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The effect of surgical trauma on the bacterial translocation from the gut
The Effect of Surgical
Trauma on the Bacterial From the Gut
Translocation
By F. Tansu Salman, M. Nilgiin Buyruk, Nezahat Gijrier, and Alaaddin Celik Istanbul, Turkey l Bacterial translocation is the passage of viable bacteria from the lumen of the gastrointestinal tract through the intestinal mucosa to other sites. It is believed that bacterial translocation may lead to infection and septicemia. The purpose of this study was to determine what factors in experimental surgical trauma lead to bacterial translocation. Two-month-old Wistar albino rats were divided into five groups: (A) control; (6) anesthesia (ether inhalation); (C) anesthesia and surgery (median laparotomy and transient compression of the intestines); (D) fasting only; and (E) anesthesia, surgery, and fasting. After 48 hours, ileum, mesenteric lymph nodes, and blood were cultured for aerobic and anaerobic organisms. In each group the number of animals with bacteria overgrowth was calculated. The incidence of bacterial translocation to mesenteric lymph nodes and blood in groups B and D were similar to the controls (P > .Ol). There was a significant increase in the number of animals with bacterial translocation in groups C and E (P < .OOl). The majority of translocating bacteria were Ecoli.
Copyrig/& o 1992 by W.6. Saunders Company INDEX WORDS: tion.
Gastrointestinal
tract,
bacterial
transloca-
T
HE GASTROINTESTINAL tract is a known reservoir of bacteria. l The microorganisms, which are normally confined to the gastrointestinal tract, can under certain circumstances translocate to extraintestinal sites: mesenteric lymph nodes (MLNs), liver, spleen, and blood. Bacterial translocation may lead to severe infection. Several studies and investigations have been performed to determine the causes and mechanisms of bacterial translocation. 1-3After hemorrhagic shock, intestinal obstruction, small intestinal transplantation, trauma, bums, abdominal radiation, and obstructive jaundice, the intestinal mucosa may not serve as a barrier against the passage of gut bacteria and bacterial translocation occurs.3e13 Recently, translocation of gram-negative bacteria in humans with nonischemic intestinal obstruction has been demonstrated.5 This experimental study was undertaken to deterFrom the Department of Pediatric SurgeT, Istanbul School of Medicine, capa, Turkey. Presented at the 38th Annual International Congress of the British Association of Paediattic Surgeons, Budapest, Hungary, July 24-26, 1991. Address reprint requests to F. Tansu Salman, MD, Department of Pediatric Surgety, Istanbul University, Istanbul School of Medicine, Capa. Istanbul 34390. Turkey. Copyright o I992 by W B. Saunders Company 0022-3468/92/2706-0002$03.00/O 802
mine whether bacterial translocation occurs with abdominal surgical procedures and to evaluate the microorganisms translocated from the gut. MATERIALS AND METHODS Two-month-old male Wistar albino rats, weighing 200 to 300 g, were divided into five groups. The control group (A) consisted of 12 rats without surgery or anesthesia. Group B consisted of 11 rats anesthesized with ether inhalation for 90 minutes without any further procedure. In group C, 12 rats were anesthetised with ether, the peritoneal cavity was opened through a median incision, and the jejunum, ileum, and colon were compressed four times by manipulation from the ligament of Treitz to the sigmoid colon, without opening the lumen. Compression for 5 minutes on each occasion was performed by applying pressure to the intestines with the hands similar to intestinal manipulation during laparotomy. Care was taken to ensure that only the intestines were manipulated. The abdomen was closed with a single layer suture. In group D, 11 animals were not fed for 48 hours without surgery or anesthesia. In group E, 12 animals were fasted for 48 hours and then subjected to the same procedure as group C. After 48 hours, all 58 rats were killed by cervical dislocation. Using sterile techniques samples from the ileum, MLNs and blood were cultured for aerobic and anaerobic organisms. The blood for bacteriology was systemic blood, taken directly from the heart under sterile conditions. In each group, the number of animals with positive bacterial cultures in the mesenteric lymph nodes and blood was calculated. Translocation incidences were evaluated by x2 analysis.
