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Acta Cirurgica Brasileira

Print version ISSN 0102-8650On-line version ISSN 1678-2674

Acta Cir. Bras. vol.12 no.3 São Paulo July/Aug./Sept. 1997

http://dx.doi.org/10.1590/S0102-86501997000300004 

4 – ORIGINAL ARTICLE

EFFECTS OF ORAL PARENTERAL NUTRITION SOLUTION ON THE MORPHOLOGY AND MECHANICAL RESISTANCE OF THE SMALL BOWEL IN RATS.1

 

José E. Aguilar-Nascimento2
Stenio A. Lima3
Alexandre C. C. Pereira3

 

 

AGUILAR-NASCIMENTO, J.E.; LIMA, S.A.;  PEREIRA, AC.C. - Effects of oral parenteral nutrition solution on the morphology and mechanical resistance of the small bowel in rats.  Acta Cir. Bras.12(3):159-62, 1997.

SUMMARY: The objective of this study was to investigate the effect of an elemental diet (ED) on the strength and on the morphology of the small bowel. Male Wistar rats were randomized to two groups to receive during 14 days either standard laboratory rat chow (N=16) or ED (N=16) containing total parenteral nutrition (TPN) solution. After this period they were killed and necropsied. The small bowel was measured and weighted with and without the contents. Bursting pressure (BP) was taken from the jejunum and ileum and histological sections of these two portions was performed to register the crypt depth (CD), vilus height (VH) and wall width (WW). All animals significantly gain weight. The bowel of animals fed with TPN solution had significantly less weight when compared with the controls either with (9.9 ± 1.9g x 7.8 ± 1.5g, p<0.05) or without (8.3 ± 1.3g x 6.5 ± 0.8g; p<0.05) the luminal contents. BP was lower in animals receiving TPN solution compared with controls in both studied segments but the difference only reached significance at the ileum (287 ± 60 x 234 ± 46 mm of Hg; p<0.05). VH, CD and WW were significantly shorter at the ileum in TPN-fed animals when compared to controls (p<0.05). This contrast was also seen at the jejunum though without significant difference. The small bowel looses mass and become less resistant when rats are fed with elemental diet though the nutritional state is maintained. The loss of mass appeared to be not only at the mucosa layer but through all the bowel wall. This occurs predominantly at the terminal part of the small bowel.
SUBJECT HEADINGS : Jejunum. Ileum. Animal nutrition. Intestinal mucosa.

 

 

INTRODUCTION

Nutritional support is essential in the management of patients after major operative procedure, trauma and mainly with gastrointestinal fistula20. Enteral feeding containing elemental or low residue diets while providing fuel requirements to the patient reduces its bowel intraluminal contents determining an favourable environment to heal anastomotic dehiscences. Although the leakage may stop in many cases, dehiscences may need operative procedures to heal. In this situation nutritional support is cardinal to maintain the patients in a fair nutritional state in order to resist the course of an operation.

However, either total parenteral nutrition (TPN) or enteral feeding with elemental diets (ED) are directly associated with atrophy of the intestinal mucosa and consequently with bacterial translocation3,9,17. This shrink of the mucosa layer is thought to be a consequence of loss of mucosa mass due to a lack of glutamine in ED or TPN formulas3. Glutamine, a non-essential aminoacid, is the principal fuel for the enterocyte and is also associated with a trophic effect to the small bowel mucosa3,9. Bowel wall atrophy may determine an impairment on its own ability to hold sutures and consequently a deficiency of withstanding an raising intraluminal pressure. In fact, colonic anastomoses created after relative bowel rest with ED were recently correlated with a retarded and diminished gain of postoperative collagen and strength in the anastomoses5,12. However, other reports failed to demonstrate a lack of mechanical resistance of colonic anastomosis created after ED regimen2 or intravenous infusion of glutamine-enriched TPN13 and no one study has determined how is the mechanical resistance of the bowel wall after elemental diets. Furthermore, it seems important to evaluate if the bowel resistance is compromised before the creation of the sutures. This could be of some importance in management of patients receiving nutritional support and at a risk of intestinal manipulation to place sutures.

The aim of this study was to verify the effect of an elemental diet on the strength and on the morphology of the small bowel.

