool for prediction of esophageal varices in cirrhotic patients. Results: This prospective case control study was conducted on 100 cirrhotic liver patients and 100 of healthy volunteers as control group. Patients were subjected to clinical examination, upper gastrointestinal tract endoscopy, abdominal ultrasonography with duplex Doppler evaluation of different portal Doppler hemodynamic indices were done for each patient. The results revealed that portal vein diameter, hepatic artery pulsatility index, portal hyper‑ tensive index, portal vein flow velocity, portal congestion index have high sensitivity for prediction of EV. However, Splenic artery resistance index, hepatic artery resistance index HARI, liver vascular index and platelet count/spleen diameter have less sensitivity for prediction of EV. Conclusion: Measuring the portal hemodynamic indices can help physicians as noninvasive predictors of EV in cir‑ rhotic patients to restrict the need for unnecessary endoscopic screening especially when endoscopic facilities are limited. Keywords: Oesophageal varices, Portal hypertension, Doppler ultrasound Esophageal varices is the most common clinical mani- Background festation of portal hypertention. Bleeding varices is the Portal hypertension is defined as hepatic venous pressure most apprehensive complication contributing to high gradient (HVPG) greater than 5 mmHg. HVPG is a sur- morbidity and mortality [2].The mortality associated with rogate for the portosystemic pressure gradient. Clinically each episode of variceal bleeding ranges from 17 to 57% significant portal hypertension is defined as a gradient [3]. greater than 10 mmHg and variceal bleeding may occur Because of the impact of upper gastrointestinal bleed- at a gradient greater than 12 mmHg [1]. ing caused by rupture of EV in the prognosis of cirrhotic patients; the Baveno IV 2005 Consensus Workshop [1, 4] *Correspondence: drmkamel01@gmail.com 2 have determined that every patient diagnosed with cir- Department of Radiodiagnosis and Interventional Radiology, Menoufia University Faculty of Medicine, Shebeen El‑Kom, Egypt rhosis should be investigated for EV, regardless of Child Full list of author information is available at the end of the article class and the cause of liver cirrhosis [5]. © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Nouh et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 2 of 11 Franchis, et  al. concluded that, endoscopic screening Examination protocol of all patients with liver cirrhosis would result in a large All patients were subjected to the following number of unnecessary endoscopies, additional burden to endoscopic units, high cost and the patient compliance • Full clinical assessment it was done by tropical with the screening program may be reduced. For these medicine specialist whose experience more than reasons, several studies have examined how to identify 5 years in the clinical field. It includes: patients with varices using noninvasive or minimally invasive methods to avoid endoscopy in patients with a • History taking With stress on history of haema- low risk of varices [6]. temesis and melena, abdominal swelling, hepatic Various studies have suggested using ultrasonographic encephalopathy, fever, edema of lower limbs and examination as simple, inexpensive, accurate and non- jaundice. invasive technique. Moreover, various Doppler ultra- • Complete General and Local examinations With sonographic indices have been shown to be of value stress on signs of liver cell failure. in assessment of the severity of EV or risks of variceal • Laboratory investigations including Complete bleeding in patients with cirrhosis. blood count. Liver function tests, Viral markers and Renal function tests. • Child-Pugh classification was calculated for all Methods studied patients to assess the severity of liver dis- Study population ease, depending on patients’ clinical and labora- This prospective case control study was conducted on tory data (16). 100 cirrhotic patients and 100 healthy volunteers as a control group. Cirrhotic patients were selected from • Ultrasound examination (including grey scale 670 patients attending the outpatient and\or inpatient and Doppler) was done to all patients and control department of Tropical Medicine and radiology depart- groups by the same consultant radiologist blinded ment, in the period between October 2017 and August to study design with experience in Doppler ultra- 2019. 570 patients were excluded due to presence of sound more than 12 years. exclusion criteria. Patients with liver cirrhosis, regardless the etiology • The procedures was done by the equipment of cirrhosis, were included in this study. While with Toshiba Nemio XG apparatus (Toshiba, Japan) of patients with hepatocellular carcinoma, active GIT by with B-mode and color Duplex Doppler ultra- bleeding, portal vein thrombosis, splenectomy or with sound at ultrasound unit of radiology depart- other severe medical condition; end stage renal disease ment. congestive heart failure or severe respiratory syndrome, • All patients were kept in a fasting state 6 h before were excluded. they were examined in the supine, right and left Patients were classified into two groups lateral positions during quiet respiration using a Cirrhotic group (Group 1) were 100 patients; 57(57%) 2–5 MHz convex probe in transverse and longitu- males and 43(43%) females. Their ages ranged from 36 to dinal scans. 78 years (50.49 ± 14.35). They were further classified into • B-mode Pelvi-abdominal ultrasound includes two subgroups after upper GI endoscopy; Group1-A: 67 evaluation of: Cirrhotic patients with esophageal varice and Group1-B: 33 Cirrhotic patients without esophageal varices. • Liver as regarding its size, echopattern, cirrho- Control group (Group 2) were 100 of healthy volun- sis, and focal lesions. teers; 69(69%) males and 31(31%) females. Their ages • Portal vein diameter (PVD; mm): It is measured ranged from 39 to 54 years (39.21 ± 13.98). at the hepatic hilum while the patient was in the The study was approved by the local Research Eth - supine position or in the left lateral decubitus ics Committee of our institute; the reference number of position. approval: 10/2017-TROP-9. All patients and controls • Portal vein cross sectional area was measured. included in this research gave written informed consent • Spleen as regarding its size, echopattern and to participate in this research. focal lesions. Nouh  et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 3 of 11 • Ascites as regarding amount (minimal, moder- endoscopy that was performed using a videoscope ate or marked) and evidence of echoes, adhe- (CLV-240; Olympus Ltd, Tokyo Japan) after fast- sions or loculations. ing 6  h prior to endoscopy, positioned in left lat- eral position and given suitable sedation. • Possible complications of procedures were • Duplex Doppler ultrasound for assessment of: explained to the patients and their relatives and • Portal venous system hemodynamics; includes written informed consents were obtained before assessment of: the endoscope. • Portal vein patency and blood flow velocity (PVFV) • Esophageal varices were graded by Paquet [13] (cm/s): grading system according to their size and depending on the degree of protrusion of varices • PVFV was measured in its mid-portion and was into esophageal lumen when the esophagus was automatically calculated on samples of the Dop- maximally relaxed. pler signal lasting more than 4  s. Three measure - ments were obtained and the average was used. Normal PVFV was (15–20 cm/s) [7]. • Grade 0 Absence of esophageal varices. • Grade I Microcapillaries on esophagogastric • Portal congestion index (PCI) was calculated using transition or distal esophagus. the following equation [8]: • Grade II 1 or 2 small varices located on distal Cross - sectional area of the portal vein (cm2) • PCI = esophagus. Mean portal vein velocity(Vmean)(cm/s) • Grade III Medium sized varices. • Hepatic and splenic arterial hemodynamics • Grade IV Large varices in any part of the esoph- includes assessment of: agus. • Hepatic artery resistance index (HARI) was calcu- lated automatically using the following equation [9]: Statistical analysis peak systolic velocity (V max)−end diastolic velocity(Vmin) HARI = peak systolic velocity(V max) • Data were collected, tabulated, statistically analyzed • Hepatic artery pulsatility index (HAPI) was calcu- using an