Influence of the chronic abdominal aortic occlusion on the femoral artery disease pattern

Abstract

We design a study to evaluate whether patients with chronic aortic occlusion have a different pattern of femoral artery atherosclerosis than patients with other forms of aortoiliac disease as well as to discuss potential causal mechanisms. From January 2008 to January 2010, 467 patients with aortoiliac occlusive disease were enrolled at Clinic of Vascular and Endovascular Surgery in Belgrade, Serbia. Among them 60 patients were divided into two groups, patients with chronic aortic occlusion (COA) and diffuse aortoiliac occlusive disease (AIOD, Leriche type II). Each group consisted of 30 patients. Those two groups were compared according to symptomatology, ABI values, femoral artery pressure gradient, atherosclerosis level in the femoral region and predictors of atherosclerosis.Patients with AIOD had severe atherosclerosis unlike patients with COA. Also, high elevation of postoperative ABIs in patients with an early atherosclerosis (0, I, II and III) was noted suggesting patent distal arterial tree. FAP gradient was significantly higher in COA group comparing with AIOD group (left: t = − 10.963, P < 0.01;right: t = − 8.962, P < 0.01). In conclusion, our data demonstrate that older patients have had more time to develop multilevel disease (AOID) and those with CAO have more isolated aortic disease chronic aortic occlusion.

Keywords

chronic aortic occlusion femoral artery disease aortoiliac occlusive disease

Introduction

Chronic aortic occlusion (COA) is generally considered to be a rare condition with an incidence of 0.15% so it is not surprising that anyone has reported a large experience with this lesion.¹ Although some reports have suggested that the peripheral vessels may be ‘protected’ from atherosclerotic disease in cases of aortic obstruction, others have found both stenoses and occlusions in the femoral and popliteal arteries in these patients.^2,3 The effect of a proximal arterial occlusion on the progression of the distal arterial disease has been discussed in the medical community for a long time^4–6 and among a quite number of a reports, the last of them concluded that there was no evidence that a proximal arterial occlusion was associated with a slower progression of distal arterial disease.^7,8 The results of the studies were mainly based on arteriographic evaluation, subjected to a sharp eye of an experienced radiologist. So, we needed the observation group which could be sufficient for atherosclerosis evaluation without any side-effect of acute vessel occlusion. That was the reason to use COA as a group of interest, and to design a study to evaluate whether patients with chronic aortic occlusion have a different pattern of femoral artery atherosclerosis than patients with other forms of aorto-iliac disease as well as to discuss potential causal mechanisms.

Methods

From January 2008 to January 2010, 467 patients with aortoiliac occlusive disease were enrolled at Clinic of Vascular and Endovascular Surgery in Belgrade, Serbia. Among them 60 patients were divided into two groups. First group consisted of 30 patients with angiographic signs of Leriche type II disease (disease confined to the abdomen) without occlusion and with patent superficial femoral arteries (AIOD group). Second (COA group) of 30 patients were characterized as either infrarenal aortic occlusion or juxtarenal aortic occlusion, based on the level of proximal extension of chronic athero-thrombotic material and level of disruption of the contrast column on standard digital subtraction angiography. Only patients with degenerative etiology of the disease were included in the study. Patients were excluded from this study if they had (1) open or endovascular lower limb revascularization and (2) acute abdominal aortic occlusion. All patients had patent superficial femoral arteries. Those two groups were compared according to symptomatology, ankle brachial index (ABI) values, femoral artery pressure gradient (gFAP), atherosclerosis level in the femoral region and predictors of atherosclerosis. Severe claudication was present in those with pain on exercise or walking in the lower extremities relieved by rest, which was considered lifestyle-limiting to the patient. After performing digital subtraction angiography with purpose of distal run off evaluation, all 60 patients underwent aortobifemoral reconstruction. Formed consent was obtained from each subject enrolled in the study. The study was approved by our institutional ethics committee.

