Intraoperative enteroscopy

Surg Endosc (2007) 21: 1111–1116 DOI: 10.1007/s00464-006-9052-4 Ó Springer Science+Business Media, LLC 2006

Intraoperative enteroscopy Ten yearsÕ experience at a single tertiary center M. Kopa´cˇova´,1 J. Buresˇ ,1 L. Vykourˇ il,2 P. Hladı´ k,2 D. Sˇimkovicˇ,2 B. Jon,2 A. Ferko,2 I. Tachecı´ ,1 S. Rejchrt1 1

2nd Department of Medicine, Charles University in Praha, Faculty of Medicine at Hradec Kra´love´, University Teaching Hospital, Sokolska´ 581, Hradec Kra´love´, 500 05, Czech Republic 2 Department of Surgery, Charles University in Praha, Faculty of Medicine at Hradec Kra´love´, University Teaching Hospital, Sokolska´ 581, Hradec Kra´love´, 500 05, Czech Republic Received: 18 June 2006/Accepted: 23 June 2006/Online publication: 14 November 2006

Abstract Background and methods: Intraoperative enteroscopy is an invasive technique for small bowel investigation. It enables us to investigate the entire small intestine and to treat pathological findings by endoscopic or surgical means at the same time. The investigation is invasive and that is why the proper indication is mandatory. Results: Forty-one intraoperative enteroscopies were performed at our center within a 10-year period. The procedure was diagnostic in 37/41 patients (90.2%); in 3 patients no pathology was found, and in 1 patient we found only previously diagnosed celiac disease. The investigation was therapeutic in 35/41 (85.4%) patients; 2 patients with small bowel ulcers did not require any intraoperative therapy. The pathological findings were arteriovenous malformations (found in 12 patients), small bowel NSAID-induced or CrohnÕs ulcers (8 patients)—ulcerations and arteriovenous malformations were simultaneously found in three patients; carcinoid of the small intestine (5 patients); Peutz-Jeghers syndrome (5 patients); bleeding polyps (2 gastrointestinal stromal tumors, 1 paraganglioma, and 1 lipoma—in 4 patients); Rendu-Osler-Weber disease (2 patients); multiple cavernous hemangiomas in blue rubber bleb nevus syndrome (1 patient); Henoch-Scho¨nlein purpura (1 patient); aortoenteral fistula (1 patient); and retrograde intussusception of MeckelÕs diverticulum (1 patient). In five patients with Peutz-Jeghers syndrome, 6-22 hamartomas (median of 18 per session) were removed by means of endoscopic polypectomy during intraoperative enteroscopy. There were no major procedurerelated complications in our series.

This work was presented in part at the 13th United European Gastroenterology Week, October 2005, Copenhagen, Denmark. Correspondence to: M. Kopa´cˇova´

Conclusions: Intraoperative enteroscopy is accepted as the ultimate diagnostic procedure for complete investigation of the small bowel. Despite the introduction of double-balloon enteroscopy into clinical practice, intraoperative enteroscopy will be reserved for those cases where double-balloon enteroscopy cannot be performed or fails to investigate the entire small intestine, especially to prevent excessive bowel resection. Key words: Intraoperative — Perioperative — Enteroscopy — Small bowel — Endoscopy

Intraoperative enteroscopy has been accepted as the ultimate diagnostic and/or therapeutic procedure for the complete investigation of the small bowel. It makes it possible to immediately solve pathological findings by endoscopic or surgical means and to perform histopathological examinations of biopsy and/or resected specimens. By visualizing the mucosa, intraoperative enteroscopy can provide information that allows more precise surgery, thereby limiting resection. The very first investigation was performed in 1976 [12]. The most widely used surgical approach is standard laparotomy, but laparoscopically assisted enteroscopy has also been reported; some authors even used an overtube. Different types of endoscopes have been used, such as pediatric colonoscopes and sonde- and pushenteroscopes. At present, a disinfected video-gastroscope is used at most centers. The introductory route may be oral or, most often, transparietal following enterotomy. Major indications for intraoperative enteroscopy are obscure gastrointestinal bleeding (in patients with negative gastroscopy, push-enteroscopy, and colonoscopy), focal pathology of the small intestine (out off the reach of the push-enteroscopy or colonoscopy), and/ or vague findings in small bowel follow-through (classic,

