Caring for Bariatric Surgery Patients in the Wound Clinic

  Despite all the efforts from healthcare providers across the continuum, obesity in this country and around the world continues to increase in epidemic proportions. In 2013, the American Medical Association began to recognize obesity as “a disease,” although it has had its own International Statistical Classification of Diseases code for years. As any disease, it should have an algorithm for its treatment.

  Billions of dollars are spent on weight-loss programs and medications each year to varying degrees of success. According to the National Institutes of Health, surgery has proven to be the only option over the last several decades to significantly promote weight loss among patients diagnosed clinically as “morbidly obese.” The success rates of bariatric surgery today vary from 60-90%, according to the National Institutes of Health. Some bariatric surgeries have been deemed safer than medications used for obesity.

  However, while surgery is very efficacious and the best option for most patients, it can have significant side effects and complications depending on the surgery performed. Providers in the outpatient wound clinic must be cognizant of these challenges as more wound care patients qualify for and undergo these procedures while living with comorbidities such as diabetes, which has long been epidemic among this patient population. This article will assist the wound care specialist in identifying who might be eligible for such surgery and the postsurgical conditions that could present in the wound clinic after referring patients for bariatric procedures.

  NOTE: Before considering the complications associated with bariatric patients that can be seen in the clinic post-surgery, providers should ensure that patients have been counseled about their decision to move forward with surgery and understand their role to promote better health by following the dieting restrictions inherent with bariatric surgery and the importance of follow up with their healthcare providers. Likewise, the wound care specialist should be confident that the referred surgeon will be vigilant in helping patients achieve appropriate compliance. The earlier patients are appropriately referred for bariatric surgery, the easier it is to reverse, prevent, and treat obesity.

Who Are The Candidates?

  Several surgical procedures are available for weight loss that have either a restrictive or malabsorptive mechanism. Some surgeries will provide both properties.

  The variety of procedures, and occasional conversions from one procedure to another, testify to the fact that a “magic bullet” solution for weight-loss surgery does not exist. Any such procedure should be viewed as a tool to assist patients in losing weight, but surgery should not be used to force weight loss. Patient compliance to guidelines specific to procedures will determine success or struggle. Patients will need to conduct dietary and lifestyle modifications to accommodate and perpetuate weight loss if they want to be healthy and see long-term success with weight control.

  Typically, insurance companies with bariatric coverage will approve surgery on patients who have a body mass index (BMI) > 40. They also will approve patients between 35 and 40 BMI and obesity-related comorbidities including diabetes, hypertension, sleep apnea, and/or a constellation of other problems such as weight-bearing joint disease. Recently, indications for bariatric surgery have been moved to lower BMIs after the US Food and Drug Administration (FDA) reviewed data regarding the safety and efficacy of bariatric surgery for patients with BMI between 30 and 35 with obesity-related comorbidities. The Lap-Band System® (Apollo Endosurgery Inc.) is the only approved procedure for patients in this lower BMI category.

  Due to significant improvement in several morbid medical conditions such as hypertension and diabetes, bariatric surgery is gaining acceptance with yet lower BMI. Outside the US, bariatric surgery has demonstrated the ability to significantly improve diabetes in BMI < 30. Both malabsorptive and pure-restrictive bariatric surgeries have demonstrated much greater success in reversing and/or improving diabetes than any treatment without surgery and BMI has slowly been placed aside as the most significant indicator for bariatric surgery. A recent Australian randomized clinical trial published in Lancet Diabetes & Endocrinology compared multidisciplinary diabetes care alone or with laparoscopic adjustable gastric band surgery. In the gastric band with multidisciplinary care, 52% of patients achieved diabetes remission compared to only 8% in multidisciplinary alone.

  Most would agree that follow up is mandatory to reassure patient compliance, but not all patients fulfill this need. Surgeries that have an adjustability embedded to them such as the laparoscopic adjustable gastric band (LAGB) are more likely to cause patients to return for follow up to determine if the band requires an adjustment. It is then the practice’s responsibility to spend the appropriate time evaluating, educating, and encouraging patients to adhere to guidelines recommended by the bariatric practice. (The wound clinic should be in the know on these.) The procedures that cannot be “adjusted” may give the false impression that follow up is not as important.

  The surgeries that promote malabsorption for the most part are not adjustable and patients tend to ignore the importance of regular follow up. Patients that now have malabsorption must follow the required multivitamin, mineral, and protein supplementation as recommended by the bariatric practice or complications (which are addressed later in this article) will occur. With increasing numbers of patients undergoing bariatric surgery, physicians other than the initial surgeon will need to become aware and involved in the follow up of such patients.

