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African Journal of Biotechnology Vol. 9 (21), pp. 3223-3230, 24 May, 2010 Available online at http://www.academicjournals.org/AJB ISSN 1684–5315 2010 Academic Journals Effects of metronidazole and probiotics
oligosaccharide on bacterial translocation in protein
malnutrition
Benakriche Ben Mehel1*, Boudali Souad1, Gorine H1, Bekada Ahmed2, Philippe Pochart3,
Saïdi Djamel1 and Kheroua Omar1
1Laboratory of Physiology of Nutrition and Food Safety. Faculty of Science. University of Oran, Algeria. 2Laboratory of Microbiology and Food Security. Faculty of Science. University of Oran, Algeria. 3Laboratory of Biology – EA 3199, Institute of Scientific and Technical Food, CNAM, Paris, France. The present study aims to evaluate the effects of metronidazole, probiotics oligosaccharide on
indigenous microflora and bacterial translocation (BT) in protein malnourished rats. Thirty male Wistar
rats were divided into three groups: protein malnourished rats PM (group1, n = 10) were fed with maize
only, protein malnourished rats (group 2, n = 10) were received metronidazole and protein malnourished
rats (group 3, n = 10) were received both metronidazole and probiotics-oligosaccharide for fifteen days.
Metronidazole (1000 mg/kg/day) was given via an orogastric feeding tube to the second and third
groups. Lyophilized probiotics-oligosaccharide (0.5 mg/g body weight/day) was given in two doses via
the same route to the third group. All animals were sacrificed after fifteen days of protein malnutrition
and cultures of the mesenteric lymph nodes (MLNs), liver, spleen and cecal contents were done. The
incidence of bacterial translocation (BT) was 30% (3/10) in protein malnourished group 1,60% (06/10) in
group 2 where protein malnutrition was associated with metronidazole and 25% (2.5/10) in group 3
whose animals were subjected to protein malnutrition associated with metronidazole and probiotics
oligosaccharide. A significant increase in the BT incidence was found in group 2 (P < 0.05), while a
significant decrease was found in group 3 when compared to group 1. The total bacterial count of cecal
flora was significantly low in group 3 than in group 1 (P < 0.01). These results suggest that the
incidence of BT in protein malnutrition is increased by using an antibiotic while probiotics-
oligosaccharide decreases this incidence in protein malnutrition induced by antibiotic. Thus, we
conclude that probiotics-oligosaccharide can effectively protect the intestinal mucosa and prevent BT
in protein malnourished infants.

Key words:
Bacterial translocation, protein malnutrition, probiotics oligosaccharide, metronidazole and

INTRODUCTION
In light of the wide usage of antibiotic drugs in developing the effects of malnutrition on the disposition of antibiotics. countries, it becomes extremely important to determine In the world, severe acute protein malnutrition (PM) affects approximately 13 mil ion children under the age of 5 and it is associated with 1 - 2 mil ion preventable child deaths each year (Col ins, 2007). Use of antibiotics promotes the *Corresponding author. E-mail: benak_benmehel@yahoo.fr. emergence of resistant organisms and multiple-antibiotic Tel: + 213773926535. Fax: + 21345301018. resistance has become a major public health issue. Nowadays, metronidazole (2-methyl-5-nitroimidazole-1- lation of the intestinal flora, especial y during an antibiotic ethanol) is widely used in the treatment of parasitic in case of diarrhea or intestinal parasites. For al the diseases and mainly against anaerobes, including Bacte- positive effects of probiotics, three conditions can be met, roïdes (Freeman et al., 1997). Metronidazole at the doses a cocktail of the best micro-organisms in sufficient used (1 mg/ml drinking water ad libitum) disrupts the intestinal bacterial flora resulting in the destruction of Protein malnutrition disrupts the normal ecology of the strict anaerobic bacteria and therefore, an overgrowth of microflora affecting strictly anaerobes (Tannock and enterobacteria in the cecal (Berg, 1981). This al ows Savage, 1974; Poxton et al., 1997), impairs host immune studying the simultaneous influence of malnutrition and response and antibacterial defenses (Reynolds et al., antibiotics. There has been a growing interest in the 1992; Chandra, 1993), enhances the susceptibility to effects of malnutrition on drug metabolism and pharma- infection and leads to mucosal atrophy (Reynolds et al., 1996). Malnutrition is a common problem for critical il Although malnutrition itself cannot be treated by drug patients and