Duodeno-Gastric-Esophageal Reflux -- What is Pathologic ? Comparison of Patients with Barrett 's Esophagus and Age-Matched Volunteers Introduction The aim of the study was to analyse pH - and bile-monitoring data in patients with Barrett 's esophagus and in age - and gender-matched controls . Introduction The incidence rates for adenocarcinoma -LRB- AC -RRB- of the esophagus and gastric cardia have risen rapidly in Western industrialized countries .1 Besides nicotine and alcohol abuse , nutritional factors , high body mass index , acidic gastric reflux , and Barrett 's esophagus are believed to be critical factors of carcinogenesis .2 -- 4 Recent studies have shown that the presence of biliary reflux in combination with acidic gastric reflux damages the esophageal mucosa and causes complications of gastro-esophageal reflux disease -LRB- GERD -RRB- , e.g. , development of Barrett 's mucosa -LRB- BM -RRB- .5,6 Duodeno-gastric reflux into the esophagus -LRB- DGER -RRB- , in particular , appears to be important to the pathogenesis of Barrett 's esophagus .7 Prolonged esophageal aspiration studies have documented increased bile acids in patients with severe esophagitis and Barrett 's esophagus .8 Eighty percent of patients with Barrett 's esophagus on proton-pump inhibitors show a normal esophageal pH profile , but 60 % show abnormal esophageal exposure to bile as measured by Bilitec 2000.9 In the past , direct and prolonged quantification of duodenoesophageal reflux has been difficult to achieve . Now , bilirubin concentration can be directly measured by spectrophotometry , based on the specific absorption at a wavelength of 453 nm . Biliary reflux can be measured with a transnasally passed , ambulatory fiberoptic probe -LRB- Bilitec 2000 -RRB- , which records bile absorption . A number of papers have already been published on the exposure of the esophagus10 -- 13 and stomach14 -- 16 using this technique . However , in these studies , the control patients were between 25 and 35 years old . In clinical practice , patients with Barrett 's mucosa tend to be older . In addition , the authors of each study used varying reference values to measure biliary reflux in the esophagus , making comparison of the measured values difficult . The aim of the present study was to analyze data of pH and bile monitoring in a collective of healthy age - and gender-matched controls and patients with Barrett 's esophagus . Subjects and Methods Subjects Selection of controls was carried out according to a strict protocol . Healthy volunteers treated from 1999 to 2000 between the ages of 40 and 60 years were included in the study . None of the controls were on acid suppressing or gut motility medications , had a history of upper gastrointestinal disease , had undergone upper or major abdominal surgery , or had had therapeutic endoscopic procedures of the upper gastrointestinal tract . Diagnostic endoscopy and barium swallows were not performed , but gallstone disease was excluded by ultrasound scan . From 1999 to 2002 , 24 patients with histologically confirmed Barrett 's mucosa were included in the study . For additional comparison , we include a group of patients with esophagitis -LRB- stage I to III according Savary and Miller -RRB- without Barrett 's esophagus , which had the same diagnostic procedures before planned laparoscopic fundoplication . During the aforementioned time span , 21 patients age older than 40 years were available for this study . Exclusion criteria were history of esophageal , gastric , or biliary surgery , history of abdominal or thoracic radiotherapy , or presence of peptic ulcer disease , active gastrointestinal bleeding , esophageal or fundic varices , esophageal or upper small intestine chronic disease , or neoplastic disease . All drugs potentially affecting gastrointestinal motility and secretion were discontinued at least 1 week before the study . Upper Gastrointestinal Endoscopy All patients underwent classical upper gastrointestinal endoscopy . If sedation was necessary , intravenous administration of propofol -LRB- up to 200 mg -RRB- was normally used , or occasionally , midazolam -LRB- up to 5 mg -RRB- was used . During endoscopy , the presence and extent of esophagitis , Barrett 's esophagus , and hiatal hernia was noted . Biopsies were taken from the Barrett 's mucosa . Ambulatory Esophageal/Gastric pH and Bile Monitoring All groups underwent esophageal manometry and 24-h pH and simultaneous bile monitoring using a standardized protocol . Ambulatory pH monitoring was performed using a transnasally inserted antimony pH electrode with a separate skin reference electrode -LRB- Synetics Medical , Stockholm , Sweden -RRB- . The data were stored on a portable digital recorder -LRB- Digitrapper MkIII , Synectics Medical Stockholm , Sweden -RRB- . Before each study , the pH probe was calibrated in buffer solutions of pH 7 and 1 . An episode of acid reflux was defined as a decrease in esophageal pH to less than 4 for more than 10 s. To quantify duodeno-esophageal reflux , a transnasally passed , ambulatory fiberoptic spectrophotometer -LRB- Bilitec 2000 , Synectics , Sweden -RRB- was used . The system consists of a miniaturized probe of 1.5-mm diameter that carries light signals into the esophagus and back via a plastic fiberoptic bundle . Before each study , the probe was calibrated in water . Corresponding to the current literature , a bilirubin absorption > 0.25 was used as a reference for noxious biliary reflux .14 The bile and pH probes were taped together and passed transnasally into the esophagus and stomach , as described in detail elsewhere .17 The upper tips of the probes were positioned 5 cm above the upper border of the lower esophageal sphincter as defined by esophageal manometry . The distal pH electrode and fiberoptic sensor were placed in the fundus of the stomach , 10 cm distal to the lower esophageal sphincter -LRB- Fig. 1 -RRB- . Controls and patients were asked to follow a strict protocol of three meals per day , with no liquids between meals . Recumbent phases of recording were permitted only at night . Patients were asked to keep a diary recording of the exact nature of meals , the supine and erect phases of measurement , and the sensations of heartburn and regurgitation . Figure 1Position of the pH - and bilirubin-probes in the stomach and in the esophagus . -LRB- UES = upper esophageal sphincter ; LES = lower esophageal sphincter -RRB- . The simultaneous biliary and pH monitoring was done with administration of a colorless `` white diet '' -LRB- WD -RRB- including liquid and solid foods with a maximum in vitro bile absorbance of 0.25 -LSB- absorbance scale ranging from 0 -LRB- plain water -RRB- to 1 -LRB- total screen -RRB- -RSB- . The meals included water , milk , toast , potatoes , chicken , dry biscuits , and fish . Data Acquisition and Interpretation After completion of the measurements , probes were withdrawn from the patients , and data were stored via interface on an IBM-compatible computer equipped with Polygram ® software -LRB- Medtronic -RRB- . The data of each second of the 24-h measurements were used for analysis . To assess the presence of gastric or esophageal biliary reflux , the percentage of time when absorbance was greater than 0.25 was calculated for the following periods : total supine , upright , and postprandial . The postprandial period was defined as 2 h after the end of meals . The percentage of time with esophageal pH lower than 4 and median gastric pH and the percentage of time with gastric pH measuring 1 , 2 , 3 -- 7 , and > 7 was also calculated for the above periods . The mean duration of the ambulatory pH and Bilitec monitoring study was 22 h , 40 min in patients and 23 h , 44 min in the controls . Statistical Analysis The SPSS -LRB- version 11.0 , Chicago , Illinois -RRB- program was used to analyze the results . For graphical presentation , we used the program MedCalc for Windows , -LRB- Version 9.0 , MedCalc Software , Belgium -RRB- . Median , interquartile range -LRB- IQR or 25th to 75th percentile -RRB- values were established . The nonparametric tests -LRB- Mann -- Whitney and Kruskal -- Wallis analysis -RRB- were used to assess the relationship between variables . Box and Whisker plots were used to present some of the data . In these plots , the