IBM personal computer with Statistical lated automatically using the following equation [10]: Package of Social Science (SPSS) version 22 (SPSS, Inc, Chicago, Illinois, USA). Quantitative data were peak systolic velocity(Vmax)−end diastolic velocity(Vmin) HAPI = mean velocity(Vmean) presented in the form of mean ( X ), standard devia- • Splenic artery resistance index (SARI) was measured tion (SD), range, and qualitative data were presented automatically using the following equation [11]: in the form of numbers and percentages. The signifi - cance were assessed using the chi-square(χ ) and Z peak systolic velocity(V max)−end diastolic velocity(V min) SARI = peak systolic velocity(V max) test (z) to study association between two qualitative • Liver vascular index (LVI) was calculated using this variables, Student t-test for comparison between two equation [10]: groups having quantitative variables, Mann–Whitney and Kruskal–Wallis tests for comparison between Portal venous flow velocity(PVFV) • LVI = Hepatic arterial pulsatility index (HAPI) two or more groups not normally distributed hav- • Portal hypertensive index (PHI) was calculated using ing quantitative variables. Logistic regression model this equation [11] as a predictive analysis test used to describe data and to explain the relationship between one dependent (HARI*0.69)×(SARI*0.87) • PHI = Portal vein mean velocity(Vmean) binary variable and one or more nominal, ordinal, • Calculation of platelet count/spleen diameter (PC/ interval or ratio-level independent variables. The SD) ratio by dividing number of platelets/ml by the receiver operating characteristic (ROC) curve was maximum bipolar diameter of spleen in millimeters performed to determine. The cutoff value with the estimated with pelvi abdominal ultrasound [12]. highest accuracy was selected as the diagnostic cut- • Upper GIT endoscopy was done by to patients group off points. Sensitivity, specificity, positive predictive by the same tropical medicine consultant blinded to value (PPV), and negative predictive value (NPV) study design with experience in GIT endoscopy more were determined. p value was considered significant than 15 years. if less than 0.05 and highly significant if less than 0.001 (Figs. 1, 2, 3). • All patients with positive data after duplex Dop- pler ultrasound underwent upper gastrointestinal Nouh et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 4 of 11 Fig. 1 67 Y male patient with chronic liver disease, a presents Doppler U/S of hepatic artery with HAPI: 2.60 and HARI: 0.84. b Presents Doppler U/S of splenic artery with SARI: 0.82, the splenic bipolar diameter is 15.3 cm. c PResents Doppler U/S of PV with MVPV: 9.4 cm/s. PV diameter is 15.0 mm. d UGIE revealed grade IV oesophageal varices. Results There was no statistical significant difference between As regards the demographic data of the studied cirrhotic the measured portal hemodynamic indices and the grade groups, there was no statistical significant difference of EV (p value > 0.05) except PC/SD ratio and PVD (p between the studied groups as regarding age and sex (p value < 0.001), Table 6. value > 0.05), Table 1. A logistic regression model showed that Portal hyper- As regards the child classification, There was high tensive index and Portal vein diameter are good predic- statistical significant difference between group 1A and tors of the presence of esophageal varices more than group 1B (p value < 0.001), Table 2. Liver vascular index Table 7. There was statistical significant difference between The accuracy of PC/SD ratio and portal hemodynamic group 1A and group 1B as regarding, liver echogenic- indices in prediction of esophageal varices are shown in ity, spleen size, splenic collaterals and ascites (p value < Table 8. 0.05) but, there was no statistical significant difference between group 1A and group 1B as regarding liver size (p Discussion value > 0.05), Table 3. Variceal bleeding occurs in 20–40% of cirrhotic patients There was high statistical significant difference between with esophageal varices and is associated with a high cirrhotic group and control group as regarding PVFV, morbidity and mortality [2]. The Baveno IV 2005 Con - PCI, HARI, HAPI, SARI and PHI (p value < 0.001) but, sensus Workshop [1, 4] have determined that every there was no statistical significant difference as regarding patient diagnosed with cirrhosis should be investigated PVD and LVI (p value >0.05), Table 4. for EV, regardless of Child class and the cause of liver cir- there was high statistical significant difference between rhosis [5]. group 1A and group 1B as regarding PC/SD ratio and all Several studies have examined how to identify patients measured portal hemodynamic indices (p value < 0.001), with varices using noninvasive methods to avoid Table 5. large number of unnecessary screening endoscopy in patients with a low risk of varices [6]. Various portal Nouh  et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 5 of 11 Fig. 2 52 y male patient with chronic liver disease, a presents Doppler U/S of hepatic artery with HAPI: 1.27 and HARI: 0.81. b Presents Doppler U/S of splenic artery with SARI: 0.62, the splenic bipolar diameter is 18 cm. c Presents Doppler U/S of PV with MVPV: 19.6 cm/s. PV diameter is 14 mm. ascites was also noticed. d UGIE revealed grade III oesophageal varices. haemodynamic indices have been shown to be predic- that, patients in Child B or C are nearly 3 times more tive of the severity of EV or risks of variceal bleeding in likely to have varices than those in Child A. patients with cirrhosis [14]. Concerning pelvi-abdominal ultrasound findings, This prospective case control study was conducted there was high statistical significant difference between on 2 groups: group 1, 100 cirrhotic patients which was group1A and group1B regarding portal vein diameter classified into two subgroups after upper GI endoscopy; (PVD), liver echogenecity, spleen size, and splenic collat- group1A, cirrhotic patients with esophageal varices and erals (p value < 0.001). These results were in agreement Group1B, cirrhotic patients without esophageal varices, with Faisal et  al. [20], and Khalil et  al. [21], who con- and group 2, 100 of healthy volunteers as a control group. cluded that, increased PVD, splenomegaly and presence As regards the demographic data of the studied cir- of splenic collaterals by ultrasound can predict EV spe- rhotic groups, 57% of cirrhotic patients were males and cially the large varices. However, This result was in con - 43% were females. Their ages ranged from 36 to 78 years troversy with Berzigotti et al. [22], who found that, there (49.31 ± 14.27) in group 1A and (52.88 ± 14.45) in group was no significant change in liver echogenicity in cir - 1B. these observations go in agreement with with Tharwa rhotic patients with varices than patients without varices. et al. [15], where males were 59.4% and Hekmatnia et al. In our study, there was no significant difference in PVD [16], who found that, the mean age was 52.1 years (range: (mm) in cirrhotic patients (12.4 ± 3.2) compared with 28–83 years). the controls (12.1 ± 1.2) with (p value >0.05). However, In our study, there was high statistical significant differ - There was high significant increase in PVD in group 1A ence between group 1A and group 1B as regarding child (13.9 ± 2.2) than group 1B (9.4 ± 2.8) with (p value < classification (p value < 0.001). This was proven by [17], 0.001) with high statistical significant increase with the Nashaat et  al. [18], and Zaman et  al. [19], who reported grades of EV with (p value < 0.001). These results were Nouh et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 6 of 11 Fig. 3 51y female patient with chronic liver disease, a presents Doppler U/S of hepatic artery with HAPI: 1.6 and HARI: 0.72. b presents Doppler U/S of splenic artery with SARI: 0.45, the splenic bipolar diameter is 14.5 cm. c presents Doppler U/S of PV with MVPV: 13.6 cm/s. PV diameter is 11.5 mm. d UGIE revealed grade I oesophageal varices. Table 1 Demographic data of the studied groups Variable Group1A Group1B Control group Test of significance Cirrhotic Pt. with EV Cirrhotic Pt. without EV (n = 100) (n = 67) (n = 33) M ± SD M ± SD M ± SD Age 49.31 ± 14.27 52.88 ± 14.45 50.33 ± 13.3 (Kruskal–Wallis test) NS < 0.48 N (%) N (%) N (%) Sex Male 40(59.7%) 17(51.5%) 69(69%) χ test = 3.72 NS Female 27(40.3%) 16(48.5%) 31(31%) 0.16 NS no