Patients with liver cirrhosis produce. Enterococcus Lactic Acid Bacteria Strain SF68 and Lactulose in Hepatic Encephalopathy: a Controlled Study

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1 The Journal ofinternational Medical Research 1987; 15: Enterococcus Lactic Acid Bacteria Strain SF68 and Lactulose in Hepatic Encephalopathy: a Controlled Study C. Loguercio, C. Del Vecchio Blanco and M. Coltorti Istituto di Medicina Generale e Metodologia Clinica, I Facoltd di Medicina e Chirurgia, University ofnaples, Naples, Italy Forty cirrhotic patients with non-advanced hepatic encephalopathy were randomly allocated into groups which were given orally either two capsules three times daily ofa preparation of Enterococcus lactic acid bacteria strain SF68 or 30 ml lactulose four times daily. The patients were evaluated over a 10-day course of treatment and for 10 days post-treatment. The Enterococcus SF68 preparation proved to be as effective as lactulose in lowering blood ammonia, and in improving mental state and psychometric performance. Moreover, the effects of Enterococcus SF68, contrary to that of lactulose, persisted longer after treatment withdrawal. Some patients reported diarrhoea and abdominal pain with lactulose. Lactulose is a standard therapy in the treatment of patients with hepatic encephalopathy. In this study, however, the use of the Enterococcus SF68 preparation was shown to offer advantages over lactulose in these patients. INTRODUCTION Patients with liver cirrhosis produce ammonia from putrefactive intestinal flora: this is considered one of the factors responsible for hepatic Received for publication 17 July 1987; accepted 6 August Address for correspondence: Dr C. Loguercio, Istituto di Medicina Generale e Metodologia Clinica, I Facolta di Medicina e Chirurgia, University of Naples, Via Pansini S, Naples, Italy. encephalopathy (HE).l In particular, there is evidence that cirrhotic patients have a greater urease-active intestinal flora, while HE cirrhotic patients show a higher urea degradation in the intestine compared with HE-free patients. Using radio-labelled markers, Hansen and Vilstrup' proved that there is increased intestinal urea hydrolysis in patients with ethanol-induced cirrhosis. The most widely used treatment of HE is aimed at modifying the intestinal flora through contact antibiotics and/or e Copyright 1987 by Cambridge Medical Publications Ltd. 335

2 C. Loguercio, C. Del Vecchio Blanco, M. Coltorti lactulose. Sometimes significant sideeffects, however, restrict the tolerance of these drugs, especially if used for longterm treatment. As an alternative, attempts have been made to modify the intestinal flora of cirrhotic patients by administering lactobacilli.t-" These early trials, however, were not always satisfactory, mainly because it was difficult to obtain an actual neocolonization of the intestine; moreover, such trials were not followed by controlled studies on an adequate number of cases. Enterococcus strain SF68 is a lactic acid bacteria (LAB), with high stability, a very short generation time and strong inhibitory effects against some enteropathogenic micro-organisms; therefore, it can rapidly modify the intestinal flora.v" Previous investigations have demonstrated that the administration of Enterococcus SF68 gives improved tolerance to oral proteic load in cirrhotic patients;' if combined with reduced dietary intake of proteins, it causes significant improvement in neuropsychiatric symptoms and blood ammonia levels in cirrhotic patients with mild HE.8 The aim of this study was to assess the effects of a preparation of Enterococcus SF68 (Bioflorine) in cirrhotic patients with non-advanced HE, who were maintained on a normal dietary intake of proteins. PATIENTS AND METHODS Forty cirrhotic patients entered the study. At enrolment 38 showed HE of grades I or II,9 while two had marked hyperammonaemia and altered psychometric performance using Reitan's test, even in the absence of any clinical signs of HE. After a 3-day baseline period patients were randomly assigned to a treatment group. Twenty patients were ~ Bioflorin is a tradename of Giuliani and is distributed by Gipharmex SpA, Italy. treated with Enterococcus SF68 which was given as two capsules three times daily after meals, each capsule containing at least 75 x 106 cells. The other 0 patients were treated with 30 ml lactulose four times a day after meals. The main features of the two groups of patients at baseline are shown in Table 1. All patients were treated for 10 days and followed-up for a further 10 days after cessation of treatment (Fig. 1). During the trial patients were maintained on a normocaloric diet, including 70 g of protein daily. Four diabetic patients received insulin and nine patients with ascites received diuretics. Throughout the study (including the 3 days pre- and 10 days post-treatment) no patient was given any other drug. The mental state of the patients was evaluated daily according to the method of Conn and Lieberthal,? as well as the occurrence of abdominal pain and meteorism, and bowel function (number of evacuations, stool consistency and ph). The following 0-4 scale was used for patient evaluation: 0, normal; 1, psychometric defects, anxiety and altered attention;, altered mood, confusion and drowsiness; 3, inappropriate behaviour, deep drowsiness, marked confusion and inarticulate speech; and 4, coma. On pre-treatment days and on days 3, 5, 7, 10, 15 and 0 of the trial, ammonia was determined in samples of arterial blood in fasting patients by an enzymatic method. In addition, on days 0, 5, 10, 15 and 0, 14 patients from each treatment group underwent a number connection test (Reitan A). The influence of learning on performance in the test was minimized by using each time five variants of the test, always in a different order.'? The results were expressed as the average of the performance times. All patients gave informed consent. Patients' score for mental condition, 336

