the incidence and risk factors of pharyngocutaneous fistula after total ...

AAMJ, VOL (12), NO (4), OCT 2014 SUPLL

AL-AZHAR ASSIUT MEDICAL JOURNAL

THE INCIDENCE AND RISK FACTORS OF PHARYNGOCUTANEOUS FISTULA AFTER TOTAL LARYNGECTOMY Mohamed Abdelrahman Shams Al-din*, Ibrahim Ibrahim Aldesoky *, Ayman abdelaziz *Ahmed Selim **and Mohamed M. El-Sawy** *Lecturer of Otolaryngology, **Professor of Otolaryngology - Department of Otolaryngology - Al Azhar University ‫ــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــ‬ ABSTRACT Pharyngocutaneous fistula (PCF) is a serious complication following total laryngectomy (TL). Its occurrence leads to increased morbidity, delay in adjuvant treatment, prolonged hospitalization, thus, affects the survival of the patients. The presence of fistula in the early post-operative period is very depressive and needs a clear and comprehensive way of management. Although a number of factors that result in PCF have been described, there is still no agreement on the most significant factors. Therefore, this study was planned to determine the incidence of the PCF after TL, prominent predisposing factors that affect fistula incidence and to identify the high-risk patients in an attempt to avoid this devastating complication. The study was done by retrospective reviewing and analysis of the patients records from 2011 – 2014. It was found that 10.3%. of the studied cases (8 out of 77 ) developed PCF. Seventy five of this cases were presented as supraglottic tumor, (75%) were presented with stage IV. In addition, 6 patients were diabetic (75%), 3 patients (38%) had low albumin, 5 patients (62%) suffered from preoperative anemia, 3 patients (38%) had preoperative RT and 5 patients (62%) underwent preoperative tracheotomy. From the 8 patients, neck dissection, unilateral or bilateral was performed in 6 patients (75%).

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Mohamed Abdelrahman Shams Al-din et al

INTRODUCTION Since

Billroth

performed

his

first

laryngectomy

in

1873,

pharyngocutaneous fistula (PCF) still one of the most serious postoperative complications following total laryngectomy (TL). In the 1950’s when Cobalt 60 radiation was developed, the incidence of PCF eventually increased in patients who required salvage surgery (Galli et al., 2009). PCF is defined as a breakdown of the mucosal closure of the pharynx, which results in dissemination of saliva into the peripheral neck (Mäkitie et al., 2003). The reported incidence ranges from 5% to 65% in the period of 70th and 80th and between 9% and 25% in the last decade. Its occurrence vastly increases the length of stay and consequently, the costs of treatment (Esteban et al., 2006). Additionally, this complication can lead to a delayed onset of complementary therapy (such as radiotherapy/chemotherapy), which in turn increases the physical and mental weakness of the patient due to the delay of oral feeding onset and voice rehabilitation, thus hampering the postoperative recovery. In rare cases, it can also lead to stenosis and pharyngeal swallowing disorders, sepsis, mediastinitis, pneumonia and death (Cecatto et al., 2014). Its presence may leads to elevation of the skin flaps with ultimate wound dehiscence, followed by necrosis of the flaps, and in the worst case scenario; carotid exposure and blowout (Javed et al., 2006). Various parameters have been implicated in fistula formation, and they may be grouped as patient factors (age, sex, smoking habit, and comorbid illness); tumor factors (pathology, tumor stage, and tumor site); and treatment factors (previous tracheostomy, preoperative radiotherapy, type of surgery,

258



concurrent neck dissection, postoperative hemoglobin levels, and postoperative radiotherapy) (Markou et al, 2004). Unfortunately, there are controversies in the literature regarding the significance of most of the aforementioned factors. Consequently, the etiology of PCF is still debated, with ongoing disagreement on the predisposing factors, and thus no preventive measure can be implemented effectively (Andrades et al., 2008).

AIM OF THE WORK This study was planned to determine the incidence of the PCF after TL, prominent predisposing factors that affect fistula incidence and to identify the high-risk patients in an attempt to avoid this devastating complication. This was done by retrospective analysis of the surgical team work database.