box represents the IQR , and the Whiskers represent the highest and lowest values . Outliers are also plotted , defined as more than 1.5 times the IQR from the 75th centile . Extreme values were defined as more than three times the IQR from the 75th centile . A receiver operator characteristic -LRB- ROC -RRB- curve was used to find a cutoff value for optimal sensitivity and specificity according Zweig and Campbell .18 The area under the curve -LRB- AUC -RRB- as a measurement of diagnostic performance of the test was used . The results are given as point with the 95 % confidence interval -LRB- 95 % CI -RRB- and graphically for presentation of all data . As the positive group , we used the patients with Barrett 's mucosa , and the negative test group was defined by the healthy volunteers . A nonparametric distribution of the area under the curve was assumpted . The assumptions for calculation of the required sample size were alpha = 0.05 , beta = 0.80 , and that a test is only valid for daily use if less than 20 % of the healthy controls and at least 80 % of the patients have positive test results . The calculated sample size for each group was 20 . Ethics The study protocol was approved by the ethics committee of the University of Cologne . Each subject gave written informed consent . Results Twenty-four patients with Barrett 's esophagus -LRB- mean age : 58 years -RRB- , 21 patients with esophagitis -LRB- mean age : 57 years -RRB- , and 19 healthy controls with a mean age of 51 years were included in the study . Patients with BM showed esophagitis grade 0 -LRB- 4 cases -RRB- , grade I -LRB- 12 cases -RRB- , and grade II -LRB- 8 cases -RRB- . The control group of patients with esophagitis showed nine cases with grade I , eight cases with grade II , and three cases with grade III . Demographics of patients and volunteers are displayed in Table 1 -LRB- the data of one volunteer was not usable due to technical problems -RRB- . Table 1Demographic Data of Patients with Barrett-Mucosa or Esophagitis and Healthy VolunteersParametersPatients with Barrett 's Esophagus -LRB- n = 24 -RRB- Patients with Esophagitis -LRB- n = 21 -RRB- Controls -LRB- n = 19 -RRB- Significance Pat . with Barrett vs ControlsAge -LRB- median -RRB- 57 years58 years51 years -- Min -- max29 -- 75 years42 -- 77 years39 -- 62 yearsGender m : f16 : 811:1011:8 n.s.BMI -LRB- median -RRB- min -- max27 .0 kg/m2 -LRB- 18.6 -- 33.1 -RRB- 26.9 kg/m2 -LRB- 17.9 -- 31.5 -RRB- 24.1 kg/m2 -LRB- 19.62 -- 27.34 -RRB- p = 0.003 Smokers -LRB- % -RRB- n = 5 -LRB- 20.8 -RRB- n = 4 -LRB- 19.0 -RRB- n = 6 -LRB- 31.6 -RRB- n.s.No alcohol % n = 3 -LRB- 12.5 -RRB- n = 5 -LRB- 23.8 -RRB- n = 5 -LRB- 26.3 -RRB- n.s.BMI Body mass index Acidic Gastric Reflux -LRB- AGR -RRB- Patients with Barrett 's esophagus , 19 of 24 -LRB- 79 % -RRB- and 20 of 21 control patients with esophagitis -LRB- 95 % -RRB- had pathologic AGR -LSB- pH < 4 in > 5 % of total measuring time -LRB- TMT -RRB- -RSB- , but also 6 of the 19 healthy controls -LRB- 32 % -RRB- showed pathologic AGR without any symptoms -LRB- p = 0.002 -RRB- . During the TMT , the median AGR was 10.6 % for Barrett patients and 3.2 % for controls -LRB- p < 0.01 -RRB- . In particular , measurements of long acid reflux -LRB- LAR -RRB- , defined as reflux pH < 4 lasting longer than 5 min , showed significant differences between patients and controls . Pathologic AGR was found in patients during both the supine and upright fasting measuring periods . In contrast , pathologic AGR in healthy controls occurred only in the upright position -LRB- Table 2 -RRB- . Table 2Median of Acidic Gastric Reflux into the Esophagus in Patients with BM or with Esophagitis and in Healthy ControlsParametersPatients with Barrett 's Esophagus -LRB- n = 24 -RRB- -LSB- median -LRB- LQ-UQ -RRB- -RSB- Patients with Esophagitis -LRB- n = 21 -RRB- -LSB- median -LRB- LQ-UQ -RRB- -RSB- Controls -LRB- n = 19 -RRB- -LSB- median -LRB- LQ-UQ -RRB- -RSB- Significance Pat . with Barrett vs ControlsPercentage of total measuring time pH < 4 -LRB- % -RRB- 10.6 -LRB- 6.2 -- 38.3 -RRB- 19.9 -LRB- 1.6 -- 71.7 -RRB- 3.2 -LRB- 0.9 -- 5.5 -RRB- p = 0.01 Percentage of upright measuring time pH < 4 -LRB- % -RRB- 11.7 -LRB- 6.03 -- 6.4 -RRB- 18.9 -LRB- 8.7 -- 60.8 -RRB- 2.4 -LRB- 0.9 -- 6.1 -RRB- p < 0.05 Percentage of supine measuring time pH < 4 -LRB- % -RRB- 10.9 -LRB- 0.4 -- 27.1 -RRB- 6.3 -LRB- 0.0 -- 13.3 -RRB- 0.3 -LRB- 0.0 -- 4.2 -RRB- p = 0.004 LQ Lower quartile , UQ upper quartile 24-h Intragastric pH and Bile Monitoring Gastric pH monitoring showed no significant differences between patients and controls for all measuring periods -LRB- Table 3 -RRB- . Gastric bilirubin exposure , indicating biliary reflux , was significantly more frequent in patients than in controls during all measuring periods -LRB- Table 3 -RRB- . Biliary exposure in the supine position typically occurred during the early hours of the morning during sleep , represented by increased absorbance over 2 -- 3 h , with a rapid return to baseline values around the time the subject resumed the upright position . Over the same time period , gastric pH monitoring showed increased pH levels to greater than 2 -LRB- Fig. 2 -RRB- . Table 3Results of 24-H Intragastric pH and Bile Monitoring in Patients with Barrett Esophagus and Healthy ControlsParametersPatients -LRB- n = 24 -RRB- -LSB- Median -LRB- LQ -- UQ -RRB- -RSB- Controls -LRB- n = 19 -RRB- -LSB- Median -LRB- LQ -- UQ -RRB- -RSB- SignificanceMedian of intragastric pH during TMT1 .3 -LRB- 1.0 -- 1.4 -RRB- 1.4 -LRB- 1.1 -- 1.7 -RRB- n.s.Bilirubin exposure percentage -LRB- % -RRB- of TMT 7.8 -LRB- 1.6 -- 17.8 -RRB- 0.0 -LRB- 0.0 -- 1.0 -RRB- p = 0.001 Bilirubin exposure percentage -LRB- % -RRB- of upright time6 .9 -LRB- 0.1 -- 12.9 -RRB- 0.0 -LRB- 0.0 -- 1.3 -RRB- p < 0.01 Bilirubin exposure percentage -LRB- % -RRB- of supine time2 .0 -LRB- 0.0 -- 28.6 -RRB- 0.0 -LRB- 0.0 -- 0.0 -RRB- p = 0.001 LQ Lower quartile , UQ upper quartile , TMT total measuring timeFigure 224h intragastric pH - and bile monitoring in a patient with Barrett 's esophagus demonstrating the duodenogastric reflux in the early morning . a. Bilitec ® - monitoring , b. pH-monitoring . Bilirubin Exposure of the Esophagus Over the TMT , the median of esophageal biliary reflux was 7.8 % for patients with Barrett 's esophagus -LRB- LQ -- UQ = 1.6 -- 17.8 % -RRB- and 3.5 -LRB- LQ -- UQ = 0.1 -- 13.5 -RRB- for control patients , in contrast to 0 % for the controls -LRB- LQ -- UQ = 0 -- 1.0 % -RRB- , p = 0.001 -RRB- . Figure 3 shows that esophageal bile monitoring in patients with Barrett 's esophagus and healthy controls varied during the total measuring and supine periods . Figure 3Results of the esophageal bile-monitoring in 24 patients with Barrett 's esophagus , 21 patients with esophagitis and 19 healthy controls a -RRB- total measuring period -LRB- Kruskal-Wallis Test = 0.01 -RRB- b -RRB- supine period -LRB- Kruskal-Wallis Test p = 0.01 -RRB- . The receiver operating curve , plotting the true positive rate -LRB- patients with Barrett 's esophagus identified by bilirubin exposure -RRB- in function of the false positive rate -LRB- healthy controls with high bilirubin exposure -RRB- is shown in Fig. 4 . With an area under the curve of 0.78 -LRB- 95 % CI = 0.56 -- 0.89 -RRB- , the ROC analysis of biliary monitoring showed the optimal value for patients at 1 % of the TMT -LSB- 75 % sensitivity -LRB- 95 % CI = 53 -- 90 % -RRB- , 84 % specificity -LRB- 95 % CI = 60 -- 96 % -RRB- -RSB- . Therefore , the cutoff value to distinguish normal vs pathologic biliary reflux using 24-h biliary monitoring in the esophagus -LRB- absorbance threshold > 0.25 -RRB- should be fixed at 1 % of TMT . Figure 4ROC-curve with 95 % confidence intervals for pathologic bile-monitoring in patients with Barrett esophagus compared to age and sex matched healthy controls . Barrett patients , 18 of 24 -LRB- 75 % -RRB- , 15 of 21 control patients with esophagitis -LRB- 71 % -RRB- , and 3 of 19 controls -LRB- 16 % -RRB- showed biliry reflux into the esophagus more than 1.1 % of the TMT -LRB- p < 0.001 -RRB- . Using this cutoff value , none of the controls , 10 of the control patients -LRB- 48 % -RRB- , and 11 of 24 Barrett 's patients -LRB- 46 % -RRB- had pathologic bilirubin exposure during sleep . Discussion The results of our