Small intestinal transit in patients with liver cirrhosis and portal hypertension: a descriptive study

Stine Karlsen
Lotte Fynne
Henning Grønbaek
Klaus Krogh
Small intestinal transit in patients with liver cirrhosis and portal hypertension: a descriptive study
R E S E A R C H A R T I C L E Open Access
Background: Gastrointestinal dysmotility may be involved in the development of bacterial translocation and infection in patients with liver cirrhosis. The aim of the present study was to describe gastric, small intestinal and colorectal motility and transit in patients with liver cirrhosis and portal hypertension using a magnet-based Motility Tracking System (MTS-1) and standard radiopaque markers.Methods:We included 15 patients with liver cirrhosis (8 Child-Pugh A, 6 Child-Pugh B, and 1 Child-Pugh C) and portal hypertension (11 males, median age 54 years (range 38-73), median hepatic venous pressure gradient 18 mmHg (range 12-37)), and 18 healthy controls (8 males, median age 58 years (range 34-64)). The gastric emptying time and small intestinal motility were evaluated by MTS-1, and the total gastrointestinal transit time was assessed by radiopaque markers and abdominal radiographs.Results: The velocity through the proximal small intestine was significantly higher in cirrhotic patients (median 1.27 metres (m)/hour, range 0.82-2.68) than in the healthy controls (median 1.00 m/hour, range 0.46-1.88) (p = 0.03). Likewise, the magnet travelled significantly longer in both fast (p = 0.04) and slow movements (p = 0.05) in the patient group. There was no significant difference in either gastric emptying time-23 minutes (range 5-131) in patients and 29 minutes (range 10.5-182) in healthy controls (p = 0.43)-or total gastrointestinal transit time-1.6 days (range 0.5-2.9) in patients and 2.0 days (range 1.0-3.9) in healthy controls (p = 0.33). No correlation was observed between the hepatic venous pressure gradient and the velocity of the magnet through the small intestine.Conclusion: Patients with liver cirrhosis and portal hypertension demonstrated faster-than-normal transit through the proximal small intestine. This may be due to an overactive bowel, as suggested by previous studies.

Background

Liver cirrhosis is a condition associated with increased morbidity and mortality. Clinically significant portal hypertension (>10 mmHg) may lead to decompensation, with complications such as ascites, oesophageal varices and hepatic encephalopathy (HE). Spontaneous bacterial peritonitis (SBP) can further complicate ascites with abdominal and systemic inflammation and lead to potentially fatal complications, such as variceal bleeding and HE [1]. Sanchez et al. proposed that gut bacteria may be translocated into the peritoneal cavity, contributing to the development of SBP [2]. An altered gastro-intestinal transit time (GITT) may enhance the intestinal bacterial overgrowth, subsequently increasing peritoneal bacterial translocation [3]. Therefore, small intestinal dysmotility may be involved in the development of cirrhotic complications.

Previous studies have suggested that cirrhotic patients demonstrate a prolonged gastric emptying time and decreased gastric compliance [4,5]. Other studies have demonstrated a prolonged total GITT related to complications of cirrhosis, such as spontaneous bacterial peritonitis and malnutrition [5,6]. Due to the difficulty of accessing the small intestine, the above studies primarily investigated gastric emptying and colonic transit time (CTT). The magnet-based Motility Tracking system (MTS-1) used in this study allows for a minimally invasive description of all segments of the gastrointestinal canal, including the small intestine [7].

We aimed to examine the small intestinal motility and transit times of the stomach, small intestine and colorectum separately. We hypothesised that small bowel motility was reduced and that segmental gastrointestinal transit times were prolonged in patients with liver cirrhosis.

Methods

Subjects

We included patients aged 18-75 years with liver cirrhosis of any origin referred for clinical investigation of the hepatic venous pressure gradient (HVPG) at the Department of Medicine V (Hepatology and Gastroenterology), Aarhus University Hospital, Denmark. If the HVPG was greater than 12 mmHg, the patient was invited to participate in the study. Of 62 consecutive patients, we included 15 (11 men, median age of 54 years, range between 38 and 73 years). In total, 38 were excluded because of comorbidities or the use of medications affecting bowel function; 6 patients did not wish to participate, and 3 patients were not included for practical reasons. Patients were compared to 18 healthy controls (8 men, median age of 58 years, range between 34 and 64 years). All patients and healthy volunteers included were without other known conditions affecting bowel function, and none had undergone abdominal surgery. All patient medications with known effects on gastrointestinal motility were ceased one day prior to beginning the investigation. All patients were characterised by their HVPG, Child-Pugh scores, and number of bowel movements per day.

The study was performed in accordance with the Declaration of Helsinki and was approved by the local ethics committee (reference number M-20110006). All subjects gave written informed consent before participation.

Hepatic venous pressure gradient measurement

The portal pressure was measured indirectly by HVPG, as previously described [8]. Under radiographic guidance, an intravascular pressure catheter was placed in a hepatic vein through the femoral vein. The free and the wedged pressures were obtained, and the difference between them represents the pressure gradient across the liver [8].

Gastric emptying and small intestinal motility

Gastric emptying, small intestinal transit time, median velocity of the magnet through the small intestine and contraction patterns were determined using the magnetbased Motility Tracking System-1 (MTS-1) (Motilis, Lausanne, Switzerland) [7]. The MTS-1 system provided information about gastrointestinal transit times and motility patterns by detecting the position of an orally ingested magnetic pill. Subjects ingested a siliconcovered magnetic pill (6×15 mm, density 1.8 g cm −3 ). A detection plate with an array of 4×4 sensors was placed in front of the subject and gave the position and orientation of the pill defined by three coordinates (position: x, y, z) and two angles (θ, ϕ). A 2D assessment was made on the magnet position within the subject by entering the detection plate location in relation to anatomical reference points, thereby defining the pill's propagating movements. Two external sensors were placed on the subject's neck and thorax, recording respiratory and movement artefacts.