RESULTS
After recovering from anesthesia and surgery all rats showed normal activity. There was no change in the body weight at the time of sacrifice 48 hours later, except in the fasting group. The mean weight loss in group D was 20 g. No significant alterations occurred in the ileal flora in all groups. Blood culture specimens in control group demonstrated negative findings; however, an occasional animal had viable bacteria (Stu~~y~ococcus aureus) in its MLN culture. In group C, in which 12 rats were placed under general anesthesia followed by intestinal manipulation, MLN cultures of 11 rats and blood cultures of 10 rats were positive. In group E, in which anesthesized 12 rats were operated and fasted for 48 hours, bacteria grew in all of the MLN cultures and in 10 of the blood cultures. In groups B and D, in which surgery was not performed, bacterial growth was observed in 4 and 5 of the MLN cultures, respectively. Three blood cultures in each of groups B and D were positive. The number of rats with bacterial translocation to MLNs Journalof Pediatric
Surgery, Vol27,
No 7 (July),
1992:
pp 802-804
BACTERIAL TRANSLOCATION
803
FROM THE GUT
Table 2. Bacteria Translocated
Table 1. The incidence of Bacterial Translocation Blood(%)
MLN (%)
Groups
From the Gut Blood
MLN NO.
%
NO.
%
A(n = 12)
1 (8)
0 (0)
B*(n = 11)
4 (36)
Ct (n = 12)
11 (92)
3 (27) 10 (83)
14
35.9
9
34.6
D* (n = 11)
3 (27) 10 (83)
P vulgaris
5
12.8
2
7.7
Et (n = 12)
5 (45) 12 (100)
K oxytoca
3
7.7
2
7.7
Total (n = 58)
33 (56.8)
26 (44.8)
S aureus
3
7.7
1
3.8
2
5.1
2
7.7
2
5.1
2
7.7
2
5.1
1
3.8
2
5.1
1
3.8
1
2.6
1
3.8
3
7.7
3
11.5
1
2.6
1
3.8
1
2.6
1
Aerobic bacteria E coli
u-Hemolytic Streptococcus *P > .Ol v control group.
Coag
tf
Enterobactef
< ,001 v control group.
(-)
Staphylococcus species
P mirabilis
and blood in each group were quantitated and the results are displayed in Table 1. In groups C and E, in which abdominal surgery was performed, bacterial translocation was more frequent than the other groups (P < .OOl) (Fig 1). The incidence of bacterial translocation to the mesenteric lymph nodes and blood in groups B and D were similar to the controls (P > .Ol). The majority of translocating bacteria were E coli, the predominant microorganism cultured from the gut. The other microorganisms cultured from the ileum, MLNs, and blood are displayed in Table 2. DISCUSSION
One of the functions of intestinal mucosa is to serve as a barrier to the passage of gut bacteria. The mechanisms of bacterial translocation are largely speculative. Factors known to influence it are: (1) integrity of the mucosal barrier; (2) intestinal overgrowth of microflora; and (3) the immunological state of the host.1,2,gDuring abdominal surgical procedures bacterial translocation is mostly faciliated when the small intestine is manipulated.’ In this study, in groups C and E, in which the intestines were compressed by intestinal handling, the increase in incidence of bacterial translocation to MLNs and blood was significant.
LI
6
C
6
E
6RlJUPS Fig 1. Comparison of bacterial translocation from ileum (black bar), MLNs (mottled bar), and blood (white bar) in five groups.