Preoperative variables

Traditional risk factors

At inclusion the presence of classic atherosclerotic risk factors was assessed, smoking, hypertension, dyslipidemia and diabetes. A patient was considered a non-smoker only if the one had absolutely no history of smoking. A patient was classified as hypertensive when arterial systolic/diastolic blood pressure values were higher then 140/90 mmHg or the patient was taking medication for high blood pressure. A patient was considered to have diabetes mellitus if he presented with basal glycemia of over 6.5 mmol/L or was being treated with oral anti-diabetic drugs or insulin. Hyperlipidemia was considered to be present if the plasma concentration of total cholesterol was over 6.2 mmol/L, triglyceride concentrations were over 2.25 mmol/L or the patient was taking lipid-reducing drugs. Cerebrovascular disease was defined as a history of transient ischemic attack or stroke, documented carotid stenosis more than 70%, or a history of carotid endarterectomy or other cerebrovascular operation. Coronary artery disease was defined as documented coronary stenosis more than 50% or a history of angina, myocardial infarction, or coronary artery angioplasty or bypass.

ABI measurement

All patients underwent ABI examination and femoral spectral analysis on admission. After participants rested supine for 15 minutes, a hand-held Doppler probe was used to measure systolic pressures in the right brachial artery, right dorsalis pedis and posterior tibial arteries, left dorsalis pedis and posterior tibial arteries, and left brachial artery. Pressures were measured twice: in the order listed and then in reverse order. ABIs were calculated by dividing average pressures in each leg by the average of the four brachial pressures.⁹ Average brachial pressures in the arm with the highest pressure were used when one brachial pressure was higher than the opposite brachial pressure in both measurement sets, and the two brachial pressures differed by 10 or more mmHg in at least one measurement set. In such cases subclavian stenosis was possible. The average leg ABI was used in all analyses.

Intraoperative variables

Intraoperatively, we measured femoral artery pressure (FAP) directly from the femoral artery and calculated gFAP as a difference between average brachial pressure (ABP) and FAP from both groins. (gFAP = ABP − FAP). During operative procedure, superficial femoral artery branch specimens from all 60 patients were collected. In all cases we took the first branch, nearly below the femoral bifurcation. Specimens for pathohistological analysis were formalin-fixed and paraffin-embedded. Afterwards, level of atherosclerosis was graduated using (American Heart Association, AHA) classification.¹⁰ Grades 0, I, II and III graded as an early atherosclerosis while grades IV, V and VI were considered as a significant atherosclerosis. Aortic reconstruction included aortobifemoral using gelatin-sealed polyester prosthesis. The 16 × 8 mm bifurcated grafts were employed in all operations.

Postoperative variables

Control ABI was taken seven days after operation and measured using blood pressure in the same crural artery. Elevation of ABI for more than 0.15 was indicative of successful reconstruction. The same ABI measurement, outlined before, was used in the postoperative assessment.

Statistical analysis

All continuous variables are represented with the mean ± standard deviation or median (range). The χ² was used to determine association between a categorical outcome and a categorical factor. The Wilcoxon rank sum test, analysis of variance, Mann-Whitney and Kruskal-Wallis test were used to determine association between a categorical outcome and a numeric factor, while the Spearman rank correlation coefficient was used to determine association between a numeric outcome and a numeric factor. Multiple logistic regressions were used to determine independent significant factors for categorical and numeric outcomes, respectively. P < 0.05 was considered to be indicative of a statistical difference. SPSS version 12.0 (release 17, SPSS Inc., Chicago, IL, USA) was used for statistical computing.

Results

These two groups were homogenous except for patients from COA group were younger but AIOD group had some more pronounced traditional risk factors. Demographic characteristics, co-morbid conditions and laboratory were showed in Table 1. Eight patients from AIOD group and six patients from COA group had angiographic signs of the crural artery occlusion due to diabetic disease. All eight of them from AIOD group developed gangrene. Only three patients from AIOD group underwent endarterectomy of the femoral bifurcation and one patient underwent endarterectomy of the deep femoral artery. Neither one patient from COA group underwent endarterectomy. Patients with AIOD had severe atherosclerosis unlike patients with COA (Table 2). Intensity of atherosclerosis of the first branch of the femoral superficial artery was showed in Table 3 and Figure 1. Only one patient from COA group had developed severe form of atherosclerosis (Table 3). There were highly significant differences in pre- and postoperative ABIs between the AIODs and COAs. Also, high elevation of postoperative ABIs in patients with an early atherosclerosis (0, I, II and III) was noted suggesting patent distal arterial three. (Kruskal–Wallis test, KW = 26.715, P < 0.01;. Figure 2). gFAP was significantly higher in COA group comparing with AIOD group (left: t = −10.963, P < 0.01; right: t = −8.962, P < 0.01). gFAP and significant aterosclerosis (IV, V and VI) are shown in Figure 3. Border line gFAP value which triggered atherosclerotic lesions development was 22.9 mmHg. (Mann–Whitney U = 11.000, P < 0.01) Furtheremore, there is significant corellation between gFAP and postoperative ABI. Figure 4 shows postoperative ABI elevation in patients with elevated gFAP, supporting the positive relationship between these two variables. (Pearson test R = 0.377).