The magnetic coordinate data were continuously sent to a computer at a sampling rate of 10 Hz during the investigation period. Custom-made software was used to picture the coordinates and angles as waves of different frequencies and amplitudes in real-time. The waves depicted by the data from the angles represented the gastro-intestinal contractions. By assessing this wave pattern, we could determine three different gastro-intestinal phases: the gastric phase, with a pattern of three contractions min −1 and medium amplitude; the small intestinal phase, with 10-14 contractions min −1 [9] and high and mixed amplitude; and the colonic phase, with up to 6 contractions min −1 and low amplitude [10]. The movements through the small intestine were divided into the following three types: fast (>15 cm min −1 ), slow (between 1.5 and 15 cm min −1 ) and very slow (<1.5 cm min −1 ) [10].

The system calibration for ambient magnetic fields was performed before each recording and subsequently every 90 minutes. The technical specifications of MTS-1 and data on its validity have recently been published [7,10].

Experimental protocol for the Motility Tracking System

After eight hours of fasting, investigations with MTS-1 started at 8 A.M. The outer abdominal size was estimated using the distances between the xiphoid process and the symphysis pubis, the superior iliac spines on both sides, and the abdominal wall and the back. The pill was ingested with 100 ml of water. During the measurements, the subject was placed on a wooden bed with the headboard in an upright position. Measurements were continued for a minimum of seven hours or until the magnetic pill was in the caecum. Small breaks for toilet visits and short walks were permitted at the subjects' request. The subjects were encouraged to not talk, sleep or move but were allowed to read or watch TV. After the magnetic pill had passed to the duodenum, a standardised breakfast (1.991 kJ, 14% protein, 45% fat, 41% carbohydrate) was served. Three hours after breakfast, a standardised lunch (1.500 kJ, 16% protein, 32% fat, 52% carbohydrate) was provided. When the magnetic pill had passed to the caecum, or after a minimum of seven hours, the investigation was terminated.

Total gastrointestinal transit time (GITT)

GITT was determined as described by Abrahamsson et al. [11]. At 12 A.M. for six consecutive days, the patient ingested a capsule containing 10 radiopaque markers. On the seventh day, a plain radiography of the abdomen was taken. The number of markers left in the different segments of the colon was counted, and the GITT was calculated based on the following formula:
GITT ¼ M þ f  D ð Þ ð Þ D
where M is the total number of markers left; D is the number of markers ingested each day; and f is the fraction of the daily markers selected for the provision of transit. In this case, f = 0.5.

Data analysis

Two investigators independently evaluated data obtained by MTS-1, and the mean values were used for all subsequent analysis. GE was the time from magnet ingestion to pyloric passage, identified by the following signs: the cessation of the characteristic gastric pattern (3 contractions min −1 ), the appearance of small intestinal contraction pattern (10-14 contractions min −1 ) and the appearance of the duodenal arch on the 2D representation ( Figure 1). The small intestinal transit time was the time from pyloric passage to ileocaecal passage, identified by the cessation of contraction patterns of 10-14 min −1 and the occurrence of a short, fast movement of the magnetic pill situated in the lower right quadrant on the 2D representation. The mean velocity of the magnetic pill within the small intestine was determined using the MTS-1 software MTS Tools (Motilis, Lausanne, Switzerland) [7].

Statistical analysis

All data are expressed as medians with ranges. GE, small intestinal propagation velocity and GITT were compared in the two groups using the Mann Whitney U-test. The correlations between HVPG and the presence of oesophageal varices and GI transit times were analysed using Spearman's rank correlation. P < 0.05 was considered statistically significant.

Results

Overall, 15 patients with cirrhosis and portal hypertension completed the study and were compared to 18 healthy controls. The aetiologies of cirrhosis were alcohol (n = 11), non-alcoholic steatohepatitis (n = 2), viral hepatitis C (n = 1) and primary biliary cirrhosis (n = 1). The Child-Pugh classifications were A (n = 8), B (n = 6) and C (n = 1). The median portal pressure was 18 mmHg (range: 12-37). Additionally, 10 out of 15 patients (67%) had previously bled from varices; 12 patients had grade 2-3 oesophageal varices; one patient had grade 1 oesophageal varices; and one patient had gastric varices without signs of oesophageal varices. One patient had no evidence of either oesophageal or gastric varices. Two patients with alcohol cirrhosis had current alcohol intake.

In all patients and healthy subjects, the number of bowel movements per day and the stool consistency were within normal limits.

Gastric and intestinal motility

The MTS-1 procedure was well tolerated by all subjects. The characteristic basic contraction frequencies of 3 min −1 in the stomach and 9-11 min −1 in the small intestine were observed in all patients and controls. In both groups, the velocity of the magnetic pill declined as it passed distally through the small intestine. Data on gastric emptying and small intestinal motility are shown in Table 1. There was no significant difference in the median fasting state gastric emptying time between patients and healthy controls (p = 0.43). the magnet propagation velocity during the first two hours in the small intestine was significantly faster in patients than in healthy controls (p = 0.03).

All participants stated that they had followed the protocol for the assessment of GITT. The median GITT was 1.6 days (range 0.5-2.9) in patients and 2.0 days (range 1.0-3.9) in healthy controls (p = 0.33). GITT was more than 3 days in one healthy subject (3.4 days), while none of the patients had a GITT longer than 3 days.

Portal hypertension and small intestinal motility

We found no correlation between the degree of portal hypertension and the velocity of the magnetic pill through the small intestine (r = −0.29, p = 0.29). There was no difference in the propagation velocity during the first two hours between the patients with no or grade 1 oesophageal varices and those with grade 2-3 oesophageal or gastric varices (p = 0.93).

Discussion

In the present study, we evaluated the small intestinal motility and transit in patients with liver cirrhosis and clinically significant portal hypertension. We used a novel magnet-based MTS-1 that provides detailed information on intestinal motility. Our main finding was that patients with cirrhosis and portal hypertension had faster-than-normal postprandial transit through the proximal small intestine. Thus, our hypothesis of reduced small bowel motility and prolonged segmental gastrointestinal transit times was rejected.

