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Ultrasonography |
1 From the Departments of Radiology (A.L., P.H., G.F., D.G., J.A.L., O.C.) and Head and Neck Surgery (F.P., V.B., P.B., P.A.), Hôpital Européen Georges Pompidou, 20 rue Leblanc, 75908 Paris Cedex 15, France. Received June 29, 2000; revision requested August 8; revision received November 20; accepted March 23, 2001. Address correspondence to O.C. (e-mail: clement@necker.fr).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Between October 1995 and June 1998, a total of 145 patients who had oropharyngeal tract cancer and who were fitted with the same totally implantable central venous catheters (CVCs) were included in the study. Follow-up included (a) estimation of the position of each catheter tip on a chest radiograph obtained immediately after surgery and (b) regular monthly Doppler US screening for catheter-related DVT.
RESULTS: Seventeen patients developed catheter-related DVT; 13 of them were asymptomatic. The mean interval between CVC implantation and detection of thrombosis was 42.2 days. Correct positioning of the distal catheter tip was associated with a significantly lower rate of catheter-related DVT. Only five of 87 patients with a correctly positioned distal catheter tip (ie, either in the superior vena cava or at the junction between the right atrium and the superior vena cava) developed thrombosis, compared with 12 of 26 patients with a misplaced catheter (P < .001). The side on which the CVC was implanted did not influence the catheter-related DVT rate.
CONCLUSION: The rate of asymptomatic catheter-related DVT is high and could be lowered with correct initial CVC positioning.
Index terms: Catheters and catheterization, complications, 907.442, 91.442, 94.442, • Chemotherapy, complications, 907.442, 91.442, 94.442 • Embolism, pulmonary, 60.721 • Veins, thrombosis, 94.442 • Veins, US, 94.12983, 94.12984
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Numerous risk factors have been established for catheter-related DVT; material, diameter, and positioning of the catheter account for most of them. For instance, clinical and in vitro studies have demonstrated that both polyurethane and silicone catheters are associated with a lower rate of catheter-related DVT (7,8), as compared with polyethylene or Teflon-coated catheters. Lokich and Becker (9) reported that an external catheter diameter of less than 2.8 mm is also linked to a lower rate of catheter-related DVT. The same authors have also reported that incorrect placement of a CVC in the superior vena cava results in a higher incidence of catheter-related DVT. It has also been reported that implantation of the CVC in the left subclavian vein carries a far greater risk of catheter-related DVT than implantation in the right vein, although no clear explanation has been suggested for this.
More recently, attention has focused on risk factors that are independent of the catheter. For instance, acquired blood coagulation disorders are commonly reported in cancer patients (10) and may be linked to the histologic findings of the tumor involved or to the type of chemotherapy used (11). There are numerous possible risk factors for catheter-related DVT, and this makes it difficult to assess the individual contribution of each factor. Moreover, most of the previously reported studies that focused on catheter-related DVT were based either on clinically symptomatic thromboses or on phlebography. In the first case, the incidence of catheter-related DVT is probably underestimated. In the latter case, phlebography itself could be responsible for some phlebitic reactions (12). The true incidence of catheter-related DVT is therefore difficult to determine.
Only a few investigators have used prospective Doppler ultrasonographic (US) screening for catheter-related DVT. In a previously published study (13), a 9% rate of asymptomatic catheter-related DVT was found in cancer patients. However, two different CVC sets were used, and specific Doppler US criteria for DVT were not evaluated. Furthermore, no risk factor for catheter-related DVT was identified.
This prospective study of 145 patients that extended for more than 3 years had two objectives: (a) to use Doppler US to estimate the incidence of asymptomatic catheter-related upper extremity DVT in a large population and (b) to study the effect of the catheter position as an individual risk factor for catheter-related DVT.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Patients
Between October 1995 and June 1998, CVCs were implanted in 145 consecutive patients (19 women and 126 men; mean age, 58.5 years; age range, 34–84 years) and were used to administer neoadjuvant chemotherapy for oropharyngeal tract cancer. The primary neoplastic sites included six nasopharyngeal, 46 oropharyngeal, 41 hypopharyngeal, 35 laryngeal, and 17 buccal tumors. Tumor staging according to the Union Internationale Contre le Cancer (UICC) 1988 TNM classification is summarized in Table 1.
