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British Journal of Radiology 75 (2002),17-23 © 2002 The British Institute of Radiology

Full paper

Hepatic haemodynamics: interrelationships between contrast enhancement and perfusion on CT and Doppler perfusion indices

M A Fuentes, MBBS1, C J Keith, MBBS1, M Griffiths, BSc, MAppSc2, G Durbridge, PGrad Dip SC, MAppSc1 and K A Miles, MBBS, FRCR, MSc, MD2

1Southern X-ray Clinics, 2nd Floor, Day Centre, The Wesley Hospital, 451 Coronation Drive, Auchenflower, Queensland 4066 and 2Centre for Medical, Health and Environmental Physics, Queensland University of Technology, 2 George Street, Brisbane, Queensland 4000, Australia

Correspondence: Dr C Keith


   Abstract
Top
 Abstract
Introduction
 Materials and methods
 Results
 Discussion
 References
 
This study compares three techniques that evaluate hepatic haemodynamics for the detection of metastatic liver disease to determine the interrelationships between the techniques and to assess their equivalence. The three techniques studied were dedicated CT measurements of hepatic enhancement, CT measurements of perfusion and Doppler perfusion indices. 53 patients with proven malignancies of either breast or colon underwent a single location dynamic CT for measurement of hepatic perfusion and enhancement, whilst a subset of 12 patients underwent both CT perfusion and Doppler perfusion studies. Statistically significant correlations were found between CT arterial phase enhancement and CT arterial perfusion (r=0.612, p<0.001), and between both of these parameters and Doppler arterial flow (r=0.867, p<0.001 and r=0.842, p<0.001, respectively). Significant correlations were also found between both the ratio of CT arterial enhancement to peak enhancement and the CT arterial perfusion with the Doppler perfusion index (r=0.797, p=0.002 and r=0.725, p=0.008, respectively). Combined CT arterial and portal perfusion correlated with peak liver enhancement (r=0.614, p< 0.001), but Doppler measurements of portal flow did not correlate with any CT parameter. Increased arterial enhancement, perfusion or flow are valuable additional radiological signs for the presence of hepatic metastases that can be elicited by incorporating any one of these methods into existing imaging protocols.


   Introduction
Top
 Abstract
 Introduction
Materials and methods
 Results
 Discussion
 References
 
Accurate staging of malignancy involving the liver is an important step in the treatment of oncology patients. Unfortunately, the methods currently used to detect distant metastases are unable to detect micrometastatic disease in the liver. At least 30% of patients undergoing curative resection for colorectal cancer have liver metastases that are too small to be detected on conventional imaging [1]. At present, a lesion must beat least 3–4 mm in diameter to be reliably detected with contrast enhanced CT or MRI. Although very sensitive to extrahepatic disease, positron emission tomography (PET) has been shown to be only equivalent to CT in the detection of liver metastases [2]. Ultrasound, such as that used in intraoperative surgical examination, has been able to depict superficial liver lesions 2 mm in diameter [3]. To adequately stage patients and thus optimize treatment, the resolving power of imaging techniques needs to be improved so that lesions less than 2 mm in diameter become detectable.

Altered hepatic haemodynamics may imply the presence of metastases, even in the absence of overt structural lesions. The biological principle underlying this is that tumour angiogenesis within liver metastases is reflected by changes in hepatic haemodynamics. These functional changes are frequently detectable before any structural abnormality is apparent, as it is the degree of physiological change within a lesion rather than its size (i.e. structure) that determines whether an abnormality is detected. Using CT, Cuenod et al [4] have demonstrated changes in hepatic perfusion with experimental metastases of an average size of only 500 µm.

Many different techniques have been proposed to detect altered hepatic haemodynamics. Using radionuclides, Parkin et al [5] showed that the hepatic arterial/portal ratio, or hepatic perfusion index (HPI), was significantly higher in those patients who had liver metastases than in normal controls. In a prospective study of colorectal patients, Warren et al [6] showed that a positive predictor of poor outcome (i.e. metastases) is an elevated HPI prior to surgery. Two CT techniques have also been proposed: specific measurements of hepatic perfusion and measurements of liver attenuation during the arterial phase of contrast enhancement. Hepatic metastases are associated with increased arterial perfusion [7] and increased arterial phase enhancement [8]. CT hepatic perfusion images can depict occult disease [9], and, in the absence of overt lesions, increased arterial phase enhancement heralds the development of metastases in the subsequent 18 months [10, 11]. Similarly, colour Doppler has been used to show that the Doppler perfusion index (DPI) is abnormal in patients with liver metastases, and that the DPI is better at predicting outcome than is the Duke's classification [12, 13]. In a comparative study between normal controls and those with hepatic metastases, Guadagni et al [14] showed that the DPI was higher in those with metastases.