significant difference in agreement with Anda et al. [23], Sarwar et al. [24] and not sensitive to presence of cirrhosis or in differentiation Kayacetin et  al. [25] who found an association between between the grades of EV presence. an increase in PVD with liver cirrhosis, presence and In our study, at a cutoff point (10.4), the sensitiv - grading of EV as well. But these results were in disagree- ity of PVD that can predict EV was 94.03%, the speci- ment with Jaheen et al. [26], who concluded that, PVD is ficity was 75.76%, PPV was 88.73%, NPV was 86.21%, Nouh  et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 7 of 11 Table 2 Child classification of the studied groups in PC/SD ratio by increase in spleen size and thrombo- cytopenia which usually occur with increase of portal Child Group 1A Group 1B Test of p Value pressure and with development of varices especially classification (n = 67) (n = 33) significance with larger risky varices. A:31 13(19.4%) 18(54.5%) χ test 0.001* Our study showed that, at cutoff point (604), the sen - B:33 23(34.3%) 10(30.3%) 14.86 sitivity of PC/SD ratio that can predict the presence of C:36 31(46.3%) 5(15.2%) EV was 61.19%, the specificity was 90.91 %, PPV was *High significant difference, P < 0.001 93.18%, NPV was 53.57 %, accuracy was 71.00% and AUC = 0.883. These results were in agreement with studies of Shekar et al. [12], Sheta et al. [30] and Nouh et  al. [27], who reported that, at cut-off values around Table 3 Pelvi abdominal ultrasound findings of the studied (600), PC/SD ratio that can predict EV with similar sen- groups sitivity, specificity , PPV & NPV. Group 1A Group 1B Test of p Value Regarding the measured portal hemodynamic indi- (n = 67) (n = 33) significance ces by Duplex Doppler ultrasound, there was high sig- N (%) N (%) nificant decrease of portal vein flow velocity (PVFV) NS Liver size Fisher exact 0.22 (cm/s), in cirrhotic patients (15.3 ± 5.1) compared with 3.1 Shrunken 22(32.8%) 6(18.2%) controls (18.2 ± 2.9) with (p < 0.001) with high signifi - (< 12 cm) cant decrease in in group 1A (12.2 ± 2.3) than group 1B Normal 44(65.7%) 27(81.8%) (21.4 ± 3.2) with (p value <0.001). Studies were done (12–16 cm) by Elhady et al. [29], Mahmoud et al. [31] and Liu et al., Enlarged 1(1.5%) 0(0%) [32] reported that (PVFV) was significantly lower in (> 16 cm) cirrhotic patients than controls. Anda et  al. [23] and Splenic size χ test 63.4 < 0.001* Elbarbary et  al. [33] Also, found that, PVFV was lower Normal 1(1.5%) 25(75.8%) (7–11 cm) in patients with EV. In contrast, Schneider et  al. [34] Enlarged 66(98.5% 8(24.2%) and Piscaglia et  al. [35] reported that, no change in (> 11 cm) PVFV between patients and controls. This may be due Liver echogenecity χ test 15.97 < 0.001* to intra- and inter observer variability or presence of Coarse 60(89.6%) 18(54.5%) collaterals which affect the velocity. Homogeneous 7(10.4%) 15(45.5%) Our study showed that, at cutoff point (15.2), the Splenic collaterals χ test 22.46 < 0.001* sensitivity of PVFV that can predict EV was 89.55%, Yes 37(55.2%) 2(6.1%) the specificity was 93.94%, PPV was 96.77%, NPV was No 30(44.8%) 31(93.9%) 81.58%, accuracy was 91.00% and AUC = 0.953. These Ascites χ test 11.86 0.008* results were in agreement with Minal et  al. [36] who No 23(34.3%) 23(69.7%) reported that, PVFV had a high sensitivity 84% for Mild 11(16.4%) 4(12.1%) detecting the EV. Moderate 19(28.9%) 4(12.1%) Regarding the portal congestion index (PCI) there Marked 14(20.9%) 2(6.1%) was a significant increase in cirrhotic patients (0.11 ± *High significant difference, P < 0.001 0.045) compared with the controls (0.071 ± 0.012) and increase in group 1A (0.1 ± 0.03) than group1B (0.05 ± 0.0.1) with (p value < 0.001). These results were in accuracy was 88% and AUC = 0.877. These results were agreement with Kayacetin et  al. [25] who found that, in agreement with Berzigotti et al. [22] and Nouh et al. PCI was significantly increased in cirrhotic group and [27] who found the best cut-off value of PVD for EV in presence of EV. prediction was (10.7) and (11.5) respectively. At cutoff point (0.1), the sensitivity of PCI that can pre - Regarding platelet count/spleen diameter ratio (PC/ dict EV was 89.35%, the specificity was 92.84%, PPV was SD), there was high statistical significant difference in 95.66%, NPV was 82.5%, accuracy was 93% and AUC = group 1A (546 ± 290.9) than group 1B (1135 ± 413.2) 0.948. this was in agreement with Moriyasu et al. [8], who and the grades of EV (725.6 ± 273.5) (567.9 ± 280.2) found that, cutoff point was (0.189) in patients with EV (347.8 ± 162.6) (293.8 ± 91.8) in grades I, II, III and with sensitivity (84.65%) and Lee et  al. [37], who found IV respectively as well (p value < 0.001). This result was that PCI cutoff point was (0.089). in agreement with Shekar et  al. [12], Agha et  al. [28], Regarding arterial indices including HARI, HAPI and Elhady et al. [29], who who explained the decrease and SARI, there was high significant increase in the in Nouh et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 8 of 11 Table 4 Comparison of portal vein diameter and different hemodynamic indices by B‑mode and color Doppler US between cirrhotic group and control group Normal values Cirrhotic group (G1) Control group (G2) p Value (Mann– (n = 100) (n = 100) Whitney test) M ± SD M ± SD Portal vein flow velocity (PVFV ) 15.3 ± 5.1 18.2 ± 2.9 < 0.001* (15–20 cm/s) NS Portal vein diameter (PVD) 12.4 ± 3.2 12.1 ± 1.2 0.38 (10–13 mm) Portal congestion index (PCI) 0.11 ± 0.045 0.071 ± 0.012 < 0.001* (0.07–0.1) Hepatic artery resistive index (HARI) 0.71 ± 0.052 0.51 ± 0.03 < 0.001* (0.5–0.7) Hepatic artery pulsatility index (HAPI) 1.34 ± 0.12 1.01 ± 0.04 < 0.001* (0.9–1) Splenic artery resistive index (SARI) 0.7 ± 0.05 0.5 ± 0.06 < 0.001* (0.5–0.7) Portal hypertensive index (PHI) 2.23 ± 0.85 1.38 ± 0.53 < 0.001* (1.3–1.8) NS Liver vascular index (LVI) 11.77 ± 4.95 11.61 ± 3.2 0.78 (10–15) NS = no significant difference, P > 0.05 *High significant difference, P < 0.001 accuracy was 84.00% and AUC = 0.881. Concerning Table 5 Comparison of different predictors in the studied SARI, at cutoff point (0.72), the sensitivity of SARI that groups in relation to presence of esophageal varices can predict EV was 77.61%, the specificity was 92.56%, Group 1A Group 1B p value PPV was 93.98%, NPV was 68.75%, accuracy was 85% (n = 67) (n = 33) (Mann– M ± SD M ± SD Whitney and AUC = 0.888. These results were in agreement with test) Child et  al. [41] and Dib et  al. [42]who found that, the presence of EV affect all measured hepatic and splenic Platelet count/spleen diam‑ 546 ± 290.9 1135 ± 413.2 < 0.001* eter (PC/SD) ratio arterial hemodynamic parameters with the best cut off Portal vein flow velocity 12.2 ± 2.3 21.4 ± 3.2 < 0.001* point for SARI for prediction of EV was (0.76) with sensi- Portal vein diameter 13.9 ± 2.2 9.4 ± 2.8 < 0.001* tivity of 85% and specificity of 77.5%. Portal congestion index 0.1 ± 0.03 0.05 ± 0.01 < 0.001* This study showed that, at cutoff point(1.3), the sensi - Hepatic artery resistive index 0.7 ± 0.03 0.6 ± 0.03 < 0.001* tivity of HAPI that can predict EV was 94.03%, the speci- Hepatic artery pulsatility index 1.4 ± 0.09 1.2 ± 0.1 < 0.001* ficity was 66.67 %, PPV was 85.14%, NPV was 84.62 %, Splenic artery resistive index 0.7 ± 0.02 0.64 ± 0.02 < 0.001* accuracy was 85.00% and AUC = 0.858. These results Portal hypertensive index 2.7 ± 0.46 1.2 ± 0.3 < 0.001* were in agreement with a study of Haktanir et  al. [43], Liver vascular index 8.8 ± 1.88 17.8 ± 3.57 < 0.001* who reported that, HAPI was significantly higher in EV with a cutoff point (1.28). *High significant difference, P < 0.001 In this study there was no statistical significant differ - ence between the measured portal hemodynamic indices cirrhotic patients than the controls (p < 0.001) with SARI and the grade of EV (p value > 0.05) except PC/SD ratio showed high statistically significant difference between and PVD as fore-mentioned. These results were in agree - group 1A and group 1B (p value < 0.001), These results ment with a study done by Hekmatnia et  al., who found were in agreement with Park et al. [38], Zhang et al. [9], that, there was no significant relationship between PCI, Piscaglia et al. [35] Dewidar et al. [39] and Nicolau et al. arterial resistance and pulsatility indices and the grades [40] who found increase in the arterial indices in cirrhotic of