study confirm that patients with Barrett 's esophagus have significantly more frequent duodenogastric reflux into the esophagus than age - and sex-matched healthy controls . In addition , this reflux , measured by acid and bilirubin exposure , remains longer in the esophagus , especially during sleep . The role of acid and nonacid reflux into the esophagus as a causative factor of symptoms and mucosal lesions has been addressed in a number of studies . Not only the duration , but possibly the composition of the reflux , is instrumental in the development of such lesions .13 Twenty-four-hour intragastric bile monitoring has provided the clinician with unequivocal evidence of excessive duodenogastric reflux -LRB- DGR -RRB- in 41 % of patients with endoscopic esophagitis , gastroesophageal reflux -LRB- GER -RRB- symptoms , and gastric symptoms suggestive of DGR .19 Reflux of duodenal contents into the stomach , especially postprandially , is a physiological event ; 20 however , biliary reflux is a large contributor to mucosal lesions in the whole stomach .21 In our study , the control group of patients with different grades of esophagitis showed no significantly different measurements of acidic or bile reflux into the stomach or the esophagus compared to Barrett 's patients . This may be caused by selection of patients with esophagitis , which were candidates for fundoplication , but both groups of patients differed significantly compared to healthy controls . Therefore , our results are of great clinical relevance especially for preoperative diagnostic . Marshall et al. compared healthy controls to patients with different grades of reflux-esophagitis and Barrett 's esophagus with regard to bile measurements in the stomach .22 In this study , the average age of the control patients was 25 years , and that of the patients in Groups I , II , and III was 42 , 50 , and 60 years , respectively . The bilitec-probe was positioned 10 cm below the lower esophageal sphincter -LRB- LES -RRB- . The threshold of bilirubin absorbance was 0.14 , and although no difference was found between groups over the TMT , gastric bilirubin exposure was higher in the supine than in the upright position . In the current study , the control group was older than that of the Marshall study . More duodeno-gastric reflux was recorded in both study and control patients during all periods of measurement . These findings may be due to improved study conditions . We used an esophageal threshold of 0.25 for bilirubin absorbance . Fein et al. ,14 in an in vitro study of absorption of different white meals , showed that the least food interference during bile monitoring was measured with an absorbance > 0.25 . Tack et al. reported the influence of meal consistency on Bilitec measurement results in healthy subjects .23 They compared two groups of young controls . The subjects took either liquid meals only , not absorbing light of the same wavelength as bilirubin , or solid food , avoiding diets that interfere with bilirubin absorbance . The authors found significant differences between the two groups using a bilirubin absorbance threshold > 0.14 with a median percentage -LRB- interquartile range -RRB- over the TMT of 10.9 % -LRB- 6.7 -- 19.3 -RRB- for solid meals and 0.3 % -LRB- 0.0 -- 2.8 -RRB- for liquid meals . Major meal artifacts were present in two-solid-meal -LRB- 10 % -RRB- and no-liquid-meal subjects . In our study , we found such a meal artifact in one patient and one control , but the values of bilirubin absorbance were lower than 0.25 , and therefore , not relevant to our results . It is not unusual for gastro-esophageal reflux to contain bile , duodenal , and pancreatic secretions . Utilization of the Bilitec spectrophotometric probe has demonstrated a higher prevalence of abnormal esophageal bilirubin exposure in patients with Barrett 's metaplasia when compared to those with erosive injury or without signs of esophagitis .6,8,10,13 In those studies , patients were consistently older than volunteers included in the control group . However , other studies have shown an increased prevalence of gastroesophageal reflux with age .24 For these reasons , we studied age and sex matched healthy controls and patients with Barrett 's esophagus or with esophagitis . We found pathologic acid and biliary reflux of the esophagus in one-third of the controls . Perhaps , this may be caused by artefacts or by violation of the protocol by the volunteers . But in a previous published study , we could show that younger healthy controls had no such pathologic reflux .17 Possibly , these phenomena are caused by relaxations which occur more often in older people . In contrast , nearly all patients with Barrett 's esophagus -LRB- 87 % -RRB- and all patients with esophagitis -LRB- 100 % -RRB- showed pathologic acidic reflux and/or bile reflux measured with combined pH and bile monitoring . Bile reflux into the esophagus during sleep , in particular , was only found in patients with BM or with esophagitis . In our study , we measured the intragastric pH and the bile reflux from the duodenum into the stomach -LRB- DGR -RRB- . The median of the intragastric pH was similar in both groups . But patients with Barrett 's esophagus had significantly longer duodenogastric reflux during the 24-h measuring period than controls . More DGR was demonstrated at night than during the day in both groups of study patients and in healthy controls . This could be associated with an alkaline shift in the pH , according to previously published studies .25 -- 27 The precise mechanism by which nocturnal DGR occurs and the roles posture plays remain unclear . Bowrey et al. were unable to establish either gastro-esophageal or duodenogastric reflux as the predominant cause of inflammation in gastric cardiac mucosa with use of the Bilitec 2000 device .16 This is understandable , as the amount of reflux into the stomach -LRB- DGR -RRB- does not necessarily correlate with DGER into the esophagus . In this study , the authors demonstrated more DGR in females during the supine period , while males presented more DGER . At the same time , there was no correlation between bile levels in the stomach and esophagus . The controls were , however , much younger than the patients . We found significant differences in bile measurements of the stomach and esophagus between BM patients and controls . In contrast to Bowrey et al. , we saw more DGER in females during the supine period and more DGR in male patients . In contrast , Banki reported similar esophageal exposure to refluxed acid and bilirubin in females and in males with Barrett 's mucosa .28 Pfaffenbach et al. 29 studied esophageal bile and acid reflux in patients with long segment Barrett 's esophagus -LRB- LSBE -RRB- , short segment Barrett 's esophagus -LRB- SSBE -RRB- and patients with gastro-esophageal reflux disease -LRB- GERD -RRB- . Subjects underwent esophageal manometry and simultaneous 24-h pH and bile monitoring -LRB- Bilitec 2000 -RRB- with an absorbance value > 0.2 for 10.9 % of the total period . GER did not differ between the groups . However , DGER differed between patients with LSBE -LRB- 14.7 % -RRB- , SSBE -LRB- 2.1 % -RRB- , and GERD -LRB- 2.1 % -RRB- . In summary , the analysis of reference values of esophageal acid and bile-reflux measurements in a collective of healthy , age - and gender-matched controls compared to patients with BM led to the following conclusions : Although about 30 % of the healthy controls showed acid reflux in pH monitoring , patients with BM had significantly more acid reflux during all measured periods.Healthy controls did not have relevant duodeno-gastric-esophageal reflux measured by bilirubin absorbance . Especially during the supine period , there was no bile reflux.The optimal threshold for pathological bile reflux is 1.1 % -LRB- bile monitoring with an absorbance of 0.25 -RRB- .

O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O B I O O O O O O O O B I O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O B O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O

bile reflux
acid reflux
esophagus
spectrophotometry

reference value bilitec
barrett’s mucosa


