Management of Short Bowel Syndrome in Nigerian Dogs Текст научной статьи по специальности «Ветеринарные науки»

2018, Scienceline Publication

Worlds Veterinary Journal

World Vet J, 8(2): 34-47, June 25, 2018

Management of Short Bowel Syndrome in Nigerian Dogs

Aboh Iku Kisani1*, John Bayo Adeyanju2, Abdullahi Teleh Elsa1 and Mamman Legbo Sonfada3

1Department of Veterinary Surgery and Theriogenology, College of Veterinary Medicine, University of Agriculture, Makurdi Benue State, Nigeria

2Department of Veterinary Surgery and Radiology, Faculty of Veterinary Medicine University of Ilorin, Nigeria 3Department of Veterinary Anatomy, Faculty of Veterinary Medicine, Usmanu Danfodiyo University, Sokoto, Nigeria "Corresponding author's Email: [email protected]

ABSTRACT

The effects of glutamine, honey, ascorbic acid and glutamine, honey, ascorbic acid combination on small bowel adaptation following 70% small intestinal resection in local Nigerian dogs were investigated. Thirty adult dogs with a median weight of 12.4kg (range 7-18 kg) were used in this study. The dogs were randomized into five groups of six dogs each following resection. Group 1 is the control group. The dogs here were not placed on any treatment. Group 2 dogs were placed on glutamine. Group 3 dogs were placed on honey. Group 4 dogs were placed on ascorbic acid and group 5 dogs were placed on glutamine, honey and ascorbic acid combination. Intestinal biopsy samples were collected at day 0, 4 weeks, 6 weeks and 8 weeks for histomorphometric study. Intestinal morphology was evaluated using light microscopy. The body weights of the dogs were monitored weekly for 4, 6 and 8 weeks in the five groups. Small intestinal adaptive response was evaluated at 4, 6 and 8 weeks post surgery. The animals treated with glutamine, honey, ascorbic acid and glutamine/ honey/ ascorbic acid combination experienced increase n intestinal villus height, villus width, crypt depth and wall thickness. The control group experienced a fall in intestinal villus height, villus width, crypt depth and wall thickness. The animals treated with glutamine, honey, ascorbic acid combination showed better therapeutic response followed by glutamine, honey and ascorbic acid in that order. There was a gradual increase in the body weight of animals in these groups. The control group did not show any appreciable adaptive response and the animals in this group progressively lost weight. It was concluded that dogs presented with short bowel syndrome could benefit from the supplementation of glutamine, honey and ascorbic acid in food.

Key words: Short bowel syndrome, Total parenteral nutrition, Intestinal resection, Small intestinal adaptive response

INTRODUCTION

Extensive resection of the small intestine can result in a condition known as Short Bowel Syndrome (SBS) (Gorman et al., 2006; Hasosah et al., 2008; Seetharam and Rodrigues, 2011; Mayeur et al., 2016; Vagholkar et al., 2016) and it occurs in both humans and animals. It is a disorder characterized by an intestinal absorptive surface area that is insufficient to support the host. This intestinal loss results in the malabsorption of fluid, electrolytes and other essential nutrients, severe diarrhea, dehydration and progressive malnutrition. Intestinal failure results when the residual bowel length cannot meet the patient's nutritional requirement thus necessitating dependence on parenteral nutrition (PN) (Donohoe and Reynolds, 2010; Norholk et al., 2012; Winkler and Smith, 2014; Mayer and Kerner, 2017). It is this dependence on parenteral nutrition that is responsible for the majority of morbidity and mortality associated with short bowel syndrome (Wales and Christison-Lagay, 2010; Vipperla and O'keefe, 2014). In dogs, intestinal resection is done because of linear foreign bodies, mesenteric volvulus, direct traumatic damage to the small bowel wall, solitary foreign body with perforation of the intestine, intussusceptions, dehiscence of a previous gastrointestinal tract surgery site and gastrointestinal tract tumor (Gorman et al., 2006). Long-term survival of patients with SBS is dependent on the adaptation of the remaining small intestine and response to pharmacological and nutritional management (Wall, 2013, Cunha-Melo and Costa, 2014; Rodriguez-Montes et al., 2016).