Surgery’s Nutritional Effects On Wound Healing

  Protein deficiency is seen in some malabsorptive bariatric surgeries and wound healing is compromised due to decreased angiogenesis and fibroblast proliferation. This results in decreased synthesis, accumulation, and remodeling of collagen.^1,2

  Hypoalbuminemia leading to tissue edema occurs with an albumin level below 3.0 g/dL. This will lead to decreased oxygen delivery as diffusion distances are increased. Wound healing is significantly compromised at levels of 2.5 g/dL.^3,4 Normal wound healing cannot occur at levels less than 2.0 g/dL.⁵ Adequate protein replacement decreases the rate of muscle catabolism, increases fibroblast activity with increased collagen synthesis, and improves immune response. Addition of diets rich in glutamine and arginine improves wound healing.

  Various vitamin deficiencies should also be anticipated. Severe vitamin C deficiency can result in dehiscence of previously healed wounds. Vitamin C is a cofactor in the hydroxylation of proline and lysine for procollagen formation. Procollagen residues are then altered intracellularly to form collagen. Ascorbic acid deficiency will impair the rate and the quality of collagen production. This will lead to delayed healing, weaker scars, and abnormal capillary formation. Vitamin C also facilitates leukocyte migration into the wound and plays a bactericidal role by contributing to the formation of neutrophil superoxides.

  Vitamin A deficiency is probably more common than reported. Vitamin A is important in most stages of wound healing since its deficiency affects monocyte and macrophage stimulation, fibronectin deposition, cellular adhesion, crosslinking of collagen, and tissue repair.⁶ Vitamin A can also ameliorate the deleterious effect of steroids in wound healing and counteract some of these effects by restoring the inflammatory response and promoting re-epithelialization and the synthesis of collagen and ground substances, but does not reverse the detrimental effects of glucocorticoids on wound contraction and infection.⁷ Vitamin A allows lysosomal membrane stabilization and phagocytosis in a wound and functions in cell-mediated cytotoxicity, cytokine production, and antibody response.⁸

  Vitamin E holds both positive and negative effects in wound healing. A known antioxidant with anti-inflammatory properties, vitamin E alters prostaglandin production by inhibiting phospholipase A2 activity, resulting in decreased collagen production and decreased inflammation. However, higher doses of vitamin E can lead to delayed wound healing.⁹ Still, diabetic patients may have some benefit in wound healing with supplementation, as vitamin E appears to influence cell differentiation, epithelialization, cell-mediated immunity, early inflammatory response, and angiogenesis.^10,11

  Vitamin K is vital in the normal clotting cascade. Hemostasis in the earlier phases of inflammatory stage of wound healing depends on blood clotting. Deficiencies in vitamin K will affect the synthesis of prothrombin and factors II, VII, IX, and X.

  Other traces of element deficiencies are commonly overlooked as well. Among the ones seen in abnormal wound healing, iron and zinc are most significant.

  Iron is an essential cofactor in the replication of DNA. Iron and ribonucleotide reductase are involved in the production of deoxyribonucleotides needed for DNA synthesis. A co-factor in the hydroxylation of lysine and proline in collagen synthesis, iron also allows for normal configuration of the collagen triple helix.

  Zinc deficiency can be present in patients with malabsorptive surgeries just as in those with profuse sweating, chronic alcoholism, cirrhosis, large burns, gastrointestinal fistulas, and severe surgical trauma. Zinc is an essential co-factor in normal cellular growth and replication. Deficiency directly impairs epithelialization and fibroblast proliferation through its effects on metalloenzymes such as RNA polymerase, DNA polymerase, and DNA transcriptase. Zinc is involved in immune responses including phagocytosis, cellular and humoral immunity, and bactericidal activity. Delayed wound healing is seen in the earlier phases with zinc deficiency.^12-14

Other Avoidable Complications

  Regurgitation after bariatric surgery is commonly seen during the first few months. Described as “spitting up food that was stuck,” this can initially be experienced 1-3 times per week and is normally attributed to not chewing food adequately or overeating. Patients must adjust to the intentionally smaller gastric pouch and the smaller opening seen on the gastric band, gastric bypass, and sleeve gastrectomy.

