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AJR 2003; 180:81-86
© American Roentgen Ray Society


MR Imaging of the Lumbar Spine: Relation of Posterior Soft-Tissue Edema-Like Signal and Body Weight

Hongyu Shi1, Mark E. Schweitzer, John A. Carrino and Laurence Parker

1 All authors: Department of Radiology, Thomas Jefferson University Hospital, 111 S. 11th St., Philadelphia, PA 19107.

Received April 29, 2002; accepted after revision June 13, 2002.

 
Address correspondence to M. E. Schweitzer.

Presented at the annual meeting of the American Roentgen Ray Society, Atlanta, April-May 2002.


Abstract
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
OBJECTIVE. Our purpose was to determine the association between posterior lumbar spine subcutaneous edema, fluid collections, and body weight on lumbar spine MR imaging.

MATERIALS AND METHODS. MR images of the lumbar spine obtained at 1.5 T of 307 consecutive outpatients (191 female, 116 male) were reviewed on the basis of MR imaging signal characteristics for the presence, degree, size, and location of presumed subcutaneous posterior soft-tissue edema and fluid collections. The patients were divided into three weight groups (<70, 70-85, or > 85 kg) and two age groups (<50 or >=50 years old). Edema was graded on a scale of 0-5 according to its length relative to the vertebral bodies. When present, the fluid collection volumes were calculated. The vertical epicenter of the signal abnormality was noted by vertebral body level.

RESULTS. Lumbar soft-tissue edema was seen in 121 patients (39%), and discrete fluid collections were seen in 53 patients (17%). Both degree of edema and volume of fluid collection were associated with increasing weight (p < 0.001 and p = 0.002, respectively) and increasing age (p < 0.001 and p = 0.01, respectively). The degree of edema in females was significantly greater than in males (p = 0.003). However, the sex of the patient did not correlate with frequency of fluid collections (p = 0.12) or volume of collections (p = 0.08). The mean epicenters of edema in females and males were at similar levels (L3.4 and L3.9, respectively, p = 0.54).

CONCLUSION. The severity of posterior lumbar subcutaneous edema and the volume of fluid collections on MR imaging are associated with increased weight.


Introduction
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
 
MR imaging is widely used to evaluate lumbar spine abnormalities. Edema-like signal in the subcutaneous soft tissue of the posterior lumbar spine is frequently noted and is considered an incidental finding. Most often this edema-like signal is ill defined and somewhat infiltrative. It is presumed to be edema on the basis of characteristic T2 hyperintensity and T1 hypointensity on MR images, as seen elsewhere in the soft tissue [1]. In some cases, the high T2, low T1 signals present as well-defined accumulations, presumably representing fluid collections. Although the precise nature of this presumed edema or fluid collection is unclear, it may be related to free fluid, partially compartmentalized fluid, or lymphatic pooling. The potential causes of the edema or fluid are numerous, including infectious, inflammatory, traumatic, hydrostatic, and even neoplastic causes. From our anecdotal experience, posterior lumbar soft-tissue edema or fluid is more commonly encountered in obese patients.

Cooper et al. [2] reported that lumbar edema accumulated at the subcutaneous fascia plane on CT. To our knowledge, no prior reports in the literature scientifically describe lumbar soft-tissue edema on MR imaging or evaluate the relation of the edema and the patient's body habitus. Consequently, in this study we investigated the correlation of body weight and the posterior lumbar and sacral subcutaneous edema or fluid collections seen on MR imaging.


Materials and Methods
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Abstract
Introduction
Materials and Methods
Results
Discussion
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Patient Population
A search of the computerized radiology data-base identified 448 consecutive lumbar spine MR imaging examinations performed at our outpatient imaging center from July 2000 to October 2000. Three hundred seventy-two of these patients, whose body weights were recorded, were included in the study. The primary reasons for these patients to undergo MR imaging were back pain, possible disk disease, or radiculopathy. Because we evaluated clinical patients rather than healthy volunteers, we used several exclusion criteria. Fifty-seven patients who had prior lumbar spine surgery, a lumbar or sacral neoplasm, diffuse osseous metastasis, severe congenital abnormality, severe scoliosis, acute diskitis or osteomyelitis, or acute lumbar spine fracture were excluded from our study. These conditions may be associated with pathologic lumbar soft-tissue edema. An additional eight patients were excluded because of inadequate images for evaluation of soft-tissue edema. In patients who had multiple MR imaging examinations during this time, only the first examination was included in our study.

The final study population consisted of 307 patients, of whom 191 were female and 116 were male (age range, 13-90 years; mean age ± SD, 50.3 ± 15.7 years). The demographic data of the patient population are listed in Table 1. This research project was approved by the institutional review board of our hospital.