Managing short bowel syndrome is challenging as the medications are expensive and patients have to use them for a very long time and there is no guarantee that the response will be favourable (Hrbaty et al., 2004).

ISSN 2322-4568

A

- ■ R

c o

S c

£¡ e

e V

S o

: d

00 4

M > a r

1 2 8 8

O R G

HH

2 A L

A R

T

g n

8

34

MATERIALS AND METHODS

Experimental animals

Thirty dogs under 2 years of age with a mean weight of 12.4 kg (range 7-18 kg) were used for this study. They were stabilized for 4 weeks by being boarded in kennels within the teaching hospital and were dewormed and treated against ectoparasites and hemoparasites. They were fed daily and water was provided ad libitum. Each animal was fasted for 12 hours prior to surgery. They were premedicated with Atropine sulphate (Jiangsu Huayang pharmaceutical, China) at a dose rate of 0.04 mg/kg and xylazine hydrochloride (XYL-M2®, VMD, Belgium) at a dose rate of 1 mg/kg body weight intramuscularly. Induction was done with thiopentone sodium (Rotexmedica, Germany) at a dose rate of 10 mg/kg body weight intravenously. The total small intestinal length in each dog was calculated and recorded as described by Kisani et al. (2017).

Surgical procedure

Each animal was aseptically prepared and a ventral midline abdominal incision was made. The intestinal tract was exteriorized. Seventy per cent of the small intestinal tract (from the result of the preliminary study) was resected beginning from a point 7cm from the duoduno-jejunal flexure (treitz ligament). The residual intestinal tract was sutured using end to end anastomosis with polyglactin 910 (vicryl® Ethicon, USA) size "0" as described earlier. A full thickness biopsy sample of the small intestinal tract (Jejunum and ileum) were collected and fixed in 10% formalin (pretreatment sample). The anastomostic site was covered with omentum and returned to the abdominal cavity. The abdominal incision was closed using standard surgical technique (Fossum, 2014). Procain penicillin (Shuazhuang co ltd, China) 20,000 iu/kg and Streptomycin (North China pharmaceutical co ltd, China)(10 mg/kg) was administered intramuscularly for 5 days post operative. Pentazocin (Bharat Parenterals ltd, India) was administered intramuscularly at the dose rate of 5mg/kg for 7 days to relieve pain.

The dogs were given 5% dextrose infusion intravenously at 10 mls/kg/hr on the second and third day post operative. They were fed bland diet gruel on the fourth post operative day and returned to normal solid diet on day five post surgery. After surgery, the animals were randomized into five groups that each group contained six animals. Group 1 was the control group. The animals in this group were not treated. They were left to attend to their normal daily ration throughout the period of experiment. Group 2: Animals in this group were placed on orally administered glutamine. The dogs were given 9.0 mg/kg/day for 4 weeks (two dogs), 12.0 mg/kg/day for 6 weeks (Two dogs) and two15.0 mg/kg/day for 8 weeks (two dogs).

Group 3: The animals in this group were placed on orally administered honey. Two dogs were placed on honey at 7.5 mls/day for 4 weeks, two dogs consumed10mls/day for 6 weeks and two dogs were administered 12.5 mls/day for 8 weeks. Group 4: The animals in this group were placed on orally administered Ascorbic acid (vitamin C). Two dogs were administered ascorbic acid 150 mg/day for 4weeks, two dogs administered on ascorbic acid 250mg/day for 6 weeks and two dogs administered 350 mg/day for 8 weeks. Group 5: The animals in this group were placed on combine dose of glutamine (9 mg/kg/day), honey (7.5 mls/day) and vitamin C (150 mg/day). Two animals were placed on this combination for 4 weeks, two animals administered for 6weeks and two animals administered for 8 weeks.