  Most patients will eventually learn to slow down how fast they eat and chew their food well. However, if regurgitation becomes frequent, potassium and/or magnesium levels often will be low. Patients will need oral replacement; however this may not be well tolerated due to the “bad taste.” Chronic regurgitation and dysphagia can be associated with gastrointestinal strictures. Healthcare professionals, especially within bariatric practices, should evaluate the patient further.

  Dysphagia to “chunkier” foods also becomes a common find. With LAGB, an upper gastrointestinal evaluation with contrast and appropriate adjustment of the band may be required. Endoscopic evaluation should be strongly considered after all procedures to evaluate and treat stenosis. Some studies demonstrate abnormal findings at endoscopy with stomal stenosis in 39% of patients with nausea, vomiting, or dysphagia referred for endoscopy.¹⁵ Such stenosis can usually be treated by balloon dilation at the time of diagnosis. Many of these patients will require repeat dilations to improve the ability to tolerate most solid foods.

  Dumping syndrome can also be seen after malabsorptive procedures such as gastric bypass and sleeve gastrectomies, but not as frequently as in other surgeries. Foods with high osmolarity, salt, or sugar can cause an osmotic overload upon entering the small intestine. These procedures also diminish the stomach’s ability to grind food into small particles, allowing undigested food to go distally and contribute to the problem. This osmotic reaction promotes release of fluid into the small intestine with vagal response. Patients will develop sweating and lightheadedness after eating high osmotic meals or if they drink fluid with a meal. Diarrhea can occur and contribute to the fatigue seen in these cases. Again, electrolyte levels must be checked and replaced (potassium in particular).

  Dehydration is commonly seen after all bariatric surgeries. Patients living with obesity commonly require significantly more water intake compared to those with normal BMI. Restrictive procedures will promote a funnel effect. As long as drinking occurs slowly, liquids will pass through the restricted, funneled area. However, a habit of gulping liquids will cause regurgitation that can lead to maladaptive behavior, resulting in patients not seeking water at a healthy amount. Also, malabsorption procedures can induce dumping syndrome if patients eat and drink at the same time. Diarrhea can cause dehydration as well as a tendency to drink less often. Patients therefore need to be encouraged to drink frequently and in between meals.

  Protein malnutrition is particularly worse with malabsorptive procedures, such as biliopancreatic diversion with or without duodenum switch, that are used less frequently than in the past due to complications; it is not as severe with gastric bypass and is mostly absent in pure-restrictive surgeries such as the gastric band. Risk increases if the patient fails to eat protein. Gastric bypass patients should be encouraged to eat significantly more protein because the procedure causes hypoproteinemia. Lack of follow up limits assessment to determine required caloric and protein needs.¹⁶ At 3-6 months post-surgery, patients will experience diffuse shedding of normal hair that can last up to 12 months. Also, the stress of weight loss disrupts the normal growth cycle of individual hairs, resulting in large numbers of growing hair simultaneously entering the dying (telogen) phase. Although there is no known treatment, this usually reverses without intervention.¹⁷ Topical Minoxidil can be very helpful.

  Anemia can develop after any bariatric surgery for different reasons, even after pure-restrictive procedures that will not cause malabsorption. Patients require follow up with dietary evaluation to ensure oral intake will include iron-rich food or appropriate iron supplements. In case of too much restriction in gastric band patients, dysphagia can develop and explain patient reluctance in choosing meats and food that refills iron storages.

  Adjustment of the band is indicated to facilitate consumption of appropriate foods. Strictures can develop in surgeries such as sleeve gastrectomy or bypass surgery and should also be addressed and corrected with endoscopic dilatations. Malabsorptive bariatric procedures reduce gastric capacity and consequently hydrochloric acid production. This reduces the conversion of Fe3+ into the more absorbable Fe2+ ion, limiting further absorption. Blood loss can also be a cause for anemia. Ulcers at the anastomoses between the stomach pouch and the small intestine can be a cause of blood loss.

  Osteopenia is a significant problem that is underestimated by patients and practices following malabsorptive bariatric procedures. According to John Dixon, MBBS, PhD, FRACGP, FRCP (Edin), International Bariatric Club, bone fracture rates are four times higher among bariatric patients. Compromised calcium absorption linked to low levels of vitamin D exacerbates the problem and a simple test of calcium level generally will miss the real picture. Chronically, the parathyroid will adapt to the tendency of low levels of calcium. Hyperparathyroidism will develop and sequestration of calcium from the bones will tend to maintain the homeostasis of calcium in the blood. Secondary hyperparathyroidism has been reported to occur in 29% of patients following gastric bypass.^18-20