Adolescents Searching for Health Information on the Internet : An Observational Study Background Adolescents ' access to health information on the Internet is partly a function of their ability to search for and find answers to their health-related questions . Adolescents may have unique health and computer literacy needs . Although many surveys , interviews , and focus groups have been utilized to understand the information-seeking and information-retrieval behavior of adolescents looking for health information online , we were unable to locate observations of individual adolescents that have been conducted in this context . Introduction The Internet has become an important tool for many people with health concerns -LSB- 1,2 -RSB- , especially for adolescents -LSB- 3,4 -RSB- . Concerns about confidentiality , coupled with the fact that many teenagers find accessing care through traditional providers difficult -LSB- 5 -RSB- , make access to information via the Internet particularly important . Given rapidly-expanding Internet access among young people , it is not surprising , then , that more than 70 % of 15 to 17 year-olds say they have used the Internet to look up health information -LRB- written communication , 2001 Dec ; Generation RX.com Survey printouts ; V. Rideout , Henry J. Kaiser Foundation , Menlo Park , CA -RRB- . This percentage is likely to increase if Internet access from home continues to rise as it has in recent years -LSB- 6 -RSB- . Because of the enormous amount of unstructured online content , it is crucial to understand how youth navigate through the Web to find health information . Prior research , primarily from library and information science literature and education literature , has highlighted several search characteristics that are either unique or more pronounced in adolescents . For example , adolescents take more time to complete online tasks than college students -LSB- 7 -RSB- , search less systematically -LSB- 7 - 10 -RSB- , have difficulty formulating search queries due to misspelling and problems with the level of specificity -LSB- 8 - 11 -RSB- , utilize less-advanced search syntax -LSB- 7 -RSB- , and rarely consider the source of Web pages -LSB- 8,9 -RSB- . While informative , this literature is based primarily on adolescents searching for answers to homework questions rather than health information . Searching for online health information involves distinctive challenges including unfamiliar terminology -LSB- 12 -RSB- ; encounters with pornography-blocking software -LRB- written communication , 2001 Dec ; Generation RX.com Survey printouts ; V. Rideout , Henry J. Kaiser Foundation , Menlo Park , CA -RRB- , -LSB- 13 -RSB- ; and the importance and difficulty of determining health information quality -LSB- 14 -RSB- . However , despite the need for research that details the online search behavior of health consumers , the authors were only able to locate a few articles in which health science researchers actually observed , recorded , and analyzed consumers of any age searching for health information -LSB- 14 - 16 -RSB- . Instead , surveys -LRB- eg , written communication , 2001 Dec ; Generation RX.com Survey printouts ; V. Rideout , Henry J. Kaiser Foundation , Menlo Park , CA ; and -LSB- 1,2,4 -RSB- -RRB- have been the predominant method used to understand health consumers ' online searching behavior , despite problems with participant recall and the inability of surveys to capture specific search tactics . In addition , the authors found a handful of studies in the medical informatics literature that have also looked at log data from particular medical Web sites , but these studies are also limited in scope since they do not observe the actual searcher or see the broader context in which the searcher is acting -LSB- 17 -RSB- -LRB- see also -LSB- 18 -RSB- for similar studies performed on search engine data -RRB- . The value of directly observing users was demonstrated in the Eysenbach study , which revealed that adults said they paid attention to the source of health sites during interviews , although this behavior was not found during the actual observations -LSB- 15 -RSB- . Observational research specific to the adolescent age group and online search behavior for health information is also sparse . There have been some good surveys that answer many useful questions concerning why adolescents go to the Internet , what they search for , if they find it , and what they do with it -LRB- written communication , 2001 Dec ; Generation RX.com Survey printouts ; V. Rideout , Henry J. Kaiser Foundation , Menlo Park , CA ; and -LSB- 4,19 -RSB- -RRB- . The only observational study we were able to locate conducted 27 focus groups where groups of adolescents searched online for health information as they discussed their own experiences -LSB- 14 -RSB- . Many of the findings concerning adolescent search behavior found in the library and information science literature were confirmed and additional issues were raised , including concerns about low health literacy and trouble judging the quality of information , that may be more pronounced in adolescents than adults . However , that study only begins to paint a picture of adolescent search behavior for online health information , because the searches were performed in a group setting and the success , failure , and specific search tactics used were not coded or analyzed . The study reported here provides a more in-depth understanding of how adolescents search for health information using the Internet and what implications this may have on access to health information . To capture enough detail , the study recorded specific actions taken by adolescents which were later coded and analyzed . Participants were encouraged to share their thought process out loud as they searched for answers to a list of predetermined health questions . The result was a rich set of both quantitative and qualitative data that was thoroughly analyzed for common themes and events . Specific questions of interest include , but are not limited to : What are the various search strategies used ? What factors contribute to finding correct and useful answers ? When using a search engine , how many results pages are viewed and utilized ? What types of search strings are entered into search engines ? Answers to these and related questions should be of interest to a number of parties including educators -LRB- eg , health educators , librarians , teachers -RRB- , Web site and search engine designers , health care practitioners , and researchers -LRB- eg , to create a sample of URLs by simulating online searching behavior -LSB- 20 -RSB- -RRB- . Methods Sample Twelve students from 1 middle school -LRB- N = 4 -RRB- and 2 high schools -LRB- N = 4 and N = 4 -RRB- in southeast Michigan were recruited for this study . Staff at each school were asked to select 4 students who were -LRB- a -RRB- comfortable using computers , -LRB- b -RRB- comfortable searching for information on the Internet , and -LRB- c -RRB- strong students who could afford to miss one class period . Students received a University of Michigan T-shirt , valued at roughly $ 8 , in return for their participation . The parent or guardian of every student signed an informed consent document that described the purpose and procedure of the study . Students also signed separate assent forms with similar information . The University of Michigan Behavioral Science Institutional Review Board approved this study and the consent and assent documents . Data Collection Three methods of data collection were used . First , one of the two members of the research team present during each of the observations coded searching behavior in real time while the second member of the research team interacted with the student . Second , TechSmith Camtasia 3.0.1 commercial tracking software -LSB- 21 -RSB- was installed on the computer . This software captured the students ' voices and took pictures of the screen -LRB- screen captures -RRB- twice per second during the entire session . Finally , a video camera was positioned to capture the screen and the students ' voices , but not the students ' images . Observations coded in real time were used to develop a more detailed and systematic coding system for use when reviewing the tracking software records . It is data from the tracking software coding that is reported here . All observations of adolescents were conducted during