Histomorphometric analysis

Small bowel biopsy specimens were obtained from the jejunum and ileum at day 0 (pre-surgical) and at 4, 6 and 8 weeks post resection-anastomosis. A total of four biopsy specimens were obtained from each patient (at the end of first and second laparotomy) and placed in 10% formalin. After routine formalin fixation, biopsy specimens were embedded in paraffin. Four-micrometer-thick (4 ^m) sections were cut perpendicular to the mucosa and stained routinely with H&E. Then using light microscopy and an eye piece micrometer at a magnification of ><100, the villus height, villus width, crypt depth and cross sectional area of the bowel mucosa were measured as explained by Joaquim et al. (2005). Five readings were taken for each parameter and the average value determined. Photomicrograph and interpretation of the slides were done using trinocular microscope and Amscope Toup View 3.7.

Statistical analysis

Data were expressed as descriptive statistics. Differences among the groups were evaluated using one way analysis of variance (ANOVA) followed by a two tailed student's t-test using SPSS version 16. The level of significance was set at 5%.

Ethical approval

This study was approved by the ethical committee of the college of veterinary medicine, university of Agriculture, makurdi, Nigeria with no.001.

35

RESULTS

Histomorphometry

Villus height

There was an increase in villus height for all the groups except the control group which experienced a fall in jejuna villus height in week 6 and 8 (Table 1) and a fall in ileal villus height in week 4 and 6. Group 5 also experienced a fall in jejuna villus height in week 6 (Table 5). The animals in group 4 showed a fall in ilea villus height in week 6. Groups 2, 3, and 5 showed statistically significant increase in villus height (Tables 2, 3 and 5) (P<0.05) while groups 1 and 4 did not cause statistical increase in villus height (Tables 1 and 4) (P>0.05).

Villus width

There was increase in villus width in all the groups. The control group and glutamine treated groups had greater increase in jejuna villus width at week 4 and a decrease in week 6 and 8 (Table 1). The control group also experienced a decrease in ilea villus width in week 4 and 6. Glutamine, honey and ascorbic acid treated groups had shown a statistically significant increase in villus width (Tables 2, 3 and 4) (P<0.05). Ascorbic acid treated group had also shown significant increase in ilea villus height.

Crypt Depth

There was an increase in crypt depth in all the groups except the control group (Tables 1-5). Glutamine, honey and glutamine honey and ascorbic acid treated groups caused a significant increase in crypt depth (P<0.05). Ascorbic acid treated animals significantly enhanced ilea crypt depth while the control group did not show any significant changes.

Wall thickness

All the groups experienced increase in wall thickness except the control group which experience increase only in the ilea wall thickness in week 8 of experiment (Tables 1-5). Group 2 (glutamine treated), group 3 (honey treated) and group 5 (glutamine/ honey/ ascorbic acid treated) animals had shown a significant increase in wall thickness (P< 0.05) Tables 2, 3 and 5). Ascorbic acids treated group had shown a significant increase in jejunal wall thickness (P<0.05) (Table 4).

Table 1. Jejunal histomorphometric analysis for dogs (Control group) post 70% small intestinal resection

Number of dogs (n = 6)

Jejunum WKs Mean ±SEM P value

1 2 3 4 5 6

0 1.104 0.937 0.696 0.787 0.814 0.925 0.877±0.058

Villus Height 4 1.024 0.861 - - - - 0.943±0.082 0.131

(VH) 6 - - 0.638 0.725 - - 0.682±0.044

8 - - - - 0.772 0.567 0.670±0.103

0 0.979 0.876 0.166 0.192 0.177 0.140 0.422±0.161

Villus Width 4 0.908 0.796 - - - - 0.852±0.056

(VW) 6 - - 0.110 0.132 - - 0.121±0.011

8 - - - - 0.145 0.102 0.124±0.022

0 0.426 0.322 0.680 0.799 0.565 0.322 0.519±0.080

Crypt Depth 4 0.357 0.248 - - - - 0.303±0.055 D 91 f, 0.216

(CD) 6 - - 0.622 0.744 - - 0.683±0.061

8 - - - - 0.528 0.282 0.405±0.123

0 1.250 0.840 1.021 0.765 0.918 0.826 0.937±0.072

Wall 4 1.038 0.597 - - - 0.818±0.221

Thickness (WT) 6 - - 0.961 0.699 - - 0.830±0.131 0.812

8 - - - - 0.887 0.795 0.841±0.046

WKs= Weeks; n= Number of dogs

36

Table 2. Jejunal histomorphometric analysis for dogs post 70% small intestinal resection