 

METHOD

Thirty-two male Wistar rats (250-280 g) entered the experimental design. They were kept at laboratory environment for three days prior the beginning of the experiment in light/dark cycles. The animals were randomised to two groups to receive ad libitum either standard laboratory rat chow (N=16) or an elemental diet (N=16) containing TPN solution (3.2% aminoacids, 16% glucose, 3.2% lipids in addition to electrolytes and vitamins).

They were weight daily until the 14th day when they were killed by an inhalatory overdose of ether. During necropsy the entire thin intestine from pylorus to ileocecal valve was dissected and freed from the mesentery. The length of small bowel was then measured vertically with a 10 g tension (in cm) and weighted (in g) before and after being flushed with saline to remove the contents.

Jejunal and ileal segments measuring approximately 4 cm long were resected at 3 cm of the distance from the pylorus and ileocecal valve. Bursting pressure was registered in these two regions according to a technique previously used and published (1). A small specimen of these two regions was resected and fixed in 15% formalin solution and sent to histological examination. Histological sections cut sagitally to the serosa were stained with eosin and hematoxylin and studied by a blind observer to groups and to segments of the bowel. The mean value of the crypt depth (CD), vilus height (VH) and wall width (WW) (in µm) was registered using a micrometer. In each specimen, the mean value of the ten best well-oriented crypts and vilus was considered to represent the data from that individual. WW, measured at the same place of CD and VH was defined as the distance from the serosa to the submucosa adjacent to the mucosa.

Data presented as mean (SD) were statistically analysed using Student’s t test or Mann-Whitney test according to the homogeneity of the sample. A 5% level was established as significance level.

 

RESULTS

In each of the two groups there was a significant gain of weight from the beginning to the end of the experiment. There was no significant difference in the weight between the groups before ( control, 266 ± 16 g vs. ED, 270 ± 9 g ) or after 14 days ( control, 301 ± 32g vs. ED, 289 ± 17 g ) of the study.

Although there was no different in the length ( control, 124 ± 11 cm vs. ED, 122 ± 8 cm ) of the small intestine between groups, the bowel of animals fed with TPN solution had significantly less weight when compared with the controls either with or without the luminal contents (Figure 1).

 


Fig. 1 - Small bowel weight (mean, SD) according to groups and intraluminal contents. * § P < 0.05 x TPN.

 

 

The findings at the bursting pressure test can be seen in figure 2. The bowel wall resistance was lower in animals receiving oral TPN solution compared with controls in both studied segments but the difference only reached significance at the ileum.

 


Fig. 2 - Bursting pressure according to groups and segment of the bowel. Data are mean (SD). * P < 0.05 TPN.

 

 

Vilus height, crypt depth and wall width were significantly shorter at the ileum in TPN-fed animals when compared to controls. This contrast was also seen at the jejunum though without significant difference (Figures 3 and 4).

 


Fig. 3 - Crypt depth (CD), vilus height (VD) and wall width (WW) at jejunum according to groups. Data are mean (SD). NS.

 

 


Fig. 4 - Crypt depth (CD), vilus height (VH) and wall widht (WW) at the ileum according to groups. * P < 0.05 x TPN. Data are mean (SD).

 

 

DISCUSSION

In the treatment of patients with anastomotic breakdown, parenteral or enteral nutrition are useful weapons20. ED are also employed to prepare the colon preoperatively11. However, there are some evidences from the current literature pointing out that physical stimulation by luminal factors is fundamental to induce intestinal hyperplasia of the mucosa10,14,17,18,19. Intraluminal nutrients seem to contribute with 70% of the energy supply for the intestinal mucosa14 and thus the entire bowel, especially the distal portions in patients receiving TPN or ED may suffer malnutrition. Glutamine is the principal fuel used by the enterocyte3,9 while the short chain fatty acids are the main nutrient to the colonic mucosa14,15. Most of the commercially found TPN solutions or ED have no glutamine or short-chain fatty acids in their composition and thus, their scarcity in the normal intraluminal contents may determine atrophy of the epithelium. In addition, the disruption of the mucosa barrier could promote bacterial translocation according to the recent literature3, 6,9,17.

