Changes in plasma lipids after jejunoileal bypass.

Changes in plasma lipids after jejunoileal bypass KAREN WHITLOW, PH D. IAN CLEATOR, MD, FRCS[C]; JIRI FROHLICH, MD, FRCT4c] Severe obesity is often accompanied by conditions that pose an enhanced risk to health, such as diabetes mellitus, hypertension, atherosclerosis and gallbladder disease.' For patients whose severe obesity cannot be treated successfully by dietary management, surgical treatment may be recommended. One of these procedures, the formation of a jejunoileal bypass, was introduced by Sherman and associates in 19652 and has been performed on several thousand patients. Many side effects of this procedure have been reported, including alterations in lipid metabolism.' Scott and colleagues3 observed a decrease in the plasma concentration of cholesterol and triglycerides. Rtissner and Hallberg4 found a change in the triglyceride and cholesterol content of very-low-density lipoprotein (VLDL) and high-density liproprotein (HDL). Moreover, Kral and coworkers5 found the cholesterol content of mesentery and temporal arterial tissue to be increased by 45% to 103% in four patients tested 22 months after surgery. This same group of researchers also found a decrease in HDL-cholesterol concentrations in seven patients tested 2 weeks to 2 years following surgery.6 Our study was designed to follow the changes in plasma lipids immediately after surgery and at various intervals for up to 3 years. Methods A jejunoileal bypass (25 cm of jejunum anastamosed to 50 cm of ileum) was performed on 23 morbidly obese patients - that is, individuals who weighed more than 120 kg, or more than twice the ideal weight - at St. Paul's HosFrom the departments of pathology and surgery. University of British Columbia, Vancouver Reprint requests to: Dr. J. Frohlich, Department of clinical biochemistry, Shaughnessy Hospital, 4500 Oak St., Vancouver, BC V6H 3N1 298

pital in Vancouver. This group consisted of 14 women and 9 men aged 17 to 54 years with a mean weight of 129 kg. With the patients fasting, blood was collected in tubes containing ethylenediamine tetra-acetic acid before the operation, 3 and 6 weeks following surgery, and at various intervals thereafter. A second group, 25 patients for whom no preoperative data were available, was studied 1, 2 and 3 years after the operation. All the blood samples were stored at - 200C. Cholesterol was analysed enzymatically,7 free cholesterol was analysed by the same procedure except for the omission of cholesterol esterase, and triglycerides were analysed by the procedure of Bucolo and David.8 All analyses were performed on an Abbott bichromatic analyser (ABA 100; Abbott Diagnostics, Diagnostic Instruments, South Pasadena, California). HDL was isolated with the use of heparin and manganese chloride, as described by Albers and colleagues.9 To minimize the analytic error all consecutive specimens from one patient were analysed in the same run. The day-today levels of precision of the analyses, based on a wide range of values, were 3% for cholesterol, 2% to 8% for free cholesterol, 5% for triglycerides, 9% to 14% for HDL-cholesterol and 10% to 14% for HDL-free cholesterol. The corresponding intrarun levels of precision were 4%, 4% to 5%, 2% to 6%, 2% and 4% to 5%. For the first group of patients the changes in composition of lipids in the plasma were expressed as percentages of each patient's own preoperative values. The percentage of change for a given time was taken as the average of all the individual percentages in this group. For the second group of patients averages of the absolute values were calculated. Results In the first group there was a