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TABLE 1 Patient Demographics

 

Imaging Technique
Imaging was performed on a 1.5-T MR imaging unit (Signa; General Electric Medical Systems, Milwaukee, WI) with a dedicated spine coil. Although imaging was performed in several planes, the subcutaneous posterior lumbar soft-tissue edema was evaluated primarily on fat-saturated sagittal T2-weighted fast spin-echo images. In cases of inadequate fat saturation, which sometimes was seen in sacral subcutaneous soft tissue, the T1-weighted non—fat-saturated images were used to confirm the presence and extent of the edema. The MR imaging parameters were as follows: echo-train length, 8; TR range/TE range for sagittal T2-weighted sequences, 3100-4000/80-90; TR/TE for sagittal T1-weighted sequences, 400/9. The following parameters were the same for all pulse sequences: section thickness, 4.0 mm; intersection gap, 1.0 mm; matrix, 512 x 192; and field of view, 30 x 30 cm.

Image Analysis
The lumbar MR images were retrospectively reviewed by one radiologist for the presence, degree, and location of subcutaneous posterior softtissue edema-like signal (for simplicity, the term "edema" is used for the remainder of the text). Lumbar edema was graded on a scale of 0-5 according to its length relative to the vertebral bodies on sagittal images: 0, no edema; 1, less than the height of one vertebra; 2, equal to or longer than the height of one vertebra but not reaching the adjacent end plate of the next vertebra; 3, spanning the height of two vertebrae; 4, equal to or longer than two vertebrae, but less than grade 5; and 5, spanning three vertebrae or longer. When a patient had multiple foci of edema, the sum of the length was used to categorize the degree of edema. Sacral edema was also graded in a similar fashion on a scale of 0-5 using the height of S1 as a reference. In some patients who had edema, well-marginated discrete accumulations of homogeneous T2 hyperintensity could also be identified, which we labeled "fluid collection." When present, the size of the fluid collection was measured in three dimensions, and the volume was calculated as the product of three dimensions multiplied by 0.5, assuming an ellipsoid shape. In cases of multiple collections, the volumes were summed. The vertical epicenter of edema was noted on a scale of 1-5 corresponding to the lumbar vertebral body levels, or as 1.5, 2.5, 3.5, or 4.5 if the epicenter was at the intervetebral disk level.

For purposes of data analysis, we divided the patients into three groups based on body weight: group 1, less than 70 kg, consisted of 102 patients; group 2, 70-85 kg, had 102 patients; and group 3, greater than 85 kg, contained 103 patients. The patients were also divided into two groups based on age (< 50 years old, 155 patients; >= 50 years old, 152 patients). The mean degree of edema in each group of patients was calculated as the summation of the products of each degree of edema and the number of patients in that degree category, then divided by the total number of patients in that group. For dichotomous dependent variables including the presence or absence of edema or discrete volume of collection in different weight, age, or sex groups, chi-square tests were computed. For ordinal and non-normally-distributed continuous variables, including the degree of edema and the volume of fluid collections in different weight, age, or sex groups, Mann-Whitney U tests and Kruskal-Wallis tests were calculated. To analyze whether the effect of weight was independent of sex and age, two-way parametric analyses of variance were calculated separately for males and females. Although the dependent variables were not normally distributed, parametric analysis of variance is robust for violations of normality provided sample sizes are equal [3]. A p value of less than 0.05 was defined as statistically significant.


Results
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Materials and Methods
Results
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With respect to location, edema was observed primarily along the deep fascia plane and extended into the deep subcutaneous fat. Typically, edema was along the midline in a triangular configuration next to the thoracolumbar fascia attachment to the posterior aspect of the spinous process (Fig. 1). The mean vertical epicenters of the edema in females (L3.4) and males (L3.9) were at similar levels (p > 0.05). The L3-L4 levels accounted for 54% of edema epicenters.



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Fig. 1. 38-year-old woman with back pain. Axial T2-weighted MR image (TR/TE, 5300/65) shows triangular form of posterior subcutaneous soft-tissue edema (arrowheads) along deep fascia plane extending to deep fat layer posterior to spinous process.