Jejunum

WKs

Number of dogs (n = 6)

Mean ±SEM

1

2

P value

Villus Height (VH)

0.753 1.026

0.876 1.162

0.922 0.730

1.317 1.117

0.684

1.341

0.779

1.431

0.791±0.037 1.094±0.068 1.217±0.100 1.386±0.045

0.0002

Villus Width (VW)

0.141 0.182

0.156 0.602

0.133 0.129 0.143

0.204 0.197

1.068

0.138

1.029

0.422±0.161 0.852±0.056 0.121±0.011 0.124±0.022

0.138

Crypt Depth (CD)

0.555 0.606

0.676 0.731

0.492 0.472\ 0.394

0.794 0.768

0.805

0.478

0.896

0.511±0.039 0.669±0.063 0.781±0.013 0.851±0.046

0.0037

Wall

Thickness (WT)

0.580 0.815

0.767 0.999

0.804 0.814 0.961

1.152 1.168

1.922

0.607

1.559

0.756±0.058 0.907±0.092 1.160±0.008 1.741±0.182

0.0003

WKs= Weeks; n= Number of dogs

3

4

5

6

Table 3. Jejunal histomorphometric analysis for dogs pre and post 70% small intestinal resection and anastomosis

Jejunum WKs Number of dogs (n = 6) Mean ±SEM P value

1 2 3 4 5 6

0 0.866 0.940 0.879 0.761 1.230 0.720 0.899±0.074

Villus Height 4 1.047 1.102 1.075±0.028 0.042

(VH) 6 8 1.173 1.073 1.631 1.124 1.123±0.050 1.378±0.254

0 0.152 0.126 0.163 0.134 0.192 0.141 0.151±0.010

Villus Width 4 0.190 0.158 0.174±0.016 0.030

(VW) 6 8 0.214 0.183 0.249 0.201 0.199±0.016 0.225±0.024

0 0.558 0.708 0.658 0.620 0.774 0.490 0.635±0.042

Crypt Depth 4 0.589 0.742 0.666±0.077 0.027

(CD) 6 8 0.870 0.920 1.084 0.802 0.895±0.025 0.943±0.141

0 0.636 0.800 0.798 0.669 0.724 0.972 0.767±0.049

Wall 4 0.787 0.984 0.886±0.099 0.0001

Thickness (WT) 6 8 1.047 0.881 1.636 1.834 0.964±0.083 1.735±0.099

WKs= Weeks, n= Number of dog

37

Table 4. Jejunal histomorphometric analysis for dogs pre and post 70% small intestinal resection and anastomosis

Jejunum WKs Number of dogs (n = 6) Mean ±SEM P value

1 2 3 4 5 6

0 0.873 0.796 0.992 0.693 0.694 0.772 0.803±0.047

Villus Height 4 0.994 0.972 0.983±0.011 0.093

(VH) 6 8 1.131 0.872 1.039 1.113 1.014±0.138 1.076±0.037

0 0.114 0.163 0.134 0.174 0.153 0.137 0.146±0.009

Villus Width (VW) 4 6 8 0.132 0.178 0.166 0.210 0.197 0.178 0.155±0.023 0.188±0.022 0.188±0.010 0.132

0 0.790 0.438 0.702 0.511 0.545 0.603 0.598±0.053

Crypt Depth (CD) 4 6 8 0.81 0.456 0.842 0.691 0.747 0.807 0.633±0.177 0.767±0.076 0.777±0.030 0.356

0 0.700 0.840 0.629 0.608 0.588 0.494 0.643±0.048

Wall Thickness (WT) 4 6 8 0.776 0.924 0.979 0.928 1.091 0.993 0.850±0.074 0.954±0.026 1.042±0.049 0.005

WKs= Weeks; n= Number of dog

Table 5. Jejunal histomorphometric analysis for dogs pre and post small intestinal resection and anastomosis