EV [16]. patients than in controls and in pateints with varices than In contrast, results published by Anda et  al. [23], patients without. showed a significant increase in PCI, HARI and HAPI This study showed that, at cutoff point (0.71), the sensi - with higher grades of EV, this could be attributed to the tivity of HARI that can predict EV was 76.12%, the speci- difference in the number of selected cirrhotic patients ficity was 91.23%, PPV was 92.11%, NPV was 67.35%, Nouh  et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 9 of 11 Table 6 Comparison of different predictors in the studied groups in relation to the grade of esophageal varices Esophageal varices Grade 1 Grade 2 Grade 3 Grade 4 p value N = 67 (n = 26) (n = 18) (n = 14) (n = 9) (Kruskal Wallis test) M ± SD M ± SD M ± SD M ± SD PC/SD ratio 725.6 ± 273.5 567.9 ± 280.2 347.8 ± 162.6 293.8 ± 91.8 < 0.001* NS Portal vein flow velocity 12.7 ± 2.4 12.2 ± 1.2 11.9 ± 3.5 11.7 ± 1.3 0.327 Portal vein diameter 12.67 ± 2.24 14.14 ± 1.7 14.74 ± 1.79 14.68 ± 1.7 0.001* NS Portal congestion index 0.13 ± 0.03 0.14 ± 0.03 0.14 ± 0.03 0.14 ± 0.03 0.551 NS Hepatic artery resistive index 0.7 ± 0.03 0.7 ± 0.03 0.7 ± 0.03 0.7 ± 0.03 0.962 NS Hepatic artery pulsatility index 1.4 ± 0.08 1.4 ± 0.12 1.4 ± 0.07 1.3 ± 0.08 0.303 NS Splenic artery resistive index 0.7 ± 0.02 0.7 ± 0.02 0.7 ± 0.02 0.7 ± 0.01 0.390 NS Portal hypertensive index 2.7 ± 0.65 2.7 ± 0.31 2.5 ± 0.51 2.8 ± 0.27 0.210 NS Liver vascular index 9.1 ± 1.98 8.6 ± 1.11 8.6 ± 2.8 8.7 ± 1.25 0.581 NS = no significant difference, P > 0.05 *High significant difference, P < 0.001 and different degree of decompensation between these specificity > 70% when comparing cirrhotic patients with studies [23]. controls and also in agreement with Faisal et al. [20] who Regarding portal hypertensive index (PHI) there was found that, PHI showed statistically significantly higher high statistical significant increase in PHI in cirrhotic values in patients with EV than those without EV. group than control group with (p value < 0.001), with At cutoff point (1.48), the sensitivity of PHI that can high statistical significant increase in PHI in group 1A predict EV was 92.43%, the specificity was 93.94 %, PPV than group 1B with (p value < 0.001) . this was in agree was 97.10%, NPV was 96.45%, accuracy was 95.00% and AUC = 0.992. %. These results were in agreement with ment with Iwao et  al. [44] who found that, PHI had a Abu El Makarem et al. [45] who found that, only PHI had Table 7 Logestic regression model to predict the presence of an independent predictive value of EV and suggested the esophageal varices in the studied groups beginning of endoscopic screening in patients with com p Value Odds ratio 95% CI pensated cirrhosis at a cutoff point of PHI (> 2.08). As regards, the liver vascular index (LVI), there was Liver vascular index 0.202 0.688 0.387–1.222 no significant difference in cirrhotic patients compared Portal hypertensive index 0.021 0 0–0.231 with the controls (p value > 0.05), this result was in con- Portal vein diameter 0.029 0.520 0.289–0.935 troversy with Jaheen et al. [26], who found that, LVI was Table 8 Accuracy of PC/SD ratio and portal hemodynamic indices in prediction of esophageal varices Index Cutoff Sensitivity (%) Specificity (%) PPV (%) NPV (%) Accuracy (%) AUC PC/SD ratio 604 61.19 90.91 93.18 53.57 71.00 0.883 Inversely proportional Portal vein flow velocity (cm/s) 15.2 89.55 93.94 96.77 81.58 91.00 0.953 Inversely proportional Portal vein diameter (mm) 10.4 94.03 75.76 88.73 86.21 88 0.877 Directly proportional Portal congestion index 0.1 89.35 92.84 95.66 82.5 93 0.948 Directly proportional Hepatic artery resistive index 0.71 76.12 91.23 92.11 67.35 84.00 0.881 Directly proportional Hepatic artery pulsatility index 1.3 94.01 66.67 85.14 84.62 85.00 0.858 Directly proportional Splenic artery resistive index 0.72 77.61 92.56 93.98 68.75 85 0.888 Directly proportional Portal hypertensive index 1.48 92.43 93.94 97.10 96.45 95.00 0.992 Directly proportional Liver vascular index 9.4 74.63 96.97 98.04 65.31 82.00 0.973 Inversely proportional Nouh et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 10 of 11 vein diameter; PVFV: Portal vein flow velocity; SARI: Splenic artery resistance significantly lower in cirrhotic patients than controls with index; UGIE: Upper gastrointestinal endoscopy. (p value = 0.018). There was high statistical significant decrease in LVI Acknowledgements There is no acknowledgement. in group 1A than group 1B with (p value < 0.001), this result was in agreement with a study done by Faisal et al. Authors’ contributions [20], who found that, LVI was lower in patients with EV MN, MK, AA and ME contributed equally to study design, data collection, analysis, and interpretation of results. All authors read and approved the final (p value=0.001). manuscript. At cutoff point (9.4), the sensitivity of LVI that can pre - dict EV was 74.63%, the specificity was 96.97 %, PPV was Funding There is no funding. 98.04%, NPV was 65.31 %, accuracy was 82.00% and AUC = 0.973. These results were in agreement with Haktanir Availability for data and materials et al. [43], who found that, the best cut off point for LVI Data will be available upon request via contacting the corresponding author. for prediction of EV was (10.36) with sensitivity of 85% and specificity of 77% and concluded that, LVI was a high Declarations sensitive and specific parameter in the diagnosis and pre - Ethics approval and consent to participate diction of EV. All study procedures were conducted in accordance with Helsinki and were However, Piscaglia et al., and Jeon et al., have reported approved by the ethical committee of Menoufia Faculty of medicine council, reference number 10/2017‑ TROP‑9. All patients and controls included in this different findings in the measured portal hemodynamic research gave written informed consent to participate in this research. indices compared with the present study results. They reported that, Doppler measurements were not useful in Consent for publication All patients included in this research gave written informed consent to publish distinguishing patients with liver cirrhosis from healthy the data contained within this study. If the patients were less than 16‑ year‑ individuals. However, clinical tests including biochem- old, deceased, or unconscious when consent for publication was requested, istry and ultrasonography would be useful in selecting written informed consent for the publication of this data was given by their parents or legal guardians. eligible patients for screening endoscopy [46, 47]. This could be attributed to the difference in the number of Competing interests patient and control groups, the difference in etiology of The authors declare that they have no competing interests. liver cirrhosis in western countries, and difference in the Author details degree of hepatic decompensation. Department of Tropical Medicine, Menoufia University Faculty of Medicine, Additional studies are required in a larger number Shebeen El‑Kom, Egypt. Department of Radiodiagnosis and Interventional Radiology, Menoufia University Faculty of Medicine, Shebeen El‑Kom, Egypt. of cirrhotic patients of different etiologies and differ - ent grades of Child classification for validation of portal Received: 24 June 2021 Accepted: 10 December 2021 hemodynamic indices and to determine universal best cut off values that can be safely recommended as nonin - vasive predictors of esophageal varices. References 1. De Franchis R (2005) Evolving consensus in portal hypertension report Conclusion of the Baveno IV consensus workshop on methodology of diagnosis and From this study, we concluded that Measuring the portal therapy in portal hypertension. J Hepatol 43(1):167–176 2. 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Role of portal color Doppler ultrasonography as noninvasive predictive tool for esophageal varices in cirrhotic patients

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Abstract