Table 1

Demographic, co-morbidities and risk factors variables: comparisons between COA and AIOD patients

No.	Variables	Sum (n = 60)	AIOD (n = 30)	COA (n = 30)	P value
1	Age (years)	59.73 ± 10.25	62.73 ± 13.64	56.73 ± 6.86	0.036*
2	Male gender	46 (76.6%)	23 (76.6%)	23 (76.6%)	P > 0.05
3	Hypertension	55 (91.6%)	30 (100%)	25 (83.3%)	0.020*
4	Smoking	47 (78.3%)	23 (76.6%)	24 (80%)	P > 0.05
5	Diabetes	14 (23.3%)	8 (26.6%)	6 (20%)	P > 0.05
6	Carotid disease	26 (43.3%)	13 (43.3%)	13 (43.3%)	P > 0.05
7	Coronary disease	17 (28.3%)	8 (26.6%)	9 (30%)	P > 0.05
8	Cholesterol	5.82 ± 1.22	6.12 ± 1.24	5.52 ± 1.20	0.062
9	LDL	3.75 ± 1.08	3.91 ± 1.14	3.60 ± 1.02	P > 0.05
10	Tryglicerids	1.85 ± 0.66	1.76 ± 0.51	1.95 ± 0.82	P > 0.05
11	HDL	1.1 ± 0.28	1.18 ± 0.30	1.02 ± 0.26	0.027*

*Significant at 5% level (0.01 _ P value _ 0.05)

Table 2

Symptomatology and operative variables: comparisons between COA and AIOD patients

No.	Variables	Sum (n = 60)	AIOD (n = 30)	COA (n = 30)	P value
1	Claudication	34 (56.6%)	10 (33.3%)	24 (80%)	0.006**
	Rest pain	16 (26.6%)	12 (40%)	4 (13.3%)
	Gangrene	10 (16.6%)	8 (26.6%)	2 (6.66%)
2	Atherosclerosis level	16 (26.6%)	16 (26.6%)	0	0.0015**
3	ABI preoperative.	0.39 ± 0.09	0.44 ± 0.08	0.35 ± 0.1	0.013*
4	ABI postoperative	0.77 ± 0.1	0.64 ± 0.1	0.90 ± 0.1	0.0015**
5	Femoral artery	L/33.41 ± 11.97	L/15.33 ± 7.5	L/51.50 ± 16.43	0.0016**
	pressure (gFAP)	R/35.1 ± 14.7	R/18 ± 12.7	R/52.21 ± 16.39	0.0016**

*Significant at 5% level (0.01 _ P value _ 0.05)

Table 3

Atherosclerosis level distribution among patients from both groups

Atherosclerosis level
Group	0	I	II	III	IV	V	VI
AIOD	1	9	2	2	3	7	6
COA	24	5	/	/	/	1	/

Figure 1

Atherosclerosis level distribution graph

Figure 2

Graph 2 shows correlation between postoperative ABI and atherosclerosis level. There is significant elevation of postoperative ABI in patients with an early atherosclerosis level (0, I, II and III). ABI, ankle brachial index

Figure 3

FAP gradient in correlation with atherosclerosis level (only level IV, V and VI.). FAP gradient value which triggered significant atherosclerotic lesions development was 22.9 mmHg. FAP, femoral artery pressure

Figure 4

Postoperative ABI comparing with FAP gradient. There is significant elevation tendency of postoperative ABI in patients with high FAP gradient. FAP, femoral artery pressure; ABI, ankle brachial index