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rapid decrease in the total and free plasma cholesterol and the total and free HDL-cholesterol concentrations during the 6 weeks following bypass surgery (P < 0.01); the concentrations then stabilized (Table I). The plasma triglyceride concentrations varied: in some patients there was a decrease following surgery, in others an increase (Table I). The esterification of cholesterol was decreased following surgery in both total plasma and HDL-cholesterol (Table II). After 6 months there was an average weight reduction of 21 % and a decrease in HDL-cholesterol levels of 34% (Table I and Fig. 1). In the second group the HDLcholesterol concentration was still below the normal range in 13 of the 25 patients when tested 1, 2 and 3 years postoperatively (Table III). The total cholesterol concentrations in these patients were below or at the lower limit of the normal range, but the concentrations of other plasma lipids were within normal limits for all but one patient, who displayed a raised level of plasma triglyceride (303 mg/dl) 3 years after surgery. Discussion In the first group of patients studied following jejunoileal bypass surgery, the decrease in plasma lipid concentrations, except for those of triglycerides, was most pronounced during the first 6 weeks following surgery. Thereafter the levels stabilized. Weight loss, however, continued for at least a year. The triglyceride concentrations did not display a uniform trend, increasing in some cases for 3 to 6 weeks following surgery - probably a reflection of the mobilization of fat from body stores - and decreasing in others. Although impaired liver function is a common side effect of jejunoileal bypass surgery,' only a small percentage of our patients had biochemical evidence of liver damage. However, a minor degree of liver dysfunction

Table II Ratio of esterified to total cholesterol in 23 patients following jejunoileal bypass surgery

Measure Normal Preoperative; mean (and SEM)

Esterified/total cholesterol In all plasma sources In HDL fraction 0.66-0.75 0.66-0.75 0.73 (0.04) 0.70 (0.12) % of preoperative value; mean (and SEM)

Postoperative 3 wk, n =20 6 wk, n =18 3 mo, n =18 4 mo, n =9 6 mo, n =13 8 mo, n =4

92 (0.9) 90 (0.9) 90 (1.2) 91(1.0) 92(1.4) 89 (6.4)

93 (1.7) 92(1.6) 87 (2.9) 88 (3.4) 88 (3.5) 89 (6.0)

Table Ill-Lipid levels 1, 2 and 3 years following jejunoileal bypass surgery in 25 patients whose preoperative data were not available Plasma lipid levels (mg/dl); mean (and SEM) Months Following Surgery

Cholesterol In all plasma sources In HDL fraction Postoperative measure 1 yr, n =10 2 yr, n =8 3 yr, n =7

Triglycerides 118 (12) 117 (20) 107 (35)

Total 118 (12) 124 (12) 131 (19)

Free 36 (2) 35(2) 25 (4)

Total 31(2) 36 (3) 40 (5)

Free 11(1) 13 (1) 16 (1)

Table I-Plasma lipid and lipoprotein patterns and weight of 23 patients following jejunoileal bypass surgery*

Measure Normalt Preoperative; mean (and SEM)

Triglycerides 70-170 mg/dl

Plasma lipid levels Cholesterol In all plasma sources In HDL fraction Total Free Total Free 150-250 mg/dl 25%-33% of total 35-65 mg/dl 25%-33% of total

151 (14) mg/dl

208 (10) mg/dl

5.6 (2.5) mg/dl 39 (2.3) mg/dl % of preoperative value; mean (and SEM)

Postoperative 3 wk, n =20 103 (7) 66 (3) 80 (4) 6wk,n=18 88 (7) 56(3) 70(4) 3mo,n=18 35 (8) 57(4) 71(4) 4 mo, n =9 80 (9) 54 (4) 59 (9) 6 mo, n =13 85 (12) 56(4) 67 (5) 8 mo, n =4 140 (35) 58 (7) 67 (9) *HDL = high-density lipoprotein; SEM = standard error of the mean. .Range of a mixed (lean and obese) population, set by the division of clinical chemistry

76 (3) 66(3) 66(4) 62 (4) 66(4) 62 (3)

Weight 70 kg

12 (0.8) mg/dl

122.8 (5) kg

89 (3) 80 (4) 83 (3) 74 (10) 85 (6) 77(12)

91(1) 89(1) 85(1) 81(2) 79 (2) 73 (3)

of the Vancouver General Hospital.