 

The mean body weight of our patient populaton was 78.5 kg (range, 45.5-145.0 kg), and the mean age was 50.3 ± 15.7 years (range, 13-90 years). Among the overall population, 121 patients (39.4%) had lumbar edema. The percentage of patients who had lumbar edema increased significantly from 22.5% in weight group 1 to 33.6% in weight group 2 and 59.2% in weight group 3 (p < 0.0001). The degree of lumbar edema also significantly increased in the heavier weight group (p < 0.0001). Among the patients with edema, 53 patients (43.8%) had lumbar fluid collections. Similarly, the percentage of patients having fluid collections also significantly increased with body weight from 9.0% in group 1 to 15.7% and 27.2% in groups 2 and 3 (p = 0.002). Furthermore, fluid collection volume significantly increased in the heavier weight group as well (p < 0.05). The values of mean degree of edema and volumes of fluid collections in each weight group and statistical data are presented in Table 2. Figures 2,3,4 illustrate the various degrees of edema in three patients from different weight groups.


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TABLE 2 Degree of Soft-Tissue Edema and Volume of Fluid Collections in Three Weight Groups

 


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Fig. 2. 52-year-old woman (weight, 54 kg) from weight group 1. Sagittal T2-weighted MR image (TR/TE, 3067/92) of lumbar spine shows no edema in posterior soft tissue.

 


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Fig. 3. Sagittal T2-weighted MR image (TR/TE, 3150/92) of lumbar spine reveals grade 4 posterior lumbar soft-tissue edema in this 40-year-old woman (weight, 79 kg) from weight group 2. Arrowheads indicate extent of edema.

 


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Fig. 4. 52-year-old man (weight, 136 kg) from weight group 3. Sagittal T2-weighted MR image (TR/TE, 4000/80) of lumbar spine shows grade 5 edema (arrowheads) and discrete fluid collection in posterior lumbar soft tissue.

 

The percentage of patients who had lumbar edema (31.0%) or fluid collections (12.3%) in the younger age group was significantly lower than that in the older age group (48.0% and 22.4%, respectively; p = 0.003 and 0.02). The degree of lumbar edema and the volume of fluid collection also increased with age (p < 0.001 and p = 0.01, respectively) (Table 3). The frequency of lumbar edema in females (46%) was significantly greater than in males (29%) (p = 0.005). The degree of edema was also more severe in females than in males. However, no correlation of sex with the frequency (p = 0.12) or volume of fluid collections was seen. The degree of soft-tissue edema and volume of fluid collections in both sexes are summarized in Table 4.


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TABLE 3 Degree of Soft-Tissue Edema and Volume of Fluid Collections in Two Age Groups

 

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TABLE 4 Degree of Soft-Tissue Edema and Volume of Fluid Collections in Two Sex Groups

 

In the sacral region, 92 patients (30%) had subcutaneous soft-tissue edema, and eight patients (3%) had fluid collections. Similarly, the percentage of patients with edema and the degree of edema were associated with increasing weight (p < 0.001, and p = 0.001, respectively). The percentage of patients with a fluid collection, however, did not increase with body weight (p = 0.41) (Table 2). Both the percentage of patients with edema and the degree of edema significantly increased in the older age group (p = 0.0008, and p = 0.001, respectively). However, the frequencies of fluid collections were not significantly different between the two age groups (p = 0.98) (Table 3). A significantly greater percentage of female patients than male patients had sacral edema (p = 0.02). The degree of edema in females was also more severe than that in males (p = 0.02). However, similar to the lumbar spine, the percentage of patients with a fluid collection was not significantly different in the female or male groups (p = 0.45). No significant difference was found in fluid collection volume between male and female groups (Table 4).

In both the female and the male groups, the degree of edema increased with heavier weight, independently of age, at either the lumbar or the sacral region (all, p < 0.05).


Discussion
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Abstract
Introduction
Materials and Methods
Results
Discussion
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We have long recognized that many patients have subcutaneous posterior lumbosacral soft-tissue edema. In this study, we showed that the MR imaging finding of posterior lumbosacral soft-tissue edema occurred more frequently and was more severe in heavy patients. The percentage of patients with posterior lumbar fluid collections and volumes of collections also increased in the heavier weight patient group. Lumbosacral soft-tissue edema was significantly more severe in female and older patient groups.

Cooper et al. [2] reported the manifestations of posterior lumbar edema on CT. Those authors noted that lumbar edema accumulated at the subcutaneous fascia plane. In our study, the posterior lumbar soft-tissue edema was observed in this fibrous plane and in the deep fat layer. Anatomically, trunk subcutaneous soft tissue (adipose tissue) is separated by the subcutaneous fascia into superficial and deep adipose layers [2, 4,5,6]. The subcutaneous fascia fuses medially with the deep lumbar fascia. The superficial adipose layer is contained within uniform and compact fascial septa, whereas the deep adipose layer is contained within a relatively loose, less organized, and more widely spaced fascial septum. The thickness of the deep adipose compartment is variable at the trunk and contributes significantly to total mass and overall body contour [4]. The observed accumulation of edema in the deep fat layer in heavier patients may be because this layer of fat is loosely packed and is thicker in obese patients.