Jejunum WKs Number of dogs (n = 6) Mean ±SEM P value

1 2 3 4 5 6

0 1.333 0.981 0.788 0.765 1.080 0.965 0.985±0.085

Villus Height 4 1.646 1.298 1.472±0.174 0.002

(VH) 6 8 1.318 1.305 1.941 1.821 1.312±0.007 1.881±0.060

0 0.135 0.127 0.132 0.164 0.130 0.152 0.140±0.006

Villus Width 4 0.191 0.187 0.189±0.002 0.0001

(VW) 6 8 0.212 0.265 0.271 0.321 0.239±0.027 0.296±0.025

0 0.574 0.961 0.413 0.592 0.536 0.882 0.660±0.087

Crypt Depth 4 0.639 1.023 0.831±0.192 0.070

(CD) 6 8 0.812 0.997 1.05 1.402 0.905±0.093 1.226±0.176

0 0.716 0.786 0.890 0.597 0.882 0.943 0.802±0.053

Wall 4 1.100 1.175 1.138±0.038 0.0001

Thickness (WT) 6 8 1.355 1.053 1.912 1.994 1.204±0.151 1.953±0.041

WKs= Weeks; n= Number of dog

38

a

b

.M-m v -tm

I»»"

SO

v

Figure 1. The jejunum of dogs at eight weeks post resection showing (a) Necrosis of villi and (b) leucocytes infiltration of laminal propria. (H&E) ><100

. . ^iT * ■ , ■ • . Ï ^ ' ts*

4 .^jfcy a

b

JB

\

Wißm

* J» -' '

' 'if ¿T-Ä 'ifl/

^^■■RtSMi^JaKL^HII9HV? SMBBfRjl

Figure 2. The Ileum of dogs at eight weeks post resection showing (a) mild necrosis and (b) moderate hyperplasia of villi (H&E) xi00

39

Figure 3. The Jejunum of dogs at eight weeks after treatment with glutamine showing (a) formation of surface epithelium (H&E) x40

Figure 4. The ileum of dogs at eight weeks after treatment with glutamine showing (a) surface epithelium (b) Hyperplastic villi (H&E) xi00

40

a

L u

a

a

WUmttBEBm&m

Figure 5. The Jejunum of dogs at eight weeks after treatment with honey showing normal villi - "a" (H&E) x40

' 4 4k

Figure 6. The ileum of dogs at eight weeks after treatment with honey showing complete recovery (H&E) x40

41

Figure 7. The Jejunum of dogs at eight weeks after treatment with ascorbic acid showing leucocytic infiltration of lamina propria of the intestinal mucosa (a) (H&E) ><100

Figure 8. The ileum of dogs at eight weeks after treatment with ascorbic acid showing thickened lamina propria infiltrated by leucocytes (arrow) (H&E) x40

42

îaTV «

k

M

+ X.--4 » Bi 'lui

¿U'ultii

ufluffiffi

a

\KkJ-iT ! fl rft'^^^M

/ J] ¿i ¿¿WJfHW.

' Mra | . 11' \rivflri hfWH Sm lu '

Figure 9. The Jejunum of dogs at eight weeks after treatment showing well formed villi (arrow) (H&E) x40

Figure 10. The Ileum of dogs at eight weeks after treatment showing well formed surface epithelium and villi (arrow) (H&E) x40

43

2.5

i ! Ii JI il i l tl

Control Glutamine Money Ascorbic G+H+A

Acid

Treatment

I WKO

I WK 4

WK6

I WKS

Diagram 1. Pre-resection and post-treatment jejunal villi height of dogs in control, glutamine, honey, ascorbic acid and glutamine/ honey/ ascorbic acid combination treated groups

2.5

iilli! il ii il

Control Glutamine Money Ascorbic G+H+A

Acid

Treatments

I WKO

I WK 4

WK 6

I WKS

Diagram 2. Pre-resection and post-treatment jejuna wall thickness of dogs in control, glutamine, honey, ascorbic acid and glutamine/ honey / ascorbic acid combination treated groups

Diagram 3. Pre-resection and post-resection jejunal crypt depth of dogs in control, glutamine, honey, ascorbic acid and glutamine/ honey/ascorbic combination acid treated groups

44

DISCUSSION

In present study, the effects of glutamine, honey, ascorbic acid and glutamine, honey and ascorbic acid combination on intestinal adaptation in Nigerian dogs suffering from short bowel syndrome following 70% small bowel resection was evaluated. Dogs in all the groups in this study had diarrhea and loss of weight which is in agreement with the findings of Gorman et al. (2006), Shaw et al. (2012) and Tappenden (2014). The reason was due to mal-absorption as a result of the loss of mucosal absorptive surface area associated with short bowel syndrome (Shaw et al., 2012; Cunha-Melo and Costa, 2014; Merritt et al., 2017).