PATIENTS & METHODS From 2011 to 2014, TL was performed in 77 patients suffering from primary laryngeal cancer in ENT Department, Al-Azhar University Hospitals by the same surgical team. Hypopharyngeal tumors were excluded from this study. In this study, preoperative, operative, and postoperative care was generally standardized. Two days prior to surgery, all patients were given pre-operative broad spectrum antibiotic and anti-reflux medications. The patient's thyroid profile, albumin and CBC were measured preoperatively and one week postoperatively. Operatively, unilateral or bilateral neck dissection was carried out as indicated. In all patients, surgical technique of TL, surgical sutures and type of pharyngeal reconstruction was the same. After placing the nasogastric tube (14F), the pharyngeal defect was repaired meticulously with 2/0 rounded Vicryl sutures. The mucosal closure was done in full thickness, vertical and continuous 259



Connell suture manner. Second-layer closure was performed by approximating the constructor muscles using rounded 2/0 Vicryl sutures. Thyroidectomy was done on the affected side in case of glottic, transglottic tumors and subglottic extension. Additionally, primary TEP for voice restoration was routinely carried out. Pharyngeal myotomy was performed after the removal of the specimen. In all patients suction drain was inserted, which were removed when the amount of wound drainage was less than 30 mL in 24 hours (picture 1).

Picture (1): skin closure, tracheostomy tube & suction drains

All the patients had similar post-operative care in the form of broad spectrum antibiotic with metronidazole, analgesics, anti-reflux and anti-emetic drugs. After surgery, patients were fed on the 3rd day through nasogastric tube. Basically, if there is no evidence of salivary leak, oral feeding was started on the 7th postoperative day in non-radiated patient. In patients who received preoperative RT, oral feeding was postponed to the 2nd week. In addition, thyroid replacement was given when indicated.

260



In the current study the patients were classified according to the occurrence of PCF into 2 groups, group A includes the patients who develop PCF and group B includes non-fistula patients. In both groups, data base was reviewed and compared for the risk factors that could influence fistula formation. These factors includes patient and tumor related factors: age, hemoglobin, albumin, thyroid hormone (T3, T4, TSH) levels, comorbid illnesses (as Diabetes mellitus, Gastroeosophageal reflux, Ischemic heart disease…), site of tumor, tumor stage, positive resection margin, prior radiotherapy, tongue base invasion, type of neck dissection and preoperative tracheostomy. The collected data were compared and analyzed with the following results.

RESULTS In this study, 77 male patients were included. From the 77 patients, 8 patients developed PCF (group A) (10.3%). The remaining 69 patients were collected in (Group B) without CF. The mean age of patients in group A was 60±0.16 years (range from 52 to 65 years). In group B, mean age was 58 (range from 38 to 74 years). In group A, (8 patients), 6 patients were presented with supraglottic tumor with transglottic extention (75%) while 2 patients were presented with glottic tumor (25%). According to the tumor stage, 2 patients were presented with stage III (25%), while 6 patients were presented with stage IV (75%). From the 8 patients, neck dissection, unilateral or bilateral was performed in 6 patients (75%). In addition, 6 patients were diabetic (75%), 3 patients (38%) had low albumin, 5 patients (62%) suffered from preoperative anemia, 3 patients (38%) had preoperative RT and 5 patients (62%) underwent preoperative tracheostomy Table (1), Figure (1).

261



Most of the PCF appeared in the beginning of the 2nd week above the stoma and in the lateral part of the suture line.

Table (1): distribution of group (A) patients in relation to known risk factors of PCF Risk Factor Tumour site

GROUB (A) Glottic Supra glottic 2 (25%) 6 (75%) Stage III Stage IV 2 (25%) 6 (75%) 6 (75%) 6 (75%) 5 (62%) 3 (38%) 3 (38%) 5 (62%)

Tumour stage Neck dissection DM Aneamia Hypoalbumineamia Preoperative RT Preoperative tracheostomy

Fig. (1): distribution of group (A) patients in relation to known risk factors of PCF 262



Patients with PCF were treated initially conservative. The treatment includes, IV antibiotics, wound packing usually with gauze performed 2-4 times daily, antireflux measures, nutritional support with high protein diet provided with through NG-tube. Repeated spitting and cuff tracheostomy tube was always performed to protect the airway against aspiration. In 5/8 patients (62%) the fistula healed with conservative management alone. Surgical repair was done in 3 patients out of 8 (38%) due to failure of healing of the fistula within 4 weeks, through primary closure and sternocledomastoid muscle (SCM) flap in one case and another case was repaired with pectoralis major flap Picture (2). One died from carotid blowout.