Background: Esophageal varices (EV ) is the most common apprehensive complication of portal hypertension in patients with cirrhotic liver. Guidelines recommend Upper gastro‑intestinal endoscopic screening for EV in patients with newly diagnosed chronic cirrhosis (Imperiale et al. in Hepatology 45(4):870–878, 2007). Yet, it is invasive, time consuming and costly. To avoid unnecessary endoscopy, some studies have suggested Doppler ultrasound exami‑ nation as simple, and noninvasive tool in prediction and assessment of severity of EV (Agha et al. in Dig Dis Sci 54(3):654–660, 2009). Our study was to assess the role of different Doppler indices of portal vein, hepatic and splenic arteries as a noninvasive tool for prediction of esophageal varices in cirrhotic patients. Results: This prospective case control study was conducted on 100 cirrhotic liver patients and 100 of healthy volunteers as control group. Patients were subjected to clinical examination, upper gastrointestinal tract endoscopy, abdominal ultrasonography with duplex Doppler evaluation of different portal Doppler hemodynamic indices were done for each patient. The results revealed that portal vein diameter, hepatic artery pulsatility index, portal hyper‑ tensive index, portal vein flow velocity, portal congestion index have high sensitivity for prediction of EV. However, Splenic artery resistance index, hepatic artery resistance index HARI, liver vascular index and platelet count/spleen diameter have less sensitivity for prediction of EV. Conclusion: Measuring the portal hemodynamic indices can help physicians as noninvasive predictors of EV in cir‑ rhotic patients to restrict the need for unnecessary endoscopic screening especially when endoscopic facilities are limited. Keywords: Oesophageal varices, Portal hypertension, Doppler ultrasound Esophageal varices is the most common clinical mani- Background festation of portal hypertention. Bleeding varices is the Portal hypertension is defined as hepatic venous pressure most apprehensive complication contributing to high gradient (HVPG) greater than 5 mmHg. HVPG is a sur- morbidity and mortality [2].The mortality associated with rogate for the portosystemic pressure gradient. Clinically each episode of variceal bleeding ranges from 17 to 57% significant portal hypertension is defined as a gradient [3]. greater than 10 mmHg and variceal bleeding may occur Because of the impact of upper gastrointestinal bleed- at a gradient greater than 12 mmHg [1]. ing caused by rupture of EV in the prognosis of cirrhotic patients; the Baveno IV 2005 Consensus Workshop [1, 4] *Correspondence: drmkamel01@gmail.com 2 have determined that every patient diagnosed with cir- Department of Radiodiagnosis and Interventional Radiology, Menoufia University Faculty of Medicine, Shebeen El‑Kom, Egypt rhosis should be investigated for EV, regardless of Child Full list of author information is available at the end of the article class and the cause of liver cirrhosis [5]. © The Author(s) 2021. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http:// creat iveco mmons. org/ licen ses/ by/4. 0/. Nouh et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 2 of 11 Franchis, et  al. concluded that, endoscopic screening Examination protocol of all patients with liver cirrhosis would result in a large All patients were subjected to the following number of unnecessary endoscopies, additional burden to endoscopic units, high cost and the patient compliance • Full clinical assessment it was done by tropical with the screening program may be reduced. For these medicine specialist whose experience more than reasons, several studies have examined how to identify 5 years in the clinical field. It includes: patients with varices using noninvasive or minimally invasive methods to avoid endoscopy in patients with a • History taking With stress on history of haema- low risk of varices [6]. temesis and melena, abdominal swelling, hepatic Various studies have suggested using ultrasonographic encephalopathy, fever, edema of lower limbs and examination as simple, inexpensive, accurate and non- jaundice. invasive technique. Moreover, various Doppler ultra- • Complete General and Local examinations With sonographic indices have been shown to be of value stress on signs of liver cell failure. in assessment of the severity of EV or risks of variceal • Laboratory investigations including Complete bleeding in patients with cirrhosis. blood count. Liver function tests, Viral markers and Renal function tests. • Child-Pugh classification was calculated for all Methods studied patients to assess the severity of liver dis- Study population ease, depending on patients’ clinical and labora- This prospective case control study was conducted on tory data (16). 100 cirrhotic patients and 100 healthy volunteers as a control group. Cirrhotic patients were selected from • Ultrasound examination (including grey scale 670 patients attending the outpatient and\or inpatient and Doppler) was done to all patients and control department of Tropical Medicine and radiology depart- groups by the same consultant radiologist blinded ment, in the period between October 2017 and August to study design with experience in Doppler ultra- 2019. 570 patients were excluded due to presence of sound more than 12 years. exclusion criteria. Patients with liver cirrhosis, regardless the etiology • The procedures was done by the equipment of cirrhosis, were included in this study. While with Toshiba Nemio XG apparatus (Toshiba, Japan) of patients with hepatocellular carcinoma, active GIT by with B-mode and color Duplex Doppler ultra- bleeding, portal vein thrombosis, splenectomy or with sound at ultrasound unit of radiology depart- other severe medical condition; end stage renal disease ment. congestive heart failure or severe respiratory syndrome, • All patients were kept in a fasting state 6 h before were excluded. they were examined in the supine, right and left Patients were classified into two groups lateral positions during quiet respiration using a Cirrhotic group (Group 1) were 100 patients; 57(57%) 2–5 MHz convex probe in transverse and longitu- males and 43(43%) females. Their ages ranged from 36 to dinal scans. 78 years (50.49 ± 14.35). They were further classified into • B-mode Pelvi-abdominal ultrasound includes two subgroups after upper GI endoscopy; Group1-A: 67 evaluation of: Cirrhotic patients with esophageal varice and Group1-B: 33 Cirrhotic patients without esophageal varices. • Liver as regarding its size, echopattern, cirrho- Control group (Group 2) were 100 of healthy volun- sis, and focal lesions. teers; 69(69%) males and 31(31%) females. Their ages • Portal vein diameter (PVD; mm): It is measured ranged from 39 to 54 years (39.21 ± 13.98). at the hepatic hilum while the patient was in the The study was approved by the local Research Eth - supine position or in the left lateral decubitus ics Committee of our institute; the reference number of position. approval: 10/2017-TROP-9. All patients and controls • Portal vein cross sectional area was measured. included in this research gave written informed consent • Spleen as regarding its size, echopattern and to participate in this research. focal lesions. Nouh  et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 3 of 11 • Ascites as regarding amount (minimal, moder- endoscopy that was performed using a videoscope ate or marked) and evidence of echoes, adhe- (CLV-240; Olympus Ltd, Tokyo Japan) after fast- sions or loculations. ing 6  h prior to endoscopy, positioned in left lat- eral position and given suitable sedation. • Possible complications of procedures were • Duplex Doppler ultrasound for assessment of: explained to the patients and their relatives and • Portal venous system hemodynamics; includes written informed consents were obtained before assessment of: the endoscope. • Portal vein patency and blood flow velocity (PVFV) • Esophageal varices were graded by Paquet [13] (cm/s): grading system according to their size and depending on the degree of protrusion of varices • PVFV was measured in its mid-portion and was into esophageal lumen when the esophagus was automatically calculated on samples of the Dop- maximally relaxed. pler signal lasting more than 4  s. Three measure - ments were obtained and the average was used. Normal PVFV was (15–20 cm/s) [7]. • Grade 0 Absence of esophageal varices. • Grade I Microcapillaries on esophagogastric • Portal congestion index (PCI) was calculated using transition or distal esophagus. the following equation [8]: • Grade II 1 or 2 small varices located on distal Cross - sectional area of the portal vein (cm2) • PCI = esophagus. Mean portal vein velocity(Vmean)(cm/s) • Grade III Medium sized varices. • Hepatic and splenic arterial hemodynamics • Grade IV Large varices in any part of the