However, there was a reduction in diarrhea in animals treated with glutamine, honey, ascorbic acid and their combination after one week of treatment. This is due to the adaptive changes taking place in the intestinal mucosa that improves absorption and digestion of nutrients (Shaw et al., 2012; Vagholkar et al., 2016; Gillard et al., 2017). This is the reason for the increase in weight observed in animals in these four groups.

Animals in the control group however, continue to experience diarrhea especially after feeding due to inadequate adaptive changes in the intestinal mucosal. Hence the gradual drop in body weight observed in this group. Glutamine is the major nutrient for the bowel. It is the primary substrate used by enterocytes. Supplementation during catabolic states improves structural integrity, function and repair of the intestinal mucosa, decreases bacterial translocation and epithelial apoptosis, improves nitrogen balance and influencing gut immune response (Chandler, 2002; Evans et al., 2003; Grimble, 2005; Larson et al., 2007). Dogs treated with glutamine (group 2) experienced significant increase (P<0.05) in Villus Height (VH), Crypt Depth (CD), Villus Width (VH) and Wall Thickness (WT). The gradual increase in body weight observed in this group may be due to enhanced absorption of nutrients from improved adaptation of the remnant small bowel. Our findings on the use of glutamine in this study, agrees with the previous work by Eyarefe et al. (2012), who used glutamine on dogs with short bowel syndrome following massive small bowel resection and observed a beneficial adaptive response by the remnant small bowel in those dogs. In this study, dogs treated with honey (group 3) showed a significant increase (P<0.05) in VH, CD, VW and WT. There was a gradual increase in body weight. There was also a complete regeneration of the intestinal epithelium. This result is also in agreement with the findings of Eyarefe et al. (2012) who also used honey to treat dogs suffering from short bowel syndrome and observed positive adaptive response.

Dogs treated with ascorbic acid showed marginal increase in VH, VW, CD and WT. It has been reported that malassimilation and increased fluid losses with diarrhea may deplete vitamin C in the body (Chandler, 2002). It may be possible that the dosage of vitamin C used in this study was not enough to compensate for the large losses that had occurred. Though the increase was not statistically significant, it was comparatively better than that of the control group. The action of ascorbic acid (vitamin C) was as a result of its powerful antioxidant property where it scavenges and mopes up reactive oxygen and nitrogen species (free radicals) in the body. These reactive species are generated by normal cell processes as well as environmental stressors and can cause damage to tissues (Halliwell and White man, 1997; Telang, 2013). Oxidative stress also occurred in the intestine in diseases and may cause increased inflammation and permeability (Chandler, 2002). Thus vitamin C reduced potential damage to tissues. All these positive effects may probably be undermined in this study, due to the insufficiency of vitamin C, which may be responsible for the low/gradual villi height, crypt depth, villi width and wall thickness. The evaluation of ascorbic acid in the treatment of short bowel syndrome did not report experimentally and there are not enough published data about this research topic.

Dogs on glutamine, honey and ascorbic acid combination (group 5) showed significant increase in VH, VW, CD and WT. This adaptive response was higher than that observed in glutamine (group 2), honey (group 3) or ascorbic acid (group 4) treated animals respectively. This showed that the combination of these three supplements had synergistic effect that could enhance small bowel adaptation in patients with short bowel syndrome. Similarly, the synergistic effect of these products has not been reported. Animals in the control group did not show any appreciable adaptive response as there was no significant increase in VH, VW, CD and WT. There was also drop in body weight.

