The American Journal of Surgery 188 (2004) 200 –203
Scientific paper
Effect of human pancreatic juice and bile on the tensile strength of suture materials M.A. Tolga Muftuoglu, M.D.*, Erkan Ozkan, M.D., Abdullah Saglam, M.D. Fourth General Surgical Department of Haydarpasa Numune Teaching and Training Hospital, Uskudar 34668, Istanbul, Turkey Manuscript received September 5, 2003; revised manuscript December 28, 2003
Abstract Background: Several suture materials are used for pancreatojejunal anastomosis. In this study, we tested the durability of these suture materials in human pancreatic juice and bile. Methods: Plain and chromic catgut, polyglactin 910, polyglycolic acid, polydioxanone, polypropylene, and silk sutures were incubated in pancreatic juice and bile that was collected from patients. Fifteen samples of each type of suture material were placed in human juices for 1, 3, and 7 days. Tensile strengths were measured with a tensionmeter. Results: Plain and chromic catgut disintegrated in pancreatic juice and pancreatic juice plus bile mixture. Polyglycolic acid and polyglactin 910 suture materials were vulnerable to pancreatic juice within 7 days. Polydioxanone retained most of its initial strength in pancreatic juice and bile. Polypropylene and silk retained 84% and 92% of their initial strength, respectively. Conclusions: We found that polidioxanone was the strongest suture material in pancreatic juice. © 2004 Excerpta Medica, Inc. All rights reserved. Keywords: Bile; Pancreatic juice; Suture materials
Surgeons have been performing various pancreaticoduodenal operations for many years. A pancreatic fistula is the most dreaded complication of pancreas surgery. Ten to 20% anastomotic dehiscence rates have been reported even by specialized centers. It is still unclear why pancreaticojejunostomy has a higher failure rate compared with surgeries for other anastomoses in the body. Various nonabsorbable and absorbable suture materials are used in pancreas surgery. Some differences exist among these materials. They are accepted to be basically safe when in use. Whether or not the type of anastomotic suture material influences fistula rate remains unclear. Gastric juice, bile, and pancreatic fluid drain into this region. Bile is an alkaline fluid containing water, electrolytes, bile salts, proteins, lipids, and bile pigments. Pancreatic fluid contains approximately 15 enzymes or precursors of enzymes. Proteolytic enzymes in the body digest catgut suture material. Other synthetic absorbable suture materials are absorbed via hydrolytic degradation. Enzymatic degra* Corresponding author. Tel.: ⫹90 532 364 37 07; fax: ⫹90 216 330 70 51. E-mail address:
[email protected]
dation elicits more reaction than do hydrolytic reactions in the body. Nonabsorbable sutures can be absorbed over the years. Sutures placed within the pancreaticojejunal anastomotic line are in contact with these highly digestive fluids. To our knowledge, only a few studies in the literature have investigated the effect of pancreatic fluid and bile on suture materials. The aim of this study was to observe the effects of pancreatic juice and bile on absorbable and nonabsorbable suture materials.
Methods A push-pull scale (IMADA Force Measurement; Hans Schmidt, Waldkraiburg, Germany), a dial-type instrument designed to measure material tension, was used in this study. Polydioxanone (PDS), vicryl polyglactin 910 (coated vicryl), polyglycolic acid (Dexon), plain catgut (surgical gut suture–plain), chromic catgut (surgical gut suture– chromic), silk, and polypropylene (Prolene) (all from Ethicon, Edinburgh, Scotland, United Kingdom) were tested. All suture materials measured 4/0, which is the most frequently preferred size for pancreaticobiliary surgery. Pancreatic
0002-9610/04/$ – see front matter © 2004 Excerpta Medica, Inc. All rights reserved. doi:10.1016/j.amjsurg.2003.12.068
M.A. Tolga Muftuoglu et al. / The American Journal of Surgery 188 (2004) 200 –203 Table 1 Mean baseline tensile strengths (mean ⫾ SD) of suture materials Plain catgut (N) Chromic catgut Polyglycolic acid Polyglactin 910 Polydioxanone Polypropylene Silk
11.2 ⫾ 0.2 12.3 ⫾ 0.2 13.2 ⫾ 0.1 13.6 ⫾ 0.2 12.6 ⫾ 0.1 12.1 ⫾ 0.1 9.6 ⫾ 0.2
N ⫽ newtons.