The basic and highly characteristic contraction frequencies of the stomach and small intestine were unaltered by portal hypertension, but the distance was covered faster both during the long periods with relatively slow transit and during the short bursts of very fast movement. Madsen et al. studied eight patients with cirrhosis and portal hypertension using scintigraphy [12]. They found no difference in the GE of solids or small intestinal transit times compared to healthy controls. The scintigraphy technique is considered the gold standard for measuring GI transit times. However, standard 30 minute-intervals between each image were used, and smaller differences in either GE or small intestinal transit times could thus have been missed. In the same study, cirrhosis patients showed faster-thannormal colonic transit times [12]. It has previously been demonstrated that patients with cirrhosis have a prolonged phase II of the fasting small intestinal migrating motor complex (MMC) [13]. We obtained data on small intestinal motility in the postprandial state, but our data also suggest an abnormally active small intestine in patients with liver cirrhosis.

Some previous studies have suggested that patients with liver cirrhosis have prolonged GE [14,15], while others found no difference [16]. The main focus of the present study was small intestinal motility, aiming for an exact determination of pyloric passage that MTS-1 provides [10]. As a detailed evaluation of GE should be performed in both the solid and the liquid phases, MTS-1 is not ideal for the description of GE. Large particles will typically pass through the pylorus during phase III of the migrating motor complex [17]. Unless magnet intake is standardised with respect to MMC or with a meal, a large variation in solid-state GE should be expected, as observed in the present study.

Our findings are in contrast with some previous studies that demonstrated prolonged gastrointestinal transit times in patients with liver cirrhosis. However, those studies investigated the total orocaecal transit times with radiopaque markers [6] or lactulose breath tests [18]. These methods do not differentiate between GE and small intestinal transit time, and differences in small intestinal transit may not be detected, especially if GE is The magnet pill moved faster through the upper small intestine in patients than in healthy controls. All data expressed as median (range).

prolonged. Furthermore, patients with liver cirrhosis often suffer from small intestinal bacterial overgrowth, making the lactulose breath test unreliable [19]. Other studies have shown both prolonged and reduced colonic transit times in cirrhotic patients [6,20]. However, GITT mainly reflects colonic transit time, and in our study, there was no difference in GITT between patients with cirrhosis and controls. It has previously been shown that a history of SBP correlates to the degree of GI alterations in patients with liver cirrhosis [21]. Additionally, there are indications that abnormalities in small intestinal motility are related to the degree of chronic liver failure [5]. In accordance with the present study, Madsen et al. found no correlation between transit times and HVPG [12]. However, this may be a type II error due to the small number of patients included in both studies.

Our findings were surprising and contrary to our hypothesis. It is unclear through which mechanisms portal hypertension may affect gastrointestinal motility. It may be that portal vein and intestinal wall blood stasis may cause an overactive bowel. We studied small intestinal motility in the postprandial state. In the fasting state, a marked change in the contraction patterns of phase II and the MMC has been previously observed [13]. Whether this behaviour indicates an overactive bowel is unknown. In healthy individuals, intestinal peristalsis, gastric acid and mucosal immunity act to protect the small intestine from bacterial overgrowth and translocation. Breath tests for small intestine bacterial overgrowth are not reliable for research purposes [22], and cultures from small intestinal fluid require invasive investigation. For these reasons, we did not investigate whether patients in the present study had small intestine bacterial overgrowth.

Previous studies have suggested that the aetiology of liver cirrhosis may influence GI transit times [3,23]. In the present study, we included patients consecutively and independently of cirrhosis aetiology. The mixed aetiology and differing representation of Child-Pugh classes in a small sample size are major limitations of the study. The main aetiology of cirrhosis was alcohol consumption, and it is well known that alcohol may affect gastrointestinal motility. However, all but two patients had abstained from drinking for at least 3 months prior to the investigation. Pancreatic insufficiency may also reduce small intestinal transit. However, none of the patients had a history of acute or chronic pancreatitis or malabsorption, and no signs of calcification in the pancreatic area were noticed on abdominal radiographs. Furthermore, autonomic dysfunction in patients with liver cirrhosis may lead to gastroparesis and an abnormal frequency of gastric contractions [24]. Compared to healthy controls, we found no differences in the contraction frequency in either the stomach or the small intestine.

There was a difference in gender between our patients and the control group. However, when stratifying the data in each group by gender, we could not detect any differences in GE, small intestinal velocity or colonic transit time. Ten out of 15 patients had a history of bleeding oesophagus varices. Oesophago-gastro-doudenoscopy had been performed in all patients, and 14 had oesophageal varices. We found no association between the presence of varices and motility patterns.

Conclusion

In conclusion, our findings indicate that GI transit is abnormally fast in the proximal small intestine of patients with liver cirrhosis and portal hypertension. More and larger studies are needed to confirm our findings and to determine the mechanisms of action. Furthermore, the associations among gastrointestinal dysmotility, bacterial overgrowth and the risk of cirrhotic complications should be studied.

Figure 1
1Magnetic sensor and duodenal arch. Tracking of the magnetic pill by 16 (4x4) external sensors. The position is defined by coordinates X, Y and Z, and the rotation is defined by the angles ϕ and θ (left). 3D representation pyloric and duodenal passage (right). The sequence displayed is 10 seconds long.

Table 1
1Gastrointestinal motility and transit times in patients with liver cirrhosis and in healthy controlsPatients with cirrhosis
Healthy controls
p

http://www.biomedcentral.com/1471-230X/12/176
AcknowledgmentsThis work was supported by The Faculty of Health Sciences, Aarhus University, Denmark, and The Novo Nordisk Foundation.Competing interestsThe authors declare that they have no competing interests.Authors' contributions SK: Involved in study design, inclusion of patients, all study related procedures, data analysis and writing first draft of the manuscript. LF: Involved in study design, study related procedures, data analysis and interpretation. HG and KK: Initiated the study, involved in study design, inclusion of patients, study procedures, data analysis and interpretation. All authors have participated in writing and finalising the manuscript, and all have approved the final submitted version of the manuscript.Submit your next manuscript to BioMed
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Small intestinal transit in patients with liver cirrhosis and portal hypertension: a descriptive study. Karlsen, BMC Gastroenterology. 12176Cite this article asCite this article as: Karlsen et al.: Small intestinal transit in patients with liver cirrhosis and portal hypertension: a descriptive study. BMC Gastroenterology 2012 12:176.