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computed tomographic [CT], and/or magnetic resonance imaging [MRI] enteroclysis). Contraindications for the procedure are refusal by the patient, acute abdomen (including perforation), and the patientÕs general lack of fitness for surgery. We introduced the first intraoperative enteroscopy in 1995. The aim of the present study was to evaluate the results gained through 10 years of experience with the procedure in our center.

course of investigation (endoscopic picture) on the screen of the monitor is very important for perfect cooperation of the endoscopist and the surgeon. The endoscopic picture is different from the standard enteroscopic picture because of trans-illumination of the small bowel wall by light from operation lamps in the theater. Thus the vascular pattern of the small intestinal wall is enhanced. An experienced endoscopist is mandatory for proper evaluation of the picture [4, 17, 18]. We prefer intraoperative enteroscopy during laparotomy through a mid-small bowel enterotomy.

Results Materials and methods Indications Within the 10-year period 1995–2005, a total of 42 intraoperative enteroscopies were indicated, but one procedure (in a 75-year-old man with bleeding of unknown origin) was abandoned in the operating theater because of generalized carcinoma. And so we performed 41 procedures on 20 men and 21 women (age range 12–83 years; mean age, 57 years). Indications for intraoperative enteroscopy were bleeding of unknown origin (28 patients), planned polypectomy in PeutzJeghers syndrome (5 patients), suspicion of small bowel tumor (7 patients), and suspicion of small intestinal lymphoma (1 patient with known celiac disease).

Preparation of the procedure All patients are admitted to the hospital at least 2 days before the procedure. The day before the investigation a standard preparation of the bowel (the same as for colonoscopy) follows (orally administrated sodium phosphate or macrogolum solution). Venous access is obtained and antibiotic prophylaxis is started before the procedure. Preparation for the procedure begins in the endoscopy unit. The endoscopic nurse sterilizes the endoscope and covers it in sterile gauze. We use a standard endothermodisinfector EDT-2 (Olympus) and have verified that high-level disinfection is achieved in all cases [34]. An endoscopy nurse has to prepare an endoscopic tower and all possible sterile accessories (BICAP Probe for electro-coagulation, endoscopic snare in the case of planned polypectomy, etc.). The disinfected endoscope is prepared immediately before the enteroscopy. The endoscopist and the theater nurse prepare the scope. The operational part of the endoscope is covered with a sterile plastic laparoscopic sleeve, which is fixed to the head of the device. This will allow the scope to be put back into the sleeve during extraction from the intestine and preserve the sterility of the operating field. The physician performing the endoscopy becomes a member of the operating team. The endoscopic nurse is not dressed aseptically, she operates the endoscopic tower and all devices. All sterile accessories are handled by the theater nurse.

Performance The patient is investigated under general anesthesia, intubated while lying supine. Retrograde overinflation of the stomach is prevented by introducing a nasogastric tube for permanent suction at the beginning of the procedure (under narcosis). After removal of possible adhesions of the small intestine the surgeon prepares the mid-small bowel enterotomy with a circular suture (only the first of our procedures in 1995 was performed by the oral route). The suture is fastened around the scope after its insertion into the intestine. The circular suture is necessary for the possibility of small bowel insufflation. The upper part of the small intestine is investigated first because of sparse bacterial load. The distal part of the intestine is clamped to prevent overinflation of the intestine and investigated later, without the need for additional enterotomies. After the investigation of each one-half of the intestine, a careful desufflation is performed. The endoscopist operates the endoscope, but insertion and extraction of the endoscope is handled by the surgeon. The possibility of monitoring the