juice was collected from 1 patient with a diagnosis of pancreatic head carcinoma who underwent pancreaticoduodenectomy with external intrapancreatic drainage catheter. Each day, 200 to 300 mL pancreatic secretion was drained into the catheter bag during postoperative days 3 to 15. Percutaneous transhepatic catheter was established in another patient with irresectable proximal bile duct carcinoma, and bile was collected into the bag. Written informed consent was obtained from these 2 patients for the use of their body fluids in this study. For the in vitro testing of suture materials, 3 types of incubation material were prepared by using the pancreatic fluid and bile (pure pancreatic fluid, pure bile, and 50%/50% mixture). Initially, to serve as the control, suture materials were tested for their baseline tensile strength. Afterward, fifteen 50-cm lengths of each suture material were incubated into bags containing pure bile, pure pancreatic juice, and the 50%/50% mixture for 1, 3, and 7 days and were stored at 37°C. Pancreatic juice and bile were replaced every 24 hours. The experiments were repeated at the end of days 1, 3, and 7. After exposure, each suture material was tied to the small hook located at the upper tip of the tensionmeter. The other end of the suture was fixed to the extension shaft, which is an attachment of the tensionmeter. The shaft was pulled gently until the suture material was torn apart, and the measurement was read and recorded from the Push-Pull Scale in newtons. Statistical analysis was performed using SPSS version 10 (SPSS, Chicago, Illinois). Kruskal-Wallis nonparemetric analysis of variance test was used to compare the mean retained tensile strengths of the suture materials. A P value ⬍0.05 was considered significant. Results are presented as mean plus/minus SD.
201
Table 2 Mean ⫾ SD (%) of retained tensile strengths of suture material in pancreatic juice Suture materials
Day 1 Retained tensile strength N (%)
Day 3 Retained tensile strength N (%)
Day 7 retained tensile strength N (%)
Plain catgut Chromic catgut Polyglycolic acid Polyglactin 910 Polydioxanone Polypropylene Silk
Dis (0) Dis (0) 12.8 ⫾ 0.1 (96) 13.2 ⫾ 0.1 (97) 12.6 ⫾ 0.0 (100) 12.1 ⫾ 0.1 (96) 8.8 ⫾ 0.1 (91)
Dis (41) Dis (73) 8.6 ⫾ 0.2 (59) 9 ⫾ 0.1 (60) 11.6 ⫾ 0.1 (95) 9.8 ⫾ 0.1 (88) 8.2 ⫾ 0.1 (91)
Dis (0) Dis (0) Dis (0) Dis (0) 11.3 ⫾ 0.1 (89) 9.4 ⫾ 0.1 (77) 8 ⫾ 0.1 (83)
DIS ⫽ disintegrated; N ⫽ newtons.
catgut retained only 45% of initial strength after 7 days in bile. Polyglycolic acid and polyglactin 910 preserved 95% to 99%, respectively, of initial tensile strength in pancreatic juice, bile, and mixture on the first day. On day 3, polyglycolic acid and polyglactin 910 retained 65% and 66%, respectively, of initial strength in pancreatic juice and 59% and 60%, respectively, in bile. Surprisingly, they disintegrated in pancreatic juice and significantly lost initial strength in bile on day 7. We found that polydioxanone had the greatest tensile strength in pancreatic juice and bile and maintained its integrity at 89% in pancreatic juice, 92% in bile, and 93% in mixture on day 7. These were the highest scores in the experiments. Nonabsorbable sutures are considered permanent sutures and provide more tensile strength compared with absorbable sutures. Tensile strength for polypropylene was 96% on day 1, 81% on day 3, and 77% on day 7 in pancreatic juice and 96% on day 1, 85% on day 3, and 81% on day 7 in bile. Again silk, lost its tensile strength by 17% and 11%, respectively, in pancreatic juice and bile on day 7. Significant differences were noted in the mean retained tensile strengths among nonabsorbable and absorbable sutures in pancreatic juice, bile, and mixture on days 1, 3, and 7 (P ⬍0.0001). Moreover, the mean tensile strengths of polydioxanone in bile, in mixture, and mainly in pancreatic juice were significantly higher than other nonabsorbable sutures on days 1, 3, and especially 7. At the end of the study, polydioxanone was the most resistant suture material to pancreatic juice and bile.