The result of this study has revealed that glutamine, honey and their combination have beneficial intestinal adaptive response in patients suffering from short bowel syndrome. However, /glutamine/ honey/ ascorbic acid combination produces higher adaptive response than glutamine, honey or ascorbic acid alone. The higher doses of these supplements produced better adaptive response than the lower doses.

CONCLUSION

Glutamine, honey and ascorbic acid given individually or in combination enhanced residual bowel efficiency and improved outcome in patients suffering from short bowel syndrome. It is therefore recommended that dogs with signs attributable to short bowel syndrome should be given supplement of glutamine, honey and ascorbic acid in food.

45

DECLARATIONS

Author's contribution

AIK, JBA and ATE performed the surgery. MLS prepared the histopathology slides and reviewed the manuscript. Competing interests

The authors have declared that no competing interest exists

REFERENCES

Chandler M (2002). Essentials of nutrition in dogs and cats with gastrointestinal disease. In practice, 528-533.

Cunha-Melo JR and Costa G. (2014). Intestinal transplantation: evolution and current status. Medicalexpress; 1(6):307-322. DOI: http://dx.doi.org/10.5935/MedicalExpress.2014.06.05

Donohoe CL and Reynolds JV (2010). Short bowel syndrome. Surgeon, 8(5):270-9. DOI: 10.1016/j.surge.2010.06.004.

Englard S and Seifter S (1986). The biochemical functions of ascorbic acid. Annual Review of Nutrition, 6: 365-406.

Evans ME, Jones DP and Ziegler TR (2003). Glutamine prevents cytokine-induced apoptosis in human colonic epithelial cells. Journal of Nutrition, 133:3065-3071.

Eyarefe OD, Emikpe BO, Akinloye SO, Alonge TO and Fayemi OE (2012). Effects of honey, glutamine and their combination on canine small bowel epithelial cell proliferation following massive resection. Niger Journal of Physiology, 27: 189-193

Fossum WT (2014). Complications of intestinal surgery. In textbook of small animal surgery, 3 rd edition, pp 460-461. Mosby Elsevier.

Gillard L, Mayeur C, Robert V, Pingenot I, Le Beyec, J, Bado A, Lepage P, Thomas M and Joly F (2017). Microbiota is involved in Post-resection Adaptation in Humans with Short Bowel Syndrome. Frontiers in Physiology, 8(224):1-13 DOI: 10.3389/fphys.2017.00224.

Gorman SC, Freeman LM, Mitchell SL and Chan DL (2006). Extensive small bowel resection in dogs and cats. 20 cases (1998-2004). JAVMA, 228 (3): 403-407. DOI: 10.2460/javma.228.3.403.

Grimble RF (2005). Immunonutrition. Current Opinion Gastroenterology, 21:216-222.

Halliwell B and Whiteman M (1997). Antioxidant and prooxidant properties of vitamin C. In: Packer L, Fuchs J, eds. Vitamin C in Health and Disease. New York, NY: Marcel Dekker; 25-94.

Hasosah M, Lemberg DA, Skarsgard E and Schreiber R (2008). Congenital short bowel syndrome: a case report and review of the literature. Canadian Journal of Gastroenterology, 22:71 -74.

Hrbaty B, Skultety J, Labas P, Reis R and Ziak P (2004). Conditions responsible for small bowel resection. Bratisl Lek Listy, 105 (2): 86-88.

Joaquim MS, Jose EA, Maria HGG, Bruno SN, Priscila ATF, Batista C, Denise MTA (2005). Effects of combined use of glutamine and growth hormone in the intestinal adaptation after massive resection of the small bowel in rats. Acta Cir. Bras. 20 (5): 382389. DOI: http://dx.doi.org/10.1590/S0102-86502005000500008.

Kisani IA, Adeyanju JB, Sonfada ML and Elsa AT (2017). In Vivo Ex-Vivo Measurement of Crown Rump and Small Intestinal Length in Nigerian Dogs: A Surgical Measure for Safe Intestinal Resection and Anastomosis. Dairy and Vet Sci J 2(4):001-003. DOI:10.19080/JDVS.2017.02.555591.