We have performed 41 intraoperative enteroscopies from 1995 until May 2005. The procedure was diagnostic in 37/41 patients (90.2%); in 3 patients no pathology was found and in 1 patient we found only previously diagnosed celiac disease, but not the suspected lymphoma. The investigation was therapeutic in 35/41 patients, two patients with small bowel ulcers did not require any therapy during surgery. Endoscopic findings Intraoperative endoscopic findings in our patients included arteriovenous malformations (12 patients); small bowel NSAID-induced or CrohnÕs ulcers (8 patients); small bowel carcinoid (5 patients); planned polypectomy because of multiple hamartomas in Peutz-Jeghers syndrome (5 patients); bleeding polyps—gastrointestinal stromal tumor, paraganglioma or lipoma (4 patients); Rendu-Osler-Weber disease (2 patients); multiple cavernous hemangiomas in blue rubber bleb nevus syndrome (1 patient); Henoch-Scho¨nlein purpura (1 patient); aortoenteral fistula (1 patient); retrograde intussusception of MeckelÕs diverticulum (1 patient); and celiac disease without lymphoma (1 patient). Three patients had arteriovenous malformations and ulcers simultaneously. In 5 patients with Peutz-Jeghers syndrome, 6–22 hamartomas (median of 18 per session) were removed during intraoperative enteroscopy. Normal findings were discovered in only 3 of our 41 patients (7.3%). Two of those 3 patients were indicated for intraoperative enteroscopy for suspicion of endocrine active tumor, 1 because of gastrointestinal bleeding (see Table 1). The youngest patient was a 12-year-old girl with blue rubber bleb nevus; the oldest were two 83year-old women with gastrointestinal bleeding (the former with bleeding arteriovenous malformation, the later with stromal tumor of the ileum). Therapy performed Possible pathology found was treated predominantly by endoscopic (14/41; 34.1%) or surgical means (19/41; 46.3%). In another 2 patients (4.9%) we chose a combined technique: in the 12-year-old girl with blue rubber bleb nevus (the small lesions were treated in an endoscopic manner, three bigger hemangiomas from 5 to 12 mm in diameter were resected by surgeon) and in a 77year-old man with a repeated episode of serious gastrointestinal bleeding (about 20 of the arteriovenous

1113 Table 1. Intraoperative endoscopic findings Findings Arteriovenous malformations Ulcers (NSAIDs, CrohnÕs disease) Arteriovenous malformations and ulcers simultaneously Carcinoid Peutz-Jeghers syndrome Bleeding polyps (stromal tumor 2, paraganglioma 1, lipoma 1) Rendu-Osler-Weber disease Multiple cavernous hemangiomas in blue rubber bleb nevus syndrome Henoch-Scho¨nlein purpura Aortoenteral fistula Retrograde intussusception of MeckelÕs diverticulum Celiac disease Normal finding Total

No. of patients 9 5 3 5 5 4 2 1 1 1 1 1 3 41

malformations were treated by electrocoagulation, and about 30 cm of the most affected part of the small intestine were resected). In general, focal lesions (tumors, submucosal polyps, bigger blue rubber bleb nevi) were resected surgically; arteriovenous malformations were treated mostly endoscopically by electrocoagulation, and hamartomas were treated by endoscopic polypectomy. Only the first of our procedures in 1995 was performed by the oral route; all others were performed via the transparietal course using enterotomy. Only in 2 cases was one more enterotomy needed because of adhesions of the small bowel; in the rest of patients the whole procedure was accomplished through one enterotomy. Forty intraoperative enteroscopies (97.6%) were complete, reaching the duodenal bulb at the proximal end and the cecum at the distal end of the small intestine. Only one procedure was interrupted without reaching the cecum, in a 72-year-old woman with massive gastrointestinal bleeding. Intraoperative enteroscopy was diagnostic in 27/28 patients (96.4%) investigated because of obscure gastrointestinal bleeding (see Table 2). In one case we did not find any source of bleeding (normal finding). In 14 others (50%) lesions were amenable to segmental resection; 9 were treated endoscopically (32%), 2 by combined surgical and endoscopic methods (7%), and the other 2 (7%) did not require any intraoperative treatment. Twelve patients were treated with electrocoagulation and/or resection because of arteriovenous malformations. Two of them (16.6%) developed repeated bleeding calling for electrocoagulation of newly evolved malformations during conventional endoscopy: an 83-year-old woman 4 years after intraoperative enteroscopy and a 68-year-old man 5 months after intraoperative enteroscopy. The source of bleeding was in the colon in the latter case. A 52-year-old woman with Rendu-Osler-Weber disease underwent reoperation for resection because of rebleeding 4 years after the first intraoperative enteroscopy. A 65-year-old woman, another patient with Rendu-Osler-Weber disease, was treated by electroco-