Pseudomonas
species
Anaerobic bacteria Clostridium
species
Peptostreptococcus Eacteroides Total
species
species
39
100
26
3.8 100
Fasting induces complex changes in host of defences. Histological changes in the small intestine include decreased intestinal mass, increased rate of epithelial cell renewal, and thinner, blunted, fused vil1i.i.” Protein deficiency may be associated with intestinal bacterial overgrowth, increased absorption of intact proteins, and decreased intracellular killing of bacteria and fungi. 1,2It is believed that mucosal integrity can be protected by balanced enteral feeding and by controlling bacterial translocation. Early enteral feeding is recommended by some authors to control bacterial translocation.‘~*Ji In this study the incidence of bacterial translocation in the fasting only group was similar to the controls (P > .Ol). Although the effect of fasting on bacterial translocation in group D was not significant in this study, the number of animals with bacterial translocation was still higher in the fasting group D than in control group A (Table 1). Anesthetic agents may significantly alter the normal balance in the turnover in the gut mucosa and, therefore, its integrity possibly related to anoxia and stress during the administration.iJl Although the effect of anesthesia on bacterial translocation in group B was not significant in this study, the number of anesthesized animals with bacterial translocation (group B) was found to be higher than that in the control group (Table 1). It is postulated that phagocytes ingest intestinal bacteria, transport them to extraintestinal sites, fail to accomplish intracellular killing, and then liberate them. Invasion of bacteria and bacterial endotoxin have been implicated in the pathogenesis of sepsis.1JJ2 In children undergoing abdominal surgery, the incidence of sepsis may be related to the number of microorganisms translocated from the intestines to the bloodstream. This study has shown that bacterial translocation
804
SALMAN
from the gut occurs with abdominal surgical procedures. Bacterial translocation can be reduced by avoiding unnecessary intestinal manipulation and prolonged fasting. This can be achieved by a delicate
ET AL
surgical technique and early enteral feeding. The mechanisms of bacterial translocation and its effects on the other organs require further microbiological, immunological, and clinical studies.
REFERENCES 1. Wells CL, Maddaus MA, Simmons RL: Proposed mechanisms for the translocation of intestinal bacteria. Rev Infect Dis l&959-979,1988 2. Alexander JW, Boyce ST, Babcock GF, et al: Proposed mechanisms of microbial translocation. Ann Surg 212~496-512, 1990 3. Sori AJ, Rush BF, Lysz TW, et al: The gut as a source of sepsis after hemorrhagic shock. Am J Surg 155:187-191,1988 4. Deitch EA, Bridges W, Baker J, et al: Hemorrhagic shock induced bacterial translocation is reduced by xanthine oxidase inhibition or inactivation. Surgery 104:191-197,1988 5. Maddaus MA, Wells C, Billiar T, et al: Simple mechanical intestinal obstruction induces translocation of gram-negative bacteria to the mesenteric lymph nodes. Surg Forum 40:186-189,1989 6. Uelasco AL, Chung RK, McGowan KL, et al: Bacterial transbcation after small intestinal transplantation. Surg Forum 40:579-S& 1988 7. Morris SE, Nauaratham N, Townsend CM, et al: Decreased
mesenteric blood flow independently promotes bacterial translocation in chronically instrumented sheep. Surg Forum 39:88-91,1988 8. Deitch EA, Berg RD: Endotoxin but not malnutrition promotes bacterial translocation of the gut flora in burned mice. J Trauma 27:161-165,1987 9. Stein GG, Bonsack M, Liberty J, et al: Abdominal radiation causes bacterial translocation. J Surg Res 46:104-107,1989 10. Deitch EA, Sittig K, Li M, et al: Obstructive jaundice promotes bacterial translocation from the gut. Am J Surg 159:7984,199O 11. Page CP: The surgeon and the gut maintenance. Am J Surg 158:485-490,1989 12. Navaratham N, Morris SE, Traber DL, et al: Endotoxin (LPS) increases mesenteric vascular resistance (MVR) and bacterial translocation (BT). J Trauma 30:1104-1115, 1990 13. Spaeth G, Specian RD, Berg RD, et al: Splenectomy influences endotoxin-induced bacterial translocation. J Trauma 30:1267-1272,199O
Trauma on the Bacterial From the Gut