How do family physicians communicate about cardiovascular risk? Frequencies and determinants of different communication formats

Stefan Neuner-Jehle
Oliver Senn
Odette Wegwarth
Thomas Rosemann
Johann Steurer
How do family physicians communicate about cardiovascular risk? Frequencies and determinants of different communication formats
R E S E A R C H A R T I C L E Open Access
Background:Patients understand information about risk better if it is communicated in numerical or visual formats (e.g. graphs) compared to verbal qualifiers only. How frequently different communication formats are used in clinical primary care settings is unknown. Methods: We collected socioeconomic and patient understanding data using questionnaires and audio-recorded consultations about cardiovascular disease risk. The frequencies of the communication formats were calculated and multivariate regression analysis of associations between communication formats, patient and general practitioner characteristics, and patient subjective understanding was performed. Results: In 73% of 70 consultations, verbal qualifiers were used exclusively to communicate cardiovascular risk, compared to numerical (11%) and visual (16%) formats. Female GPs and female patient's gender were significantly associated with a higher use of verbal formats compared to visual formats (p = 0.001 and p = 0.039, respectively). Patient subjective understanding was significantly higher in visual counseling compared to verbal counseling (p = 0.001). Conclusions: Verbal qualifiers are the most often used communication format, though recommendations favor numerical and visual formats, with visual formats resulting in better understanding than others. Also, gender is associated with the choice of communication format. Barriers against numerical and visual communication formats among GPs and patients should be studied, including gender aspects. Adequate risk communication should be integrated into physicians' education.

Background

A major challenge in preventive medicine is to effectively inform patients about the risks and benefits of possible treatment options. Risk can be communicated by words (verbal qualifiers, e.g., "your risk is high" or "this is not good for your health"), by numerical formats (absolute percentages, relative percentages, natural frequencies), by visual formats, or by a combination of these methods [1,2]. Although there is no clear evidence as to which format is the best for communicating risk most effectively, recent research allows a ranking (hierarchy) of the different risk communication formats in terms of effectiveness and patient understanding: the use of natural frequencies, graphical formats (e.g., bar charts), and combinations of these are more comprehensive than percentages or a purely verbal translation of risk [3][4][5][6], and patients prefer these formats as opposed to percentages [7]. Patient characteristics as age, education, cultural background, psychosocial aspects as well as literacy influence a patient's understanding of information about risk and communication preferences [8]. The numeracy of patients refers not only to the capacity of understanding numerical formats accurately, but also to graphical formats. Numeracy has an impact on risk perception, adherence to interventions and even health outcomes [9]. Also physician characteristics are important determinants of which formats are used, thus leading to a large variation in the use of risk communication formats among primary care providers [10]. Growing evidence suggests that involving patients in decision-making has positive effects in terms of patient satisfaction, adherence, and even health outcomes [11,12]. Patients increasingly seek more active participation in healthcare decisions, though not all of them to the same degree [13], and there has been a call for a shift towards a meaningful dialogue between patients and physicians and shared decision making [14].

Cardiovascular disease (CVD) is a major issue in public health, contributing excessively to the overall morbidity and mortality of populations in industrialized societies [15]. Only a minority of people with cardiovascular risk factors (CVRF) who qualify for prophylactic interventions to lower their risk is treated adequately [16,17]. Possible explanations are low adherence of doctors to guidelines and ineffective risk communication between doctors and patients [18]. Furthermore, cardiovascular risk is often perceived inappropriately by primary care patients, leading to over-or underestimation of the risk. Communicating risk by understandable formats has the potential to correct inappropriate risk perception [19]. Systematic reviews suggest that providing adults at moderate to high CVD risk with information about their global CVD risk (using different communication formats) improves their accuracy of risk perception and probably increases their intent to initiate CVD prevention [12,20]. Gain-framed messages (e.g. presenting a survival benefit), as apposed to lost-framed messages (e.g. presenting a potential damage), shorter timeframes (5 or 10 years until realisation of the risk, versus 15 or 20 years) and visual formats seem to enhance understanding of risk and to increase the selfefficacy to prevent CVD [21].

Thus, improving comprehension and the effectiveness of risk communication in the field of CVD is an important and challenging task in medicine with public health consequences. How often primary care physicians use the various risk communication formats while counseling patients with CVRF is yet unknown.

The aim of this study was to investigate how frequent verbal, numerical, and visual formats, or a combination of formats, are used in the CVRF communication process between primary care physicians and patients. An additional aim was to identify patient and GP characteristics associated with different counseling formats. In contrast to previous research studying the effectiveness of different risk communication formats in healthy volunteers [2,4,6], we chose a real physician-patient encounter and assessed the primary outcome (counseling format) by audio-recordings rather than self-reporting.

Methods

Procedure

To investigate how CVD risk is communicated, primary care physicians audio-taped counseling sessions with patients at CVD risk. The sessions were part of the usual care performance of the general practitioners (GPs; specialists for general and internal medicine). In three northern and central Swiss cantons (Zurich, Lucerne, and Zug), all GPs approved by the Swiss Medical Doctors Federation (Foederatio Medicorum Helveticorum, FMH) who were either running a medical office independently or employed in a medical office were invited to participate by information leaflet sent to postal addresses provided by the FMH. The recruitment and instruction of doctors started in December 2008, and data were collected until the end of February 2010. The study was received and approved by the ethical committees of the cantons of Zurich, Lucerne and Zug.

The doctors who were willing to participate were visited and provided with information about the aims of the study in so far that we told them that the study is about investigating risk communication in daily practice. The participants were further introduced to the details of how to collect the requested data and provided with the required materials (digital audio-recorder, several copies of a GP questionnaire, several copies of a patient questionnaire), as they had to collect all data by themselves. No suggestions were given to physicians on the method or program of risk calculation. No information was given neither to physicians nor patients as to what we exactly planned to analyze in the interviews, in order to avoid desirability bias. The doctors were informed about the planned analysis only after data collection, including the right to withdraw the data (which none of the GPs finally did).