pids are not known, we can only speculate on the role of the intestine in the development of these changes. A comparison of the effects of such surgical procedures for obesity as jejunoileal bypass and gastroplasty with simple dietinduced weight loss is warranted. So far the reports of changes in HDL-cholesterol following diet-induced weight loss are conflicting,11'13 and there have been no reports on changes in the plasma lipids of patients undergoing gastroplasty. We thank the nurses and staff of the gastrointestinal clinic at St. Paul's Hospital, Vancouver. This study was supported by a grant from the Department of National Health and Welfare. References 1. BRAY GA, GREENWAY FL, BARRY RE, BENFIELD JR. FIsER RL, DAHM5 WT, ATKINSON RL, SCHWARTZ AA:

Surgical treatment of obesity: a review of our experience and an analysis of published reports. Jut J Obes 1977; 1: 331-367 2. SHERMAN CD JR, MAY AG, NYE W, WATERHOUSE C: Clinical and meta-

bolic studies following bowel bypassing for obesity. Ann NY Acad Sci 1965; 131: 614-622 3. Scorr HW JR, DEAN RH, LEQUIRE V, SWIFT LL, YOUNGER RK, BUTTS WH: Alterations in plasma lipid

concentrations in normal and hyperlipidemic patients with morbid obesity before and after jejunoileal bypass. Am J Surg 1978; 135: 341-347 4. R6SSNER 5, HALLBERG D: Serum lipoproteins in massive obesity. A study before and after jejunoileal

shunt operation. Acta Med Scand 1978; 204: 103-110 5. KRAL JG, BONDJERS 6: Increased

arterial-tissue cholesterol after intestinal bypass in severe obesity. Lancet 1978; 2: 288-289 6. KRAL JG, BONDJERS G, GUSTAFSON A: Serum and arterial tissue cholesterol in severely obese patients

(abstr). Eur J Cliii invest 1978; 8: 339 7. ALLAIN CC, PooN LS, CHAN CS, RICHMOND W, FU PC: Enzymatic

determination of total serum cholesterol. Cliii Chem 1974; 20: 470-475 8. BUcoLo G, DAVID H: Quantitative determination of serum triglycerides by the use of enzymes. Cliii Chem

1973; 19: 476-482 9. ALBERS ii, WARNICK GR, WIEBE D, KING P, STEINER P, SMITH L, BRECKENRIDGE C, CHOW A, KUBA K, WEIDMAN 5, ARNE'IT H, WOOD P,

SHLAGENHAFT

A:

Multi-laboratory

comparison of three heparin-Mn2 + precipitation procedures for estimating cholesterol in high-density lipoprotein. Cliii Chern 1978; 24: 853856 10. GORDON I, CASIELLI WP, HJORTLAND MC, KANNEL WB, DAWBER TR: Diabetes, blood lipids and the role of obesity in coronary heart dis-

ease risk for women. The Framingham study. Ann Intern Med 1977; 87: 393-401 II. MILLER NE: The evidence for the antiatherogenicity of high density

lipoprotein in man. Lipids 1978; 13: 914-919 12. WilsoN DE, LEES RS: Metabolic relationships among the plasma lipoproteins. Reciprocal changes in the concentrations of very low and low density lipoproteins in man. J Clin invest 1972; 51: 1051-1057 13. HOWARD BV, SAVAGE PJ, NAGULESPARAN M, BENNION U, DAvIs M,

BENNETT PH: Changes in plasma lipoproteins accompanying diet therapy in obese diabetics. Atherosclerosis 1979; 33: 445-456