Results Comments The measurements are listed in Tables 1, 2, 3, and 4. Plain and chromic catgut were highly susceptible to digestion by pancreatic juice, and plain catgut was the weakest suture material in this experiment. Even at the end of the first day, plain and chromic catgut disintegrated in pancreatic juice and mixture. Plain and chromic catgut retained 41% and 73%, respectively, of initial strength 3 days after exposure to bile. Plain catgut disintegrated and chromic
Currently available different surgical suture materials, including absorbable and nonabsorbable types, have provided satisfactory performance for many years in surgical practice. Surgical suture materials are widely used in pancreatic surgery. Biliary and especially pancreatic surgery still have a high fistula rate. We do not have enough data to explain this complication. Various factors are involved in
202
M.A. Tolga Muftuoglu et al. / The American Journal of Surgery 188 (2004) 200 –203
Table 3 Mean ⫾ SD (%) retained tensile strengths of suture material in bile Suture materials
Day 1 Retained tensile strength N (%)
Day 3 Retained tensile strength N (%)
Day 7 Retained tensile strength N (%)
Plain catgut Chromic catgut Polyglycolic acid Polyglactin 910 Polydioxanone Polypropylene Silk
6.1 ⫾ 0.1 (55) 9.2 ⫾ 0.2 (76) 13.1 ⫾ 0.0 (99) 12.8 ⫾ 0.1 (94) 12.6 ⫾ 0.1 (100) 11 ⫾ 0.1 (91) 9 ⫾ 0.1 (93)
4.6 ⫾ 0.1 (41) 8.2 ⫾ 0.1 (73) 7.8 ⫾ 0.1 (59) 8.2 ⫾ 0.2 (60) 12 ⫾ 0.1 (95) 10.6 ⫾ 0.1 (88) 8.8 ⫾ 0.1 (91)
Dis (0) 5.4 ⫾ 0.1 (45) 4.2 ⫾ 0.1 (31) 5.1 ⫾ 0.1 (37) 11.6 ⫾ 0.1 (92) 10.4 ⫾ 0.1 (85) 8.6 ⫾ 0.1 (89)
N ⫽ newton; Dis ⫽ disintegrated.
this issue. Could suture material be a factor in the occurrence of fistula [1]? We tried to answer the question of whether or not any risk of fistula formation arises from different suture materials. Pancreatic juice was collected by way of intrapancreatic drainage catheter during our experiment. Pancreatic enzymes are proteolytic, lipolytic, and amylolytic. Whereas lipase and amylase are secreted as active forms, the others are proenzymes, meaning that these proenzymes were not activated by intestinal enterokinase because they did not come in contact with the intestinal wall in our study. Therefore, our experimental design perfectly meets appropriate conditions to test the resistance of the suture materials in the setting of pancreatic anastomosis as well as Whipple procedure. Plain catgut is a natural absorbable suture material obtained from the collagen of the submucosal layer of sheep. Because of the high protein content of plain and chromic catgut, both are sensitive to proteolytic digestion. Catgut has become less popular among surgeons, who now favor synthetic absorbable sutures. Synthetic absorbable sutures—such as polyglycolic acid, polyglactic acid, and polydioxanone— degrade more slowly and produce less inflammatory reaction. These synthetic sutures are reabsorbed by hydrolysis. Polyglycolic acid and polyglactic acid are completely reabsorbed within 60 to 90 days. They retain 70% of initial strength at 10 days and 30% at 20 days. Polydiox-
anone is a monofilament synthetic absorbable suture, the absorption of which is completed within 180 days. It loses 50% of initial strength after 35 days. Hydrolytic and enzymatic reactions take place throughout the body and vary from site to site. Hence the selected suture material must maintain its strength for a reasonable time in different parts of the body. Limited numbers of articles have been published that investigate this issue. Previous studies have provided evidence of deleterious effects of gastrointestinal fluids on suture materials. In 1977, Mizuma et al. studied catgut, polyglycolic acid, and nylon in canine bile and pancreatic juice [1,2]. They demonstrated slower and more consistent loss of strength with polyglactin 910 and polyglycolic acid compared with catgut sutures. Deveney and Way showed that polyglactin 910 and polyglycolic acid were superior to catgut for use in gastrointestinal anastomoses [2]. In our study, catgut disintegrated in pancreatic juice, bile, and mixture within 24 hours. Plain catgut disintegrated and chromic catgut retained only 45% of initial strength in bile on day 7. Many published studies exist showing that synthetic suture materials can provide better clinical performance compared with catgut [1– 4]. Therefore, the clinical use of catgut suture material has significantly decreased during the last decade. We found that polyglactin 910 and polyglycolic acid sutures were vulnerable to pancreatic juice and bile after 3 days, and they disintegrated in pancreatic juice on day 7. The results of
Table 4 Mean ⫾ SD (%) retained tensile strengths of suture material in mixture Suture materials
Day 1 Retained tensile strength N (%)
Day 3 Retained tensile strength N (%)
Day 7 Retained tensile strength N (%)
Plain catgut Chromic catgut Polyglycolic acid Polyglactin 910 Polydioxanone Polypropylene Silk
Dis (0) Dis (0) 12.9 ⫾ 0.1 (97) 13 ⫾ 0.1 (95) 12.4 ⫾ 0.0 (98) 10.8 ⫾ 0.1 (90) 9.1 ⫾ 0.2 (94)
Dis (0) Dis (0) 7.9 ⫾ 0.1 (59) 8.2 ⫾ 0.1 (60) 12.2 ⫾ 0.1 (96) 10.4 ⫾ 0.1 (86) 9 ⫾ 0.1 (93)
Dis (0) Dis (0) Dis (0) 2.9 ⫾ 0.2 (21) 11.8 ⫾ 0.1 (93) 10.2 ⫾ 0.1 (84) 8.9 ⫾ 0.1 (92)
N ⫽ newtons; Dis ⫽ disintegrated.