Translocation
By F. Tansu Salman, M. Nilgiin Buyruk, Nezahat Gijrier, and Alaaddin Celik Istanbul, Turkey l Bacterial translocation is the passage of viable bacteria from the lumen of the gastrointestinal tract through the intestinal mucosa to other sites. It is believed that bacterial translocation may lead to infection and septicemia. The purpose of this study was to determine what factors in experimental surgical trauma lead to bacterial translocation. Two-month-old Wistar albino rats were divided into five groups: (A) control; (6) anesthesia (ether inhalation); (C) anesthesia and surgery (median laparotomy and transient compression of the intestines); (D) fasting only; and (E) anesthesia, surgery, and fasting. After 48 hours, ileum, mesenteric lymph nodes, and blood were cultured for aerobic and anaerobic organisms. In each group the number of animals with bacteria overgrowth was calculated. The incidence of bacterial translocation to mesenteric lymph nodes and blood in groups B and D were similar to the controls (P > .Ol). There was a significant increase in the number of animals with bacterial translocation in groups C and E (P < .OOl). The majority of translocating bacteria were Ecoli.
Copyrig/& o 1992 by W.6. Saunders Company INDEX WORDS: tion.
Gastrointestinal
tract,
bacterial
transloca-
T
HE GASTROINTESTINAL tract is a known reservoir of bacteria. l The microorganisms, which are normally confined to the gastrointestinal tract, can under certain circumstances translocate to extraintestinal sites: mesenteric lymph nodes (MLNs), liver, spleen, and blood. Bacterial translocation may lead to severe infection. Several studies and investigations have been performed to determine the causes and mechanisms of bacterial translocation. 1-3After hemorrhagic shock, intestinal obstruction, small intestinal transplantation, trauma, bums, abdominal radiation, and obstructive jaundice, the intestinal mucosa may not serve as a barrier against the passage of gut bacteria and bacterial translocation occurs.3e13 Recently, translocation of gram-negative bacteria in humans with nonischemic intestinal obstruction has been demonstrated.5 This experimental study was undertaken to deterFrom the Department of Pediatric SurgeT, Istanbul School of Medicine, capa, Turkey. Presented at the 38th Annual International Congress of the British Association of Paediattic Surgeons, Budapest, Hungary, July 24-26, 1991. Address reprint requests to F. Tansu Salman, MD, Department of Pediatric Surgety, Istanbul University, Istanbul School of Medicine, Capa. Istanbul 34390. Turkey. Copyright o I992 by W B. Saunders Company 0022-3468/92/2706-0002$03.00/O 802
mine whether bacterial translocation occurs with abdominal surgical procedures and to evaluate the microorganisms translocated from the gut. MATERIALS AND METHODS Two-month-old male Wistar albino rats, weighing 200 to 300 g, were divided into five groups. The control group (A) consisted of 12 rats without surgery or anesthesia. Group B consisted of 11 rats anesthesized with ether inhalation for 90 minutes without any further procedure. In group C, 12 rats were anesthetised with ether, the peritoneal cavity was opened through a median incision, and the jejunum, ileum, and colon were compressed four times by manipulation from the ligament of Treitz to the sigmoid colon, without opening the lumen. Compression for 5 minutes on each occasion was performed by applying pressure to the intestines with the hands similar to intestinal manipulation during laparotomy. Care was taken to ensure that only the intestines were manipulated. The abdomen was closed with a single layer suture. In group D, 11 animals were not fed for 48 hours without surgery or anesthesia. In group E, 12 animals were fasted for 48 hours and then subjected to the same procedure as group C. After 48 hours, all 58 rats were killed by cervical dislocation. Using sterile techniques samples from the ileum, MLNs and blood were cultured for aerobic and anaerobic organisms. The blood for bacteriology was systemic blood, taken directly from the heart under sterile conditions. In each group, the number of animals with positive bacterial cultures in the mesenteric lymph nodes and blood was calculated. Translocation incidences were evaluated by x2 analysis.