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Catheter Maintenance
The same type of catheter was used for all of the patients and consisted of totally implantable ports with silicone-coated catheters (Braun Celsite ST 301; Braun Celsa, Chasseneuil, France). The catheters were surgically positioned with general anesthesia during the initial diagnostic endoscopy. The subclavian vein contralateral to the tumor was punctured. This procedure has been described in detail elsewhere (5). The ideal position of the catheter tip was considered to be the junction between the right atrium and the superior vena cava. Qualified nurses were responsible for maintaining all of the catheters, which were carefully flushed with heparin solution after each infusion. The CVC was flushed with 10 mL of saline solution and then filled with 5 mL of a solution containing 50 IU of heparin sodium (Heparine Sodique; Dakota, Créteil, France) per milliliter. The catheter type, chemotherapy protocol, and port maintenance were the same for all 145 patients, none of whom had any history of DVT.
Imaging Follow-up
The position of each catheter was determined on an immediate conventional postoperative anteroposterior chest radiograph, which was retrospectively reviewed by two radiologists (A.L., D.G.) and assessed in consensus on the basis of three parameters. First, the CVC implantation in the left or the right subclavian veins was assessed. Second, the exact position of the distal tip of each catheter was assessed in terms of five venous segments (Fig 1): segment 1, right atrium and superior vena cava junction; 2, superior vena cava; 3, junction between superior vena cava and the innominate veins—catheters were classified into segment 3 if their distal tip was not vertical, as in segment 2, but rather horizontal, as in segment 4, and in alignment with the superior vena cava; 4, innominate (or brachiocephalic) veins; and 5, aberrant topography, including right atrium and jugular veins. Third, the estimated length of the catheter between the CVC port and the distal tip was assessed.
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DVT screening was performed by using prospective US scans. US was performed during the 1st month after the catheter was installed and was repeated monthly for at least 3 consecutive months, covering three neoadjuvant chemotherapy cycles (Fig 2). Patients who kept their CVC in place after 3 months continued to undergo monthly US. All US scans were obtained with a Sonolayer model SSA-270A (Toshiba, Tokyo, Japan) by one radiologist (either D.G. or J.A.L.) using a 5.0-MHz linear-array transducer and standardized machine settings in a preset carotid arterial imaging program. Longitudinal and transverse US scans of the internal jugular vein and the subclavian vein were obtained. Color Doppler and spectral Doppler scans of these vessels were also obtained. Thrombosis was identified on the basis of three US signs: (a) lack of normal vein compressibility, (b) lack of color signal from the vessel on the color Doppler scan, and (c) lack of signal from the vessel on the spectral Doppler scan. The mean elapsed time (in days) between catheter placement and catheter-related DVT was noted for each patient.
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Statistical Analysis
We tested for statistical links between the incidence of catheter-related DVT and the length of the CVC, the side of implantation, and the position of the distal tip. Patients were assigned to two groups: Patients in group A had the distal CVC tip in segments 1 or 2; and in group B, the CVC tip was in the other segments (ie, incorrectly positioned). Data related to thrombosis for these two groups were compared by using a modified 
2 test for small expected values with Yates correction. The mean catheter lengths in the patients who developed thrombosis and those who did not were compared by using the Student t test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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During the first 3 months after CVC implantation, 17 (11.7%) of 145 patients developed catheter-related DVT. All thromboses were ipsilateral to the catheter; nine patients displayed combined subclavian and internal jugular venous thrombosis. Four patients presented with isolated internal jugular venous thrombosis, and the remaining four patients displayed isolated subclavian venous thrombosis. In none of these 17 patients was the disease spread (in particular, regional lymph node involvement as assessed with clinical examination and US) associated with thrombosis.
