RESEARCH ARTICLE Results Obtained with the Laparoscopic Approach to the Bile Duct for the Treatment of Choledocholithiasis in 101 Cases Belén Martin Arnau1, Manuel Rodriguez Blanco2, Victor Molina Santos3, Antonio Rabal Fueyo4, Antonio Moral Duarte5, Santiago Sánchez Cabús6 A b s t r ac t Background: The optimal treatment for choledocholithiasis (CLT) is currently the subject of debate, as there is no clear evidence that a two-step (endoscopic plus surgical) approach is superior to a one-step surgical procedure. Materials and methods: We analyzed the results obtained from 101 consecutive patients diagnosed with CLT using magnetic resonance cholangiopancreatography (MRCP) or computed tomography (CT) scan undergoing cholecystectomy and laparoscopic exploration of the bile duct, carried out at our center between 2006 and 2019. In this analysis, special emphasis was made on the permanent resolution of the CLT and the associated complications. Results: The mean surgical time was 142 ± 36.7 minutes. In patients with a CLT diagnostic test more than 7 days previously, the presence of CLT was checked using intraoperative cholangiography (IOC), which was negative in 25% of patients, while in the rest, a primary exploration was performed using a choledochoscope via choledochotomy in 82.2% of patients and via the transcystic approach in two cases. A T-tube drain was inserted in 18.9% of patients. The conversion rate was 0.9%, due to a technical difficulty in removing the CLT in one patient. The laparoscopic approach treated the CLT permanently in 97/101 cases (96%), while four patients (3.9%) required postoperative endoscopic retrograde cholangiopancreatography (ERCP) due to residual cholelithiasis. A total of 15.8% of patients experienced a postoperative biliary fistula, which was resolved using conservative management in 86.7% of them, while two patients required surgical treatment and insertion of a percutaneous drain, respectively. The average postoperative stay duration was 6.5 ± 7.3 days. None of the patients showed signs of biliary stricture in the long-term postoperative follow-up. Conclusion: In our experience, the laparoscopic approach for one-step elective treatment of CLT is a safe option, with a very small number of complications and satisfactory short- and long-term results. Furthermore, despite preoperative identification of CLT, it helped to avoid unnecessary exploration of the bile duct in 25% of patients. Keywords: Cholangiopancreatography endoscopic retrograde, Choledocholithiasis, Laparoscopic cholecystectomy, Laparoscopic common bile duct exploration. World Journal of Laparoscopic Surgery (2021): 10.5005/jp-journals-10033-1447 Introduction 1–6 Department of Digestive Surgery, Hospital Sant Pau, Barcelona, Approximately, 9 to 16% of patients with cholelithiasis can Catalonia, Spain experience concomitant choledocholithiasis (CLT).1,2 For many Corresponding Author: Belén Martin Arnau, Department of years, intraoperative cholangiography (IOC) was routinely carried Digestive Surgery, Hospital Sant Pau, Barcelona, Catalonia, Spain, out during open cholecystectomy with the aim of diagnosing e-mail:amartinar@santpau.cat inadvertent CLT, and in patients in whom it was diagnosed, an How to cite this article: Arnau BM, Blanco MR, Santos VM, et al. exploration of the main bile duct was carried out.3,4 Subsequently, Results Obtained with the Laparoscopic Approach to the Bile Duct for with the implementation of laparoscopic surgery to treat the Treatment of Choledocholithiasis in 101 Cases. World J Lap Surg cholelithiasis and thanks to the advances in preoperative imaging 2021;14(2):119–125. techniques and the experience gathered in laparoscopy, the Source of support: Nil approach to CLT treatment has evolved. Nowadays, attempts are Conflict of interest: None made to diagnose CLT preoperatively, and, in general, endoscopic retrograde cholangiopancreatography (ERCP) is carried out, followed by laparoscopic cholecystectomy (LC) (a two-step procedure), which has emerged as the standard treatment.5 technical difficulty, this approach can have benefits compared to However, the use of ERCP has been associated with morbidity the conventional ERCP and LC procedures, reducing the duration and mortality rates of up to 15 and 1%, respectively, and it has a of the hospital stay and the total cost, and even has a higher rate CLT recurrence rate of 10 to 15%,5 as well as an increase in the cost of permanent treatment for CLT. (whether direct or indirect) associated with a two-step procedure. In this study, we describe the results associated with the In contrast, the surgical treatment of CLT using a laparoscopic use of the one-step laparoscopic approach for treating CLT and approach is currently feasible thanks to the increase in the cholelithiasis. experience and availability of choledochoscopes adapted for the laparoscopic approach, allowing for the exploration of the bile M at e r ia l s and Methods duct laparoscopic common bile duct exploration (LCBDE) and Between September 2006 and March 2019, we carried out 101 cholecystectomy to be carried out simultaneously.6 Despite its consecutive cholecystectomy procedures with the laparoscopic © Jaypee Brothers Medical Publishers. 