January 2002 . Each school provided a room in which to conduct the observations . Students were brought to the observation room one at a time . Two researchers were present at every observation . For each student , one of the researchers first reviewed the assent form to introduce the project and obtain the student 's permission to participate . The students were then asked 14 questions about demographics -LRB- age , race/ethnicity , and gender -RRB- and their prior computer use -LRB- eg , how often they use computers or the Internet , what health topics they have searched , which search engines they used , and whether they have a computer and access to the Internet at home -RRB- . Once the brief interview had been completed , the observed searches began . To help the students understand the procedure and to reinforce the importance of thinking out loud while doing their searches , each student was first asked to do an easy non-health-related search looking for the next day 's local weather forecast . As with the subsequent health-related searches , the local-weather question was first read to the student by a researcher and then a card with the question on it was set next to the computer in case the student needed to read it . As part of the think-aloud protocol , the experimenter asked the student to talk out loud about what they were doing , so that researchers could better understand the reasons behind the searching behavior . If a student stopped talking during the search , he or she was reminded by the observers to `` keep talking , '' but the experimenters did not ask students to elaborate on any specific thing they said . Concurrent verbal reports more accurately reflect a subject 's mental state at the time of observed behaviors than do retrospective reflections , and this minimal think-aloud protocol has been shown to slow subjects down , but not to qualitatively change their problem solving behavior -LSB- 22 -RSB- . After the students completed the practice local-weather search , they were given a sequence of up to 6 predetermined health information questions -LRB- see Table 1 -RRB- , 1 at a time . Questions were framed in a way that took into consideration the broader information concern that the question attempted to resolve . To eliminate confounding by learning effects between searches , we used a 6 x 6 Latin square to determine the order in which the questions were presented to the participants . The computer that students used was provided by the researchers , but connected to the school 's network so that the students were protected from controversial or pornographic material by the same blocking or filtering software used by the school . The 3 different schools used 3 different filtering systems . Each observation session lasted one class period . No time limit was given for each question , but when the class period ended , any ongoing search was terminated and any remaining questions were skipped . Table 1 Health-related questions Your aunt was just told she has diabetes . She is n't sure what kinds of food she can or ca n't eat . Using the Internet , find some information for your aunt about what foods she should or should not eat . A friend recently started taking a drug called Paxil for depression . He seems to be tired all the time , and even falls asleep in class . Use the Internet to find out if the drug might be making him sleepy . Your older brother has a problem with drinking too much alcohol . He wants to go to a local Alcoholics Anonymous meeting . Use the Internet to help him find a local meeting . You want to get an HIV test , but you do n't want anyone to know . You also do n't have any money to pay for it . Use the Internet to find a place to get a free and confidential HIV test . For class , you need to learn about medicine that can help people stop smoking . Using the Internet , find the names of these medicines . You are about to get a tattoo , but a friend warned you that some places spread infections like HIV and hepatitis . Use the Internet to find out if this is true . Topics for the health-related questions were chosen based upon responses to a survey of adolescents conducted by the Kaiser Family Foundation -LRB- written communication , 2001 Dec ; Generation RX.com Survey printouts ; V. Rideout , Henry J. Kaiser Foundation , Menlo Park , CA -RRB- . Certain topics including homosexuality , teen pregnancy , and abortion were purposefully avoided so as not to expose participants to overly-controversial information . Data Analysis After all the observations were completed , 3 researchers including a physician , health educator , and human-computer interface specialist met as a group to review the real-time coding results and to clarify or augment the coding scheme before the definitive final coding of the tracking-software records . The final coding scheme was designed to record data on the person searching , the question being asked , the time it took to find an answer , the search strategy utilized -LRB- eg , utilize search engine or directly type in URL -RRB- ; search strings used ; number of search engine results pages reviewed ; number of pages viewed within a particular site ; and the use of menus , advertisements , and directories . One of the 3 coders was assigned as a primary reviewer for each of the observation sessions . The assigned primary reviewer was responsible for a detailed coding of the observation session and any coding problems were resolved in a second group discussion . The reviewers classified each of the answers found by the students as correct or incorrect , complete or incomplete , and , for location questions only , useful or not useful . To avoid being overly narrow in our classification of correct for the more open-ended questions such as the question on healthy foods for a person with diabetes , we used the following general rule for classification : to be considered correct , the content of the answer had to be the kind of information that might be discussed in a medical school or school of public health . This classification system was validated in previously-published work by the research team and resulted in a high inter-rater reliability -LRB- κ = 0.84 -RRB- -LSB- 13 -RSB- . The more-specific questions such as the question asking about a location for an Alcoholics Anonymous meeting were considered correct if the student found a Web page listing a meeting location and time or contact phone number . Answers were complete if the students were able to answer all parts of the question . For example , if the student found a discussion about HIV transmission by tattoo parlors , but did not find an answer about hepatitis it was classified as incomplete . Useful answers pertained to location questions . An Alcoholics Anonymous meeting in another state was not useful . A summary measure classifying each search as successful , partially successful , or unsuccessful was computed using the correct , complete , and useful ratings . To obtain a rating of successful , the answer had to be complete , correct , and useful . If the student gave up before finding an answer , the search was classified as unsuccessful . Results Twelve middle school students and high school students in southeast Michigan participated . Students ranged in age from 12 to 17 years old , with a mean of 14 years . Half of the students were female . Of the 12 students , 7 were white , 2 were African American , 1 was Indian American , 1 was Hispanic , and 1 was Asian American . Of the 12 students , only the 6 oldest students had searched for health information on the Internet before . The variation by age is consistent with other findings that youth age 15 to 17 years are significantly more likely to have looked up health information -LRB- 32 % -RRB- than youth age 12 to 14 years -LRB- 18 % -RRB- -LSB- 23 -RSB- . All of the students , however , had computers and access to the Internet at home . Students reported using a computer from 1 hour per week to 3 hours per day , with a mean of 12.3 hours per week . Eleven students attempted all 6 searches , while the remaining student attempted 3 , for a total of 69 searches . One search was not included since the Internet connection was not working properly , making a total of 68 searches that were analyzed . Searches took an average