The clinical staging in the patients with catheter-related DVT is summarized in Table 2. Four patients (24%) with catheter-related DVT were symptomatic: two patients complained of ipsilateral upper extremity swelling and pain, one patient complained of isolated ipsilateral pain in the forearm, and one patient complained of forearm pain associated with superficial venous collateral circulation. The other 13 patients were asymptomatic. The mean interval between catheter placement and the onset of thrombosis was 42.2 days (range, 10–83 days).
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It proved impossible to review 32 of the chest radiographs obtained immediately after surgery: 12 images were missing, and in the remaining 20, poor contrast made it impossible to assess the exact position of the catheter tip. A total of 113 postoperative chest radiographs were analyzed. Sixty-three (55.8%) revealed catheters implanted in the left vein, and 50 (44.2%) showed catheters implanted in the right vein. A similar proportion was found in the group of 96 patients who did not develop DVT during follow-up: 52 (54%) had a catheter implanted in the left subclavian vein and 44 (46%) in the right subclavian vein. Eleven (65%) of the 17 patients with catheter-related DVT had their CVC implanted in the left vein and the remaining six (35%) in the right. However, no significant difference in the incidence of thrombosis was found between patients with the catheter in the right vein and those with the catheter in the left vein (P = .3).
The positions of the catheter tips are summarized in Table 3. Three (5%) of 62 patients whose catheters were in segment 1 eventually developed thrombosis. Two (8%) of 25 patients with catheters in segment 2 developed thrombosis. Five (71%) of seven patients with catheters in segment 3 developed thrombosis, and five (42%) of 12 patients whose catheters were positioned in segment 4 developed thrombosis. Two (67%) of three patients with catheters located in the internal jugular vein developed thrombosis. None of the other patients developed thrombosis, including those whose catheters were located in the right atrium. Overall, five (6%) of 87 patients in group A (ie, with their catheter in segments 1 or 2) developed DVT, whereas 12 (46%) of 26 patients in group B developed thrombosis. The risk of thrombosis was thus significantly higher in patients in group B, that is, in those with the distal extremity of the catheter positioned neither in segment 1 nor in segment 2 (P < .001; 2 Yates correction, 22.5; smallest expected value, 3.9).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The risk of catheter-related DVT is often underestimated, mainly because most studies (2,4–6,14–17) are based on varying diagnostic criteria. The identification of catheter-related DVT is usually based solely on clinical criteria. Our 11.7% rate of catheter-related DVT is much closer to that presented in the few studies (1,18–21) that focused on prospective radiologic screening for catheter-related DVT. In our study, none of the patients with catheter-related DVT showed any evidence of cancer metastasis. For instance, none exhibited any extensive cervical lymph node involvement as assessed with clinical examination and US. We did not examine these patients for specific blood coagulation disorders (mutations affecting protein C, protein S, antithrombin III), but such disorders are known to be rare in the general population, and so we believed we were justified in attributing the thrombosis to catheter-related DVT. We thus conclude that findings of studies focusing on the clinical disclosure of catheter-related DVT have underestimated its true incidence. Because the incidence of catheter-related DVT is not low, careful monitoring of all patients with CVC is of crucial importance.
A correct follow-up procedure cannot be based solely on clinical screening for upper extremity DVT. We report a 76% incidence rate of totally asymptomatic patients with DVT. Similar or even higher rates have been reported in several prospective studies (1,19–21) in which diagnostic phlebography for catheter-related DVT was investigated. For instance, De Cicco et al (19) systematically screened a group of 127 patients for thrombosis by using phlebography performed 8 days, 30 days, and then every 2 months after catheter implantation; these investigators found a 6% rate of symptomatic patients with catheter-related DVT.
The use of Doppler US in the diagnosis of catheter-related DVT has been debated. Doppler US of the subclavian vein is believed to be less sensitive than US of the jugular vein because the subclavian vein lies further down. Therefore, subclavian US apparently is technically more difficult to perform and could fail in the diagnosis of DVT. However, we found only four patients in whom subclavian DVT occurred in isolation, and two were symptomatic.