nutritional support is mandatory. therapy, it can induce situations where drugs are the The effect of probiotics oligosaccharide in combination primary form of treatment. The treatment of infections is with antibiotics on protein malnutrition has not been the most common and severe drug-related problem asso- proposed until now as an alternative to the use of prophylactic antibiotics. Antibiotic prophylaxis is intended In addition, probiotics were used in conjunction with to prevent the potential of bacterial contamination as a antibiotic therapy to prevent or lessen the severity of situation risk. It is unknown if modification of the intestinal antibiotic-associated diarrhea in children (Vanderhoof et flora with such a multispecies probiotics mixture with al., 1999), although a meta-analysis of this issue showed fructo oligosaccharide reduces bacterial overgrowth and significant problems in study design in several studies bacterial translocation from the gut and, consequently, alters the course of disease. Therefore, the present study A malnourished individual is known to be much more was as an attempt to assess if modification of intestinal susceptible to infections. In light of the wide usage of flora by a specifical y designed, multispecies probiotics antibiotic drugs in developing countries, it becomes extre- mixture with fructo oligosaccharide changes disease mely important to determine the effects of malnutrition on course using a wel -established rat model of protein the disposition of antibiotics (Jung and Shahl, 1986). The gut microflora is an important constituent of the intestinal mucosa barrier and this has led to the concept of probiotics therapy, that is, the application of potential y MATERIALS AND METHODS
beneficial microorganisms (Ful er, 1992). Probiotics is a microbial dietary adjuvant that beneficial y affects the Animals and diets
host physiology by modulating mucosal and systemic Thirty male Wistar rats weighing 60 - 70 g and aged 28 days were immunity, as wel as improving nutritional and microbial used. Al animals were obtained with approval from the Animal balance in the intestine tract. They are nonpathogenic Research Center of Bab Ezzour University, Algeria. The rats were microorganisms that, when administered in adequate housed in stainless-steel cages in an animal room maintained at 22 amounts, confer a health benefit on the host. Probiotics ± 2°C on a 12-h light cycle. After three days of acclimatization, they bacteria are noninvasive, yet they need to interact with had free access to water ad libitum and conventional y, pel et food (UAR, Vil emoisson-sur- Orge, France). The conventional y diet is gastrointestinal (GI) epithelial cel s to elicit their containing proteins, fat, carbohydrate, vitamin and minerals (Table immunomodulatory effects. Probiotics have been shown to induce various epithelial cel responses by competing We propose here a new experimental model of malnutrition, with pathogenic bacteria for host adhesion binding sites, based on exclusive use of maize. This diet, similar to that improving epithelial cel barrier function (Myl yluoma et consumed by the severely malnourished children in poor countries, is severely deficient in essential acid amine and vitamins (Ribeiro et Probiotics and prebiotics can be used to either prevent During fifteen days of experimental feeding period, animals were or reduce the severity of microbe-induced gut divided into three groups of 10 rats each. A protein malnourished inflammation. The best known prebiotics are fructo- rats (group 1, n = 10) were fed only with maize, a protein oligosaccharides, sugars of plant origin. It has interesting malnourished rats (group 2, n = 10) were received an antibiotic properties such as stimulating the growth of probiotics (Metronidazole) and a protein malnourished animals of group 3 (n = and renewal of cel s in the intestinal mucosa. 10) received both Metronidazole and Probiotics Oligosaccharide. The malnourished rats of the three groups were fed with maize (diet PROBIONAT® is a product of both a probiotics and poly-deficient in essential amino acids) with 10 g/kg of rat/day (EPE Fructo-oligosaccharide (FOS); it is advisable for its regu- Grope Avicole de l’Ouest, Mostaganem, Algeria); the composition of Table 1. Standard diet for rats (UAR, Vil emoisson-sur- Orge, France).
Co-products of the cereals transformation Oil cakes and other nitrogenized products of vegetable origin Nitrogenized product Caloric value = 2900 kcal /kg. Ration day laborer = 18 – 25 g. Table 2. Composition of maize (EPE Groupe Avicole de l’Ouest, Mostaganem, Algeria).