of 5 minutes and 41 seconds , ranging from just under a minute to nearly 24 minutes . This time frame is essentially the same as Eysenbach recorded for adults -LSB- 15 -RSB- . Although direct comparison is inappropriate since different questions were asked , the similar order of magnitude is suggestive . Overall Search Strategy As students thought aloud , the researchers got a sense of what students were looking at on each page . Students seemed to skip around a lot , and did n't skim results pages or specific Web sites in any methodical or thorough ways , sometimes missing links or text that contained the answer to questions . This is also consistent with findings from non-health-related searching behavior as summarized in Hsieh-Yee -LSB- 24 -RSB- . Table 2 Distribution of pages viewed per site Pages Viewed Per Site Sites n % Cumulative % 1 143 70.4 70.4 2 27 13.3 83.7 3 11 5.4 89.2 4 8 3.9 93.1 5 8 3.9 97.0 6 2 1.0 98.0 8 1 0.5 98.5 9 1 0.5 99.0 15 2 1.0 100.0 Total 203 100 Students used multiple methods to locate Web sites that they believed contained answers to the 68 questions . In 60 cases , the student started looking for an answer by visiting a search engine and entering in a search term or phrase . In 2 cases , the student started by selecting from directory menus -LRB- eg , choosing the topic health -RRB- . In 6 cases , the student started by entering a URL -LRB- other than a search engine -RRB- directly into the browser address bar . In total , there were 215 attempts to access non-search-engine or directory Web sites . Nearly all of these attempts were made by following a link from a search engine either after a search or through the use of a directory . Of the 215 attempted site visits , 4 were broken links , 3 were blocked by the filters utilized at certain schools , and 5 were PDF files -LRB- read by Acrobat Reader -RRB- which students either could not download or chose not to download because downloading was too slow . This left 203 sites that were viewed with an average of 1.8 pages viewed per site . The distribution of pages visited per site is shown in Table 2 . Note that the distribution is roughly consistent with a power law as observed in previous studies -LSB- 25 -RSB- . At a reviewer 's request , this data was looked at on an individual student level . Students varied a great deal in the total number of visited sites . Eleven of the 12 students went only 1 page deep on the majority of visited sites . Although the individual-level data is not large enough to analyze more rigorously , the power law seems to operate on an individual level as well as the aggregate level . Even when students found a Web site that contained the answer to a question , they did not always find the answer . One example is the Alcoholics Anonymous site -LSB- 26 -RSB- where 8 of the 11 students ended up while searching for a local meeting . Although there was a link to a site that contained local information , only 3 of the 8 students were able to find the link , 1 of whom only found it on the second visit to the Alcoholics Anonymous site , after viewing a total of 16 pages within the site . Similarly , 6 of the 11 students who searched for whether or not Paxil causes drowsiness visited the official Paxil site -LSB- 27 -RSB- . Only 3 of the 6 students were able to successfully answer the question based upon the information they found at the site . Two of them failed to find the list of side effects and 1 of them found the list but did not understand it enough -LRB- or read it carefully enough -RRB- to answer the question correctly . Search Engine Tactics Seven search engines were used , including 2 meta-search engines -LRB- Dogpile and Locate.com -RRB- . The meta-search engine Locate.com offers the user a number of search engines to choose from . Searches performed from the Locate.com Web site that utilized another search engine -LRB- eg , Yahoo! -RRB- are reported as if the search occurred on the destination search engine -LRB- eg , Yahoo! -RRB- . Table 3 summarizes the number of times that a particular search engine was used . If a search engine was used multiple times while searching for an answer to the same question , it is only counted once . Because students occasionally switched search engines while trying to answer the same question , there are more searches using a search engine -LRB- 79 -RRB- than there are attempts to answer questions -LRB- 68 -RRB- . In total , 6 of the 12 students used only Google , 1 used only Yahoo! , and the remaining 5 changed search engines at some point . Table 3 Search engine usage Search Engine Times Used n % Google 38 48.1 Yahoo! 13 16.5 Ask 12 15.2 MSN 7 8.9 Hotbot 6 7.6 Dogpile 2 2.5 AltaVista 1 1.3 A total of 132 search phrases were entered into the various search engines . Only 104 of those search phrases were unique . The most-frequent 2 phrases used were `` diabetes '' and `` Paxil , '' each of which had 5 occurrences . There was an average of 3.6 words typed in per search phrase and 80 % of the time there were 4 or fewer words per search phrase . Table 4 Distribution of search-result links viewed Bands of Search-Result Links Viewed Chosen Links n % Cumulative % Results 1-10 137 82.5 82.5 Results 11-20 8 4.8 87.3 Results 21-30 11 6.6 94.0 Results 31-40 4 2.4 96.4 Results 41-50 4 2.4 98.8 Results 51-60 1 0.6 99.4 Results 61 or more 1 0.6 100.0 Of the 132 search phrases , 30 contained at least 1 word that was misspelled -LRB- eg , `` tatoo , '' `` Alchoholics , '' or `` smokeing '' -RRB- , despite the fact that students could read the correctly-spelled word on the index card containing the question . Some search engines -LRB- eg , Google -RRB- offer a feature that recommends an alternate search string with the correct spelling of a word . For example , if a student typed `` alchoholics anonymous , '' the first page of results began with , `` Do you mean ` alcoholics anonymous ? ' '' Students were offered a new search string with correct spelling on 15 separate occasions , but only noticed and used it 6 times . The remainder of the times they used the results that were offered for the incorrect spelling . Of the 7 students who were offered corrected spelling suggestions , only 2 ever used them . Once a search string was entered into a search engine , students varied in the number of results pages that were viewed . Students viewed only the first results page 78 % of the time and 4 pages or less of results 93 % of the time . Because search engines report a different number of links per page of search results , Table 4 reports how often links were selected from the first 10 results , the second 10 , and so on . Only 3 blocked links were encountered during all of the searches , suggesting that blocking software did not have a significant impact on these results . Successful Searching Characteristics Of the 68 questions that students attempted to answer , 7 searches were abandoned after the student gave up or , in 2 cases , when the class period ended . Of the remaining 61 searches , 47 were successful in finding a complete , correct , and useful answer to the health question and the remaining 14 were unsuccessful . Six of the unsuccessful answers were completely incorrect and not useful , 4 were useful but only partially correct , and 4 were fully correct but not useful . Several factors contributed to the success of finding a correct , complete , and useful answer . One important factor was the individual who was performing the search . Although every student answered at least 1 question correctly there was wide variation in the number of correct answers . Two students successfully answered 6 out of 6 questions , 3 students successfully answered 5 questions , 4 students successfully answered 4 questions , and the remaining 3 students only successfully answered 1 or 2 questions . While our sample of students was too small to draw conclusions from , no distinct patterns were observed that would indicate that race , gender , Internet experience , or health searching experience were significant determinants of success . However , the older adolescents -LRB- 16-17 year olds -RRB- were successful 87 % of the time -LRB- 26 of 30 -RRB- as compared to 68 % -LRB- 21 of 31 -RRB- for the younger adolescents . Another important factor was the difficulty level of the questions themselves . Table 5 shows the failure rate for each question . The 4 partially-correct answers were split evenly between the Alcoholics Anonymous and tattoo questions . All 4 of the correct but not useful answers resulted from the HIV test question . Table 5 Unsuccessful searches by search topic Search Topic Unsuccessful Searches n % HIV test 8 38.1 Paxil 4 19.0 Alcoholics Anonymous 3 14.3 tattoo 3 14.3 smoking 2 9.5 diabetes 1 4.8 Total 21 100.0 Certain search actions led to sites that contained the answer more often than others . Overall , students found answers on 22 % of the sites they accessed -LRB- 47 of 215 -RRB- . They accessed sites in 5 ways . Although not often taken , the action with the highest probability of success -LRB- 47 % ; 7 of 15 -RRB- was following a link from 1 non-search-engine site -LRB- eg , www.aa-intergroup.org -RRB- to another site -LRB- eg , www.alcoholics-anonymous.org -RRB- . In most of these cases , the student accessed the first site directly from a search engine . Clicking on search engine results led to a site where students found an answer 21 % of the time -LRB- 35 of 166 -RRB- . Success rates were similar for following a recommended link from a list or menu provided by the search engine -LRB- 18 % ; 4 of 22 -RRB- . Directly typing in a URL , bypassing search engines entirely , was successful only 9 % of the time -LRB- 1 of 11 -RRB- . A sponsored link from a search engine was followed only once , and the student found an incorrect answer on that site . Another contributing factor related to success was misspelling of search terms . Of the 14 completed but unsuccessful searches , 29 % -LRB- 4 searches -RRB- had at least 1 misspelling compared to only 15 % -LRB- 7 searches -RRB- of the 47 successful searches . Perhaps even more telling , both successful and unsuccessful searches with misspellings took students 1.5 minutes longer on average than searches without misspellings . Observations confirmed that some students were unable to find an answer until they discovered and corrected their misspelling , resulting in higher quality and more-relevant results . Other search characteristics did not have statistically significant impacts on whether searches were successful , although this may have been due to small sample sizes . For example , the search engines were not significantly different in their percentages of successful searches . Similarly , the average number of words per search string was not significantly related to search success rate . -LRB- Data not shown . -RRB- Qualitative Analysis Certain common behaviors of the adolescent searchers were observed which were not apparent from the quantitative analysis . First , the students were very comfortable and confident while searching online for health information . Most students knew where they wanted to start the search and navigated using quick mouse clicks and shortcut keys . However , this characteristic was likely over-represented in our population due to their strong academic performance and Internet proficiency . Second , several searchers did not take much time in formulating a search strategy or -LRB- when applicable -RRB- choosing search terms . Instead , these searchers seemed to type in the first search string that came to mind . If the results were not what were anticipated , another search string was typed in , sometimes without even clicking on any results from the first search string . The overall approach was a trial-and-error method with frequent backtracking . The most-common problem with search strings was that they were not specific enough . For example , 2 different students typed in the search string `` hiv '' when looking for a place that administers free and confidential HIV tests . Third , most students quickly scanned pages , jumping from place to place within a page , rarely reading an entire paragraph . In some cases the answer to a question was contained on a page , but the student left before finding it . In other cases a link that would have led to the answer was missed . This finding supports prior research on adolescent search behavior related to nonhealth topics -LSB- 7 - 10 -RSB- . Fourth , students mentioned that they purposefully avoided sponsored links and advertisements , despite the fact that many of the search engines present these results first . The qualitative data confirmed this practice , as only 1 sponsored link was ever selected . Finally , little to no attention was paid to the source of the answer . In the vast majority of cases , once an answer was located , it was simply assumed to be correct . Discussion When compared with prior research , the findings of this study show many similarities and a few key differences between the behaviors of adolescents and adults while searching for health information . This study found that adolescents searching for health information utilized search engines nearly every time . This finding was similar to that for adults as described in the Eysenbach study -LSB- 15 -RSB- . These observational studies also suggest that after-the-fact survey questions concerning the use of search engines may underestimate this behavior . For example , 2 nationally-representative surveys reported that 58 % of youth -LRB- written communication , 2001 Dec ; Generation RX.com Survey printouts ; V. Rideout , Henry J. Kaiser Foundation , Menlo Park , CA -RRB- and 81 % of adults -LSB- 1,2 -RSB- started seeking health information at search engines . Our study found that adolescents relied upon links from only the first few results pages , and rarely explored far within any site . These results also were similar to adult searching behaviors -LSB- 15 -RSB- , although youth seem to be more likely to search beyond the first 10 search results . Adolescents often chose search strings that were too general and/or contained misspellings , so that they did not always find useful sites that were available . Eysenbach also reported search strings by adults that were too general -LSB- 15 -RSB- , however , spelling seems to be more of a problem with youth . Adolescents were unsystematic in their reading of Web sites and some sites were poorly organized so that they did not always find the information they were looking for , even when it was present in a site they examined . Future research is needed to better understand if adolescents do not understand information provided on these sites , whether they simply have less patience , or some other explanation . In summary , many of the specific search tactics are similar for adults and adolescents , but a few issues related to spelling , browsing of Web sites , and understanding of content are notably different . Simulation of Searches The results from this study have implications for anyone who simulates adolescent health searches , for providers of health information , and for educators . There are many reasons to simulate adolescent health searches . For example , an educator preparing a lesson plan may want to informally simulate searches in order to anticipate what students are likely to find if given certain particular search tasks . A researcher may want to simulate adolescent searches more systematically to evaluate the availability and accessibility of information on particular topics , to evaluate which search engines should be recommended to adolescents , or to evaluate whether the installation of filtering software will have a detrimental impact on accessibility of health information -LSB- 13 -RSB- . Because many of the search behaviors modeled by these simulations are similar for both adolescents and adults , results from studies that simulated one or the other group likely apply to both groups . The results of this study suggest that such simulations can focus on the use of search engines , but that very-broad search terms and , especially for adolescents , common spelling errors should be considered . Ads and other nonresult links can be ignored . Since more than 80 % of the links that were followed appeared in the top 10 results , and more than 95 % were among the top 40 , a search simulation need not consider result links beyond these . Providers of Internet Health Content Given the patterns of adolescent searching behavior found in this study , providers of health content can do several things to increase the probability