  Unfortunately, the process will lead to bone demineralization in gastric bypass patients and other malabsorptive surgeries.^21-23 Patients will require bone scans, parathyroid, calcium, and vitamin D levels for better evaluation. The majority of the patients with secondary hyperparathyroidism will respond to replacement of vitamin D with normalization of parathyroid hormone. Vitamin D and calcium supplementation at the usual recommended daily requirements did not normalize parathyroid hormone levels in some studies.¹⁹

  Fat malabsorption can be experienced after some surgeries and is frequently seen in the biliopancreatic diversion and duodenum switch (although, there has been a reduction in the number of these surgeries due to higher rates of complications). The procedure involves a gastric restriction and diversion of bile and pancreatic enzymes into the distal ileum.²⁴ A segment of small bowel will then be able to absorb all the nutrients that require bile and pancreatic enzymes. Additionally, protein deficiency and fat-soluble vitamin (A, D, E, and K) deficiencies are more pronounced. Due to fat malabsorption, severe vitamin D deficiency will develop along with an already reduced ability to absorb calcium.²⁵ Patients will also present with bone fractures due to osteopenia. Fat-soluble vitamins will be deficient in 66% of patients within four years of surgery. Up to 50% will develop hypocalcemia, and all patients with low vitamin D will have secondary hyperparathyroidism.^{26, 27} The treatment in these patients will mandate use of pancreatic enzyme replacement. Some patients will report some weight regain, a reason for noncompliance.

  Understanding physiologic metabolism and absorption of minerals and vitamins is crucial to proper prevention and treatment of potential disarrangement seen after bariatric surgery. Normally, the duodenum and proximal jejunum are the primary sites of small bowel digestion and absorption.²⁸ Pancreatic enzymes convert starch molecules into simple sugars such as oligosaccharides and disaccharides.²⁹ These sugars are then broken down further into monosaccharides by specific disaccharidases enzymes present in the brush border of the intestinal mucosa.²⁹ The presence of protein and fat in the proximal duodenum will cause release of cholecystokinin that will stimulate the release of bile and lipase.²⁸ Protein digestion is completed in the duodenum by pancreatic proteolytic enzymes in the brush border of the small intestine.^28,30 Dipeptides and tripeptides are absorbed by specific transporters, as are individual amino acids.²⁸ Triglycerides are digested into monoglycerides and fatty acids by pancreatic lipase in the small intestine. Cholesterol and cholesterol esters combine with bile salts to create micelles.²⁸ The distal ileum absorbs vitamin B12/intrinsic factor complex in addition to 95% of intestinal bile acids that are “recycled” back to the liver for reuse.²⁸

  Several minerals (eg, calcium, iron), vitamins, trace elements (eg, zinc, selenium), and most of the remaining luminal fluid water are absorbed before reaching the colon. Most vitamins enter the bloodstream by passive diffusion in their original form.³¹ Mineral absorption into the body can be divided into three stages: intraluminal, which involves the chemical interactions that occur in the stomach and intestines; translocation, which involves passage across the membrane into the intestinal mucosal cells; and mobilization, in which minerals are either stored within the cells or are carried across the intestinal cells into the bloodstream.³¹ Similar to amino acid and monosaccharide absorption, minerals require the presence of specific carriers and utilize adenosine triphosphate for active transport.

  The colon is the site of absorption for water, salts, and vitamins created by bacterial action within the organ.³¹ These specific vitamins are synthesized when colon bacteria digest materials that have not already been absorbed before they reach the large intestine; vitamins K and B12, thiamin, and riboflavin are included in this group.³¹ The colonocytes usually utilize butyric acid for energy. Years after bypass surgery, cells will adapt and start absorbing carbohydrates. This explains why patients who have not followed dietary recommendations can regain most or all the excess weight.

Addressing The Pain Component

  All NSAIDs (nonsteroidal anti-inflammatory drugs), including aspirin and cyclooxygenase-2 inhibitors, have ulcerogenic capabilities; their use should be avoided at all costs in gastric bypass patients. They unfortunately are also the ones proven to really provide some relief of pain. However, obesity commonly causes weight-bearing joint disease. Patients will have to choose between constant joint pain and the risks of ulcers in some instances. Marginal ulcers can be seen in up to 27% of patients.¹⁵ Another significant contributor for anastomoses ulcers is smoking. Discussions regarding the concerns of smoking and ulcers should be disclosed and heavily prohibited in patients contemplating bariatric surgery that uses any anastomosis. Addiction to smoking may cause more care planning difficulty.