agulation during conventional endoscopy 3 years after intraoperative enteroscopy. In the whole group, the rebleeding rate was 4/28 patients (14.3%). Complications We have had no major immediate procedure-related complication so far, only a few mucosal tears without the need for additional treatment. One patient died within 5 hours after intraoperative enteroscopy of complications of diagnosed aortoenteral fistula (post-hemorrhagic shock). A second patient, a 77-year-old man with a repeated episode of serious gastrointestinal bleeding, developed postoperative complications leading to death. In this patient about 20 arteriovenous malformations were treated by electrocoagulation, and the most affected part of the small intestine was resected (30 cm long). The patient required reoperation 3 days later after dehiscence of the wound with a hematoma of the abdominal wall. He developed a stroke and pneumonia. In spite of intensive therapy he died of septic shock 18 days after intraoperative enteroscopy. Absceding pyelonephritis, pneumonia, and encephalomalacy were found at autopsy. Long-term results In 5 patients (12%) findings were definitively resolved by resection immediately after intraoperative enteroscopy during the same anesthesia (1 patient with MeckelÕs diverticulum; 1 with lipoma; 2 patients with stromal tumor; and 1 patient with paraganglioma of the small bowel). Seven of our 41 patients (17%) have died during the 10-year study period (median of follow-up 37 months; mean 41 months), including the two patients mentioned above. The remaining 5 patients died of conditions unrelated to intraoperative enteroscopy: 1 died of terminal liver cirrhosis, 2 of heart failure, and 2 of generalized carcinoma. We have no information about 3 of our 41 patients (7%). The remaining 26 of the 41 patients (63%) are followed-up in our department or in cooperating gastroenterological units elsewhere. The re-bleeding rate in our group of patients with gastrointestinal bleeding was 4/28 patients (14.3%) during the 10-year period.

Discussion Intraoperative enteroscopy is the sole method for investigating the entire small intestine and providing a immediate resolution of the pathological findings. Specific indication for the procedure is necessary because of the invasive nature of the method. We performed the first intraoperative enteroscopy in our center in 1995, but the next investigation was not performed until 1998, when the methodology was developed and the investigation became routine. Nowadays from 6 to 8 intraop-

1114 Table 2. Comparison of intraoperative enteroscopy (IOE) results in patients with GI bleeding

Study

No. of patients

Diagnostic

Complete enteroscopy

Curable IOE

Rebleeding rate

Perioperative mortality

Hartmann et al. [13] Kendrick et al. [14] Lau et al. [22] Lewis et al. [25] Ress et al. [35] Zaman et al. [50] Kopa´cˇova´ et al. (this study)

47 70 17 23 44 14 28

34/47 72% 52/70 74% 17/17 100% 17/23 74% 31/44 70% 8/14 57% 27/28 96%

100% 100% 94% 57% NR 93% 96%

34/47 72% 35/70 50% NR 11/23 48% 31/44 70% 8/14 57% 25/28 89%

NR 22/70 31% 1/17 6% 9/23 39% 23/44 52% 7/14 50% 4/28 14%

1/47 4/70 1/17 1/23 5/44 0/14 2/28

2% 6% 6% 4% 11% 0% 7%

NR: not reported Perioperative mortality–within 30 days after surgery

erative enteroscopies on average are needed per year in our department (serving as a tertiary center for 1 million population). Intraoperative enteroscopy was diagnostic in 37/41 patients (90.2%) in our 10-year series. Normal findings were obtained in only 3 of our 41 patients (7.3%), and 1 patient had only previously diagnosed celiac disease (2.4%). The yield of the investigations was very high and the indications can be considered as correct. The major indication for intraoperative enteroscopy is gastrointestinal bleeding of unknown origin (obscureovert or obscure-occult bleeding in patients with negative gastroscopy, push-enteroscopy, and colonoscopy and with negative imaging investigations—computed tomography (CT)- and/or magnetic resonance imaging (MRI)-enteroclysis, nuclear scan, etc.) [7, 11, 13, 14, 17, 18, 20, 27, 42, 45, 46]. Intraoperative enteroscopy is accepted as the ultimate diagnostic procedure for complete investigation of the small bowel in patients with obscure gastrointestinal bleeding [25, 29]. Small intestinal bleeding is difficult to diagnose, and enteroscopy is the most effective intraoperative procedure for small bowel lesion localization. The most common sources of small bowel bleeding are considered arteriovenous malformations and nonsteroidal anti-inflammatory drug–induced injury [1, 40]. Total intraoperative enteroscopy is effective in detecting the bleeding point in the small intestine; it is still the gold standard [1, 7, 14, 20, 27, 28, 45]. In our series, intraoperative enteroscopy was diagnostic in 27/28 patients (96.4%) investigated for obscure gastrointestinal bleeding: 14 (50%) had lesions amenable to segmental resection, 9 were treated endoscopically (32%), and 2 by combined surgical and endoscopical methods (7%). Another 2 patients (7%) did not require any intraoperative treatment. We consider our results to be very satisfying (see Table 2). Hartmann et al. [13] give results of a study comparing capsule endoscopy by using intraoperative enteroscopy as a standard in patients with obscure GI bleeding. Lewis et al. [25] reported 23 intraoperative enteroscopies in patients with chronic transfusion-dependent gastrointestinal bleeding. They concluded that surgical exploration and performance of intraoperative enteroscopy may be indicated in patients with obscure gastrointestinal bleeding. Zaman et al. [50] presented a study that included 14 patients who underwent intraoperative enteroscopy; the terminal ileum was reached in 13. A bleeding