During the next three months, GPs identified eligible patients among those in their practice and asked them to participate based on the following inclusion criteria: 35 to 65 years of age (in order to adapt to the age range of risk calculators; exceptionally younger or older participants could be included if the GP calculated their risk by other methods), and with at least one risk factor of the following -lipid disorder; high blood pressure (using internationally accepted cut-off points), and ongoing tobacco smoking. Exclusion criteria were: cognitive deficiency (dementia, stroke); terminal disease with poor prognosis in terms of survival time; acute somatic or psychiatric disorder; and clinical manifestation of any CVD. Patients willing to participate signed an informed consent form before starting the counseling session. These sessions were audio-taped, and patients and GPs completed a questionnaire immediately after the session.

Patient questionnaires referred to their age, gender, level of education, ethnicity, and the presence of CVD in first degree relatives. The self-rated understanding of the received information, the awareness (estimate) of the risk of developing CVD, and the anxiety regards developing CVD were measured on a visual analogue scale (VAS) ranging from 0 (low level of understanding, awareness, and anxiety) to 100 (highest level of comprehension, awareness, and anxiety) points. In addition, patients documented a translated 8-item-set of a validated index of the need and expectation for medical information, the autonomy preference index (API) [22,23]. The GP questionnaire asked for an estimate of the patient's risk of developing CVD and an estimate of the patient's anxiety towards developing CVD, again measured on a VAS, ranging from 0 (low level of risk and anxiety) to 100 (highest level of risk and anxiety) points.

All audio tapes and questionnaires were collected by the principal investigator three months after the first visit. After the recorded files were transcribed, data from each counseling session were classified independently by two researchers into different format categories: verbal, numerical, visual, or combined. In case of disagreement, discussion of the interview would follow in order to reach consensus; if this would not be possible, data would be excluded. In fact, there was no disagreement among raters in the communication format classification of interviews.

A consultation was classified as "visual format" if the information from the audio-taped interview indicated the use of a table or graph. The total counseling time and the ratio of patient talking time to total consultation time was calculated from the audio record.

Participants

Out of 1188 primary care physicians invited to participate in the study, 35 (2.9%) were willing to participate. Finally, 22 primary care physicians (1.9% of invited GPs) enrolled 77 patients (1-9 patients each). For seven patients, audio records were incomplete due to technical reasons and, therefore, excluded from the main analysis. No values were missing in the questionnaires. The baseline characteristics of the physicians and patients are summarized in Table 1. The median age of the participating primary care physicians was 46.5 years (IQR 38 -57 years), and 64% were male. The GPs had a median 11 years (IQR 5 -20 years) of experience as a primary care physician. The median age of patients was 51 years (IQR 45.5 -59 years), and 58% were male.

Data analysis

For our main outcome, the prevalence of different risk communication formats, we calculated the frequency of each format and the corresponding 95% confidence intervals. We tested bivariate associations between the different counseling formats and patient and physician characteristics using the Kruskal-Wallis and Fisher's exact tests for continuous and categorical variables, respectively. The intraclass correlation coefficient was calculated to assess the agreement between different counseling formats in GPs who recorded at least two encounters. To further investigate independent determinants of the counseling format used (verbal-numericalvisual) we performed a multinomial logistic regression analysis including all physician and patient characteristics showing at least a borderline significant (i.e. p<0.1) bivariate association with the counseling format. In addition, the model was controlled for the clustering effect by the GP. In a secondary analysis, we investigated whether the counseling format was an independent determinant of the level of understanding by performing a multiple linear regression. Potential confounding factors, such as patient age and gender, education, API, total counseling time, patient's self-assessed level of CVD risk, and anxiety, were included as covariates. For the quantitative analysis, we used the SPSS Statistical

Results

In 51 of 70 consultations (73%; 95% CI 62-84%), GPs communicated cardiovascular risk to their patients using verbal qualifiers only. In eight consultations (11%; 95% CI 4-19%), the GPs combined such verbal qualifiers with numerical information. Graphical formats were exclusively used in one consultation (1.4%; 95% CI 0.3-8%) and together with numerical information in 10 consultations (14%; 95% CI 8-24%). Among the 18 consultations in which GPs presented numerical information to their patients, they exclusively used absolute percentages in 10 sessions, combined absolute risk information and natural frequencies in seven sessions, and used relative risk information to communicate the patient's risk in one session.

The majority of visual formats (91%) were tables with a color-coding system analogous to traffic light colors, indicating low, medium, and high risk values. The underlying risk calculation was always based on a 10-years timeframe. Only one doctor used another graphical format, a survival curve. Bar charts or population diagrams were not used at all in our study sample.

Ten of 16 GPs (62.5%) who provided more than one consultation used the same risk communication format throughout the sessions without variation, whereas six GPs switched between different formats. The intraclass correlation for the counseling formats used was 0.63 (95% CI 0.41-0.85; p < 0.01) in GPs who performed more than one consultation on risk, indicating a significant clustering effect.

The mean consultation time for communicating risk was 9 min 46 sec (SD, 5 min 35 sec), ranging from 1 min 26 sec to 32 min 04 sec. During the consultations, patients were talking 24% of the time. On average, GPs' estimate of patients' CVD risk was 29 (range: 0-81) on the VAS scale (0-100), whereas patients' mean estimate of their own CVD risk was 28 (range: 3-100). In the direct comparison between GPs' and patients' CVD risk estimates (estimates on the same patient), they differed by 17. Results of the bivariate analysis between risk counseling formats and patient and physician characteristics are listed in Table 2. Gender was the only GP characteristic strongly associated with the communication format; only one female physician used numerical formats and none used visual formats (Figure 1). Patient gender and degree of subjective understanding the given information were patient determinants associated with the communication format. Female patient gender remained significantly associated with a higher use of purely verbal qualifiers compared to visual formats when controlled for practice type (i.e. a single workplace medical office vs. a primary care center with several physicians), duration of GP-patient relationship, patient subjective understanding, the ratio of patient talking time to total consultation time, and the clustering effect of the GP (OR 1.4, p = 0.039). The use of a visual format resulted in significantly higher subjective perceived patient understanding compared to pure verbal counseling (adjusted mean (SE) difference of 10.3 (2.7) points on the 0-100 VAS scale), which remained independently associated when controlled for patient age and gender, education, API, total counseling time, patient's self-assessed level of CVD risk and anxiety, and GP clustering effect (Figure 2). None of the other potential covariates analyzed showed any association with the communication format.