Although, according to Haire et al (22), Doppler US is highly specific, it has low sensitivity in the diagnosis of catheter-related DVT. However, their study included only 32 control venograms, and their Doppler US did not include color Doppler analysis. Although Doppler US was the cause of the underestimation of the incidence of short segmental vessel occlusions, it has been proven to be more convenient and to have lower risk than phlebography. In addition, phlebography involves the use of contrast material, which has both nephrotoxic and allergic risks. Phlebography is also suspected of promoting DVT in some cases (12). Because screening for catheter-related DVT can be expected to be repeated in patients with CVCs, our assessment of the risk of phlebography includes the repeated exposure to x rays and the inconvenience of repeated venous puncture.
The reported (23) sensitivity and specificity of Doppler US for screening catheter-related DVT are as high as 94% and 96%, respectively, if several parameters such as lack of vein compressibility, direct visualization of the thrombus, and a lack of spontaneous flow or fluctuation of flow during respiration are assessed together. We acknowledge that we lacked a small-headed Doppler transducer, which could have been used when examining distal segments of the subclavian veins. Moreover, a decrease in the normal pulsatile signal waveform on Doppler images was not taken into account when diagnosing catheter-related DVT in our study. We thus believe that our reported rate of catheter-related DVT may even be underestimated.
Of the 17 patients who developed DVT, 14 (82%) did so within the first 2 months after catheter implantation, with a mean interval of 42.2 days between catheter placement and the catheter-related DVT, in accordance with the findings in previously reported studies (13,16). Some authors believe that catheter-related DVT is triggered by trauma caused by the initial venous puncture, and this could account for the early onset of catheter-related DVT. However, the endothelial healing and thrombotic processes that follow venous puncture do not usually last for more than 8 days (24). Our study did not provide any further understanding of the timing of catheter-related DVT.
There are many risk factors for catheter-related DVT. Most studies, even those prospectively screening for catheter-related DVT with either Doppler US (18) or phlebographic examinations (1,21), usually include a small number of patients presenting with differing disorders, treatments, and types of CVC. For instance, Stanislav et al (25) suggested that the position of the catheter tip could influence the incidence of catheter-related DVT, but their study population was fitted with a variety of CVCs. Our study involved a large population presenting with similar disorders, treatments, and catheter types. We deliberately chose a totally implantable port with a silicone-coated catheter because lower rates of catheter-related DVT have been reported (7,8) with this type of device. Consequently, only a small number of parameters influenced the rate of catheter-related DVT, and a statistical link between CVC position and catheter-related DVT incidence was demonstrated.
Initial correct positioning of the CVC is indeed critical in lowering the risk of catheter-related DVT. Only 6% of patients in group A who had a correctly positioned distal catheter tip developed thrombosis, compared with 46% in group B. On the other hand, we found no statistically significant difference in the catheter-related DVT rate between patients with catheters implanted in the left and those with catheters implanted in the right subclavian vein. In our study, 23% (26 of 113) of catheters were incorrectly positioned. We acknowledge, however, that determination of the position of the distal tip of the catheter solely on the basis of interpretation of a conventional chest radiograph obtained immediately after surgery cannot be considered to be a state-of-the-art method. For instance, 32 of the chest radiographs were considered to be uninterpretable, in 20 cases because of inadequate contrast. The best assessment procedure would probably be to obtain a venous angiogram immediately after surgery. Unfortunately, this was not possible in our department.
Authors of recent studies (4,16,26,27) have indeed reported incorrect positioning rates that verge on zero after radiologic placement of CVC checked by angiograms immediately after surgery, and this procedure is associated with rates of secondary DVT close to zero. However, these data were based on clinical follow-up findings, which, as we have mentioned, probably considerably underestimate the incidence of asymptomatic thrombosis. However, correct positioning of CVCs alone does not ensure thrombosis-free evolution. In our study, 14 patients with incorrectly positioned catheters did not develop catheter-related DVT. Also, five patients with correctly positioned catheters did develop catheter-related DVT. Therefore, our findings show that correct positioning of the CVC significantly (P < .001) lowers the risk of secondary thrombosis but does not totally eliminate it.