RESULTS
After recovering from anesthesia and surgery all rats showed normal activity. There was no change in the body weight at the time of sacrifice 48 hours later, except in the fasting group. The mean weight loss in group D was 20 g. No significant alterations occurred in the ileal flora in all groups. Blood culture specimens in control group demonstrated negative findings; however, an occasional animal had viable bacteria (Stu~~y~ococcus aureus) in its MLN culture. In group C, in which 12 rats were placed under general anesthesia followed by intestinal manipulation, MLN cultures of 11 rats and blood cultures of 10 rats were positive. In group E, in which anesthesized 12 rats were operated and fasted for 48 hours, bacteria grew in all of the MLN cultures and in 10 of the blood cultures. In groups B and D, in which surgery was not performed, bacterial growth was observed in 4 and 5 of the MLN cultures, respectively. Three blood cultures in each of groups B and D were positive. The number of rats with bacterial translocation to MLNs Journalof Pediatric
Surgery, Vol27,
No 7 (July),
1992:
pp 802-804
BACTERIAL TRANSLOCATION
803
FROM THE GUT
Table 2. Bacteria Translocated
Table 1. The incidence of Bacterial Translocation Blood(%)
MLN (%)
Groups
From the Gut Blood
MLN NO.
%
NO.
%
A(n = 12)
1 (8)
0 (0)
B*(n = 11)
4 (36)
Ct (n = 12)
11 (92)
3 (27) 10 (83)
14
35.9
9
34.6
D* (n = 11)
3 (27) 10 (83)
P vulgaris
5
12.8
2
7.7
Et (n = 12)
5 (45) 12 (100)
K oxytoca
3
7.7
2
7.7
Total (n = 58)
33 (56.8)
26 (44.8)
S aureus
3
7.7
1
3.8
2
5.1
2
7.7
2
5.1
2
7.7
2
5.1
1
3.8
2
5.1
1
3.8
1
2.6
1
3.8
3
7.7
3
11.5
1
2.6
1
3.8
1
2.6
1
Aerobic bacteria E coli
u-Hemolytic Streptococcus *P > .Ol v control group.
Coag
tf
Enterobactef
< ,001 v control group.
(-)
Staphylococcus species
P mirabilis
and blood in each group were quantitated and the results are displayed in Table 1. In groups C and E, in which abdominal surgery was performed, bacterial translocation was more frequent than the other groups (P < .OOl) (Fig 1). The incidence of bacterial translocation to the mesenteric lymph nodes and blood in groups B and D were similar to the controls (P > .Ol). The majority of translocating bacteria were E coli, the predominant microorganism cultured from the gut. The other microorganisms cultured from the ileum, MLNs, and blood are displayed in Table 2. DISCUSSION
One of the functions of intestinal mucosa is to serve as a barrier to the passage of gut bacteria. The mechanisms of bacterial translocation are largely speculative. Factors known to influence it are: (1) integrity of the mucosal barrier; (2) intestinal overgrowth of microflora; and (3) the immunological state of the host.1,2,gDuring abdominal surgical procedures bacterial translocation is mostly faciliated when the small intestine is manipulated.’ In this study, in groups C and E, in which the intestines were compressed by intestinal handling, the increase in incidence of bacterial translocation to MLNs and blood was significant.
LI
6
C
6
E
6RlJUPS Fig 1. Comparison of bacterial translocation from ileum (black bar), MLNs (mottled bar), and blood (white bar) in five groups.