Physiologically, extracellular edema has two general causes: abnormal leakage of fluid from the plasma to the interstitial spaces across the capillaries, and failure of the lymphatics to return fluid from the interstitium back into the blood [7]. Many conditions can cause fluid accumulation in the interstitium by means of increased capillary pressure, decreased plasma protein, increased capillary permeability, and blockage of lymph return [7].

In obese patients, soft-tissue edema may occur for the following reasons. First, elevated intraabdominal pressure has been shown in obese patients [8, 9]. The elevated abdominal pressure produces increased inferior vena cava pressure [10, 11] and, presumably, increased peripheral venous and capillary pressure; as a result, filtration into the interstitium increases. Increased abdominal pressure likely also impedes lymphatic drainage in the abdominal lymph channels. Because the lumbar subcutaneous lymph joins the abdominal lymphatics, they could also be affected. Second, obesity is associated with expanded circulatory volume [12], which in turn could translate to increased intravascular pressure. Third, capillary permeability to albumin increases in overweight women with swelling syndrome [13]. This mechanism may also contribute to the soft-tissue edema seen in our obese patients. Fourth, in obese patients, the cutaneous vasoconstrictive response to sympathetic activation is reduced, which may result in increased peripheral capillary blood flow and capillary permeability [14]. Fifth, obesity is associated with glomerulopathy, nephrotic syndrome [15, 16], and related hypoalbuminemia. Although we did not have direct measurements of serum albumin levels, potentially lumbar soft-tissue edema results from the low intravascular albumin and decreased colloid osmotic pressure. Sixth, slowed lymphatic drainage was found in patients who had lipedema—an entity of leg edema in obese patients [17]. However, whether this mechanism also applies to the soft tissue of the back in obese patients remains to be elucidated. Finally, in obese individuals external intermittent compression of the lymph vessel related to muscular contraction and body movement may be decreased, thereby minimizing lymph flow.

Our study showed that both the degree of the posterior lumbar soft-tissue edema and the frequency of fluid collections increased significantly in older patients. Advanced age and greater body weight were independently associated with soft-tissue edema. Other factors besides obesity likely also contributed to the edema in older patients. One practical explanation is that older patients tend to have more coexisting medical problems such as cardiac or renal dysfunction than younger patients. In these conditions, patients may be volume overloaded, and venous circulation may be impaired. In addition, the plasma protein level may also decrease because of renal insufficiency. As a result, lumbar soft-tissue edema occurs. Second, in elderly patients, physical activity is presumably less than in a young population, and lymphatic and venous return related to adjacent tissue pumping decreases. In this preliminary and retrospective study, unfortunately, these relevant data were not recorded at the time that MR imaging was performed. A study designed to collect these clinical data and to measure lean body mass and truncal obesity may in the future clarify these results.

The fact that females had a higher frequency of edema than males can probably be explained simply by their greater adipose tissue content, particularly in the loose deep trunk fat layer, provided comparison is made with males having the same body weights and heights. Male patients generally have greater lean body mass than females. This hypothesis can be tested by correlation of edema with the subcutaneous fat thickness in the posterior lumbar soft tissue, comparing female and male patients. This correlation was not accomplished, however, because the data were not collected at the time that MR imaging was performed. The compression of posterior lumbar subcutaneous fat with the patient in the supine position precluded precise measurement of the fat thickness, and in some patients the extreme posterior fat was not included in the field of view.

Posterior lumbar soft-tissue edema seen in obese patients without other abnormal findings in proximity may be explained by the patients' body habitus. However, readers should be cautious in applying these results to clinical practice. Careful scrutiny of the adjacent structures such as osseous spine, paraspinal musculature, and skin should be performed before one attributes the posterior lumbar and sacral edema only to the body habitus. In one of our female patients (body weight, 55 kg), diffuse paraspinal muscular edema coexisted with severe posterior lumbar soft-tissue edema. This edema was related to the patient's known diagnosis of polymyositis (Fig. 5).



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Fig. 5. 53-year-old woman with history of polymyositis who presented with acute back pain. Sagittal T2-weighted MR image (TR/TE, 4000/84) shows severe subcutaneous soft-tissue edema (arrowheads) and edema in erector spinae muscles (arrows).