Discussion

The majority (73%) of primary care physicians participating in this study used exclusively verbal formats to communicate cardiovascular risk to their patients. The combination of numerical and visual formats was used to a minor degree, as was the combination of verbal and numerical formats. Our findings demonstrate a gap between the recommendations of medical associations, which favor numerical and visual formats for communicating risk, and the reality in clinical practice.

In our study, the frequency of the use of verbal formats in risk communication appeared to be associated with gender; female physicians communicated risk more often in verbal formats than male physicians. We found the same association, though to a lesser degree, in female patients, independent of the GP's gender. There are only few data existing on this gender issue in doctor-patient communication; a recent systematic review showed that female doctor-patient dyads are talking longer and combine different communication styles in one consultation in comparison to mixed or male dyads [24]. To our knowledge, the gender association in risk communication formats has not been described previously and merits further research. This tendency of female physicians and female patients to communicate exclusively in a verbal format should also be addressed in the development of medical education programs and tools.

The statistically quantifiable association between the use of visual formats and understanding rated by patients in our study is not necessarily translating into a clinically relevant benefit of understanding among patients. Though, it is consistent with data from the literature, which show that visual formats are easier to understand than other, especially verbal, formats [5][6][7]. Only a few studies address the visual formats used by the physicians in our study [25]. However, compared to verbal and numerical formats alone, findings for other visual formats such as "risk ladders" [26], population charts [27], pie charts [28], and histograms [29][30][31] suggest better understanding, increased risk perception, higher risk aversion, and better acceptance of interventions in patients. Restrictions on the use of visual formats should not be forgotten: depending on the skills of  14 (12)(13)(14)(15)(16)(17)(18) 19 (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24) 0.070 Data are given as median (IQR) or n(%) and do not necessarily sum to n = 77 due to missing values.The Kruskal Wallis test for continuous data and Fisher's exact test for categorical data were performed to test for overall effect across counseling formats. * p<0.05 vs. verbal, # p<0.05 vs. numerical and vs. verbal. a person to understand graphics [32] and the danger to manipulate patients by emphasizing parts of the graphic [33][34][35][36]. The same is true for numerical formats. Moreover, some visual formats (e.g., survival curves and scales) need additional verbal or numerical explanations to be sufficiently clear [37,38], and others, such as population figures, are not easier to understand than numerical formats [39]. The use of colors as additional information in visual formats, which was also used by participating physicians, seems to be powerful and familiar to patients, providing them with an important reference point about the severity of risk (e.g., the red color indicating urgency and necessity to stop proceeding in the same way as until now) [40].

Nevertheless, a high proportion of patients in our sample indicated that they subjectively understood the communicated risk fairly well when confronted with verbal qualifiers or numerical formats alone. Sixty-three percent of GPs used their preferred format without variation, which indicates that, in addition to the associations with doctor and patient gender, the choice of the communication format depends more on physician characteristics than those of the patient.

The difference between GPs' and patients' estimates of CVD risk and the anxiety of developing CVD is significant. Previous research already reported a high frequency of underestimation of CVD risk (and, to a minor degree, overestimation) among patients with CVD risk [19]. In the absence of biometric data from patients in our study population in order to calculate their CVD risk, it is not possible to tell whether rather patients' or GPs' estimate of risk is closer to the real CVD risks. The result is nevertheless noteworthy as it makes obvious that to a certain extent physicians are not able to fully transfer their risk estimation to their patients.

Strengths

This study is the first to provide data from a real clinical setting targeting the use of different formats in communication of CVRF between physicians and patients. We chose a study design that optimally handles desirability or reporting bias, in contrast to studies using selfreported data from questionnaires, as our main covariate (i.e. risk communication format) is not self-reported but recorded and objectively analyzed.

Limitations

Due to the small sample size, especially the number of GPs, the generalizability of our results is limited. The participation rate of doctors (1.9%) was low. We think that GPs are not used to making audio recordings of their own consultations, and this may be a major psychological barrier for participation. The drop-out rate of 37% was explained by the physicians who were willing to participate but unable to enroll patients because of their high work load and lack of time. Physician age, gender, and experience in ambulatory primary care in our sample matches well with the statistics reported by the FMH, but the sample size is far too small to be representative of the entire population of Swiss primary care doctors. Moreover, the recruitment strategy might have led to selection bias towards a group of doctors with more motivation and skills in communication techniques. However, this bias may support our findings as one would expect that less motivated colleagues might also be less likely to catch up with the recent recommendations of their medical associations.

Possible explanations of the findings

One reason for the high extent of verbal qualifier use compared to other formats might be that primary care physicians are not sure about the numerical facts regarding risk. Several studies suggest that, regardless of specialization, physicians often face problems understanding medical statistics [41][42][43]. Also, many of the physicians may not know the effects of different formats of risk communication on patient understanding and their emotional perception of risk. Many physicians might judge risk presentation as verbal "value" to be good enough, not being aware of the low correlation between objective risks and perceived risk in patients. Similarly, the need and desire of patients to obtain maximum information, which was also shown in our study by the API, might be underestimated by physicians. A second reason is that teaching activities regarding communication skills are still at a low level in the professional education of Swiss physicians. Consequently, many doctors do not feel comfortable with different communication techniques. Furthermore, analogous to findings in the use of calculation and communication tools to predict cardiovascular risk in primary care, doctors face many barriers, such as distrust in their validity or their contribution to encourage decision making, lack of time, and low reimbursement [44].