esoph- includes assessment of: agus. • Hepatic artery resistance index (HARI) was calcu- lated automatically using the following equation [9]: Statistical analysis peak systolic velocity (V max)−end diastolic velocity(Vmin) HARI = peak systolic velocity(V max) • Data were collected, tabulated, statistically analyzed • Hepatic artery pulsatility index (HAPI) was calcu- using an IBM personal computer with Statistical lated automatically using the following equation [10]: Package of Social Science (SPSS) version 22 (SPSS, Inc, Chicago, Illinois, USA). Quantitative data were peak systolic velocity(Vmax)−end diastolic velocity(Vmin) HAPI = mean velocity(Vmean) presented in the form of mean ( X ), standard devia- • Splenic artery resistance index (SARI) was measured tion (SD), range, and qualitative data were presented automatically using the following equation [11]: in the form of numbers and percentages. The signifi - cance were assessed using the chi-square(χ ) and Z peak systolic velocity(V max)−end diastolic velocity(V min) SARI = peak systolic velocity(V max) test (z) to study association between two qualitative • Liver vascular index (LVI) was calculated using this variables, Student t-test for comparison between two equation [10]: groups having quantitative variables, Mann–Whitney and Kruskal–Wallis tests for comparison between Portal venous flow velocity(PVFV) • LVI = Hepatic arterial pulsatility index (HAPI) two or more groups not normally distributed hav- • Portal hypertensive index (PHI) was calculated using ing quantitative variables. Logistic regression model this equation [11] as a predictive analysis test used to describe data and to explain the relationship between one dependent (HARI*0.69)×(SARI*0.87) • PHI = Portal vein mean velocity(Vmean) binary variable and one or more nominal, ordinal, • Calculation of platelet count/spleen diameter (PC/ interval or ratio-level independent variables. The SD) ratio by dividing number of platelets/ml by the receiver operating characteristic (ROC) curve was maximum bipolar diameter of spleen in millimeters performed to determine. The cutoff value with the estimated with pelvi abdominal ultrasound [12]. highest accuracy was selected as the diagnostic cut- • Upper GIT endoscopy was done by to patients group off points. Sensitivity, specificity, positive predictive by the same tropical medicine consultant blinded to value (PPV), and negative predictive value (NPV) study design with experience in GIT endoscopy more were determined. p value was considered significant than 15 years. if less than 0.05 and highly significant if less than 0.001 (Figs. 1, 2, 3). • All patients with positive data after duplex Dop- pler ultrasound underwent upper gastrointestinal Nouh et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 4 of 11 Fig. 1 67 Y male patient with chronic liver disease, a presents Doppler U/S of hepatic artery with HAPI: 2.60 and HARI: 0.84. b Presents Doppler U/S of splenic artery with SARI: 0.82, the splenic bipolar diameter is 15.3 cm. c PResents Doppler U/S of PV with MVPV: 9.4 cm/s. PV diameter is 15.0 mm. d UGIE revealed grade IV oesophageal varices. Results There was no statistical significant difference between As regards the demographic data of the studied cirrhotic the measured portal hemodynamic indices and the grade groups, there was no statistical significant difference of EV (p value > 0.05) except PC/SD ratio and PVD (p between the studied groups as regarding age and sex (p value < 0.001), Table 6. value > 0.05), Table 1. A logistic regression model showed that Portal hyper- As regards the child classification, There was high tensive index and Portal vein diameter are good predic- statistical significant difference between group 1A and tors of the presence of esophageal varices more than group 1B (p value < 0.001), Table 2. Liver vascular index Table 7. There was statistical significant difference between The accuracy of PC/SD ratio and portal hemodynamic group 1A and group 1B as regarding, liver echogenic- indices in prediction of esophageal varices are shown in ity, spleen size, splenic collaterals and ascites (p value < Table 8. 0.05) but, there was no statistical significant difference between group 1A and group 1B as regarding liver size (p Discussion value > 0.05), Table 3. Variceal bleeding occurs in 20–40% of cirrhotic patients There was high statistical significant difference between with esophageal varices and is associated with a high cirrhotic group and control group as regarding PVFV, morbidity and mortality [2]. The Baveno IV 2005 Con - PCI, HARI, HAPI, SARI and PHI (p value < 0.001) but, sensus Workshop [1, 4] have determined that every there was no statistical significant difference as regarding patient diagnosed with cirrhosis should be investigated PVD and LVI (p value >0.05), Table 4. for EV, regardless of Child class and the cause of liver cir- there was high statistical significant difference between rhosis [5]. group 1A and group 1B as regarding PC/SD ratio and all Several studies have examined how to identify patients measured portal hemodynamic indices (p value < 0.001), with varices using noninvasive methods to avoid Table 5. large number of unnecessary screening endoscopy in patients with a low risk of varices [6]. Various portal Nouh  et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 5 of 11 Fig. 2 52 y male patient with chronic liver disease, a presents Doppler U/S of hepatic artery with HAPI: 1.27 and HARI: 0.81. b Presents Doppler U/S of splenic artery with SARI: 0.62, the splenic bipolar diameter is 18 cm. c Presents Doppler U/S of PV with MVPV: 19.6 cm/s. PV diameter is 14 mm. ascites was also noticed. d UGIE revealed grade III oesophageal varices. haemodynamic indices have been shown to be predic- that, patients in Child B or C are nearly 3 times more tive of the severity of EV or risks of variceal bleeding in likely to have varices than those in Child A. patients with cirrhosis [14]. Concerning pelvi-abdominal ultrasound findings, This prospective case control study was conducted there was high statistical significant difference between on 2 groups: group 1, 100 cirrhotic patients which was group1A and group1B regarding portal vein diameter classified into two subgroups after upper GI endoscopy; (PVD), liver echogenecity, spleen size, and splenic collat- group1A, cirrhotic patients with esophageal varices and erals (p value < 0.001). These results were in agreement Group1B, cirrhotic patients without esophageal varices, with Faisal et  al. [20], and Khalil et  al. [21], who con- and group 2, 100 of healthy volunteers as a control group. cluded that, increased PVD, splenomegaly and presence As regards the demographic data of the studied cir- of splenic collaterals by ultrasound can predict EV spe- rhotic groups, 57% of cirrhotic patients were males and cially the large varices. However, This result was in con - 43% were females. Their ages ranged from 36 to 78 years troversy with Berzigotti et al. [22], who found that, there (49.31 ± 14.27) in group 1A and (52.88 ± 14.45) in group was no significant change in liver echogenicity in cir - 1B. these observations go in agreement with with Tharwa rhotic patients with varices than patients without varices. et al. [15], where males were 59.4% and Hekmatnia et al. In our study, there was no significant difference in PVD [16], who found that, the mean age was 52.1 years (range: (mm) in cirrhotic patients (12.4 ± 3.2) compared with 28–83 years). the controls (12.1 ± 1.2) with (p value >0.05). However, In our study, there was high statistical significant differ - There was high significant increase in PVD in group 1A ence between group 1A and group 1B as regarding child (13.9 ± 2.2) than group 1B (9.4 ± 2.8) with (p value < classification (p value < 0.001). This was proven by [17], 0.001) with high statistical significant increase with the Nashaat et  al. [18], and Zaman et  al. [19], who reported grades of EV with (p value < 0.001). These results were Nouh et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 6 of 11 Fig. 3 51y female patient with chronic liver disease, a presents Doppler U/S of hepatic artery with HAPI: 1.6 and HARI: 0.72. b presents Doppler U/S of splenic artery with SARI: 0.45, the splenic bipolar diameter is 14.5 cm. c presents Doppler U/S of PV with MVPV: 13.6 cm/s. PV diameter is 11.5 mm. d UGIE revealed grade I oesophageal varices. Table 1 Demographic data