2021 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (https://creativecommons.org/licenses/by-nc/4.0/), which permits unrestricted use, distribution, and non-commercial reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Results Obtained with the Laparoscopic Approach for Elective Choledocholithiasis exploration of the bile duct in patients with CLT diagnosed via an In these patients, given that the main bile duct remained intact, imaging study. an abdominal drain was not routinely placed. The data from these patients were collected prospectively in a database and were analyzed retrospectively. The variables Choledochotomy Approach analyzed were as follows: Preoperative data: Age, sex, liver This approach was carried out in cases in which the requirements function tests, and diagnostic imaging studies [ultrasound, for a transcystic approach were not met (multiple or large-size computed tomography (CT) scan, and magnetic resonance CLT, small-diameter cystic duct) or if the transcystic approach was cholangiopancreatography (MRCP)]. The intraoperative unsuccessful. data included the following: Surgical time, transcystic or Exploration of the bile duct was carried out using a longitudinal transcholedochal approach, the performance of IOC, use of choledochotomy on the anterior surface measuring around 2 cm sealants, and the need for conversion. In the postoperative period, in length. The techniques used to remove the stones were lavage we recorded the duration of the hospital stay, postoperative with the saline solution under pressure to facilitate the removal complications (pancreatitis, bile leakage, cholangitis, and of the small stones and using the Dormia basket and/or balloon bleeding), and follow-up data on the recurrence of stones, as well catheter to move the stones toward the abdominal cavity via the as the need for subhepatic or biliary drainage, the time to removal choledochotomy or else toward the duodenum. In all cases, a of the drain and the associated complications. choledochoscope was subsequently used in the distal and proximal direction to rule out the presence of the residual CLT. Patient Selection After the removal of the CLT, the choledochotomy incision was Patients were included who had clinical and laboratory signs that closed over a Kehr drain, which was passed progressively, and in were suggestive of CLT (pain of probable biliary origin and jaundice) accordance with experience, to the primary closure with individual that was confirmed with an imaging study, and those with signs of 4/0 braided absorbable sutures, except in cases of acute cholangitis. associated cholecystitis were excluded. Radiological diagnosis of In these patients, a Jackson Pratt® no. 13 low-pressure closed- CLT was carried out via abdominal ultrasound in 15 patients (14.8%), suction abdominal drain was inserted.10 CT scan in 6 patients (5.9%), and MRCP in 80 patients (79.2%). Informed consent was obtained from all patients after they Complication Assessment had been given information about their disease, the up-to-date We used the ClavienDindo (CD) classification to stratify the severity.7 treatment options, and the possibility of conversion to conventional Bile leakage was defined as persistent bile drainage of over open surgery. 50 mL/day for more than 3 days.7 Surgical Technique Statistics All patients received antibiotic and antithrombotic prophylaxis in The continuous variables were compared using the Student’s t-test line with the center’s policy. The supine position was used, allowing or the MannWhitney U test, as appropriate. The Chi-squared test the fluoroscopic C-arm to be inserted to carry out the IOC. was used to compare categorical variables. p <0.05 was considered As standard, an IOC was carried out in all patients, except those to be statistically significant. Unless specifically stated otherwise, with CLT demonstrated by an imaging study (abdominal ultrasound, the data are shown as a mean ± standard deviation. CT scan, or MRCP) in the 7 days prior to the surgical intervention. If The statistical analysis was carried out using the commercially an image suggestive of CLT was observed in the IOC (filling defect available STATA software for Windows version 14. or no passage of contrast to the duodenum), a surgical exploration of the bile duct was carried out. R e s u lts The procedure was carried out using a LC technique with the use