I BOOKS I This list is an acknowledgement of books received. it does not preclude review at a later date ELECTROMEDICAL INSTRUMENTATION. A Guide for Medical Personnel. P. Bergveld. 134 pp. lIlust. Cambridge University Press, Cambridge, 1980. $34.50, clothbound; $10.95, paperbound. ISBN 0-521-21892-6, clothbound; ISBN 0-52129305-7, paperbound FRONTIERS OF HORMONE RESEARCH. Vol. 7. The Entero-Insular Axis. Satellite Symposium to the 10th IDF-Meeting, Gottingen, September 7-8, 1979. Edited by W. Creutzfeldt. 310 pp. IlIust. S. Karger AG, Basel, 1980. $69. ISBN 3-8055-0795-X HANDBOOK OF ENDOCRINOLOGY. Diagnosis and Management of Endocrine and Metabolic Disorders. 2nd ed. Richard S. Dillon. 760 pp. IlIust. Lea & Febiger, Philadelphia, 1980. $62.50 (Can.). ISBN 0-8121-0642-3 HEMATOLOGY: Principles and Procedures. 3rd ed. Barbara A. Brown. 385 pp. lIlust. Lea & Febiger, Philadelphia, 1980. $26.50 (Can.). ISBN 0-8121-0707-1 INFLAMMATORY BOWEL DISEASE. 2nd ed. Edited by Joseph B. Kirsner and Roy G. Shorter. 693 pp. IlIust. Lea & Febiger, Philadelphia, 1980. $88.75 (Can.). ISBN 0-8121-0698-9 INTRODUCTION TO REFERENCE SOURCES IN THE HEALTH SCIENCES. Fred W. Roper and Jo Anne Boorkman. 252 pp. Illust. Medical Library Association, Inc., Chicago, 1980. $19. ISBN 0-912176-08-3 INVISIBLE ARMIES. The Impact of Disease on American History. Howard N. Simpson. 239 pp. The Bobbs-Merrill Company, Inc., New York, 1980. $12.95. ISBN 0-672-52659-X MANUAL OF LABORATORY IMMUNOLOGY. Julia E. Peacock and Russell H. Tomar. 228 pp. IlIust. Lea & Febiger, Philadelphia, 1980. $20.50 (Can.), paperbound. ISBN 0-8121-0719-5 MEDICAL STAFF COST CONTAINMENT 1980. Digest and Selected Bibliography. Division of Medical Services, American Hospital Association. 66 pp. IlIust. American Hospital Association, Chica-

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go, 1980. $7, members; $8.75, nonmembers. ISBN 87258-314-7 PEDIATRIC CARDIOLOGY. P. Syamasundar Rao and Max D. Miller. 298 pp. Illust. Medical Examination Publishing Co., Inc., Garden City, New York, 1980. $19.50, paperbound. ISBN 0-87488-140-4 EXAMINATION PERIODIC KEALTH MONOGRAPH. Report of a Task Force to The Conference of Deputy Ministers of Health. Task Force on the Periodic Health Examination. 194 pp. Illust. Canadian Government Publishing Centre, Hull, P0, 1980. $18.50 in Canada; $22.20 outside Canada PRACTICAL POINTS IN PLASTIC SURGERY. Stephen H. Miller, William P. Graham III, Thomas S. Davis. 453 pp. Illust. Medical Examination Publishing Co., Inc., Garden City, New York, 1980. $20, paperbound. ISBN 0-87488-719-4 PROGRESS IN HORMONE BIOCHEMISTRY AND PHARMACOLOGY. Volume 1. Michael Briggs and Alan Corbin. 301 pp. lIlust. Eden Press. Westmount, P0, 1980. $34.95. ISBN 0-88831-076-5 PROGRESS IN RESPIRATION RESEARCH. Vol. 13. Pulmonary Embolism. Selected Papers of the International Symposium on Pulmonary Circulation III, Prague, July 2-4, 1979. Edited by J. Widimsky. 189 pp. lIlust. S. Karger AG, Basel, 1980. $87. ISBN 3-80550487-X CURRENT OF SELF-ASSESSMENT KNOWLEDGE I.J CHILD & ADOLESCENT PSYCHIATRY. 2nd ed. Edited by G. Pirooz Sholevar. 188 pp. Medical Examination Publishing Co., Inc., Garden City, New York, 1980. $15, paperbound. ISBN 0-87488-287-7 SIXTH REPORT ON THE WORLD HEALTH SITUATION. 1973-1977. Part I: Global Analysis. World Health Organization. 290 pp. Illust. World Health Organization, Geneva, 1980. Price not stated, paperbound. ISBN 92-4-158004-6. Available from the Canadian Public Health Association, Ottawa

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