Another issue contributing to our observations is the trust and confidence of patients in their doctors. As we know from research in the field of shared decision making, many patients prefer not to decide themselves, but to leave the decision to the doctor [13], or prefer to know his opinion rather than being informed of facts [11]. Asked for a personal opinion, the physician may prefer verbal communication formats to others, taking the risk of inducing different meanings and confusion in patients. Similarly, by purposes like reassuring or persuading, GPs may prefer verbal formats, as was shown e.g. for clinical geneticists [45]. The asymmetry in mean talking time indicates a more one-sided sort of communication (with the physician as a source of information), rather than an interactive discussion among equal partners. Moreover, the straightforward use of verbal qualifiers by doctors is a time-saving approach not requiring any preparation time, unlike choosing adequate numbers or drawing graphs.

At present, several programs are in development in Switzerland, yielding to patient-centered health-promoting activities in primary care settings [46]. Within these programs, risk communication is a major issue. Visual formats like colour-coded graphics are emphasized, in order to transport information about risk to patients in the most understandable way and to facilitate discussion about risk between physician and patient [47].

Conclusion

In summary, our data demonstrate a gap between the recommendations from medical associations and clinical reality in communicating CVD risk. The verbal formats that are mainly used are rated lowest in recommendations regarding understanding and effectiveness. Similarly, the highly recommended formats, such as natural frequencies and visual formats like bar charts, were rarely or never used by the primary care physicians in our study. Visual formats resulted in significantly higher subjective understanding of the information given. Also, gender is significantly associated with the choice of communication formats, which was unknown thus far for CVD risk communication.

As implication for clinical practice, relevant barriers towards the use of "highly ranked" communication formats among doctors and patients are to be identified and addressed. Furthermore, strategies for improving communication skills among doctors should be developed, such as practicable tools and medical education programs. The gender aspect should be addressed, especially in regard to target groups of interventions. The results of our study stress the need for developing health-promoting programs in primary care that would more clearly focus on a transparent communication on risk. Our final intention is to close the gap between theory and daily clinical practice in the field of CVRF communication, which does not necessarily mean that doctors and patients have to change their communication style -it might lead to input for the further development of theoretical models adapted to reality.

List of abbreviations CVD: cardiovascular disease; CVRF: cardiovascular risk factor; VAS: visual analogue scale; FMH: Swiss federation of physicians; GP: general practitioner; IQR: interquartile range; API: autonomy preference index; SD: standard deviation.

5 points (SD 17.3). For the estimates of the anxiety of developing CVD, the mean estimate of GPs was 31 (range: 1-98), the mean estimate of patients 26 (range: 0-100). On average, the estimates of GPs and patients differed by 16.0 points (SD 16.4) in the direct comparison.

Figure 1 Figure 2
12Applied risk communication format depending on the gender of the GPs (bars show the frequencies of consultations conducted by female GPs and male GPs). Association between the subjectively perceived level of understanding and the applied risk communication format. Difference between the communication formats regarding to the mean estimates of subjectively perceived unterstanding: p = 0.001 for visual vs. verbal format and p = 0.12 for visual vs. numerical format.

Table 1
1Baseline characteristics of physicians (n = 22) and patients (n = 77) Software Package (SPSS version 14, SPSS Inc, Chicago, Illinois).Physician characteristics Median
IQR
n
% of cases

Age, years
46.5
38-57

Experience as a GP, years 11
5-20

Workload, % (100% = 5
days working per week)

100
77.5-100

Sex, males
14
63.6
Practice type, solo
9
40.9

Practice location, urban
10
45.5

rural
12
54.5

Patient characteristics

Age, years
51
45.5-59

Sex, male
45
58.4

Ethnicity, Swiss origin
66
86.8
Education level, Primary
11
14.3

Secondary
38
49.4

High school
5
6.5

Academic
23
29.9

Number of cardiovascular
risk factors = 1

49
63.3

2
23
29.9

3
5
6.5

Cardiovascular risk factor

Lipid disorder
41
53.2
Hypertension
45
58.5

Tobacco smoking
24
31.2

Total
110
142.9

Table 2
2Patient and GP characteristics and communication formatsCharacteristic

AcknowledgementsThe authors would like to thank all of the GPs and their assistants who collected data for this study, as well as all the patients who took part. We also thank Helen Binnerts for the transcription of the interviews. Funding was received from the Swiss Academy of Medical Sciences (SAMW). The funding agency had no role in the design process, the data collection, the analysis, and the interpretation of data, nor in the writing of the manuscript or the decision to submit the manuscript for publication.Authors' contributions SNJ conceived the study, carried out data collection, performed statistical analysis and drafted the manuscript. OW participated in the design and writing of the manuscript. OS participated in statistical analysis and writing of the manuscript. JS and TR participated in the design of the study. All authors read and approved the final manuscript.Competing interestsThe authors declare that they have no competing interests.
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Diagnostic Pathology Use of virtual slide system for quick frozen intra-operative telepathology diagnosis in Kyoto, Japan

Yasunari Tsuchihashi
Louis Pasteur Centre for Medical Research
12-7 Taniguchi Kakinouchi616-8012Ukyo, KyotoJapan

Terumasa Takamatsu
CLARO Inc
56-10036-8203Honcho, Hirosaki, AomoriJapan

Yukimasa Hashimoto
Yamashiro Public Hospital
74-1Kizu-Ikeda, KizuKyotoJapan

Tooru Takashima
Yamashiro Public Hospital
74-1Kizu-Ikeda, KizuKyotoJapan

Kooji Nakano
Yamashiro Public Hospital
74-1Kizu-Ikeda, KizuKyotoJapan

Setsuya Fujita
Louis Pasteur Centre for Medical Research
12-7 Taniguchi Kakinouchi616-8012Ukyo, KyotoJapan