of four trocars (American technique), as previously described.7 Between September 2006 and March 2019, we carried out 101 After completely dissecting the triangle of the Calot, a small incision LCBDE procedures due to lithiasis at our center. Table 1 shows the was made in the cystic duct following proximal clipping of the duct demographic characteristics. to prevent the stones from sliding into the common hepatic duct. Seventy-two patients (71.2%) had diagnostic radiology studies A small-diameter catheter (4.5 Fr) was inserted through the cystic for CLT carried out more than 7 days before the intervention. These duct to carry out the IOC and to detect any images suggestive patients underwent an IOC, the result of which showed no CLT in 14/72 of CLT or any anatomical variations, if applicable. If any images patients (19.4%) and a clear presence of CLT in 54/72 patients (75%). minimally suggestive of CLT were observed, surgical exploration In the remaining 4/72 cases (5.5%), normal bile-duct morphology with a choledochoscope was indicated. Table 1: Demographic characteristics of the study population subjected Transcystic Approach to LCBDE This approach was used in cases with a large cystic duct, which (n = 101) % allowed the material to be inserted for the removal or a single CLT Sex (♀/♂) 55/46 54.4/45.6 of a smaller size than the cystic duct. After dilating the cystic duct with the laparoscopic dissector, Middle ages 69.3 ± 16.8 the stones were removed from the main bile duct using a pressure Abdominal surgical history 24 23.5 infusion of saline solution and subsequently, in all cases, with the Gynecological 11 10.9 assistance of a Dormia basket8 or a balloon catheter (Fogarty®).9 Appendectomy 6 5.9 After the CLT expulsion maneuvers, a flexible choledochoscope Billroth gastrectomy II 3 2.9 was used10 to check that there was no residual CLT. The LC was then Eventroplasty 2 1.9 completed in the usual way. Left hemicolectomy 2 1.9 120 World Journal of Laparoscopic Surgery, Volume 14 Issue 2 (May–August 2021) Results Obtained with the Laparoscopic Approach for Elective Choledocholithiasis was observed up to the outlet, but with no signs of the passage of stay duration was 6.5 ± 7.3 days, being longer for the group contrast to the duodenum. In these cases, pressure infusion of saline undergoing the transcholedochal approach (6.7 ± 7.6 days) than for solution was carried out, with subsequent insertion of a balloon the transcystic approach (2 ± 0.0 days) although without statistically catheter through the transcystic route. In three cases (4.16%), no significant differences (p = 0.38). stone release was observed and the subsequent IOC was performed Sixteen patients (18.5%) experienced a biliary fistula that normally. In one patient (1.3%), a transcystic choledochoscopy was persisted for 19 ± 17.3 days (International Study Group of Liver able to be carried out, which ruled out the presence of the residual Surgery classification of the severity of bile leakage). 31 Two of stones (Flowchart 1). From the laboratory perspective, the patients these patients had a Kehr drain in situ, and 14 belonged to the with and without CLT (definitively diagnosed during the intervention) primary-closure group. Conservative management was carried did not have significantly different preoperative levels of aspartate out in 14 patients with the drain remaining in situ until resolved. aminotransferase (90.6 ± 93.9 vs 107.0 ± 154.9, p = ns), alanine Two patients required treatment to resolve the biliary fistula; one transaminase (131.7 ± 157.8 vs 163.8 ± 156.9, p = ns), total bilirubin required reintervention for surgical drainage of the biloma, and (39.0 ± 49.5 vs 23.5 ± 21.1, p = ns), gamma-glutamyl transferase the other required insertion of a percutaneous drain. Neither of (819.2 ± 848.4 vs 541.7 ± 431.8, p = ns), and alkaline phosphatase these two cases had a T-tube in situ. No statistically significant (373.0 ± 390.2 vs 275.5 ± 195.9, p = ns). It should be highlighted that differences were found between the presence of a biliary fistula in these laboratory results were only available for 66 patients in the patients with and patients without a Kehr drain (21.5 vs 13.3%, p = 1) 3 weeks prior to the surgical intervention. (Table 2). The medical complications are summarized in Table 3. A In the patients with confirmed CLT, the exploration of the bile total of six patients experienced medical complications in the form duct was realized using the transcystic approach in two patients of pneumonia, urinary tract infection, and postoperative adynamic (2.5%) and the transcholedochal approach in 97.5% (81/83). The ileus, which progressed well with medical treatment. CLT was satisfactorily resolved in all patients undergoing the The overall mortality for the series was 1.9% (2/101), secondary