Humidity
Carbonhydrate
Calories
maize was given in (Table 2). Food intake was measured daily at The MLNs, spleen and liver were removed and al organs were 17 h. Induction of malnutrition after 15 days with this diet was weighed separately. The MLN complex was placed in a sterile published earlier (Dock et al., 2003; Dock-Nascimento et al., 2007). grinding tube and homogenized with 9 volume of brain– heart Metronidazole (Hikma Pharmaceuticals, Jordan) was given via infusion using sterile ground-glass stoppers (Heimo et al., 2001). To orogastric feeding tube to the rats of groups 2 and 3 for 15 days determine the bacterial concentrations of homogenates, each organ with the dose of 1 g/kg of animal/day). A complex of lyophilized was diluted in decimal steps up to 1.105 in a sterile solution. After probiotics (Lactobacil us acidophilus, Lactobacil us rhamnosus, manual grinding, 1 ml of the homogenate was transferred into a Bifidoboctenium lactis, Bifidoboctenium longum, Bifidoboctenium tube containing 9 ml of physiologic serum; from this dilution 100 µl bifidum, Steptococcus thermophilus) and Fructo-Oligosaccharides aliquots were plated on DRIGALSKI agar plates for enterobacteria (PROBIONAT® Safetynat Limited Epps Building Bridge Road, culture (Sanofi, Diagnostic Pasteur; France). Spleen and liver was France) in the form of a capsule contained about 109 germs in analyzed in the same way as the MLNs. Al agar plates for aerobic lyophilisate of 390 mg. It was given as three doses per day via culture were incubated at 37°C under aerobic conditions for 1 day orogastric feeding tube (1 mg/g of body per day) to the rats of group and then interpreted. The gram-negative enteric was identified 3 (10 mg/ 10 ml). On the day 15 of this treatment, the animals were using the API 20 E system (Analytab Products, Plainview, New sacrificed by cervical dislocation and a 0.5 ml blood sample was col ected from the inferior vena cava for blood cultures. Quantitative culture results were determined by the number of Using sterile procedures, the chest and abdominal cavities were Colony Forming Units per gram of tissue, calculated from the reflected with sterile forceps and the exposed viscera were dilutions of organ homogenate and positive tissue cultures. We did swabbed with a sterile, cotton-topped applicator stick, which was not study obligate anaerobic because these organisms are rare then placed in a tube of brain-heart infusion. The tube was members of the intestinal flora of rodents early in life (Raibaud P, incubated aerobical y at 37°C for 24 h to test the bacterial 1988) and because they have a low tendency to translocate to extra intestinal sites (Stefen EK et al., 1988; Stefen EK et al., 1983). The Table 3. Incidence and sites of bacterial translocation (BT) in each group after 15 days of treatment.
Incidence of
PM, protein-malnourished group; BT, bacterial translocation; MLN, mesenteric lymph nodes. *P < 0.01 compared to group 1, †P < 0.05 compared to groups 1 and 2, ‡P < 0.05 compared to group 1 and ¶ P < 0.05 compared to Mesenteric Lymph Nodes (MLNs), spleen, liver and cecal contents Table 4. Number of translocating bacteria in terms of FCU per
were removed and homogenized for quantitative cultures. The gram of mesenteric lymph nodes in each group after 15 days colony-forming units (CFU) of bacteria per gram of tissue were Statistical analysis
Data were expressed as means ± standard error of the mean. The Mean ± standard error of mean × 103 colony-forming units per differences between the different groups were evaluated by chi square analysis with the Yates correction. Continuous data are expressed as mean 6 SEM and analyzed with analysis of variance (ANOVA) and the Student unpaired t test. A P-value < 0.05 was The results of quantitative MLNs cultures are shown in Table 4. Although the number of translocating bacteria per gram of MLNs was decreased by the administration The incidence of bacterial translocation was 30% (3/10) of probiotics oligosaccharide, there was a significant high in protein-malnourished group 1 (PM), 60% (6/10) in rats difference between groups 2 and 1 (P < 0.001) and between of group 2 (where PM was associated with groups 3 and 1 (P < 0.05). In addition, the difference bet- metronidazole) and 25% (2.5/10) in group 3 (where ween groups 2 and 3 was significantly high (P < 0.001). protein malnutrition was associated with metronidazole There was a significant difference between groups 1 and and probiotics oligosaccharide) (Table 3). The incidence 2 (400 ± 95 UFC/g Vs 160 ± 43 UFC/g, P < 0.05) as of BT in group 3 was not significantly different from that of shown in Table 5. The total bacterial counts, Gram- group 1 (P > 0.05). The same result was obtained when negative and Gram-positive, of cecal flora were signi- comparing group 2 to group 1 (P > 0.05). The difference ficantly low in group 1 than that in group 3 (400 ± 95 in the incidence of BT between groups 2 and 3 was UFC/g versus 36 ± 4 UFC/g, P < 0.001). 