For the most part, these different techniques for assessing hepatic haemodynamics have been developed independently. Thus, the extent to which the results of one technique can be extrapolated toanother is unknown. The only comparative study to date has shown a significant correlation between CT perfusion values and radionuclide measurements of HPI [15]. The aim of this study is to compare three techniques, dedicated CT measurements of hepatic enhancement, CT measurements of perfusion and Doppler perfusion indices, so as to determine the interrelationships between them and to assess their equivalence.


   Materials and methods
Top
 Abstract
 Introduction
 Materials and methods
Results
 Discussion
 References
 
Patients
This study consisted of 53 patients (28 females, 25 males) with a mean age of 61.45 years (range 33–87 years). All patients underwent a single location dynamic CT for measurement of hepatic perfusion and enhancement, whilst a subset of 12patients underwent both CT perfusion and Doppler perfusion studies. Patients were fasted for at least 6 h prior to being scanned, and the CT and ultrasound examinations were performed within 1 h of each other. All patients had proven malignancies of either the colon (49 patients) or breast (4 patients). 22 patients displayed overt metastases on structural imaging. Separate readers, who were blinded to the results of the other technique, reviewed the ultrasound and CT examinations. In all cases, perfusion CT was included within a clinically indicated conventional CT as part of an ongoing study approved by the Hospital Ethics Committee. Informed written consent was obtained from all patients.

CT image acquisition
A single location dynamic sequence of images was acquired at the appropriate level as determined from a conventional series of unenhanced helical images (CT Twin; Elscint, Haifa, Israel). Patients were instructed to breathe quietly throughout the duration of the scan and to avoid any deep breaths. Oral contrast medium was used in every examination (Ioscan 10 ml, sodium diatrizoate 3.705 g; Iotech, Rosebery, Australia). 50 ml of iv contrast medium was injected through an 18 G cannula at 7 ml s-1 (Isovue 370, 370 mg iodine ml-1; Bracco, Milan, Italy).

A section thickness of 10 mm was selected. The section for study was chosen to include any focal liver lesions or, if no focal lesions could be identified, a mid liver section was selected to minimize potential movement artefact. If possible, the spleen was included in the section. The first image in the series was obtained at the same time as the contrast medium injection was commenced, giving an unenhanced image to use in determining baseline attenuation values. Data acquisitions of 1 s duration were then performed every 3 s for approximately 35 s. Images were reconstructed and transferred to a personal computer for analysis.

CT data analysis
The CT images were exported via DICOM to Winfun (University of Cambridge Radiology Department, Cambridge, UK), a PC-based program developed for the determination of CT perfusion. A region of interest (ROI) was drawn within the aorta and the margins of the liver and spleen. ROIs are made as large as possible while at the same time avoiding partial volume effects. Thresholding was performed to eliminate regions containing fat or bone by excluding all pixels less than -50 HU or greater than 200 HU. Pixels experiencing a fall of 10 HU or more during the sequence compared with the initial baseline image were also removed from calculations. Time–attenuation curves were generated for the liver, spleen and aorta.

Hepatic enhancement measurement
Time–attenuation data from the aortic area ofinput were used to determine peak aortic enhancement. The liver receives an influx of contrast medium at two different times owing todelay as part of the bolus traverses the splanchnic vasculature to arrive in the portal vein later than in the hepatic artery. Therefore, to ensure a measure of purely arterial enhancement, CT attenuation was measured at 5 s prior to the time of splenic peak attenuation and baseline attenuation was subtracted (Espleen-5). Peak liver enhancement (Epeak) was also measured and the ratio Espleen-5/Epeak was calculated.