Pseudomonas
species
Anaerobic bacteria Clostridium
species
Peptostreptococcus Eacteroides Total
species
species
39
100
26
3.8 100
Fasting induces complex changes in host of defences. Histological changes in the small intestine include decreased intestinal mass, increased rate of epithelial cell renewal, and thinner, blunted, fused vil1i.i.” Protein deficiency may be associated with intestinal bacterial overgrowth, increased absorption of intact proteins, and decreased intracellular killing of bacteria and fungi. 1,2It is believed that mucosal integrity can be protected by balanced enteral feeding and by controlling bacterial translocation. Early enteral feeding is recommended by some authors to control bacterial translocation.‘~*Ji In this study the incidence of bacterial translocation in the fasting only group was similar to the controls (P > .Ol). Although the effect of fasting on bacterial translocation in group D was not significant in this study, the number of animals with bacterial translocation was still higher in the fasting group D than in control group A (Table 1). Anesthetic agents may significantly alter the normal balance in the turnover in the gut mucosa and, therefore, its integrity possibly related to anoxia and stress during the administration.iJl Although the effect of anesthesia on bacterial translocation in group B was not significant in this study, the number of anesthesized animals with bacterial translocation (group B) was found to be higher than that in the control group (Table 1). It is postulated that phagocytes ingest intestinal bacteria, transport them to extraintestinal sites, fail to accomplish intracellular killing, and then liberate them. Invasion of bacteria and bacterial endotoxin have been implicated in the pathogenesis of sepsis.1JJ2 In children undergoing abdominal surgery, the incidence of sepsis may be related to the number of microorganisms translocated from the intestines to the bloodstream. This study has shown that bacterial translocation
804
SALMAN
from the gut occurs with abdominal surgical procedures. Bacterial translocation can be reduced by avoiding unnecessary intestinal manipulation and prolonged fasting. This can be achieved by a delicate
ET AL
surgical technique and early enteral feeding. The mechanisms of bacterial translocation and its effects on the other organs require further microbiological, immunological, and clinical studies.
REFERENCES 1. Wells CL, Maddaus MA, Simmons RL: Proposed mechanisms for the translocation of intestinal bacteria. Rev Infect Dis l&959-979,1988 2. Alexander JW, Boyce ST, Babcock GF, et al: Proposed mechanisms of microbial translocation. Ann Surg 212~496-512, 1990 3. Sori AJ, Rush BF, Lysz TW, et al: The gut as a source of sepsis after hemorrhagic shock. Am J Surg 155:187-191,1988 4. Deitch EA, Bridges W, Baker J, et al: Hemorrhagic shock induced bacterial translocation is reduced by xanthine oxidase inhibition or inactivation. Surgery 104:191-197,1988 5. Maddaus MA, Wells C, Billiar T, et al: Simple mechanical intestinal obstruction induces translocation of gram-negative bacteria to the mesenteric lymph nodes. Surg Forum 40:186-189,1989 6. Uelasco AL, Chung RK, McGowan KL, et al: Bacterial transbcation after small intestinal transplantation. Surg Forum 40:579-S& 1988 7. Morris SE, Nauaratham N, Townsend CM, et al: Decreased
mesenteric blood flow independently promotes bacterial translocation in chronically instrumented sheep. Surg Forum 39:88-91,1988 8. Deitch EA, Berg RD: Endotoxin but not malnutrition promotes bacterial translocation of the gut flora in burned mice. J Trauma 27:161-165,1987 9. Stein GG, Bonsack M, Liberty J, et al: Abdominal radiation causes bacterial translocation. J Surg Res 46:104-107,1989 10. Deitch EA, Sittig K, Li M, et al: Obstructive jaundice promotes bacterial translocation from the gut. Am J Surg 159:7984,199O 11. Page CP: The surgeon and the gut maintenance. Am J Surg 158:485-490,1989 12. Navaratham N, Morris SE, Traber DL, et al: Endotoxin (LPS) increases mesenteric vascular resistance (MVR) and bacterial translocation (BT). J Trauma 30:1104-1115, 1990 13. Spaeth G, Specian RD, Berg RD, et al: Splenectomy influences endotoxin-induced bacterial translocation. J Trauma 30:1267-1272,199O