transcystic approach, while four patients (3.9%) who underwent the to bleeding complications. Overall, three patients (2.9%) transcholedochal approach had residual CLT. The primary closure experienced postoperative bleeding, with two cases requiring of the choledochotomy was carried out in 80.2% (65/81), with reintervention: One patient experienced liver cirrhosis that had choledochorraphy over a Kehr drain in 19.8% (16/81) of patients. The not been previously diagnosed, presenting with decompensation patients with a Kehr drain maintained this in situ for 26.3 ± 23.7 days and subsequent multiple organ failure following bleeding of before it was removed. the cystic artery, eventually resulting in death; another patient All procedures were carried out using a laparoscopy except one experienced a hypovolemic shock secondary to a pseudoaneurysm case (0.9%) in which conversion to open surgery was performed of the gastroduodenal artery, eventually resulting in death despite due to difficulties in removing the CLT. There were no statistically emergency reintervention; the third case of bleeding corresponded significant differences in the conversion rate according to the to a hematoma in the surgical bed, which was treated conservatively approach (0.9 vs 0%, p = 0.98). (Tables 3 and 4). The mean surgical time was 142 ± 36.7 minutes, with the The postoperative stay duration was 6.5 ± 7.3 days. None of the transcystic route being 170 ± 14.1 minutes and the transcholedochal patients showed clinical, laboratory, or radiological signs of biliary route being 141 ± 36.9 minutes (p = 0.28). The mean postoperative stricture in the long-term postoperative follow-up. Flowchart 1: Outline of the results World Journal of Laparoscopic Surgery, Volume 14 Issue 2 (May–August 2021) 121 Results Obtained with the Laparoscopic Approach for Elective Choledocholithiasis Overall, the LCBDE approach achieved full resolution of the CLT The best approach for treating CLT and cholelithiasis remains in 96.4% of patients (80/83). Three patients (3.6%) required removal the subject of discussion. A Cochrane review concluded that there of residual CLT via ERCP, two of which were detected via trans- were no significant differences in morbidity, mortality, and failure Kehr cholangiography and two as a result of persistent cholestasis rate between the LCBDE approach and the two-step endoscopic confirmed via MRCP due to not having a Kehr drain in situ. approach. However, individual trials have suggested that the one- step procedure gives a lower morbidity result, a shorter duration Discussion of hospital stay, and is more cost-effective than the two-step approach.15–17 Cholelithiasis is a highly prevalent condition in our environment. From a theoretical perspective, the LCBDE approach would It is estimated to affect 10% of the population in Spain, and a allow to prevent the inconveniences of two-step treatment of considerable percentage of these cases (9–16%) can be associated CLT and also the inconveniences of the open exploration.18,19 with concomitant CLT.11,12 This represents a considerable However, laparoscopic exploration of the bile duct has not been problem that is in need of a suitable strategy to resolve it. universally adopted, even to date, more than 30 years after the LC For years, the European Association for Endoscopic Surgery was introduced. The reasons for this delay are the good results and has recommended that these patients be treated even when convenience associated with endoscopic treatment, as well as the asymptomatic.13 Treatment options include a one-step procedure technical difficulties related to the laparoscopic exploration of the [cholecystectomy with exploration of the bile duct, whether bile duct, as it requires an instrument that is not always available, via an open or laparoscopic approach (LCBDE)] or a two-step as well as operating room availability for the procedure to be procedure with ERCP before or after LC. While ERCP has emerged performed, as it is technically demanding and requires a high level as the gold standard for treating CLT, we must not forget that of experience.20,21 this is a technique that is associated with potentially severe In this study, we present the experience accumulated at complications, such as acute pancreatitis (1.8–8.6%), cholangitis our center in terms of the CEBLAS approach executed in the (1–5%), bleeding (0.76–2.3%), and bowel perforation (0.3–1.2%), context of elective treatment of CLT in a series of more than 100 following endoscopic sphincterotomy (ES).14 patients carried out over 13 years. We have confirmed that it is feasible and reproducible and is associated with a low number Table 2: Biliary fistula of failures and complications, with a CLT resolution success rate Fistula of 96.4% (80/83) in patients diagnosed intraoperatively with CLT with a resolution rate of 97% (98/101) for the whole series. Kehr drain Yes Not Total These results are comparable to those reported in the literature Yes 1.9% (2) 13.8% (14) 16 regarding exploration with ERCP and open exploration of the Not 13.8% (14) 70.2% (71) 85 main bile duct, with lower morbidity and mortality rates than Total 16 85 101 these approaches. 