Common Bariatric Surgeries

  Gastric Band
  A restrictive surgical procedure. A silicone band and an injection port are surgically placed. Silicone band is placed around the upper part of the stomach and molds the stomach into two connected chambers. The superior part of the stomach, the “pouch,” will promote satiety when distended. The sensation of being “satisfied,” not “hungry,” will facilitate weight loss. Patients will enjoy early sensation of not being hungry and satiety will last hours. The injection port is attached to the abdominal wall, underneath the skin. The port is connected to the band by means of soft tubing. The port will allow adjustments, if needed. The device can be properly optimized to maintain a sense of satiety that will greatly facilitate patients in regaining control of the constant hunger. The band does not alter the digestive function. Consumed food passes through the digestive tract in the normal manner.

  Gastric Bypass
  Uses a combination of restriction and malabsorption. Surgeon creates a small gastric pouch by firing staples that will permanently divide the upper and lower portion of the stomach. Surgeon then attaches a Y-shaped loop of the small intestine (jejunum) directly to the pouch. Ingested food and liquids go down through the “alimentary” loop, and bile and pancreatic enzymes go separately through the alimentary loop. This allows intake to bypass a large portion of the small intestine. The gastric pouch causes patients to feel satiety sooner and eat less food; bypassing a portion of the small intestine means the patient’s body absorbs fewer calories. Bile and pancreatic enzymes needed for digestion and absorption will only join the “alimentary” loop further down where it meets the “bile and pancreatic” loop.

  Vertical Sleeve Gastrectomy
  A restrictive bariatric surgery used in the past as the first step in a two-stage procedure such as duodenum switch with biliopancreatic diversion. Due to significant morbidity associated with the second stage, sleeve gastrectomy has been used as a bariatric procedure by itself. During this procedure, the surgeon creates a small, sleeve-shaped stomach. It is larger than the stomach pouch created during Roux-en-Y bypass and is about the size of a banana. Not as common as the malabsorptive procedures, the sleeve can also be associated with some vitamin and mineral deficiency in the long term. It has been reported that deficiencies in intrinsic factor, vitamins such as D and B12 and minerals such as iron, and zinc.³² The grinding effect of the normal stomach is reduced, as is the amount of acid and intrinsic factor. After surgery, the patient will experience satiety as with any restrictive surgery. Food is seen to leave the stomach faster and can rarely causes dumping syndrome.

  Biliopancreatic Diversion
  Biliopancreatic diversion with duodenal switch (BPD/DS) is very similar to gastric bypass. Instead of a small stomach pouch, the surgeon creates a sleeve-shaped stomach, then attaches the final section of the small intestine to the stomach sleeve. A greater segment of the intestine is bypassed to ensure far fewer calories are absorbed. Also, bile and pancreatic enzymes will join the alimentary loop distally in the small intestine. Patients tend to lose more weight compared to other surgical procedures; however, there is a significantly higher incidence of complications. Due to significant compromise in fat digestion, patients tend to experience abdominal bloating and foul-smelling stool. Fat-soluble vitamin absorption is commonly reduced.

References

1. Huang CS, Forse RA, Jacobsone BC, Farraye FA. Endoscopic findings and their clinical correlations in patients with symptoms after gastric bypass surgery. Gastrointest Endosc. 2003;58:859-866.

2. Moize V, Geliebter A, Gluck ME, Yahav E, Lorence M, Colarusso T, Drake V, Flancbaum L: Obese patients have inadequate protein intake related to protein intolerance up to 1 year following Roux-en-Y gastric bypass. Obes Surg. 2003;13:23–28.

3. Bolognia JL, Braverman IM. Skin manifestations of internal disease. Harrison’s Principles of Internal Medicine. 15th ed. Braunwald E, Ed. New York. McGraw-Hill;2001, p. 315–330.

4. Shaker JL, Norton AJ, Woods MF, Fallon MD, Findling JW. Secondary hyperparathyroidism and osteopenia in women following gastric exclusion surgery for obesity. Osteoporos Int. 1991;1:177–181.

5. Goode LR, Brolin RE, Hasina A. Bone and gastric bypass surgery: effects of dietary calcium and vitamin D. Obes Res. 2004;12:40–46.

6. Fujioka K, Lee M, Dailey GE: Secondary hyperparathyroidism after bariatric surgery for morbid obesity (Abstract). Obes Res. 2004;12:A37.