Diagnostic Pathology Use of virtual slide system for quick frozen intra-operative telepathology diagnosis in Kyoto, Japan
10.1186/1746-1596-3-S1-S6BioMed Central Page 1 of 2 (page number not for citation purposes) Proceedings * Corresponding authors
We started to use virtual slide (VS) and virtual microscopy (VM) systems for quick frozen intraoperative telepathology diagnosis in Kyoto, Japan. In the system we used a digital slide scanner, VASSALO by CLARO Inc., and a broadband optic fibre provided by NTT West Japan Inc. with the best effort capacity of 100 Mbps. The client is the pathology laboratory of Yamashiro Public hospital, one of the local centre hospitals located in the south of Kyoto Prefecture, where a fulltime pathologist is not present. The client is connected by VPN to the telepathology centre of our institute located in central Kyoto. As a result of the recent 15 test cases of VS telepathology diagnosis, including cases judging negative or positive surgical margins, we could estimate the usefulness of VS in intra-operative remote diagnosis. The time required for the frozen section VS file making was found to be around 10 min when we use ×10 objective and if the maximal dimension of the frozen sample is less than 20 mm. Good correct focus of VS images was attained in all cases and all the fields of each tissue specimen. Up to now the capacity of best effort B-band appears to be sufficient to attain diagnosis on time in intra-operation. Telepathology diagnosis was achieved within 5 minutes in most cases using VS viewer provided by CLARO Inc. The VS telepathology system was found to be superior to the conventional still image telepathology system using a robotic microscope since in the former we can observe much greater image information than in the latter in a certain limited time of intra-operation and in the much more efficient ways. In the near future VS telepathology will replace conventional still image telepathology with a robotic microscope even in quick frozen intra-operative diagnosis.

Introduction

The practical applications of virtual slide (VS) or virtual microscopy (VM) system have been confined to such fields as education, conferences or consultations, where we are allowed enough time to digitize whole a slide specimen and make up a VS before starting observation. How-from 9th European Congress on Telepathology and 3rd International Congress on Virtual Microscopy Toledo, Spain. 15-17 May 2008 ever through the recent rapid technical progresses of digital slide scanner for VS, the time required for making up a VS file is greatly shortened to the order of 10 min or so, so that we can now utilized VS and VM for quick frozen intra-operative telepathology diagnosis. For the last 15 years our telepathology project in Kyoto, Japan has been conducted using a static image telepathology system equipped with a remote controllable robotic microscope [1]. The system can now be called "conventional", in contrast to the "novel", VS telepathology system. In this paper we report our first trial of applying VS telepathology system to quick frozen intra-operative telepathology diagnosis. Merits of the use of VS system will be discussed.

Materials and methods

We used a highly elaborate digital slide scanner, VAS-SALO, by CLARO Inc., Aomori, Japan [2] in a client pathology laboratory of Yamashiro Public Hospital in the south of Kyoto, Japan, where fulltime pathologist is not present by a well-trained cytotechnician is present. The client terminal is connected to our telepathology diagnostic centre in central Kyoto by a broadband optic fibre provided commercially by NTT-Wes Inc., Japan that has a best-effort capacity of 100 Mbps. The broadband was used solely for image data transmission and the client terminal and our telepathology diagnostic centre formed a VPN, called a B-Flets group. The time required for VS making of each frozen section was measured. At the same time, the time and accuracy of the remote observation of the VS by a VS viewer provided by CLARO Inc. were checked and recorded. Usefulness of VS telepathology diagnosis is estimated in terms of time required, VS quality, and of accuracy of diagnosis. The VS telepathology diagnosis was compared to those by conventional telepathology system by making diagnoses using VS and conventional systems successively for a same frozen section slide specimen.

Results

In the last 6 months we conducted 15 test cases of quick frozen VS diagnosis. The time required for VS making was around 10 min if we use ×10 objective and if the specimen measures less than 20 mm in the maximal dimension. VS making was successful for all the tissue section cases. i.e., good focus of VS images was achieved in all the frozen section cases and in all the tissue fields of each case. Telepathology observation and diagnosis by VS viewer were achieved within 5 min and all the telepathology diagnoses were correct. The best effort type B-band optic fibre maintained sufficient capacity to attain remote diagnosis on line and on time.

Discussion

Owing to the rapid and accurate digitalization of the whole of a glass slide specimen by VASSALO it was now clear that we can successfully use VS telepathology system even for quick frozen intra-operative telepathology diagnosis where time is quite limited for a technician and a remote pathologist. Telepathology diagnosis was easier and more comfortable in the novel VS telepathology system than in the conventional telepathology system since we can obtain desired images easier in VS system than in the conventional system. We can attain much greater image information processing in the VS system than in the conventional telepathology system in a certain limited time.

Conclusion

VS system was used for quick-frozen intra-operative telepathology diagnosis in Kyoto, Japan. The VS system was found to attain correct diagnosis on time, i.e., VS making within 10 min and VS telepathology observations/diagnoses within the next 5 min. The novel VS telepathology system was found to be superior to the conventional still-image system in terms of time required for diagnosis and of ease and accuracy of the diagnosis. The use of VS system will be expanded from education to actual diagnosis including quick frozen intra-operative diagnosis. In the near future the conventional telepathology system to support regional medicine will be replaced by VS telepathology system.
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AcknowledgementsThis article has been published as part of Diagnostic Pathology Volume 3 Supplement 1, 2008: New trends in digital pathology: Proceedings of the 9th European Congress on Telepathology and 3rd International Congress on Virtual Microscopy. The full contents of the supplement are available online at http://www.diagnosticpathology.org/supplements/3/S1
Yasunari Tsuchihashi, Masahiro Morishima, Kanae Nakasato, Ikuo Tofukuji, Setsuya Fujita: Shift to the broadband in practical telepathology in Kyoto, Japan. Abstract. 8th European Congress on Telepathology and 2nd International Congress on Virtual Microscopy. 91Yasunari Tsuchihashi, Masahiro Morishima, Kanae Nakasato, Ikuo Tofukuji, Setsuya Fujita: Shift to the broadband in practical telepathology in Kyoto, Japan. Abstract. 8th European Congress on Telepathology and 2nd International Congress on Virtual Microscopy 2006:91.