Hepatic perfusion measurement
The technique has been described in detail elsewhere [15]. Perfusion values, expressed as blood flow per unit volume of tissue (ml min-1 ml-1) were calculated using the equation: Go


Using the above equation, the maximum rate of enhancement prior to the splenic peak and the aortic peak gave the arterial perfusion. The maximum rate of enhancement after the splenic peak and aortic peak was used to obtain the portal perfusion. The HPI was calculated to express the proportion of total liver perfusion that is arterial, as given by: Go


where AP is arterial perfusion (ml min-1 ml-1) and PP is portal perfusion (ml min-1 ml-1).

Measurement of DPI
Doppler studies were performed using a commercially available ultrasound unit with duplex and colour Doppler facilities (Gateway fx; Diasonics, Bedford, UK). All studies were performed with a 3.5 MHz convex linear array probe. For Doppler studies, the transducer frequency was 2.4 MHz with a pulse repetition frequency of between 1 kHz and 9 kHz.

Values for DPI were obtained using the technique previously described by Leen et al [12]. Hepatic arterial Doppler traces were obtained from the common hepatic artery with the patient supine. Portal vein traces were obtained with thepatient in an oblique position, 45° to the left.Doppler traces were obtained during suspended respiration. The angle of insonation varied between 53° and 68°. The Doppler gate was opened to encompass the entire width of the vessel, with the resulting diameter used for determination of the vessel cross-sectional area, as required for calculation of volume flow.

Volume flows were calculated for the hepatic artery and the portal vein from the product of the time-averaged blood velocity and the cross-sectional area for each vessel. The DPI was determined from the hepatic artery blood flow volume divided by the total (hepatic arterial and portal) liver blood flow volume.

Statistical analysis
Regression analyses were performed using Microsoft Excel. A comparison was made between CT enhancement values and CT perfusion values. Both CT enhancement and CT perfusion measurements were then compared with the results of the Doppler ultrasound examinations. An r-value >0.7 was considered a good correlation, r=0.4–0.7 a moderate correlation and r< 0.4 a poor correlation. A p-value of < 0.05 was taken to be statistically significant for a single independent test. Where multiple comparisons between the three techniques were made, a Bonferroni adjustment requires that individual p-values be <0.015 to ensure an overall p-value of 0.05.


   Results
Top
 Abstract
 Introduction
 Materials and methods
 Results
Discussion
 References
 
The ranges for values of CT perfusion parameters and DPI were comparable with those for amixed group of patients with and without metastases found in previous publications [9, 12–14, 16–18]. Statistically significant correlations of a moderate nature were found between CT arterial enhancement and CT arterial perfusion (r=0.612, p<0.001), CT arterial enhancement and CT HPI (r=0.482, p<0.001) and CT peak enhancement and CT total perfusion (r=0.614, p<0.001). Table 1Go provides a summary of the correlations between CT enhancement and CT perfusion measures.


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  		Table 1. r- and p-values for correlation between CT enhancement measures and CT perfusion measures

 
Statistically significant good correlations were found between CT arterial enhancement, CT arterial perfusion, CT total perfusion and CT HPI with Doppler arterial flow (r-values=0.867, 0.842, 0.809 and 0.815, respectively; p-values all <0.001). A significant correlation was also found between both the ratio of CT arterial enhancement to peak enhancement and CT arterial perfusion with DPI (r=0.797, p=0.002 and r=0.725, p=0.008, respectively). Moderate correlations were found between CT arterial enhancement to peak enhancement with Doppler arterial flow (r=0.62, p=0.031), and CT total perfusion and CT HPI with DPI (r=0.672, p=0.017 and r=0.677, p=0.016, respectively). Doppler measurements of portal venous flow demonstrated no correlation with any CT parameter (see Table 2Go).


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  		Table 2. r- and p-values of CT enhancement measures and CT perfusion measures correlated against Doppler perfusion measures

 
Figure 1Go displays the correlation between CT arterial enhancement and CT arterial perfusion with Doppler arterial flow.



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  		Figure 1. CT arterial enhancement ( x ) and CT arterial perfusion (•) against Doppler arterial flow.