Chun et al. reported that the vilus height and the crypt depth were higher in pectin-fed rats compared with controls receiving no fiber7. In accordance to these observations the TPN-fed animals had atrophy of the mucosa and their small bowel were less resistant. Moreover atrophy was found not only at the epithelium but at the entire bowel wall. This suggest that mucosal malnutrition may interfere with the morphology of other layers of the bowel wall. Colonic anastomoses seem to become more resistant when the mucosa is irrigated with short-chain fatty acids solution2,16 and low residue diets promote a marked depression of collagen turnover in the colonic wall5,12. If this also occurs at the small bowel the healing of anastomoses in these conditions could be impaired.

During the early phase of healing the mechanical resistance of the anastomoses depends almost exclusively on the capacity of the bowel wall to hold the sutures8. This ability is particularly important during the early period after the creation of anastomoses when dehiscence is most common. Therefore, the findings of diminished bowel mass associated with loss of mechanical strength after oral TPN suggest that anastomosis created in these conditions are at risk.

There are some controversies about the effects of intraluminal fibers on the morphology of different parts of the small bowel7,17. Our findings showed that the morphological alterations promoted by an elemental diet in the rat model are more evident at the ileum than at the jejunum. This may suggest that the upper part of the small bowel is less compromised than the lower one when ED are used.

Although prudence is necessary to extrapolate the findings of an experimental research to the clinical setting the overall results suggest that the small bowel looses mass and become less resistant when rats are fed with elemental diet though the nutritional state is maintained. The loss of mass appeared to be not only at the mucosa layer but through all the bowel wall. Apparently the changes, especially the lack of resistance, occurs chiefly at the terminal part of the small bowel.

 

REFERENCES

1. AGUILAR-NASCIMENTO, J.E.; CENTENO-NETO, A.; SPILIOTIS, J; ASTRE, C.; JOYEUX, H. - Influência do preparo per-operatório do cólon com polivinilpirrolidona-iodo na cicatrização da anastomose primária do cólon esquerdo obstruído. Estudo em ratos. Rev Bras Colo Proct, 11:61-6; 1991        [ Links ]

2. AGUILAR-NASCIMENTO, J.E.; MATHIE, R.T.; MAN, W; WILLIAMSON, R.C.N - Enhanced intra-anastomotic healing by operative lavage with nutrient solutions in experimental left-sided colonic obstruction.  Br. J Surg82:461-4; 1995.        [ Links ]

3. ALVERDY, J.C. - Effects of glutamine-supplemented diets on immunology of the gut. J.Parent.Enter.Nutr., 14:109S-13S, 1990.        [ Links ]

4. BIONDO-SIMÕES, M.L.P.; CAVAZANA, W.C.; ADUR, R.C. - Influência da dieta alimentar sobre a cicatrização de anastomoses do cólon distal em ratos. Rev.Bras. Colo-Proctol., 15:13-8; 1995.        [ Links ]

5. BLOMQUIST, P.; JIBORN, H.; ZEDERFELDT, B.- The effect of relative bowel rest on healing of colonic anastomoses. Acta Chir. Scand., 150:671-5, 1984.        [ Links ]

6. CAMPOS, A.C.L.; MATIAS, J.E.F.; KOTZER, L.M.S.; MADI, K.; COELHO, J.C.U. - Translocação bacteriana em ratos recebendo nutrição parenteral com ou sem oclusão intestinal. Rev Col Bras Cir, 21:136-42; 1994        [ Links ]

7. CHUN, W.; BAMBA, T; HOSODA, S. - Effect of Pectin, a soluble fiber diet, on function and morphological parameters of the small intestine in rats. Digestion, 42:22-9, 1989        [ Links ]

8. CRONIN, K.; JACKSON, D.S.; DUNPHY, J.E. - Changing bursting strength and collagen content of the healing colon. Surg. Gynecol. Obstet., 126:747-53, 1968.        [ Links ]

9. DEITCH, E.A.; WINTERTON, J; BERG, R. - Effect of starvation, malnutrition and trauma on the GI tract flora and bacterial translocation. Arch Surg, 122:1019-24; 1987        [ Links ]

10. DOWLING, R.H.; RICKEN, E.O.; LAWS, J.W.; BOOTH, C.C. - The intestinal response to high bulk feeding in the rat. Clin. Sci., 32:1-9; 1967         [ Links ]