Picture (2): PCF

with extensive

skin loss

263



Picture (3): Pharyngocutaneous Fistula after Total Laryngectomy In group B (69 patients), 45 patients were presented with glottic tumor (65%) while 24 patients were presented with supraglottic tumor (35%). According to the tumor stage, 53 patients were presented with stage III (77%), while 16 patients were presented with stage IV (23%). From the 69 patients, neck dissection, unilateral or bilateral, was performed in 42 patients (60%), 24 patients (27%) had low albumin, and 39 patients (56%) suffered from preoperative anemia. In addition, 6 patients were diabetic (9%), 3 patients experienced preoperative RT (4%) and 3 patients underwent preoperative tracheostomy (4%) Table (2), Figure (2). Table (2): distribution of group (B) patients in relation to known risk factors of PCF. Risk Factor

GROUB (B) Glottic Supra glottic 45 (65%) 24 (35%) Stage III Stage IV 53 (77%) 16 (23%) 42 (60%) 6 (9%) 39 (56%) 24 (27%) 3 (4%) 3 (4%)

Tumour site Tumour stage Neck dissection DM Aneamia Hypoalbumineamia Preoperative RT Preoperative tracheostomy

264



Fig (2) : distribution of group (B) patients in relation to known risk factors of PCF. Table (3) : comparison between the 2 groups regarding the different risk factors

Supraglottic glottic Stage III StageIV DM Neck dissection Preoperative treacheostomy Preoperative RT Aneamia Hypoalbumineamia

Total No 30 47 55 22 12 48 8

GROUP (A) With PCF 6 (20%) 2(4.3%) 2 (3.6%) 6 (27.3%) 6 (50%) 6 (12.5 %) 5 (62.5 %)

GROUP (B) Without PCF 24 (80%) 45(95.7%) 53 (96.3%) 16 (72.7%) 6 (50%) 42 (87.5 %) 3 (37.5%)

6 44 27

3 ( 50%) 5 (11.3 %) 3 (11.1 %)

3 (50%) 39 (88.6 %) 24 (88.9%)

265



Figure (3) : graphic presentation of the comparison between the 2 groups regarding the different risk factors

266



DISCUSSION One of the most serious complications of the surgical treatment of hypopharyngeal and laryngeal surgery is the pharyngocutaneous fistula (PCF). The etiology of such condition is multifactorial; comorbid patient conditions and local factors that affect wound healing can predispose to and affect both fistula formation and chances for healing. The presence of the PCF usually has a negative influence on the patient outcome. Skin infection and necrosis of the flap is very dangerous consequence of PCF as it may lead to carotid blow out. Hospital stay, patient convalescence and psychic condition are greatly affected Due to concerns regarding radiation-related toxicity and hindered wound healing, it is commonly considered a contraindication for the initiation of postoperative radiation therapy (RT) ( Lau et al., 2011.) In this study, we reviewed the possible etiologies for PCF in the literatures and the patient records were reviewed and analyzed to assess the possible risk factors including age, diabetes, and hemoglobin, and albumin level, site of tumor, tumor stage, prior RT, and preoperative tracheostomy. In the present study we found that, the significant risk factors in the 8 patients who developed PCF were; the presence of preoperative tracheostomy, preoperative RT and the presence of anemia or diabetes. Also the presence of the tumour in the supraglottic area with transglottic extension, or the presentation of the patient in advanced stage (IV) was observed as a risk factor. The incidence of PCF after TL fluctuates in different studies all over the world. In this study, the rate of PCF is 10.3% (8 out of 77 patients). This rate goes with the results obtained from the literature, according to which the rate varies from 8.7% to 28.6%.