42% of the total significant (P < 0.05), 60% (6/10) in group 2 and 25% bacterial count was Gram-negative in group 1, 51% in group 2 and 13% in group 3. Metronidazole caused a Bacterial translocation was detected only in the MLNs slight overgrowth of Gram-negative bacteria in group 2. (3/10, 30%) of the rats of group 3 which were treated with Otherwise, this decrease in the Gram-negative population probiotics oligosaccharide. However, it was detected in of cecal flora was significant (P < 0.01). No micro- the MLNs (4/10, 40%), spleen (2/10, 20%) and liver organisms were isolated from the blood samples. (3/10, 30%) of group 2. The incidence of BT was significantly high in the MLNs of group 2 than that of group 1 (P < 0.05). Regarding the liver, the same result DISCUSSION
was obtained in group 2 comparing to groups 1 and 3 (P < 0.05). The incidence of BT in the MLNs was not These results suggest that protein-malnutrition induced significantly different between groups 2 and 3 (P > 0.05), translocation of enterobacteria. Metronidazole acted or between groups 1 and 3 (P > 0.05). These data specifical y on the strict anaerobic bacteria by reducing indicated that BT did not spread beyond the MLNs in their numbers in cecal flora which explains the high rates protein malnourished rats treated with probiotics of overgrowth and translocation of enteric bacteria in the Table 5. Quantitative results of Gram-negative, Gram-positive and total bacteria in cecal cultures for each group after
Gram-negative
Gram-positive
3. PM + antibiotic + Probiotics-Oligosaccharide Mean ± SEM X 102 colony-forming units per gram cecal content. *P < 0.05 and **P < 0.01 compared to group 1. malnourished group received metronidazole. (1985) found that the cecal overgrowth of enteric In this context, the current observation is that the PM bacilli caused an enhanced BT after the admini- and the PM particularly associated with metronidazole stration of Metronidazole (500 Units/ml) in PM rats, results in overgrowth cecal bacteria. This bacterial but the mean of enteric cecal population was overgrowth is most marked in the Gram negative. These significantly decreased by the administration of high levels of intestinal bacterial population help to explain the dose of penicil in (1500 Units/ml). Al of these col apse of the strictly anaerobic bacterial flora by the use studies demonstrate that oral antibiotics given in a of metronidazole and the consequent apparition of dose dependent manner may inhibit the growth of bacterial translocation in the GLM, spleen and liver. anaerobic bacteria and allow intestinal overgrowth In previous studies, we found that protein malnutrition of facultative anaerobic Gram-negative bacil i. and malnutrition associated with metronidazole pro- Therefore, the administration of oral antibiotics may mote bacterial overgrowth in cecal and translocation enhance BT to the MLNs and other organs after PM, of enterobacteria to MLNs (Benakriche et al., 2008). which impairs both humoral and cel ular immunity in Berg and Garglinton (1979) demonstrated that addition to the damage of local barriers. In the pre- penicil in, clindamycin, or metronidazole given orally sent study, we found that oral antibiotic treatment to specific pathogen-free mice for 4 days decreased enhances BT and promotes the spread of trans- the cecal population of indigenous bacteria, espe- locating bacteria to the liver in PM rats. However, cially anaerobic bacteria. A decreasing anaerobic antibiotic treatment is usual y required in the treat- population allows the cecal overgrowth of indi- ment of the inflammatory victims. Bacterial overgrowth genous, Gram-negative facultative anaerobic enteric in the smal intestine has been documented in children bacilli and enhances BT to the MLNs. Berg et al. with severe malnutrition and might contribute directly to (1988) demonstrated that a combination of anti- ineffective solubilisation, digestion and absorption of lipid biotics and immunosuppressive drugs promotes the systemic spread of translocating bacteria, resulting Despite knowledge in the area of overgrowth and in lethal sepsis. General y, metronidazole is considered intestinal bacterial translocation, probiotics and prebiotics as a safe drug because of its relative high therapeutic remain a hot topic. They are the subject of several index and limited duration of treatment. Deitch et al. studies which have shown in mice and rats that some (1985) reported that the administration of antibiotics probiotics like S. boulardi , B. longum, P. acnes, L. reduces the levels of indigenous GI tract flora and helveticus, L. rhamnosus and oligosaccharide have a delays colonization by indigenous bacteria in the protective