11. GLOTZER, D.J.; BOYLE, P.L.; SITEN, W.L - Preoperative preparation of the colon with an elemental diet. Surgery, 74:703-7, 1973.        [ Links ]

12. MARTÍNEZ-MAS, E.; VÁSQUEZ-PRADO, A.; LARROCHA-GRAU, M.; ARTIGUES-SANCHEZ, E.; LLORIS-CARSÍ, J.M. - The impact of low-residue enteral feeding on the healing of colonic anastomoses. Hepatogastroenterology, 40:481-4; 1993.        [ Links ]

13. McCAWLEY, R.; PLATELL, M.B.; HALL, J.; McCULLACH, R. - Effects of glutamine infusion on colonic anastomosis in the rat. J Parenter Enter. Nutr., 15:437-9; 1991        [ Links ]

14. ROEDIGER, W.E.W. & RAE, D.A. - Trophic effect of short chain fatty acids on mucosal handling of ions by the defunctioned colon. Br. J. Surg., 69:23-5, 1982.        [ Links ]

15. ROEDIGER, W.E.W. - Metabolic basis of starvation diarrhoea: implications for treatment. Lancet, 2:1082-4, 1986.        [ Links ]

16. ROLANDELLI, R.H.; KORUDA, M.J.; SETTLE, R.G.; ROMBEAU, J.L. - Effects of intraluminal infusion of short-chain fatty acids on the healing of colonic anastomosis in the rat. Surgery, 100:198-203, 1986.        [ Links ]

17. SPAETH, G.; SPECIAN, R.D.; BERG, R.D.; DEITCH, E.A. - Bulk prevents bacterial translocation induced by oral administration of total parenteral solution. J.Parent.Enter.Nutr., 14:442-7, 1990.        [ Links ]

18. STRAGAND, J.J.; HAGEMAN, R.F. - Effect of luminal contents on colonic cell replacement. Am.J.Physiol, 233:E208-E211; 1977.        [ Links ]

19. VAHOUNY, GV; TRUE, L.; IFRAIM, J. - Stimulation of intestinal cytokinetics and mucin turnover in rats fed wheat bran or cellulose. Am. J. Clin. Nutr., 41:895-900; 1985.        [ Links ]

20. WAITZBERG, D.L. - Nutrição enteral e parenteral na prática clínica - São Paulo, Ed. Atheneu; 1a Ed.; 1990.        [ Links ]

 

 

AGUILAR-NASCIMENTO, J.E.; LIMA, S.A.; PEREIRA, A.C.C. - Efeitos da administração oral da nutrição parenteral total na morfologia e resistência mecância do intestino delgado, em ratos. Acta Cir. Bras., 12(3):159-62, 1997.

RESUMO: Foram submetidos a ração padrão de laboratório 16 ratos e outros 16 receberam nutrição parenteral total (NPT) por via oral, durante 14 dias. Os animais de ambos os grupos ganharam peso, sem diferença estatistica. Na necrópsia retirava-se o segmento intestinal a partir do piloro até a valva ileocecal. Não houve diferença no comprimeto do intestino delgado em ambos os grupos. Porém, o intestino dos animais alimentados com NTP apresentaram diminuiçao significante de peso comparado com o grupo controle, independentemente da presença ou não de conteúdo. A resistência intestinal era menor no grupo NTP comparado ao controle, sendo mais significante no íleo. A altura dos vilos, a profundidade das criptas e a extensão da parede eram significantemente menores no íleo no grupo NTP comparado ao controle. Este achado foi observado também no jejuno, mas sem diferença significante. Conclui-se que nos ratos alimentados com NTP o intestino delgado perde massa e torna-se menos resistente, principalmente no íleo,apesar da manutenção do estado nutricional. A perda de massa aparece não apenas na mucosa mas em toda a parede intestinal.
DESCRITORES: Jejuno. Ileo. Nutrição animal. Mucosa intestinal.

 

 

Address reprint request to:
Prof. Dr. J.E. Aguilar-Nascimento
Rua das Margaridas, 426 Jd. Cuiabá
78020-230 Cuiabá - MT
e-mail : aguilar@nutecnet.com.br

Accepted for publication on April, 1997

 

 

1. Department of Sugery, Faculdade de Medicina da Universidade do Mato Grosso, Brazil
2. MD PhD
3. MD

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