M.A. Tolga Muftuoglu et al. / The American Journal of Surgery 188 (2004) 200 –203
polyglycolic acid and derivatives in our study are not in concordance with previous studies. However, some studies have reported significant differences regarding the tensile strengths of polyglycolic acid sutures. Deveney and Way found that polyglactin 910 and polyglycolic acid anastomotic sutures in dog jejunum dissolved in 21 and 22 days, respectively [2]. Again, as reported by Tian et al., polyglycolic acid and derivatives disintegrated in human pancreatic juice in 5 to 8 weeks [5]. Proteolytic enzymes are not responsible for the disintegration of polyglactin 910 and polyglycolic acid because these materials do not contain proteins, which makes them insensitive to proteolysis. Also, proteolytic enzymes were in the inactive form in our experiment. It is wise to speculate that active enzymes in pancreatic juice (amylase and lipase) may cause the disintegration of polyglactin 910 and polyglycolic acid. Polydioxanone suture materials retained most of their initial strength in pancreatic juice and bile. Polydioxanone was the strongest material among the tested absorbable and nonabsorbable suture materials. To our knowledge, no previous study has evaluated the effect of pancreatic juice and bile on polydioxanone. Silk is a nonabsorbable suture material, but its use has been diminishing during recent years. Mizuma et al. stated that silk maintained its strength in dog pancreatic juice for 14 days [1]. Our study did not confirm their results. We found that silk retained its initial strength at 83% in pancreatic juice and at 89% in bile on day 7. Polypropylene is a monofilament nonabsorbable suture that maintains its tensile strength for ⬎2 years. Our findings demonstrated that polypropylene lost its initial strength by 4%, 19%, and 23% in pancreatic fluid on days 1, 3, and 7, respectively. This finding presents important information because it has not been demonstrated before by any other study. This might be partially explained by the fact that most of the existing data on suture materials originate from test results of skin and subcutaneous tissue. Tensile strengths in skin may not express the same tensile strengths elsewhere in the body, especially in the pancreas. Anastomotic leakage is of paramount importance in gastrointestinal surgery, especially in pancreatic surgery. The pancreatic anastomotic leakage rate remains high despite the advancement of surgical techniques and medical tech-
203
nology [6]. It is impossible to claim that suture material is the only contributing factor in the occurrence of fistula formation. Various factors have been proposed in relation to anastomotic leakage. They can be grouped into factors related to the disease, factors related to the procedure, and factors related to patients’ and surgeons’ experiences. A soft and friable pancreatic parenchyma has also been found to be a risk factor of pancreatic anastomotic leakage. None of these factors has been proven to be the only significant factor predisposing to anastomotic leakage [7]. In summary, catgut and silk have lost their popularity and thus their use has diminished in recent years. Nonabsorbable sutures are used in the mucosal layer of pancreatic anastomosis. Polyglycolic acid and polyglactin 910 are the widely preferred suture materials in pancreatic surgery. The present study showed that polyglycolic acid and polyglactin 910 are not appropriate for use in pancreatic surgery. In our clinic, we stopped using polyglactin 910 in pancreas surgery after we saw the preliminary results of our study. Our choice of suture material in pancreas surgery is now polydioxanone [8], which meets the requirements of pancreatic surgery for high resistance to the digestive effect of pancreatic juice and bile and association with less inflammatory reaction. References [1] Mizuma K, Lee PC, Howard JM. The disintegration of surgical sutures on exposure to pancreatic juice. Ann Surg 1977;186:718 –22. [2] Deveney KE, Way LW. Effect of different absorbable sutures on healing of gastrointestinal anastomoses. Am J Surg 1977;133:86 –94. [3] Howes EL. Strength studies of polyglycolic acid versus catgut sutures of the same size. Surg Gynecol Obstet 1973;137:15–21. [4] Hermann JB. Changes in tensile strength and knot security in surgical sutures in vivo. Arch Surg 1973;106:707–12. [5] Tian F, Appert HE, Howard JM. The disintegration of absorbable suture materials on exposure to human digestive juice: an update. Am Surg 1994;60:287–91. [6] Yeo CJ, Cameron JL, Sohn TA, et al. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes. Ann Surg 1997;226:248 – 60. [7] Poon RTP, Lo SH, Fong D, et al. Prevention of pancreatic anastomotic leakage after pancreaticoduodenectomy. Am J Surg 2002;183:42–52. [8] Muftuoglu MAT, Saglam A. A novel reconstructive procedure after pancreaticoduodenectomy: J pouch dunking pancreaticojejunostomy. Hepatogastroenterology 2003;50:2233–5.