Disscusion

It is difficult to assess the rate of progression of arterial disease in clinical practice which probably is best answered in a prospective longitudinal observation. Serial arteriography examinations or serial measurements of the ABI have been used to compare the progression of atherosclerotic disease in the lower extremities.¹¹ Marked inter-observer variability is associated with the interpretation of the functional importance of arterial lesions visualized on arteriograms. A lot of earlier reports pronounced by Bomberger et al. ^5,12–14 investigated atherosclerosis progression in experimental conditions, using tight abdominal aortic constrictions in cholesterol fed rabbits, indicating that even a small reduction in blood pressure below normal levels has a marked inhibiting effect on the induction of atherosclerosis. Some other results showed that following reversal of high-grade mid-thoracic stenosis of the aorta, the distal aorta was no longer protected from the development of the atherosclerosis lesions.^5,13,15 The mechanisms proposed for the protective effects suggest that a proximal arterial occlusion lowers the shearing forces and reduces the insult to the distal arterial wall.^5,12 On the other hand, one of the major problems encountered is impossibility of creation in vivo human model for vessel occlusion investigation due to well-known reasons. For this purpose we choose to observe groups of patients with COA and to compare hemodynamical and morphological characteristics in the area below partial and complete occlusion. As demonstrated by our data and those of other investigators, COA tends to occur in relatively young patients who have a history of tobacco abuse.^16,17 It affects younger people giving a less chance for atherosclerosis in distal arterial tree to evolve. Only one patient from COA group developed severe form of atherosclerosis. Since all types of aortoiliac occlusive disease has the same degenerative etiopathogenesis, then the question is why patients with aortic occlusion have diminished distal arterial tree atherosclerosis, despite proximal disease progression (cerebrovascular insult, coronary artery disease, etc.)? In our study both groups had nearly the same percentage of carotid and coronary artery disease. Furthermore, there is a significant elevation of ankle brachial indices after aortobifemoral reconstructions, which are almost nearly 1.00, compared with patients who were treated due to AIOD. On the other hand ABI is relatively insensitive in identifying the lower-extremity atherosclerosis progression.¹¹ Secondly, usually small caliber of the common and superficial femoral artery as well as deep femoral artery in those patients suggests long time period without sufficient flow, making vessels spared of sheared stress forces and subsequent atherosclerotic lesions. According to our pathohistological results, the femoral artery region is spared of atherosclerosis in patients with COA. We found that the correlation between gFAP of 22.9 mmHg and lack of the atherosclerosis in distal atrial tree is probably an association and not necessary an influencing factor making this gradient an incipient trigger of an atherosclerotic lesions development. On the other side, Bomberger et al.^12,13 in his study found that a modest systemic pressure reduction of approximately 20 mmHg below normal levels produced a 50% reduction in cellularity indicating that the smooth muscle cell content of the arterial wall is very sensitive to abnormal decreases in pressure. By intermittent gFAP measurement atherosclerosis progression could be predicted. Low pressure gradients should signal the need for intervention resulting in obliteration of the gradient would only serve to accelerate distal disease progression. According to this distal arteries would be best protected by allowing the proximal arteries to develop more disease and thus higher pressure gradients, or even to ‘therapeutically’ occlude the proximal arteries. Though perhaps good for the distal arteries, patients presented with this plan would likely not go along.

There are few limitations of our study. First, some patients with aortic occlusion may have had pre-existing atherosclerosis which developed during the time prior to aortic occlusion, which could be difficult to assess. Second, we choose to take the first branch of the superficial femoral artery for pathohistological analysis. In some specimens early occlusion of the branch artery origin could slower atherosclerotic disease progression making pathohistological analysis negative despite evident disease signs of the main arterial tree. On the other hand, from an ethical standpoint sacrifice of the patent superficial femoral artery would be inappropriate. Also, assessing atherosclerosis at the femoral level does not actually represent the distal vasculature. There are other weaknesses of the study that should be acknowledged, particularly the selection bias that underestimating the extent of distal disease since this study was based upon angiographic information only and also the no causal relationship between the findings. Finally, since COA tends to be rare disease number of patients was too small for definite conclusions.

Conclusion

In conclusion, our data demonstrate that older patients have had more time to develop multilevel disease (AOID) and those with CAO have more isolated aortic disease. A protection mechanism of the occluded vessel may possibly be suggested by our data. Further studies are needed for speculations to be confirmed.

Footnotes

Acknowledgments

Presented study is a part of a scientific research project (Grant OI175008) supported by the Ministry of Education and Science of the Republic of Serbia.

Conflict of interest: None.

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