7. Coates PS, Fernstrom JD, Fernstrom MH, Schauer PR, Greenspan SL: Gastric bypass surgery for morbid obesity leads to an increase in bone turnover and a decrease in bone mass. J Clin Endocrinol Metab. 2004;89:1061–1065.

8. Collazo-Clavell ML, Jimenez A, Hodgson SF, Sarr MG: Osteomalacia after Roux-en-Y gastric bypass. Endo Pract. 2004;1:195–198.

9. von Mach MA, Stoeckli R, Bilz S, Kraenzlin M, Langer I, Keller U: Changes in bone mineral content after surgical treatment of morbid obesity. Metabolism. 2004;53:918–921.

10. Consensus Development Conference Panel: NIH conference: gastrointestinal surgery for severe obesity. Ann Intern Med. 1991;115:956–961.

11. Chapin BL, Lemar HJ Jr, Knodel DH, Carter PL: Secondary hyperparathyroidism following Biliopancreatic diversion. Arch Surg. 1996;131:1048–1052.

12. Slater GH, Ren CJ, Siegel N, Williams T, Barr D, Wolfe B, Dolan K, Fielding GA: Serum fat-soluble vitamin deficiency and abnormal calcium metabolism after malabsorptive bariatric surgery. J Gastrointest Surg. 2004;8:48–55.

13. Newbury L, Dolan K, Hatzifotis M, Low N, Fielding G: Calcium and vitamin D depletion and elevated parathyroid hormone following biliopancreatic diversion. Obes Surg. 2003;13:893–895.

14. Caspary WF. Physiology and pathophysiology of intestinal absorption. Am J Clin Nutr. 1992;55:299S–308S.

15. Levin RJ. Digestion and absorption of carbohydrates from molecules and membranes to humans. Am J Clin Nutr. 1994;59:690S–698S.

16. Murray RK, Kotlikoff MI. Receptor-activated calcium influx in human airway smooth muscle cells. J Physiol. 1991;435:123–144.

17. Senel O, Cetinkale O, Ozbay G, et al. Oxygen free radicals impair wound healing in ischemic rat skin. Ann Plast Surg. 1997;39(5):516–23.

18. Breslow RA, Hallfrisch J, Guy DG, et al. The importance of dietary protein in healing pressure ulcers. J Am Geriatr Soc. 1993;41:357–62.

19. Daly JM, Reynolds J, Sigal RK, et al. Effect of dietary protein and amino acids on immune function. Crit Care Med. 1990;18:S86.

20. Doweido JP, Nompleggi D. The role of albumin in human physiology and pathophysiology. Part III. Albumin and disease states. J Parenter Enteral Nutr. 1991;15:476.

21. Dempsey DT, Mulled JL, Buzby GP. The link between nutritional status and clinical outcome: can nutritional intervention modify it? Am J Clin Nutr. 1998; 47(Suppl 2):352–6.

22. Robson MC, Phillips LG, Lawrence WT. The safety and effect of topically applied recombinant basic fibroblast growth factor on the healing of chronic pressure sores. Ann Surg. 1992;216(4):401–6.

23. Weinzweig J, Levenson SM, Rettura G, et al. Supplemental vitamin A prevents the tumor-induced defect in wound healing. Ann Surg. 1990;211:269.

24. Anstead GM. Steroids, retinoids, and wound healing. Adv Wound Care. 1998;11(6):277–85.

25. Ross AC. Vitamin A and protective immunity. Nutr Today. 1992;27:18.

26. Ehrlich HP, Hunt TK. The effects of cortisone and anabolic steroids on the tensile strength of healing wounds. Ann Surg. 1969;170:203–6.

27. Tanka TH, Fujiwara H, Torisu M. Vitamin E and the immune response. Immunology. 1979;38:727.

28. Taren DL, Chavpil M, Weber CW. Increasing the breaking strength of wounds exposed to preoperative irradiation using vitamin E supplements. Int J Vit Nutr Res. 1987;57:133.

29. Argren MS. Studies on zinc in wound healing. Acta Derm Venereol. 1990;154(Suppl):1.

30. Argren MS, Franzen L. Influence of zinc deficiency on breaking strength of 3-week-old skin incisions in the rat. Acta Chir Scand. 1990;156:667.

31. Lansdown AB, Sampson B, Rowe A. Sequential changes in trace metal, metallothionein and calmodulin concentrations in healing skin wounds. J Anat. 1999;195(Pt 3):375–86.

  Michael Baptista is bariatric and general surgeon with Florida Surgical Physicians, Jacksonville, FL.