of the studied groups Variable Group1A Group1B Control group Test of significance Cirrhotic Pt. with EV Cirrhotic Pt. without EV (n = 100) (n = 67) (n = 33) M ± SD M ± SD M ± SD Age 49.31 ± 14.27 52.88 ± 14.45 50.33 ± 13.3 (Kruskal–Wallis test) NS < 0.48 N (%) N (%) N (%) Sex Male 40(59.7%) 17(51.5%) 69(69%) χ test = 3.72 NS Female 27(40.3%) 16(48.5%) 31(31%) 0.16 NS no significant difference in agreement with Anda et al. [23], Sarwar et al. [24] and not sensitive to presence of cirrhosis or in differentiation Kayacetin et  al. [25] who found an association between between the grades of EV presence. an increase in PVD with liver cirrhosis, presence and In our study, at a cutoff point (10.4), the sensitiv - grading of EV as well. But these results were in disagree- ity of PVD that can predict EV was 94.03%, the speci- ment with Jaheen et al. [26], who concluded that, PVD is ficity was 75.76%, PPV was 88.73%, NPV was 86.21%, Nouh  et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 7 of 11 Table 2 Child classification of the studied groups in PC/SD ratio by increase in spleen size and thrombo- cytopenia which usually occur with increase of portal Child Group 1A Group 1B Test of p Value pressure and with development of varices especially classification (n = 67) (n = 33) significance with larger risky varices. A:31 13(19.4%) 18(54.5%) χ test 0.001* Our study showed that, at cutoff point (604), the sen - B:33 23(34.3%) 10(30.3%) 14.86 sitivity of PC/SD ratio that can predict the presence of C:36 31(46.3%) 5(15.2%) EV was 61.19%, the specificity was 90.91 %, PPV was *High significant difference, P < 0.001 93.18%, NPV was 53.57 %, accuracy was 71.00% and AUC = 0.883. These results were in agreement with studies of Shekar et al. [12], Sheta et al. [30] and Nouh et  al. [27], who reported that, at cut-off values around Table 3 Pelvi abdominal ultrasound findings of the studied (600), PC/SD ratio that can predict EV with similar sen- groups sitivity, specificity , PPV & NPV. Group 1A Group 1B Test of p Value Regarding the measured portal hemodynamic indi- (n = 67) (n = 33) significance ces by Duplex Doppler ultrasound, there was high sig- N (%) N (%) nificant decrease of portal vein flow velocity (PVFV) NS Liver size Fisher exact 0.22 (cm/s), in cirrhotic patients (15.3 ± 5.1) compared with 3.1 Shrunken 22(32.8%) 6(18.2%) controls (18.2 ± 2.9) with (p < 0.001) with high signifi - (< 12 cm) cant decrease in in group 1A (12.2 ± 2.3) than group 1B Normal 44(65.7%) 27(81.8%) (21.4 ± 3.2) with (p value <0.001). Studies were done (12–16 cm) by Elhady et al. [29], Mahmoud et al. [31] and Liu et al., Enlarged 1(1.5%) 0(0%) [32] reported that (PVFV) was significantly lower in (> 16 cm) cirrhotic patients than controls. Anda et  al. [23] and Splenic size χ test 63.4 < 0.001* Elbarbary et  al. [33] Also, found that, PVFV was lower Normal 1(1.5%) 25(75.8%) (7–11 cm) in patients with EV. In contrast, Schneider et  al. [34] Enlarged 66(98.5% 8(24.2%) and Piscaglia et  al. [35] reported that, no change in (> 11 cm) PVFV between patients and controls. This may be due Liver echogenecity χ test 15.97 < 0.001* to intra- and inter observer variability or presence of Coarse 60(89.6%) 18(54.5%) collaterals which affect the velocity. Homogeneous 7(10.4%) 15(45.5%) Our study showed that, at cutoff point (15.2), the Splenic collaterals χ test 22.46 < 0.001* sensitivity of PVFV that can predict EV was 89.55%, Yes 37(55.2%) 2(6.1%) the specificity was 93.94%, PPV was 96.77%, NPV was No 30(44.8%) 31(93.9%) 81.58%, accuracy was 91.00% and AUC = 0.953. These Ascites χ test 11.86 0.008* results were in agreement with Minal et  al. [36] who No 23(34.3%) 23(69.7%) reported that, PVFV had a high sensitivity 84% for Mild 11(16.4%) 4(12.1%) detecting the EV. Moderate 19(28.9%) 4(12.1%) Regarding the portal congestion index (PCI) there Marked 14(20.9%) 2(6.1%) was a significant increase in cirrhotic patients (0.11 ± *High significant difference, P < 0.001 0.045) compared with the controls (0.071 ± 0.012) and increase in group 1A (0.1 ± 0.03) than group1B (0.05 ± 0.0.1) with (p value < 0.001). These results were in accuracy was 88% and AUC = 0.877. These results were agreement with Kayacetin et  al. [25] who found that, in agreement with Berzigotti et al. [22] and Nouh et al. PCI was significantly increased in cirrhotic group and [27] who found the best cut-off value of PVD for EV in presence of EV. prediction was (10.7) and (11.5) respectively. At cutoff point (0.1), the sensitivity of PCI that can pre - Regarding platelet count/spleen diameter ratio (PC/ dict EV was 89.35%, the specificity was 92.84%, PPV was SD), there was high statistical significant difference in 95.66%, NPV was 82.5%, accuracy was 93% and AUC = group 1A (546 ± 290.9) than group 1B (1135 ± 413.2) 0.948. this was in agreement with Moriyasu et al. [8], who and the grades of EV (725.6 ± 273.5) (567.9 ± 280.2) found that, cutoff point was (0.189) in patients with EV (347.8 ± 162.6) (293.8 ± 91.8) in grades I, II, III and with sensitivity (84.65%) and Lee et  al. [37], who found IV respectively as well (p value < 0.001). This result was that PCI cutoff point was (0.089). in agreement with Shekar et  al. [12], Agha et  al. [28], Regarding arterial indices including HARI, HAPI and Elhady et al. [29], who who explained the decrease and SARI, there was high significant increase in the in Nouh et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 8 of 11 Table 4 Comparison of portal vein diameter and different hemodynamic indices by B‑mode and color Doppler US between cirrhotic group and control group Normal values Cirrhotic group (G1) Control group (G2) p Value (Mann– (n = 100) (n = 100) Whitney test) M ± SD M ± SD Portal vein flow velocity (PVFV ) 15.3 ± 5.1 18.2 ± 2.9 < 0.001* (15–20 cm/s) NS Portal vein diameter (PVD) 12.4 ± 3.2 12.1 ± 1.2 0.38 (10–13 mm) Portal congestion index (PCI) 0.11 ± 0.045 0.071 ± 0.012 < 0.001* (0.07–0.1) Hepatic artery resistive index (HARI) 0.71 ± 0.052 0.51 ± 0.03 < 0.001* (0.5–0.7) Hepatic artery pulsatility index (HAPI) 1.34 ± 0.12 1.01 ± 0.04 < 0.001* (0.9–1) Splenic artery resistive index (SARI) 0.7 ± 0.05 0.5 ± 0.06 < 0.001* (0.5–0.7) Portal hypertensive index (PHI) 2.23 ± 0.85 1.38 ± 0.53 < 0.001* (1.3–1.8) NS Liver vascular index (LVI) 11.77 ± 4.95 11.61 ± 3.2 0.78 (10–15) NS = no significant difference, P > 0.05 *High significant difference, P < 0.001 accuracy was 84.00% and AUC = 0.881. Concerning Table 5 Comparison of different predictors in the studied SARI, at cutoff point (0.72), the sensitivity of SARI that groups in relation to presence of esophageal varices can predict EV was 77.61%, the specificity was 92.56%, Group 1A Group 1B p value PPV was 93.98%, NPV was 68.75%, accuracy was 85% (n = 67) (n = 33) (Mann– M ± SD M ± SD Whitney and AUC = 0.888. These results were in agreement with test) Child et  al. [41] and Dib et  al. [42]who found that, the presence of EV affect all measured hepatic and splenic Platelet count/spleen diam‑ 546 ± 290.9 1135 ± 413.2 < 0.001* eter (PC/SD) ratio arterial hemodynamic parameters with the best cut off Portal vein flow velocity 12.2 ± 2.3 21.4 ± 3.2 < 0.001* point for SARI for prediction of EV was (0.76) with sensi- Portal vein diameter 13.9 ± 2.2 9.4 ± 2.8 < 0.001* tivity of 85% and specificity of 77.5%. Portal congestion index 0.1 ± 0.03 0.05 ± 0.01 < 0.001* This study showed that, at cutoff point(1.3), the sensi - Hepatic artery resistive index 0.7 ± 0.03 0.6 ± 0.03 < 0.001* tivity of HAPI that can predict EV was 94.03%, the speci- Hepatic artery pulsatility index 1.4 ± 0.09 1.2 ± 0.1 < 0.001* ficity was 66.67 %, PPV was 85.14%, NPV was 84.62 %, Splenic artery resistive index 0.7 ± 0.02 0.64 ± 0.02 < 0.001* accuracy was 85.00% and AUC = 0.858. These results Portal hypertensive index 2.7 ± 0.46 1.2 ± 0.3 < 0.001* were in agreement with a study of Haktanir et  al. [43], Liver vascular index 8.8 ± 1.88 17.8 ± 3.57 < 0.001* who reported that, HAPI was significantly higher in EV with a cutoff point (1.28). *High significant difference, P < 0.001 In this study there was no statistical significant differ - ence between the measured portal hemodynamic indices cirrhotic patients than the controls (p < 0.001) with SARI and the grade of EV (p value > 0.05) except PC/SD ratio showed high statistically significant difference between and PVD as fore-mentioned. These results were in agree - group 1A and group 1B (p value < 