267



Arain et al., 2013 studied the incidence of PCF in a series of 77 patients; they

found

that

28.6%

of

their

laryngectomy

patients

develop

pharyngocutaneous fistula. They contribute such high incidence of PCF mainly to of the large number of patients undergoing radiotherapy and chemotherapy as primary treatment for laryngeal cancers as a part of the organ preservation protocol. Dedivitis, et al., 2007 reported that, PCF was encountered in 7 patients out of 55 (12.7%) had total laryngectomy for laryngeal cancer. In addition, Saki et al., 2008 reported the incidence of 13%, (19 out of 146) patients underwent total laryngectomy. Although many factors were described for the development of PCF, there is still no agreement on the most significant factors (Paydarfar and Birkmeyer 2006). Regarding the age, in the present study we found the mean age of the PCF group was 60±0.16years (range from 52 to 65 years). Owing to the small range of age it is difficult to link between the age and the incidence of PCF. This finding is in comparable with that obtained by Arain et al., 2013, where their mean age was 57 years (range from 23-80 years). In the study of Seikaly and Park 1995, on 22 patients underwent TL, they didn’t found a statistical evidence regarding the influence of the age of the patient on the development of PCF Also, Parikh et al. 1998 in their retrospective study on 125 consecutive TL, found no association between pharyngocutaneous fistula and age. In the present study, PCF was seen frequently in patients subjected to preoperative tracheostomy. About 5 out of 8 patients with PCF (62%) had preoperative tracheostomy. Fifty percent of all patients underwent preoperative tracheostomy (12 patients), developed PCF postoperatively. This is considered as a risk factor in fistula formation. It may be explained by the fact that, 268



tracheostomy can cause tissue infection, necrosis and possible skin loss which lead to closure of the skin flaps under tension and contributes to wound dehiscence. However, Saki et al., (2008) didn’t observe any significant relation between the performance of preoperative tracheostomy and the development of postoperative PCF. Also, in another study, a retrospective data were collected on 145 patients treated with total laryngectomy/pharyngolaryngectomy at the Victoria Hospital in London. It was found that (25%) patients developed a postoperative PCF. But the authors didn’t observe any increase in PCF rates with either preoperative tracheostomy or primary TEP (Dowthwaite et al., 2012). In the present study, 3 patients (38%) of those who develop PCF after TL, experienced RT as primary treatment. On the other hand, in group B 3 patients (4%) had preoperative RT. The total number of patients exposed to radiotherapy prior to treatment is 6 patients. Three of them (50 %) develop PCF. Therefore, the relation between the preoperative RT and PCF is significantly high. With increased reliance on organ preservation protocols, an increased number of patients receive chemotherapy and radiotherapy as a treatment for laryngeal cancers is observed. Though this has offered good loco-regional disease control, the association of previous radiotherapy with the formation of PCF has been well established. In the study done by Arain et al., 2013, there were 17 patients who had received prior external beam radiotherapy. Fifteen (88.2%) of 17 patients developed PCF compared to only 11.7% of non-irradiated patients. Radiation is known to be toxic to normal tissues and impair surgical wound healing which is significantly manifested microscopically by obliterative endarteritis and fibrosis.

269



Statistical analyses showed a significant correlation between PCF and preoperative radiotherapy, which might be attributed to the diminished healing capacity of the irradiated tissues. (Markou et al, 2004). RT affects the microvasculature of tissue, leading to subintimal fibrosis, endarteritis, and thrombus formation. This leads to impaired vascularity and increased fibrosis that diminish tissue oxygenation and alter wound healing (Marx and Johnson 1988). Salvage TL after RT is associated with an increased risk of wound complications and predispose to fistula formation (Weber et al., 2003). Johansen et al., 1988 reported a fistula rate of 80% in 21 patients undergoing salvage TL following RT. Grau et al (2003) reported in a large series of 472 patients undergoing salvage laryngectomy after RT. Eighty nine patients of them (21%) developed PCF. In addition, Wakisaka et al., 2008 in his study on 66 patients underwent salvage TL after RT, 20 patients (30.3%) developed a post-operative PCF. These data support the results of the present study regarding the role of prior RT as an important predictor of PCF formation. In the present study, 6 patients out of 8 who developed PCF had diabetes (75%). On the other hand, in group B 6 patients out of 69 (9%) had diabetes. The total number of diabetic patients in this study was (12). Six of them (50 %) develop PCF. Diabetes is one of the well-known intrinsic factors which affect wound healing. Diabetes can decrease or impair growth factor production, angiogenic response, macrophage function, and collagen accumulation, quantity of granulation tissue, and fibroblast migration and proliferation. These factors basically compromise the immune system and lead to circulatory disorders, ischemia and hypoxia of the tissues which predispose to infection and affect wound healing (Harold and Marjana, 2007). 270