 

We acknowledge several limitations to this study. First, the subjects were not healthy volunteers. Instead, we selected patients from an outpatient imaging center. We assume that this population is generally mobile and less likely to have debilitating conditions than inpatients. In addition, this group represents patients typically seen clinically. Second, the degree of obesity was not directly measured. Instead, weight was used as a reference for the degree of obesity. Factors such as height of the patient and fat distribution were not directly incorporated into the data analysis. In future studies, direct analysis of the relation of edema and obesity can be performed by collecting data such as height, skin fold thickness, and anthropometric measurements as well as body weight. Third, we presume the abnormal edema-like signal was edema or discrete fluid collections, on the basis of the MR imaging signal characteristics. The precise nature of this abnormal signal remains unclear. Sonographic evaluation of these areas and examination of the aspirates from the fluid collections seen on MR imaging may elucidate this issue. These evaluations were not performed in our observational study.

In summary, we conclude that lumbosacral subcutaneous soft-tissue edema is associated with increased body weight, female sex, and older age. Because body weight reflects the degree of obesity in patients with similar height, we postulate that the underlying risk factor is obesity.


Acknowledgments
 
We thank William Morrison for his assistance in printing the figures.


References
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
 

  1. Schweitzer ME, Tran D, Deely DM, Hume EL. Medial collateral ligament injuries: evaluation of multiple signs, prevalence and location of associated bone bruises, and assessment with MR imaging. Radiology 1995;194:825 -829[Abstract/Free Full Text]
  2. Cooper M, Hacking JC, Dixon AK. Sacral edema: computed tomographic and anatomical observations. Clin Anat 1995;8:56 -60[Medline]
  3. Kerlinger FN. Foundations of behavioral research, 2nd ed. New York: Holt, Rinehart and Winston, 1972: 286-288
  4. Markman B, Barton FE Jr. Anatomy of the subcutaneous tissue of the trunk and lower extremity. Plast Reconst Surg 1987;80:248 -254[Medline]
  5. Williams PL, Warwick MD, Bannister LH. Gray's anatomy, 37th ed. Edinburgh: Churchill Livingstone, 1989: 595
  6. Thorek P. Anatomy in surgery. New York: Springer-Verlag, 1985:369 -370
  7. Guyton AC, Hall JE. Textbook of medical physiology, 9th ed. Philadelphia: Saunders, 1996: 308-310
  8. Sugerman HJ, Windsor A, Bessos M, Wolfe L. Intra-abdominal pressure, sagittal abdominal diameter and obesity comorbidity. J Intern Med 1997;241:71 -79[Medline]
  9. Sugerman HJ, Windsor A, Bessos M, Kellum J, Reines H, DeMaria E. Effects of surgically induced weight loss on urinary bladder pressure, sagittal abdominal diameter and obesity co-morbidity. Int J Obes Relat Metab Disord 1998;22:230 -235[Medline]
  10. Ridings PC, Bloomfield GL, Blocher CR, Sugerman HJ. Cardiopulmonary effects of raised interabdominal pressure before and after intravascular volume expansion. J Trauma 1995;39:1071 -1075[Medline]
  11. Bloomfield G, Saggi B, Blocher C, Sugerman HJ. Physiologic effects of externally applied continuous negative abdominal pressure for intra-abdominal hypertension. J Trauma 1999;46:1009 -1014[Medline]
  12. Messerli FH, Christie B, DeCarvalho JG, et al. Obesity and essential hypertension: hemodynamics, intravascular volume, sodium excretion, and plasma rennin activity. Arch Intern Med 1981;141:81 -85[Abstract/Free Full Text]
  13. Valensi P, L'Hermite F, Behar A, Sandre-Banon D, Cohen-Boulakia F, Attali JR. Extra cellular water and increase in capillary permeability to albumin in overweight women with swelling syndrome. Int J Obes Relat Metab Disord 2000;24:126 -130[Medline]
  14. Valensi P, Smagghue O, Paries J, Velayoudon P, Lormeau B, Attali JR. Impairment of skin vasoconstrictive response to sympathetic activation in obese patients: influence of rheological disorders. Metabolism 2000;49:600 -606[Medline]
  15. Kambham N, Markowitz GS, Valeri AM, Lin J, D'Agati VD. Obesity-related glomerulopathy: an emerging epidemic. Kidney Int 2001;59:1498 -1509[Medline]
  16. Shimomura Y, Murakami M, Shimizu H, et al. Improvement of nephrotic syndrome in a massively obese patient after weight loss and treatment with an anti-allergic drug. J Med 1990;21:337 -347[Medline]
  17. Bilancini S, Lucchi M, Tucci S, Eleuteri P. Functional lymphatic alteration in patients suffering from lipedema. Angiology 1995;46:333 -339

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