The long-term follow-up of patients with CVC was insufficient in our study. Our study was deliberately divided into two parts; during the first part, we focused on the first 3 months after CVC implantation. Patients could easily be followed up in our unit during this period. Moreover, surgery performed at the end of the third cycle of chemotherapy varied from one patient to another and could therefore have influenced the secondary DVT rate.
During the initial 3 months, we reported a 11.7% risk of secondary DVT. Then the rate of thrombosis decreased during the second part of the study. The findings of this prospective study do not allow us to suggest the appropriate frequency of Doppler US examinations beyond the 3rd month after catheter placement. First, only 32 of 47 patients who kept the CVC in place beyond the 3rd month complied with regular follow-up examinations. Second, we acknowledge that both the type and the extent of the surgical procedures performed after the third cycle were not the same for all patients. Moreover, patients with lymph node involvement underwent radical lymphadenectomy, which removed the ipsilateral internal jugular vein. Although CVCs were implanted in the vein contralateral to the tumor, we were unable to evaluate the effect of this radical surgery on the patency of the contralateral venous system.
We are also unable to correlate the incidence of thrombosis and the long-term clinical outcome in our patients. Because only two of 17 patients with catheter-related DVT had an intermediate probability of pulmonary embolism at ventilation-perfusion scintigraphy (a rate of 8%), the rate of pulmonary embolism in our study was lower than that reported in similar studies (28). However, our screening method for pulmonary embolism was insufficient; only 12 of 17 patients with catheter-related DVT actually underwent lung scintigraphy. One patient refused to undergo lung scintigraphy. The remaining four patients were treated as outpatients and were not referred to our department. Moreover, none of them underwent pulmonary angiography (to confirm suspected pulmonary embolism) or dynamic lung helical CT, which appear to be more specific than scintigraphy and could have depicted any superior vena cava thromboses that remain undetected at peripheral Doppler US. The results of lung scintigraphic studies were thus not taken into account in this study.
A future step in our work will be to demonstrate that infraclinical pulmonary embolism occurs in patients with catheter-related DVT. However, longitudinal studies performed for longer periods will be necessary to relate these adverse events (DVT and pulmonary embolism) to the long-term clinical outcome.
Moreover, such studies will be needed to assess the influence of early curative treatment on the basis of prospective Doppler US findings. If long-term follow-up shows no significant decrease in the incidence of pulmonary embolism and no change in life discomfort or even in long-term outcome, the use of systematic Doppler US should be questioned. Larger study populations will also be needed to find out whether preventive anticoagulant therapies are effective in patients undergoing the placement of CVCs, as recent reports have suggested (20,29).
In conclusion, DVTs occurred in 11.7% of our patients following the placement of a CVC. Correct positioning of the distal extremity of each catheter is crucial for lowering this rate and can routinely be assessed on a conventional chest radiograph. Follow-up could include systematic monthly Doppler US scans obtained for at least the first 3 months after catheter placement because more than 76% of catheter-related DVT are totally asymptomatic. This follow-up appears to be indicated if incorrect placement of the CVC is confirmed with chest radiography. The long-term follow-up effect of DVT on long-term clinical outcome and the incidence of infraclinical pulmonary embolism call for further investigation.
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FOOTNOTES |
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Author contributions: Guarantors of integrity of entire study, A.L., P.B., D.G.; study concepts, D.G., P.B.; study design, V.B., J.A.L., P.B.; literature research, A.L., D.G.; clinical studies, F.P., P.H., J.A.L., D.G.; data acquisition, A.L., D.G.; data analysis/interpretation, A.L., D.G., P.B., P.A.; statistical analysis, A.L., P.B., P.A.; manuscript preparation, A.L., O.C.; manuscript definition of intellectual content, A.L., P.B.; manuscript editing, P.B., O.C.; manuscript revision/review, G.F., A.L., O.C., P.A.; manuscript final version approval, G.F.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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