Arain et al., 2013 showed that diabetes and post-operative anemia were statistically associated with the development of PCF. The association between diabetes and PCF is not surprising keeping in mind that surgery and anesthesia impair glucose control by aggravating insulin resistance, with the resultant hyperglycemia causing impaired wound healing and leukocyte function leading to increased susceptibility to infections. In the present study, PCF was identified in patients with anemia and hypoalbunemia. 3 patients (38%) of those develop PCF had low albumin and 5 patients (62%) suffered from preoperative anemia were associated with PCF. It has been reported that approximately 35% to 50% of patients with head and neck cancer have clinical malnutrition. In 1993 Moses et al., documented a 28% fistula rate in patients with low hemoglobin level of less than 11.5 gm/dl. Cavalot et al., (2000), showed a nine-fold increase in the risk of fistula in patients who had a hemoglobin level of less than 12.5g/dl postoperatively. Aydogan et al., (2003) stated that, malnutrition and anemia were associated with bad wound healing and poor prognosis in patients undergoing head and neck surgery. The impact of the loco-regional characteristics of tumor (site, stage and differentiation) on the formation of PCF in our work is studied and it appeared to play a role in the development of fistula. In this study, 6 patients in group A out of 8 (75%) were presented with primary supraglottic tumor, while the other 2 patients (25%) were presented with primary glottic tumor. regarding the tumor stage, 2 patients were presented with stage III (25%), while 6 patients were presented with stage IV (75%). This is may be explained by the fact that supraglottic tumours or advanced stage laryngeal tumour require creation of large defect after resection of large part of pharyngeal mucosa leading to closure under tension, these were considered as a risk factor for fistula formation. 271



Virtaniemi et al., 2001 noted that supraglottic tumors had significantly more leak than glottic tumors. They attributed that, tumors in this location are usually advanced and discovered late with frequently spills over the surroundings (aryepiglottic mucosa, piriform fossa, vallecula or the base of tongue). This generally requires resection of large parts of pharyngeal mucosa than glottic lesions. This leads to larger defect and tense closure, which is potential risk for wound break down and development of PCF. On the other hand Arain et al., 2013, found no significant relation between these oncological factors and the formation of PCF in their study. In the present study, management of the PCF, initially, conservative. We found that, most fistulas healed by secondary intention. Surgical intervention was considered if healing is not accomplished after 4 weeks. Additionally, proper tumor selection for RT, avoidance of unnecessary tracheostomy and meticulous surgical techniques will help in prevention of this devastating event

CONCLUSION In conclusion, patients with, preoperative tracheostomy, preoperative RT, anemia, diabetes, hypoalbumineamia and supraglottic tumors are associated with an increased risk of PCF formation. Good control of patient comorbidity factors such as controlling of diabetes, correction of anemia, albumin, are considered the key factor for good wound healing and to prevent this serious complication from occurring In addition, attention to meticulous surgical technique, closure of the neopharynx by Vicryl suture in a Connel’ manner suture (watertight suture line), second layer of closure, adequate use of drains, will decrease the risk of fistula formation The increased awareness towards this catastrophic complication will limit the use of pre-operative tracheostomy, improve the techniques of radiotherapy 272



and push toward establishment of more fine and meticulous methods for the primary repair of the neo-pharynx

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‫‪AAMJ, VOL (12), NO (4), OCT 2014 SUPLL‬‬

‫‪AL-AZHAR ASSIUT MEDICAL JOURNAL‬‬

‫انًهخص انعربي‬ ‫يعدل اإلصببت وعىايم انخطر نالصببت ةاننبسىر انبهعىيي انجهدي بعد االستئصبل انكهي لنحنجرة‬ ‫و حيد عبد انرحًن شًس اندين* ‪ ,‬ابراهيى ابراهيى انسىقي *‪,‬ايًن عبد انعزيز انشهبني*‬ ‫‪ ,‬احًد سهيى** ‪,‬يحًد انصبوي**‬