 

   Discussion
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
References
 
There is an increasing body of evidence that assessment of liver haemodynamics can aid the detection of hepatic metastases. The processes that lead to altered hepatic haemodynamics in the presence of metastases are complex (see Figure 2Go). All tumours, whether primary or secondary, must establish their own blood supply to promote growth. This process is known as angiogenesis orneovascularization. Within the liver, the new blood vessels are derived almost exclusively from the arterial system [19, 20]. Portal connections may exist but are generally draining veins [21, 22]. Thus, angiogenic changes due to hepatic metastases will lead to increased arterial perfusion. Additional factors result in alterations in the portal circulation. Compression of portal radicles by metastases as well as margination of white blood cells in portal vessels result in reduced portal flow [23]. Humoral factors that reduce portal flow have also been proposed [16]. These changes in the portal circulation also have important secondary effects upon arterial flow owing to the physiological buffer response. The buffer response results from admixture of blood within the liver sinusoids and describes the reciprocal increase in arterial flow that occurs when portal flow is reduced. This response is well recognized in the human liver but may be less prominent in other species [2]. The processes that reduce portal perfusion therefore further amplify the increased arterial perfusion that results from neovascularization. Without this amplification, the changes from arterialization alone may not be detectible, particularly for micrometastatic disease where the proportion of liver replaced by tumour is very small.



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  		Figure 2. Factors contributing to altered hepatic perfusion with metastases.

 
Changes in CT measurements of liver perfusion and enhancement as well as Doppler ultrasound can be considered physiological correlates for the microvascular processes described above. Arterialization of metastases will be directly related to the increased arterial perfusion measured on CT as well as increased hepatic arterial flow on Doppler ultrasound. Similarly, changes in the portal microcirculation would be anticipated to translate to reduced portal perfusion and portal venous flow measurements, and both effects will combine to produce increased HPI and DPI. Hepatic parenchymal enhancement will reflect these haemodynamic changes. The degree of hepatic enhancement in the arterial phase is directly dependent upon the arterial perfusion, whereas peak hepatic enhancement will reflect a combination of arterial and portal perfusion. The ratio of arterial phase enhancement to peak hepatic enhancement would therefore be equivalent to the HPI.

The correlations observed in this study largely confirm the relationships outlined above. Significant correlations were found between CT measurements of arterial perfusion and arterial phase enhancement. Peak hepatic enhancement correlated most closely with combined arterial and portal (i.e. total) perfusion, although it appeared to be more closely related to arterial than to portal perfusion. There was also a significant but weak correlation between the ratio of arterial to peak hepatic enhancement and HPI. The fact that the correlations between hepatic perfusion and enhancement are only moderate or weak can be explained by the fact that, for a given dose of contrast medium, tissue enhancement is not only determined by perfusion but also by the patient's weight and cardiac output. The diagnostic reliability of hepatic enhancement measurements could potentially be improved by administering contrast medium on a dose per weight basis, or by using corrections such as the recently proposed standardized enhancement value (SEV) [17].

Doppler ultrasound measurements of hepatic arterial flow correlated strongly both with CT measurements of perfusion and with CT enhancement (Figure 1Go). On the other hand, Doppler measurements of portal venous flow demonstrated no correlation with any CT parameter. Although the DPI correlated with the ratio of arterial to peak liver enhancement, a similar correlation was also found between DPI and CT arterial perfusion measurements. There are several potential explanations for the lack of correlation between CT and ultrasound assessments of portal haemodynamics. An important difference between CT and ultrasound is that CT assesses perfusion (i.e. blood flow per ml of liver tissue) whereas ultrasound assesses total liver blood flow. An increase in the size of the liver could, in itself, result in an increase in total liver flow but produce no change in perfusion at tissue level. Liver size is clearly an important consideration for patients with metastases. A further consideration is that hepatic portal perfusion is not accurately assessed by either of the CT techniques used in this study. The slope of the liver time–attenuation curve in the portal phase will be underestimated owing to the fact that increasing portal phase enhancement occurs at a time when arterial enhancement is falling as a result of venous washout of contrast medium delivered to the liver via the arterial system. Second, use of the aorta as the input function will not take into account the bolus spreading that occurs as contrast medium passes through the spleen and gut. Corrections for these sources of error have been proposed but increase the complexity of the technique [18]. Measurements of portal phase enhancement would be similarly affected.