Larson SD, Li J, Chung DH and Evers BM (2007). Molecular mechanisms contributing to glutamine-mediated intestinal cell survival. American Journal of Physiology- Gastrointestinal Liver Physiology, G 1262-G 1271. DOI: 10.1152/ajpgi.00254.2007.

Mandl A, Szarka A and Banhegyi G (2009). Vitamin C: update on physiology and pharmacology. British Journal of Pharmacology, 157:1097-1110. DOI: 10.1111/j.1476-5381.2009.00282.x.

Mayeur C, Gillard l, Beyec JL, Bado A and Joly F (2016). Extensive Intestinal Resection Triggers Behavioral Adaptation, Intestinal Remodeling and Microbiota Transition in Short Bowel Syndrome. Microorganisms, 4: 16; DOI: 10. 3390/microorganisms40100169)

Mayer O and Kerner JA (2017). Management of short bowel syndrome in postoperative very low birth weight infants,Seminars in Fetal & Neonatal Medicine 22, 49e56 DOI:http://dx.doi.org/10.1016/j.siny.2016.08.001

Merritt RJ, Cohran V, Raphael BP, Sentogo T, Volpert D, Warner BW and Goday PS (2017). Intestinal Rehabilitation Programs in the Management of Paediatric Intestinal Failure and Short Bowel Syndrome. JPGN, 65: 588-596. DOI: 10. 1097/ MPG. 0000000000001722.

Narholk LM, Holst JJ and Jeppesen PB (2012) "Treatment of adult short bowel syndrome patients with teduglutide," Expert Opinion on Pharmacotherapy, 13 (2): 235-243. DOI:10.1517/14656566.2012.644787.

Rodriguez-Montes JA, Albero JS and Lopez PJT (2016). Surgical Options in Short Bowel Syndrome. Journal of Paediatric Care Insight, 1(1): 1-5. DOI: 10.24218/ jpci.2016.01.

Scolapio JS, Mcgreevy K, Tennyson GS and Burnett OL (2001). Effect of glutamine in short-bowel syndrome. Clinical Nutrition, 20(4): 319-323.

Seetharam P and Rodrigues G (2011). Short Bowel Syndrome: A Review of Management Options. Saudi Journal of Gasteroenterology, 17(4); 229-235. DOI. 10.4103/ 1319-3767.82573.

Shaw D, Gohil K and Basson MD (2012). Intestinal mucosal atrophy and adaptation. World J Gastroenterol, 18(44): 6357-6375. DOI: 10.3748/wjg.v18.i44.6357

46

Tappenden KA (2014). Pathophysiology of Short Bowel Syndrome: Considerations of Resected and Residual Anatomy, Journal of Parenteral and Enteral Nutrition, 38 suppl.1: 14S-22S. DOI: 10.1177/0148607113520005

Telang P (2013) Vitamin C in dermatology. Indian Dermatology Online Journal, 4: 143-146. DOI: 10. 4103/ 2229-5178.110593

Vipperla K, Stephen J and O'Keef SJ (2014). Targeted therapy of short-bowel syndrome with teduglutide: the new kid on the block. Clinical and Experimental Gastroenterology, 7: 489-495. DOI: 10.2147/CEG. S42665.

Vagholkar K, Iyengar M, Vagholkar S, Pawanarkar A, Ansari S, Pathan S and Bhupatkar A (2016). Short bowel syndrome. International Surgery Journal, 3(2):452-455. DOI:http://dx.doi.org/10.18203/2349-2902.isj20160672

Wales PW and Christison-Lagay ER (2010). Short bowel syndrome: epidemiology and etiology. Seminar in Pediatric Surgery, 19(1): 3-9. DOI:10.1053/j.sempedsurg.2009.11.001.

Wall EA (2013). An overview of short bowel syndrome management: adherence, adaptation, and practical recommendations. Journal of the Academy of Nutrition and Dietetics, 113: 1200-1208. DOI:10.1016/j.jand. 2013.05.001

Winkler MF and Smith CE (2014). Clinical, social, and economics impact of home parenteral nutrition in short bowel syndrome. Journal of Parenteral and Enteral Nutrition, 38: 32-37. DOI:10.1177/0148607113517717.

47