source was identified in 8 (57%), including angiodysplasias, lymphoma, carcinoid, and a nevus-like lesion. Kendrick et al. [14] published results from 70 patients who underwent intraoperative enteroscopy for obscure gastrointestinal bleeding: 52 patients with overt bleeding and 18 with occult bleeding. A lesion was identified and treated in 52 patients (74%)—in 39 in the overt group and 13 in the occult group. Ress et al. [35] reported 44 intraoperative enteroscopies. A site-specific source was seen in the small bowel in 31 of their patients (70%). Lau et al. [21] diagnosed angiodysplasias in 6 patients with gastrointestinal bleeding; lesions were treated by segmental resection. The same group of authors [22] operated on 49 patients with bleeding lesions in the small intestine. Intraoperative enteroscopy was performed on 17 of their patients. Duggan et al. [8] refer to the case of 4-month-old infant with a prolonged illness caused by an occult intestinal stricture that escaped conventional radiological and surgical methods and required intraoperative enteroscopy. The second important indication is focal disease of the small bowel. The method has chiefly been used in patients with Peutz-Jeghers syndrome, an inherited, autosomal dominant disorder characterized by hamartomatous polyps in the gastrointestinal tract, mostly in the small bowel (small bowel in 78% of the patients, colon 42%, stomach 38%, and rectum 28%), and pigmented mucocutaneous lesions. This syndrome also predisposes to gastrointestinal, pancreatic, breast, uterine, and other malignancies [23, 33]. During the first 3 decades of life, bleeding, obstruction and/or intussusception are common complications in patients with Peutz-Jeghers syndrome. Intraoperative enteroscopy may obviate the need for repeated urgent operations and small bowel resections leading to a short bowel syndrome. Patients are candidates for prophylactic laparotomy and polypectomy of hamartomas within the entire small bowel [26, 39, 41]. The frequency of intraoperative polypectomies in Peutz-Jeghers syndrome is dictated by enteroclysis and/or wireless capsule endoscopy; a finding of larger polyps (1.5–2 cm in diameter) is indication for another procedure [33]. The recommended interval of small bowel follow-through is from 2 to 3 years [26]. In our 5 patients with Peutz-Jeghers syndrome, 6–22 hamartomas (median of 18 per session) with a diameter up to 40 mm were removed during intraoperative enteroscopy. Not one of our patients has been referred for a repeated procedure; the first such