effect against bacterial translocation. In addition, it has been shown that fructo-oligosaccharide However, Beaugerie and Petit (2004) postulated that not only have a protective effect against bacterial trans- giving oral antibiotic treatment to protein malnou- location but also stimulates the proliferation of Bifido- rished victims disrupts the ecological balance of indigenous bacterial flora and causes the intestinal It was reported that protein malnutrition decreases the overgrowth or colonization of the intestines by exo- number of lactobacil i and strict anaerobic bacteria of the endogenous flora resulting in enterobacteria overgrowth Pseudomonas aeruginosa, or Staphylococcus sp. Based on this theoretical suggestion, the same Recent studies have shown that probiotics, which researchers investigated the effects of oral antibi- have been used in the treatment of intestinal otics on bacterial overgrowth and bacterial translo- cation in protein malnourished rats. Deitch et al. Clostridium difficile colitis, are effective for maintaining intestinal equilibrium and reducing BT. Probiotics promote an increasing anaerobic population of translocation, but it enhanced the functional gastrointestinal tract flora (Duffy, 2000; Mattar et al., adaptation of the remaining intestinal segments. 2001) but anaerobic bacterial overgrowth may not be Another study by Berg et al. (1993) investigating the important for BT because anaerobic bacteria rarely effects of S. boulardi on the translocation of C. translocate to the MLNs. On the other hand, anae- albicans in antibiotic-decontaminated specific patho- robic bacterial overgrowth have many beneficial gen free mice revealed that it decreased the effects such as: strengthening gut mucosal barrier incidence of C. albicans translocating to the MLNs, function, balancing microbial ecology, adhering to liver, kidneys and also the number of translocating the intestinal mucosa, impeding invasive pathogens, C. albicans per gram MLNs, spleen, and kidneys. metabolizing dietary proteins and enzymes by intes- The present study, which was conducted to tinal microflora and promoting resilience of the evaluate the effects of probiotics oligosaccharide on epithelium to gut mucosal permeability. Col ins and BT in protein malnutrition associated with metro- Gibson (1999) reported that smal -bowel colonization nidazole treatment, showed that probiotics oligo- by Escherichia coli K1A and BT was decreased by saccharide significantly decreased the population of the administration of the probiotics oligosaccharide Gram-negative bacteria in cecal flora. Although we and suggested that probiotics oligosaccharide may be could not examine the anaerobic flora, these data used for the treatment of BT and sepsis. correlate with that of other reports in which It has been recently shown that impaired gut barrier probiotics increase the anaerobic bacterial count and mucosal immune function by malnutrition can be and decrease the Gram-negative facultative anae- reversed by L. casei used as an oral adjuvant of robic and aerobic bacteria count in the GI tract renutrition diet. The clinical significance of these findings (Mattar et al., 2001; Ishibashi and Yamazaki, 2001). wil be important, as wel as improving mucosal immunity, Anaerobic bacteria are generally decreased by may also induce protection against enteropathogens antibiotic treatment and this ecological imbalance (Gauffin et al., 2004). Probiotics can protect the intestine allows Gram negative bacteria to proliferate and by competing with pathogens for attachment, strength- enhances BT (Berg, 1981). The results of our study ening tight junctions between enterocytes and enhancing suggest that probiotics oligosaccharide may coun- the mucosal immune response to pathogens (Lei and teract this undesirable side effect of antibiotics. Interestingly, the incidence of BT in the rats treated Hirofumi et al. (1999) demonstrated that two kinds of with probiotics oligosaccharide (group 3) was not probiotics derived from different bacterial genera significantly higher than that of the group 1, but was enhanced epithelial cel proliferation of the gut without significantly higher than that of the rats given the altering the gross population levels of cecal microflora. In antibiotic alone (group 2). Although there was no humans in vivo, lack of protective effect of probiotics (L. significant difference in the incidence of BT and the plantarum 299V) on bacterial translocation to lymph number of translocating bacteria per gram of MLN nodes was confirmed by the same team and same between groups 2 and 3, we found that probiotics methodology for combining oligosaccharide with L. oligosaccharide decreased the incidence of BT from acidophilus, B. lactis Bb12, S. thermophilus and L. that which occurred in group 1 and also decreased bulgaricus (Anderson et al., 2004). the number of translocating bacteria. Furthermore, the administration of probiotics oligosaccharide salmonel a numbers in cecal contents and mucosa and ensured that BT was limited to the MLNs, whereas it caused a major increase in infection-induced diarrhea. In extended to the liver in rats not given probiotics addition, FOS enhanced translocation of salmonel a. oligosaccharide. Selection of strains was based on their Thus, in contrast to most expectations, FOS dose- in vitro antibacterial and immunomodulatory properties. L. dependently impairs the resistance to salmonel a acidophilus, L. rhamnosus, B. lactis, B. longum, B. infection in rats (Sandra et al., 2003). bifidum, S. thermophilus and fructo-oligosaccharides L. fermentum KLD has previously been used as both a were selected for their ability to suppress the growth of prophylactic and therapeutic agent in the treatment of Gram- negative bacteria and their antimicrobial effects. gastrointestinal disturbances and is an interesting The lower incidence of BT in the rats given oral candidate probiotic strain (Marteau et al., 2001). probiotics oligosaccharide may not only related to Zaouche et al. (2000) investigated the effects of S. improved intestinal ecological balance, but also to boulardi on bacterial overgrowth and translocation in the effects of probiotics oligosaccharide on host rats with resected smal intestine and found that it immune responses, including stimulation of the production and secretion of intestinal s-IgA, enhan- cing both phagocytic activity and the maturation of Bhan MK (1996). The gut in malnutrition. In: Walker WA, Durie PR, Hamilton JR, Walker-Smith JA, Watkins JB, eds. Pediatric gastrointestinal diseases: pathophysiology, diagnosis, management. Protein malnutrition is known from biopsy studies to be associated with vil ous atrophy, decreased vil ous-crypt Brewster DR, Manary MJ, Menzies SI, O'Loughlin V, Henry RL (1997). ratio and increased cel ularity of the lamina propria. Intestinal permeability in kwashiorkor. Arch. Dis. Child, 76: 236-241. Although severe mucosal injury occurs only in a Brunser O, Reid A, Monckeberg F, Maccioni A, Contreras I (1968). Jejunal mucosa in infant malnutrition. Am. J. Clin. Nutr., 21: 976-983. proportion of malnourished children, it is more common in Chandra RK (1993). Nutrition and the immune system. Proceed. Nutr. kwashiorkor; possibly due to the effect of protein deple- tion on mucosal recovery (Viteri et al., 1973; Brunser et Col ins S (2007). Treating severe acute malnutrition seriously. Archi al., 1968; Bhan, 1996), atrophy of intestinal vil i facilitates Col ins MD, Gibson GR (1999). Probiotics, prebiotics, and synbiotics: the breakdown of the mucosal barrier and thus, trans- approaches for modulating the microbial ecology of the gut. Am. J. location of bacteria from endogenous flora. Abnormal intestinal permeability in kwashiorkor correlates with Cremonini F, Di Caro S, Bartolozzi F (2001). The impact of probiotics in disease severity and improves only slowly with nutritional antibiotic-associated diarrhea: a meta-analysis of placebo control ed Deitch EA, Maejima K, Berg R (1985). Effect of oral antibiotics and On the other hand, abnormal intestinal permeability is a bacterial overgrowth on the translocation of the gastrointestinal tract feature of bacterial translocation in malnourished adult microflora in burned rats. J. Traumatol, 25: 385-392. patients with multi-organ failure secondary to trauma, Deitch EA (1990). Bacterial translocation: is it of clinical significance? Dock-Nascimento DB, Junqueira K, Aguilar-Nascimento JE (2007). In conclusion, probiotics oligosaccharide may protect Rapid restoration of colonic goblet cel s induced by a hydrolyzed diet the balance of GI tract flora by inhibiting the growth containing probiotics in experimental malnutrition. Acta Cirúrgica of Gram-negative bacteria and assisting the growth Dock DB, Aguilar-Nascimento JE, Latorraca MQ (2003). Enhanced of anaerobic bacteria. On the other hand, it may immunological response influenced by probiotics during the recovery enhance the host immune responses. These effects of experimental malnutrition. Rev. Braz. Clin. Nutr. 18: 157-162. of probiotics oligosaccharide may lower the incidence Duffy LC (2000). Interactions mediating bacterial translocation in the of BT and the number of translocating bacteria in immature intestine. J. Nutr. 130(2):432–436. Freeman CD, Klutman NE, Lamp KC (1997). Metronidazole: a protein malnourished victims being treated with therapeutic review and update. Drugs, 54: 679-708. metronidazole. Thus, probiotics oligosaccharide may be Ful er R (1992). History and development of probiotics. In: Probiotics. effective in preventing BT to the MLNs and other The Scientific Basis. Ed. 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