‫*يذسط االَف ٔ االرٌ ٔ انذُجشح – غت االصْش ثُ‪** ٍٛ‬اسزبر االَف ٔ االرٌ ٔ انذُجشح – غت‬ ‫االصْش ثُ‪ٍٛ‬‬ ‫ــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــــ‬ ‫‪ٚ‬عزجش انُبسٕس انجهعٕي‪ ٙ‬انجهذ٘ يٍ اليعبعفبد الخط‪ٛ‬شح ثعذ جشادخ اال سزئصبل انكه‪ ٙ‬نمدُجشح‪.‬‬ ‫ٔ ‪ٚ‬ؤد٘ دذٔصّ إنٗ ص‪ٚ‬بدح يعذالد عٕدح اإلصبثخ ثبالٔساو ‪ٔ ,‬انزأخش ف‪ ٙ‬انعالط االشعبع‪ ٙ‬انًسبعذ‪ٔ ,‬‬ ‫ص‪ٚ‬بدح يذح االسزشفبء نفزشاد غٕ‪ٚ‬هخ‪ٔ ,‬ثبنزبن‪ٚ ٙ‬ؤد٘ ان‪ ٙ‬ص‪ٚ‬بدح ركهفخ انعالط ‪ .‬كًب لذ ‪ٚ‬ؤد٘ ان‪ ٙ‬انزٓبة‬ ‫يٕظع‪ ٙ‬ف‪ ٙ‬انجشح انز٘ لذ ‪ًٚ‬زذ ان‪ ٙ‬دسجخ فمذ جضء يٍ انجهذ ٔ ركشف انشش‪ٚ‬بٌ انسجبر‪ ٔ ٙ‬سثًب دذٔس‬ ‫َض‪ٚ‬ف شذ‪ٚ‬ذ يُّ ‪ٚ‬ؤد٘ ان‪ ٙ‬انٕفبح‪.‬‬ ‫ٔ ‪ٚ‬ذزبط انزعبيم يع ْزا انًشض ان‪ ٙ‬غش‪ٚ‬مخ ٔاظذخ ٔشبيهخ ف‪ ٙ‬انًعبنجخ ‪ٔ .‬سغى أٌ عذدا يٍ‬ ‫انعٕايم انز‪ ٙ‬رؤد٘ إنٗ دذٔس ْزا انُبسٕسلذ رى ٔصفّا اال اَّ ال ‪ٕٚ‬جذ دزٗ ا‪ ٌٜ‬ارفبق عهٗ انعٕايم‬ ‫األكضش أًْ‪ٛ‬خ‪.‬‬ ‫نزنك‪ ,‬رى رخط‪ٛ‬ػ ْزِ انذساسخ ثٓذف رذذ‪ٚ‬ذ يذٖ اَزشبس انُبسٕس انجهعٕي‪ ٙ‬انجهذ٘ ثعذ جشادخ‬ ‫االسزئصبل انكه‪ ٙ‬نمدُجشح ‪ ٔ,‬كزنك رذذ‪ٚ‬ذ انعٕايم االسبس‪ٛ‬خ انز‪ ٙ‬لذ رؤد٘ ان‪ ٙ‬اإلصبثخ ةْزا انُبسٕس‪ .‬كًب‬ ‫رٓذف انذساسخ ان‪ ٙ‬رذذ‪ٚ‬ذ انًشظٗ رٔ٘ انًخبغشانًشرفعخ ف‪ ٙ‬يذبٔنخ نزجُت ْزِ انًعبعفبد انًذيشح‪.‬‬ ‫ٔلذ رى رنك ثبسزخذاو انزذه‪ٛ‬م االدصبئ‪ ٙ‬للبعذح انج‪ٛ‬بَبد انخبصخ نهفش‪ٚ‬ك انجشاد‪ ٙ‬انز٘ اجش٘ ‪ 77‬جشادخ‬ ‫اسزئصبل كه‪ ٙ‬نمدُجشح ف‪ ٙ‬يسزشف‪ٛ‬بد جبيعخ االصْش ف‪ ٙ‬انفزشح يٍ ‪ ٔ 2011‬دز‪.2014 ٙ‬‬ ‫ٔلذ ٔجذ أٌ ‪ .