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procedure was performed in 1999. Pennazio and Rossini [31] reported 3 patients (of total 7 in follow-up) who underwent polypectomy during intraoperative enteroscopy (for removal of 10–25 polyps; mean 16 per session). In the remaining 4 patients multiple polypectomy was performed by means of push-enteroscopy and retrograde ileoscopy [31]. The same procedure is indicated in patients with familial adenomatous polyposis and juvenile polyposis [36]. The third effective indication is a clinical suspicion of an active small bowel endocrine tumor. The primary tumor (carcinoid in our patients) could be very small, measuring only a few millimeters, and undetectable for the surgeon. We have recognized primary small intestinal carcinoid in 5 patients. Thus, an endoscopically found primary tumor could be easily resected by surgical means. In our series, bleeding polyps were identified in another 4 patients at intraoperative enteroscopy: gastrointestinal stromal tumors (2 patients), paraganglioma (1 patient), and lipoma (1 patient). In a comparison of preoperative radiography and intraoperative enteroscopy in CrohnÕs disease, Esaki et al. [10] identified intestinal lesions in 23 patients by intraoperative enteroscopy and in 19 patients by radiography. Similarly Lescut et al. [24] state that 65% of patients operated on for CrohnÕs disease had lesions of the small intestine detected by intraoperative endoscopy, and those lesions had gone unrecognized before surgery in more than half of the cases [24]. The intraoperative localization procedure is simple and effective, and its is recommended that it be used more freely [10, 24]. Promising results with the clinical applications of capsule endoscopy have been reported recently [16, 47]. The method has chiefly been used in patients with obscure gastrointestinal bleeding [30, 38, 44]. A diagnostic capsule endoscopy will direct appropriate medical, endoscopic, or surgical intervention, depending on whether the lesion is single or multiple, and whether the patient is a candidate for intraoperative enteroscopy. Intraoperative endoscopy should be strongly considered in patients with recurrent bleeding and a nondiagnostic evaluation. Intraoperative enteroscopy is highly recommended in young patients (< 50 years of age) because there is an increased frequency of small bowel tumors and MeckelÕs diverticulum, which are amenable to surgical therapy [2, 5, 19]. We use capsule endoscopy prior to intraoperative enteroscopy to specify the indication for the procedure. Bolz et al. [3] evaluated their initial results comparing capsule endoscopy and intraoperative enteroscopy in obscure gastrointestinal bleeding. Both methods were diagnostic in 18/21 (86%) patients. Capsule endoscopy underestimated the extent of angiodysplasias in two persons. Hartmann et al. of the same group [13], presented a prospective study comparing wireless capsule endoscopy with intraoperative enteroscopy in 47 patients with obscure gastrointestinal bleeding. Capsule endoscopy identified lesions in 100% of the patients with ongoing overt bleeding, 67% of the patients with previous overt bleeding, and 67% of the patients with obscure-occult bleeding. Compared with intraoperative enteroscopy, the sensitivity, specificity, and positive and negative predictive values of capsule

enteroscopy were 95%, 75%, 95%, and 86%, respectively [13]. It must be stressed that both push-enteroscopy and intraoperative enteroscopy still have a precise and valid role in the management of patients with small bowel diseases [32]. Capsule endoscopy will probably become a first-line tool for detecting abnormalities of the small bowel, and very probably this will entail redefining some diagnostic algorithms for diseases involving the small bowel [32, 37, 43]. Recent reports on double-balloon enteroscopy suggest that this new method may be able to replace at least intraoperative enteroscopy in many circumstances [15, 48]. In a retrospective analysis conducted at four European medical centers, a total of 62 patients with suspected or documented small-bowel diseases were investigated by double-balloon enteroscopy. A total of 89 procedures were performed (26 and 9 patients from the oral or the anal route, respectively; 27 patients from both). However, the entire small bowel was completely explored in only 10 patients (16.2%) [6]. We have introduced double-balloon enteroscopy in our department recently. At present we perform all push-enteroscopy, double-balloon and intraoperative enteroscopy, and wireless capsule endoscopy. We do not consider these methods competitive but complementary with the proper indications. Intraoperative enteroscopy still remains a unique method of small bowel investigation and concurrent resolution of the pathological findings. The investigation is invasive, so a precise indication is imperative. One of the advantages of intraoperative enteroscopy is that on the other side of the small bowel wall is a surgeon. It allows the endoscopist to be more invasive. Perfect teamwork between the surgeon, endoscopist, and anesthesiologist is indispensable. The indications for intraoperative enteroscopy have been diminished over recent years since the development of double-balloon (push-and-pull) enteroscopy [37, 49]. Despite the introduction of the double-balloon procedure into clinical practice [6, 9, 48], intraoperative enteroscopy will be reserved for those cases where doubleballoon enteroscopy could not be performed or it fails to investigate the entire small intestine. Its particular value will be in preventing excessive bowel resection. Acknowledgments. The study was supported by the research project: MZO 00179906 from the Ministry of Health, Czech Republic.

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