0.001), These results ment with a study done by Hekmatnia et  al., who found were in agreement with Park et al. [38], Zhang et al. [9], that, there was no significant relationship between PCI, Piscaglia et al. [35] Dewidar et al. [39] and Nicolau et al. arterial resistance and pulsatility indices and the grades [40] who found increase in the arterial indices in cirrhotic of EV [16]. patients than in controls and in pateints with varices than In contrast, results published by Anda et  al. [23], patients without. showed a significant increase in PCI, HARI and HAPI This study showed that, at cutoff point (0.71), the sensi - with higher grades of EV, this could be attributed to the tivity of HARI that can predict EV was 76.12%, the speci- difference in the number of selected cirrhotic patients ficity was 91.23%, PPV was 92.11%, NPV was 67.35%, Nouh  et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 9 of 11 Table 6 Comparison of different predictors in the studied groups in relation to the grade of esophageal varices Esophageal varices Grade 1 Grade 2 Grade 3 Grade 4 p value N = 67 (n = 26) (n = 18) (n = 14) (n = 9) (Kruskal Wallis test) M ± SD M ± SD M ± SD M ± SD PC/SD ratio 725.6 ± 273.5 567.9 ± 280.2 347.8 ± 162.6 293.8 ± 91.8 < 0.001* NS Portal vein flow velocity 12.7 ± 2.4 12.2 ± 1.2 11.9 ± 3.5 11.7 ± 1.3 0.327 Portal vein diameter 12.67 ± 2.24 14.14 ± 1.7 14.74 ± 1.79 14.68 ± 1.7 0.001* NS Portal congestion index 0.13 ± 0.03 0.14 ± 0.03 0.14 ± 0.03 0.14 ± 0.03 0.551 NS Hepatic artery resistive index 0.7 ± 0.03 0.7 ± 0.03 0.7 ± 0.03 0.7 ± 0.03 0.962 NS Hepatic artery pulsatility index 1.4 ± 0.08 1.4 ± 0.12 1.4 ± 0.07 1.3 ± 0.08 0.303 NS Splenic artery resistive index 0.7 ± 0.02 0.7 ± 0.02 0.7 ± 0.02 0.7 ± 0.01 0.390 NS Portal hypertensive index 2.7 ± 0.65 2.7 ± 0.31 2.5 ± 0.51 2.8 ± 0.27 0.210 NS Liver vascular index 9.1 ± 1.98 8.6 ± 1.11 8.6 ± 2.8 8.7 ± 1.25 0.581 NS = no significant difference, P > 0.05 *High significant difference, P < 0.001 and different degree of decompensation between these specificity > 70% when comparing cirrhotic patients with studies [23]. controls and also in agreement with Faisal et al. [20] who Regarding portal hypertensive index (PHI) there was found that, PHI showed statistically significantly higher high statistical significant increase in PHI in cirrhotic values in patients with EV than those without EV. group than control group with (p value < 0.001), with At cutoff point (1.48), the sensitivity of PHI that can high statistical significant increase in PHI in group 1A predict EV was 92.43%, the specificity was 93.94 %, PPV than group 1B with (p value < 0.001) . this was in agree was 97.10%, NPV was 96.45%, accuracy was 95.00% and AUC = 0.992. %. These results were in agreement with ment with Iwao et  al. [44] who found that, PHI had a Abu El Makarem et al. [45] who found that, only PHI had Table 7 Logestic regression model to predict the presence of an independent predictive value of EV and suggested the esophageal varices in the studied groups beginning of endoscopic screening in patients with com p Value Odds ratio 95% CI pensated cirrhosis at a cutoff point of PHI (> 2.08). As regards, the liver vascular index (LVI), there was Liver vascular index 0.202 0.688 0.387–1.222 no significant difference in cirrhotic patients compared Portal hypertensive index 0.021 0 0–0.231 with the controls (p value > 0.05), this result was in con- Portal vein diameter 0.029 0.520 0.289–0.935 troversy with Jaheen et al. [26], who found that, LVI was Table 8 Accuracy of PC/SD ratio and portal hemodynamic indices in prediction of esophageal varices Index Cutoff Sensitivity (%) Specificity (%) PPV (%) NPV (%) Accuracy (%) AUC PC/SD ratio 604 61.19 90.91 93.18 53.57 71.00 0.883 Inversely proportional Portal vein flow velocity (cm/s) 15.2 89.55 93.94 96.77 81.58 91.00 0.953 Inversely proportional Portal vein diameter (mm) 10.4 94.03 75.76 88.73 86.21 88 0.877 Directly proportional Portal congestion index 0.1 89.35 92.84 95.66 82.5 93 0.948 Directly proportional Hepatic artery resistive index 0.71 76.12 91.23 92.11 67.35 84.00 0.881 Directly proportional Hepatic artery pulsatility index 1.3 94.01 66.67 85.14 84.62 85.00 0.858 Directly proportional Splenic artery resistive index 0.72 77.61 92.56 93.98 68.75 85 0.888 Directly proportional Portal hypertensive index 1.48 92.43 93.94 97.10 96.45 95.00 0.992 Directly proportional Liver vascular index 9.4 74.63 96.97 98.04 65.31 82.00 0.973 Inversely proportional Nouh et al. Egypt J Radiol Nucl Med (2022) 53:4 Page 10 of 11 vein diameter; PVFV: Portal vein flow velocity; SARI: Splenic artery resistance significantly lower in cirrhotic patients than controls with index; UGIE: Upper gastrointestinal endoscopy. (p value = 0.018). There was high statistical significant decrease in LVI Acknowledgements There is no acknowledgement. in group 1A than group 1B with (p value < 0.001), this result was in agreement with a study done by Faisal et al. Authors’ contributions [20], who found that, LVI was lower in patients with EV MN, MK, AA and ME contributed equally to study design, data collection, analysis, and interpretation of results. All authors read and approved the final (p value=0.001). manuscript. At cutoff point (9.4), the sensitivity of LVI that can pre - dict EV was 74.63%, the specificity was 96.97 %, PPV was Funding There is no funding. 98.04%, NPV was 65.31 %, accuracy was 82.00% and AUC = 0.973. These results were in agreement with Haktanir Availability for data and materials et al. [43], who found that, the best cut off point for LVI Data will be available upon request via contacting the corresponding author. for prediction of EV was (10.36) with sensitivity of 85% and specificity of 77% and concluded that, LVI was a high Declarations sensitive and specific parameter in the diagnosis and pre - Ethics approval and consent to participate diction of EV. All study procedures were conducted in accordance with Helsinki and were However, Piscaglia et al., and Jeon et al., have reported approved by the ethical committee of Menoufia Faculty of medicine council, reference number 10/2017‑ TROP‑9. All patients and controls included in this different findings in the measured portal hemodynamic research gave written informed consent to participate in this research. indices compared with the present study results. They reported that, Doppler measurements were not useful in Consent for publication All patients included in this research gave written informed consent to publish distinguishing patients with liver cirrhosis from healthy the data contained within this study. If the patients were less than 16‑ year‑ individuals. However, clinical tests including biochem- old, deceased, or unconscious when consent for publication was requested, istry and ultrasonography would be useful in selecting written informed consent for the publication of this data was given by their parents or legal guardians. eligible patients for screening endoscopy [46, 47]. This could be attributed to the difference in the number of Competing interests patient and control groups, the difference in etiology of The authors declare that they have no competing interests. liver cirrhosis in western countries, and difference in the Author details degree of hepatic decompensation. Department of Tropical Medicine, Menoufia University Faculty of Medicine, Additional studies are required in a larger number Shebeen El‑Kom, Egypt. Department of Radiodiagnosis and Interventional Radiology, Menoufia University Faculty of Medicine, Shebeen El‑Kom, Egypt. of cirrhotic patients of different etiologies and differ - ent grades of Child classification for validation of portal Received: 24 June 2021 Accepted: 10 December 2021 hemodynamic indices and to determine universal best cut off values that can be safely recommended as nonin - vasive predictors of esophageal varices. References 1. De Franchis R (2005) Evolving consensus in portal hypertension report Conclusion of the Baveno IV consensus workshop on methodology of diagnosis and From this study, we concluded that Measuring the portal therapy in portal hypertension. J Hepatol 43(1):167–176 2. 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Journal

Egyptian Journal of Radiology and Nuclear Medicine – Springer Journals

Published: Jan 4, 2022

Keywords: Oesophageal varices; Portal hypertension; Doppler ultrasound

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