22–24 Two-sided Fisher´s exact = 1 For the whole series, the presence of CLT was confirmed in 82.2% (83/101) either via IOC or via a preoperative imaging study (MRI or CT scan). Seventy-two patients underwent surgery Table 3: Postoperative complications more than 7 days after the diagnostic test, and, as such, the Complications N % first intraoperative task was to confirm the presence of CLT via IOC. Surprisingly, 14 patients had a normal IOC, and a further 4 Biliary fistula 16 15.8 patients had an IOC that was unclear. Finally, these 18 patients Residual choledocholithiasis 4 3.9 (25% of the patients with a diagnostic study for CLT more than Bleeding 3 2.9 7 days previously) did not have CLT, and surgical exploration of Residual collection 3 2.9 the bile duct was, therefore, not necessary. In comparative terms, Caledonian stenosis 0 0 some authors, such as Del Pozo et al., have reported up to 12.5% Paralytic ileus 1 0.9 “blank ERCP.”25 Pneumonia 2 1.9 The ideal approach for the surgical exploration of the bile duct Urinary infection 3 2.9 is the transcystic approach, which is technically easier and has the advantage of keeping the main bile duct intact. However, its use has limitations and indications that are mainly determined by the Table 4: Postoperative complication grouped according to CD diameter of the cystic duct, the number and size of the stones, classification and the potential presence of an endoprosthesis in the main bile duct, as well as the inability to carry out a proximal exploration Postoperative complication of CD N % of the common hepatic duct with the choledochoscope through Minor 21 20.8 the cystic duct. 21–23 In our series, this approach could only be I 17 16.8 used in two patients (1.9%) with a 100% success rate. For the rest II 4 3.9 of the patients, the transcholedochal approach was used, even Major 8 7.9 though this is a technically demanding approach that requires the IIIa 5 4.9 advanced laparoscopic experience.26,27 This approach was used in 97.5% of patients (81/83). The flexible choledochoscope is a highly IIIb 1 0.9 useful tool in the exploration of the main bile duct, both in direct IV 0 0 visualization of the intraluminal calculi and in the removal with the V 2 1.9 assistance of a Dormia basket or Fogarty vascular catheter.18,28–30 122 World Journal of Laparoscopic Surgery, Volume 14 Issue 2 (May–August 2021) Results Obtained with the Laparoscopic Approach for Elective Choledocholithiasis We used the choledochoscope in all cases with diagnostic imaging A randomized trial published by Bansal et al. shows how studies more than 7 days previously or in cases with CLT diagnostic the rate of complications between the LCBDE approach and the IOC to confirm its removal. ERCP were comparable, with most of the LCBDE group having a The postoperative stay following LC is generally short (from CD classification of I and the ERCP group having sphincterotomy 1 to 3 days) and increases significantly if the procedure includes distributed among the rest of the CD classifications. 36 It should be laparoscopic exploration of the bile duct (from 1 to 7 days). 22,30–32 highlighted that, of the rest of the complications, postoperative In our study, the mean postoperative stay duration for all patients bleeding was a severe complication in our series, which required was 6.5 ± 7.3 days. As a result of the wide disparity in the number reintervention in two patients. In terms of the modified CD of patients in each group, we did not find any statistically classification,7 most of the complications were minor (20.8%), with significant differences between the transcystic approach and 7.9% of major complications. Of these, it is worth highlighting a the choledochotomy group (6.7 ± 7.6 vs 2 days, p = 0.38). The mortality rate of 1.9% (two cases), both of which were secondary to transcystic approach is a technique that has very good results, bleeding. One of the cases was a patient with previously unknown with resolution in 90% of cases if a flexible choledochoscope is cirrhosis, who presented with decompensation and subsequent available and in 60% when radiology-guided, with a short, rapid multiple organ failure following bleeding, meaning this was a postoperative recovery period. Furthermore, it keeps both the high-risk patient. The other patient experienced hypovolemic main bile duct and the sphincter of Oddi intact, which makes it shock secondary to pseudoaneurysm of the gastroduodenal particularly interesting; whenever possible, this should be the artery, with emergency reintervention to control the bleeding, route of choice. 