The method used in this study to measure arterial phase enhancement on CT differs from that originally described by Platt et al [8] and subsequently adopted by Sheafor et al [11]. Platt et al performed hepatic enhancement measurements as part of a three-phase contrast enhanced spiral CT examination using 150 ml of contrast medium administered at 3 ml s-1. Arterial phase enhancement was determined from the images acquired 25 s after commencement of contrast medium injection. To enable comparison of perfusion measurements and arterial enhancement measurements within one examination, and because a three-phase examination is not standard practice at our institution, we elected to determine arterial phase enhancement from liver time–density curves derived from a single location dynamic sequence following a 50 ml bolus of contrast medium given at 7 ml s-1. On the basis that the time of peak splenic enhancement can be used to separate hepatic arterial and portal phases [15], hepatic enhancement 5 s prior to the time of peak splenic enhancement was used to provide a consistent measure of arterial phase enhancement with no portal contribution.

Notwithstanding the above differences in CT and Doppler assessments of the portal circulation, it is unclear whether a portal assessment needs to be included as part of the evaluation of hepatic haemodynamics for the detection of micrometastases. Leen et al [12] did include a portal assessment in their work reporting that Doppler ultrasound can identify those patients with colorectal cancer who are at an increased risk of developing hepatic metastases. A separate study by Guadagni et al [14], however, found that hepatic arterial flow alone, but not the DPI, was significantly increased in patients with metastases. Similarly, Leggett et al [7] found that arterial perfusion more reliably distinguished patients with and without metastases than did HPI. Furthermore, Platt et al [10] report that increased arterial phase enhancement heralds the subsequent development of overt metastases. Thus, an assessment of the arterial circulation alone, by whichever method, may be all that is required for detection of metastatic liver disease. The results of this study indicate that all methods for assessing the arterial circulation are broadly equivalent.

Given the equivalence of all three methods to assess arterial haemodynamics for the detection of hepatic metastases, and given that all three methods are readily incorporated into existing imaging protocols, the question arises as to which is the appropriate method to choose. This choice is likely to be determined by the existing conventional imaging strategies in use at any particular institution for a given tumour type. For instance, some centres may consider ultrasound the most appropriate conventional imaging technique for detection of hepatic metastases in patients with tumour types such as breast cancer that demonstrate a low preponderance for retroperitoneal spread. For these patients, inclusion of Doppler ultrasound into the existing assessment would be the most expedient way of using hepatic haemodynamics to improve the detection of metastases, thereby avoiding the inconvenience and expense of an additional CT. On the other hand, CT may be considered the most suitable conventional imaging technique for patients with tumours such as colorectal cancer that are known to spread to the liver and retroperitoneal lymph nodes. For these patients, hepatic haemodynamics would be most conveniently assessed with one of the CT techniques.

The two CT techniques each have their own advantages and disadvantages. Assessment of arterial phase hepatic enhancement, as originally described by Platt et al, utilizes a three-phase examination with spiral acquisitions before contrast medium administration, during the arterial phase and during the portal phase. This technique is associated with a relatively high radiation dose and, because no dedicated software is currently available, attenuation measurements can be quite time consuming. Dedicated CT perfusion measurements, on the other hand, require a dedicated single slice technique and specialized software. If current imaging strategies within an institution adopt a three-phase examination technique to optimize detection of structural liver lesions, then measurements of arterial phase enhancement would be the easiest method to evaluate hepatic haemodynamics. Otherwise, provided that suitable software is available, the benefits of absolute quantification in physiological terms, inherent corrections for cardiac output and contrast medium dose, and lower radiation burden favour the use of dedicated CT perfusion measurements.

The availability of a range of methods for evaluating hepatic haemodynamics may have impeded general acceptance of any technique for detection of metastatic disease to the liver, with potential users uncertain as to which method to adopt. This study is the first to compare the various CT and Doppler ultrasound techniques that have been proposed, and indicates that all methods for assessing the hepatic arterial circulation are broadly equivalent. Increased arterial enhancement, perfusion or flow are valuable additional radiological signs for the presence of hepatic metastases that can be elicited by incorporating any one of these methods into existing imaging protocols.


   Footnotes
 
Funding was provided by The Wesley Research Institute. Back

Received for publication May 24, 2001. Revision received September 18, 2001. Accepted for publication September 24, 2001.


   References
Top
 Abstract
 Introduction
 Materials and methods
 Results
 Discussion
 References
 

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