that adolescents will find their sites . Since adolescents rely primarily on the first few results from search engines and do not tend to look at ads , it is important to ensure that health sites appear near the top of the results for searches on health terms . Choices of keywords in the domain name , page title , meta tags , and the first few sentences , as well as links from other sites , can all affect placement in search results . It may also be useful to include some common misspellings in meta-tag keywords and in the body of the text in order to make a site appear in the results page of searches using those misspellings of related search terms . Because most major English-language search engines no longer use the keyword feature of meta tags , site designers are left with the difficult task of working misspelled words -LRB- eg , misspelt -RRB- into the text without coming across as poor spellers themselves . It is also important that the site descriptions displayed in search engines be attractive to adolescent searchers : while our study did not analyze the various reasons that adolescents chose to follow one link over another , we did observe that they made choices based upon the link descriptions and did not simply select the first link offered . Books and articles , software , and consulting services are all widely available to improve search engine placement and to influence the short summary text that search engines extract for display in search results -LSB- 28,29 -RSB- . Organizations that invest large amounts of money in developing sophisticated health-information sites would do well to spend a little bit more to ensure these sites are easily found . Another area that Internet content providers should focus on is within-site navigation . Because students tend to skip around from place to place within a page and read little in sequence , it is important that sites with a significant adolescent audience are well organized , concise , and understandable . Long paragraphs , too many links , and difficult vocabulary all decrease the likelihood of adolescents finding health information they are seeking , even if it is contained within a site . Internet content producers should attempt to understand the needs of the site visitors and build hierarchal structures that reflect those needs . For example , if one of the primary needs of individuals visiting the Alcoholics Anonymous site is to find a local meeting , the first page of the site should include an obvious link -LRB- eg , `` Find an AA Meeting Near You '' -RRB- that leads to another page that returns the nearest meetings after entering in a zip code or city name . While ease of within-site navigation is important for all visitors to health information sites , some information providers may want to develop sites targeted specifically to adolescents . While they might like the targeted information once they found it , we observed that adolescents tend to rely on general-purpose search engines . Thus , developing special youth-targeted versions of information sites may be of somewhat limited utility , unless also accompanied by advertising or education campaigns that make adolescents more likely to find such sites . Rather than changing Web sites or their presentation in search engines , it may also be useful to undertake education campaigns to improve the search strategies and tactics that adolescents use when seeking health information . It may be helpful to guide them towards youth-oriented directories or search engines , rather than general-purpose search engines . For example , both Yahoo! and Google offer directories with subcategories of sites designed for teens that cover various health topics . This approach may be facilitated by including links to such resources on the Web browser 's starting page in schools and libraries . Alternatively , adolescents might be taught techniques for formulating and refining search terms at general-purpose search engines , adding or dropping more-specific words based on the kinds of results returned . They might also be taught to notice potential search term misspellings based on surprising search results . Finally , adolescents might also be taught techniques for systematically exploring within a Web site to find the kind of information they are looking for . Limitations and Future Research There are several important limitations to the interpretation of these results . First , this was not a representative or random sample of adolescents . It was a small convenience sample with a selection bias toward adolescents with strong Internet searching skills . While the results can not be generalized to all adolescents and do not capture the full range of adolescent searching experience , we can assume that the average adolescent would have had even more trouble than our study participants in finding health information on the Internet . Second , the health-related search questions were deliberately constructed to avoid controversial topics such as safe sex , abortion , and homosexuality . Given that adolescents are often faced with health problems related to sexuality , their actual search behavior and success at finding health information related to sexuality may not be reflected in our results . Another concern is that participants may have changed their search behavior because of the presence of observers and because they were aware that their search behaviors were being recorded . For example , students who had trouble finding an answer may have persisted in their search longer than they would have in a nonresearch setting . Alternatively , because students knew they had several search questions to answer during a single class period , they may not have been as persistent as they might have been with a more personally-relevant question and less-restricted search time . Thus , the data here reflect a rough estimate of persistence for an adolescent looking for health-related information . Also , searching was conducted individually , while in practice many searches both at home and at school are conducted with friends , teachers , or family close by . While it is difficult to know how this would affect searching behavior without future research , it is possible that students would act differently -LRB- eg , receive help with spelling -RRB- . Finally , while components of our classification scheme for successful versus unsuccessful searching have been previously validated , the overall scheme was modified to more accurately code the search results as correct , complete , and useful . A more-systematic validation of coding schemes for health information search results is an important area for future research . More research is needed to validate the results presented in this article , as well as determine if results vary for different populations -LRB- eg , age , race , and experience with health searching -RRB- and different health questions -LRB- eg , finding a practitioner versus finding the answer to a question -RRB- . Additionally , instead of focusing on how adolescents currently search for health information , future studies may also want to explore interventions aimed at improving their searches . For example , should health portal sites designed for adolescents or online directories be used ? Or would the current practice of using common search engines , but with adolescents learning improved search tactics be more effective ? Also , which search strategies lead to sites that are the most likely to be accurate and influence adolescents to change their behavior ? Conclusions This study provides a useful snapshot of current adolescent searching patterns . The results have implications for constructing realistic simulations of search behavior , and for both information providers and educators . Analyzing search behavior through actual observation should be a cornerstone in any effort to improve adolescents ' access to health information .

O O O O O O O B O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I I O O B O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O 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O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B O O O O O O B O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O 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