33 which was a severe complication leading to massive bleeding The overall complication rate in our series was 28.7% (29 and eventually resulting in death. Three patients experienced a patients). Most of these complications were of surgical origin, postoperative residual intra-abdominal collection that progressed particularly postoperative biliary fistula (16 patients, 15.8%) and well with antibiotic treatment. In most studies, the mortality rate residual CLT (4 patients, 3.9%). In terms of biliary fistula, most cases of the laparoscopic exploration of the main bile duct is 0 to 1% in did not require specific treatment, given that these were low-flow the hands of experienced biliary surgeons. This rate is similar to fistulas that did not affect the patients’ general clinical condition. the incidence found in the open exploration of the bile duct, 37–41 No relationship was found between the presence of a postoperative as well as for the endoscopic approach (0–1.5%).42–44 biliary fistula and the insertion of a Kehr drain (1.9 vs 13.8%, p = ns). Some authors describe postoperative bleeding as a very rare This has already been reported in other studies, such as the recent complication but one which is responsible in most cases for early meta-analysis by Poddal et al., in which no differences were found reintervention. It usually occurs after a difficult cholecystectomy in terms of a biliary fistula between those with a Kehr drain in situ or in patients with coagulation abnormalities, with patients with and those without, and they report 3.9% of cases with biliary cirrhosis being those at the highest risk. Generally speaking, this peritonitis following Kehr removal, with no significance compared type of intervention restricts surgeons to use local hemostatic to the primary-closure group. 34 agents and to insert a suction drain in the subhepatic position. In our study, the choledochotomy was sutured over the Kehr It is important to highlight the serious nature of a reintervention, drain in 18.9% of patients. Closure over the Kehr drain provides as 10% of patients undergoing further surgery will have severe biliary decompression, as well as drainage in cases of cholangitis, complications.45–47 and allows us to obtain images of the biliary system after the After long-term follow-up of over 24 months, we did not operation, providing an access through which residual stones can observe any cases of bile duct stricture or cholangitis, in line with be removed. It also has its drawbacks, in that it could open up a route other studies. We, therefore, consider that another benefits of for bacteremia, accidental premature dislocation, and obstruction, this approach should be highlighted, as carrying out ERCP with and it could be associated with bile leakage and peritonitis after ES causes increasing repeat cholangitis, as we have previously its removal. Given this, it was removed in our study after a mean mentioned. period of 3 weeks (range: 10–105 days). Our study has some limitations, in that it is a retrospective However, the presence of residual CLT, while uncommon study with a relatively small sample size. This study represents our (four cases, 3.9%), always required another invasive procedure experience to date in laparoscopic exploration of the bile duct. to be performed, generally an endoscopic procedure, for it to be resolved. Interestingly, in most cases (3/4), an exploration of the bile duct had been carried out via direct vision with a C o n c lu s i o n flexible choledochoscope, which is considered to be the best In our experience, the laparoscopic approach for one-step elective diagnostic technique for CLT. The reasons behind what happened treatment of CLT and cholelithiasis is a safe option, with a very could be explained by the presence of small-size calculi or their small number of complications and satisfactory short- and long- intrahepatic migration; it is worth noting that, of these four terms results, making use of the benefits of the minimally invasive patients, two underwent confirmation with IOC and the other approach and avoiding the inconveniences of ERCP, as well as the two with choledochoscopy. We consider that the surgeon’s open approach. Furthermore, despite preoperative identification experience in carrying out the procedure and maneuvering the of CLT, it allowed us to avoid an unnecessary exploration of the bile choledochoscope could have had an effect on there not being any duct in 25% of patients. residual CLT observed intraoperatively, as the four cases recorded corresponded to patients from the start of the series. 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