٪10.3‬يٍ انذبالد انز‪ ٙ‬رًذ دساسزٓب (‪ 8‬يٍ ‪ )77‬دذس نٓب االصبثخ ثبنُبسٕس‬ ‫انجهعٕي‪ ٙ‬انجهذ٘‪ٔ .‬كبٌ يعظى انًشظ‪ ٙ‬انز‪ ٍٚ‬اص‪ٛ‬جٕا ثٓزا انُبسٕس (‪ٚ )٪75‬عبٌَٕ يٍ ٔ سو سشغبَ‪ ٙ‬ف‪ٙ‬‬ ‫انذُجشح ف‪ ٙ‬انًُطمّ يب فٕق االدجبل انصٕر‪ٛ‬خ ‪ ٔ ,‬كبٌ اغهجٓى (‪ )٪75‬ف‪ ٙ‬انًشدهخ انشاثعخ يٍ انًشض ‪.‬‬ ‫ثبإلظبفخ إنٗ رنك‪ ,‬كبَذ ‪6‬يُٓى ‪ٚ‬عبٌَٕ يٍ داء انسكش٘ (‪ 3 ٔ ,)٪75‬يشظٗ يُٓى (‪ )٪38‬نذ‪ٓٚ‬ى‬ ‫اَخفبض انضالل‪ 5 ٔ,‬يشظٗ (‪ٚ )٪62‬عبٌَٕ يٍ فمش انذو لجم انجشادخ‪ 3 ٔ,‬يشظٗ (‪ )٪38‬رهمٕا عالجب‬ ‫اشعبع‪ٛ‬ب لجم انجشادخ ‪ .‬كًب خعع ‪ 5‬يشظٗ (‪ )٪62‬نجشادخ شك انمصجخ انٕٓائ‪ٛ‬خ لجم جشادخ اسزئصبل‬ ‫انذُجشح‪ .‬كًب نٕدظ اٌ ‪ 6‬يشظ‪ ٙ‬يٍ ‪ )٪75( 8‬انز‪ ٍٚ‬اص‪ٛ‬جٕا ثبنُبسٕس رى اجشاء جشادخ اسزئصبل نهعمذ‬ ‫انهًفبٔ‪ٚ‬خ يٍ انشلجخ سٕاء ف‪ ٙ‬جبَت ٔادذ يٍ انشلجخ أ يٍ انجبَج‪ ٍٛ‬يع جشادخ االسزئصبل انكه‪ ٙ‬نهذُجشح‪.‬‬ ‫ٔ ‪ٚ‬زعخ يٍ ْزا انجذش اًْ‪ٛ‬خ ثعط انعٕايم ٔ يذ٘ اسرجبغٓب ثض‪ٚ‬بدح ادزًبل دذٔس ْزِ‬ ‫انًعبعفبد انخط‪ٛ‬شح يضم رعشض انًش‪ٚ‬ط نهعالط االشعبع‪ ٙ‬لجم انجشادخ ٔ اجشاء جشادخ انشك‬ ‫انذُجش٘ لجم انجشادخ ٔٔجٕد انٕسو ف‪ ٙ‬يُطمخ يب فٕق االدجبل انصٕر‪ٛ‬خ ٔ انًشدهخ انز‪ ٙ‬رمذو ف‪ٓٛ‬ب‬ ‫انًش‪ٚ‬ط نهعالط ‪ .‬كًب ‪ٚ‬زعخ اًْ‪ٛ‬خ انس‪ٛ‬طشح عه‪ ٙ‬يشض انسكش٘‪ٔ ,‬رصذ‪ٛ‬خ فمش انذو ٔ َمص انضالل ف‪ٙ‬‬ ‫انشئ‪ٛ‬س‪ ٙ‬نذسٍ انزئبو انجشٔح‪.‬‬ ‫ح‬ ‫و َع يضم ْزِ انًعبعفبد د‪ٛ‬ش آَب يٍ انعٔايم‬

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