3 Enterococcus LAB SF68 Table 1 Baseline characteristics of the 40 patients studied No. of patients Sex, male/female Age (years), median (range) No. of alcoholics" No. with hepatitis B surface antigen Blood ammonia (~g/dl), mean ±SE (normal <90 I!g/dl) Glutamic pyruvic transaminase (VII), mean ± SE (normal, <40 VII) Prothrombin time (%), mean ± SE Serum albumin (g/dl), mean ± SE Mental status, score: 0 1 No. on diuretic treatment No. ofinsulin-dependent diabetics Enterococcus SF68-treated 0 13M/7F 58 (5-66) ± ± ± ± Lactulose-treated 0 13M/7F 57 (35-68) ± ± ± ± Alcohol consumption: males ~80 g/day; females )60 g/day, Enterococcus SF68~treated group: 0 patients 40 patients Lactulose-treated group: 0 patients I Baseline 1 I - -I 0 4 Treatment I Follow~up I r r---'''''--'--'''---'''''--'--'''--9""1""-,0- I I 1I I 13 I 14 I I 5 I 16 I 17 I I 8 I I 9 I 0 Study period (days) Norrnocaloric diet, 70 g protein daily Evaluations: mental state, bowel functions, presence/absence of abdominal pain, meteorism - every day blood ammonia-on days-i.o, 3, 5, 7,10,15,0 Reitan's test - on days -, -I, 0,5, 10, 15,0 Fig. I. Scheme to illustrate the experimental design. 337

4 C. Loguercio, C. Del Vecchio Blanco, M. Coltorti abdominal pain, meteorism and the number of evacuations per day were submitted to the non-parametric analysis of variance (Kruscal-Wallis' test). Owing to the non-homogeneity of basal values the covariance analysis was used for data from Reitan's test. RESULTS The baseline parameters did not differ significantly between the treatment groups. All patients completed the treatment period. Five patients given lactulose and four given Enterococcus SF68 did not arrive for post-treatment follow-up. On day 15, two patients given lactulose showed marked hyperammonaemia and a worsening of HE and, therefore, were withdrawn from the study. One patient given Enterococcus SF68 had constipation on day 10, with a higher level of blood ammonia and worsened HE and, consequently, was then given lactulose. In all patients in the group given lactulose an increased number of bowel evacuations (Table ) and decreased faecal ph were observed during treatment. In five cases, meteorism and abdominal pain were reported; in a further case diarrhoea and abdominal pain made it necessary to halve the lactulose dose. Patients given Enterococcus SF68 reported no side-effects. Table Number of bowel evacuations per day during the study in both groups of patients (mean ± SD) Period ofstudy Pre-treatment (days - to 0) During treatment (days 1-10) Post-treatment (days 11-0) Enterococcus SF68-treated 1.75 ± ± ±0.75 Lactulosetreated 1.4 ± ± ± 0.67 Table 3 Statistical comparison of blood ammonia levels during the study period in both groups of patients (see also Fig. ) Statistical comparison F P Analysis of variance Between treatments Lactulose, between times Enterococcus SF68, between times Comparison between times within treatments Basal vs days 3-10 Day 10 vs days 15-0 Basal vs days NS 6. < < Lactulosetreated P<O.OOl P<O.OOOI NS Enterococcus SF68-treated P<0.005 NS P<

5 t;.) t;.) 'D , } o:l t:q 60.L ~l o Enterococcus SF68-treated / o, I --, , I I I I Study period (days) Fig.. Changes in blood ammonia levels during the study period in both groups of patients (see also Table 3) Lactulose-treated ttl a(1)... o non o cen r ;l> ~ (Zl "T] 0-, 00

6 w ~ Enterococcus SF68-treated 185 Lactulose-treated '-" '" (l) E E::: "'" ~. -, '\.".. ". '"" ',,~ -,.~~... -:~.,,-.,... '" ''', ". ". ". ". "'" ~. E-< ", -,, -,, -, ~\\\ <. ",... ". '. -, -,, -,,... -, <, <, " <, ',,'. '<, -'~ ~ <,~.", '-.. <.».~... 50~/ i I 50..!.7"/ I I Before treatment After treatment Before treatment After treatment Fig. 3. The results of Reitan's test in cases with initial values greater than the mean + SDs (l.e, > s) before and after treatment in both groups of patients. o t'"" o 0<1 c: (I).., Q. 0 o a. o <: o=r ~ o I:l:l ~ ::l (') 9 ~ o o S d.

7 Enterococcus LAB SF68 Figure shows the change in blood ammonia levels during the study period; the relevant statistical analysis (analysis of variance for trends) is shown in Table 3. In both groups a marked reduction in ammonia levels was observed (P < in both treatments). Although the effect of lactulose seems to be slightly faster, there was no statistically significant difference between the treatments. During the 10 days' post-treatment follow-up, ammonia levels in the group given lactulose returned to baseline values, while in the group given Enterococcus SF68 they were unchanged. With both treatments there was a statistically significant improvement of mental status (P < 0.000, with no difference between the groups. In particular, Table 4 shows the changes in mental status at the end of both treatments and after 10 days' post-treatment follow-up. Covariance analysis on the results of Reitan's test showed a statistically significant reduction in performance times at the end of both treatments, which was similar in the two groups studied (p <0.00l) due to the contrast between the basal versus treatment period and follow-up data. Figure 3 shows the results of Reitan's test in cases with high initial values (greater than the mean + SDs of the control population, i.e. > s). After treatment withdrawal, the improvement persisted until Table 4 Changes in mental status (graded from 0 to 4) before (day 0) and immediately after treatment (day 10), and 10 days post-treatment (day 0) Enterococcus SF68-treated Laetulose-treated Case no. Day 0 Day 10 Day 0 Day 0 Day 10 Day I I 1 I * * * Value on day

8 C. Loguercio, C. Del Vecchio Blanco, M. Coltorti day 0 in all patients, except for three given lactulose and one given Enterococcus SF68. Among patients who had HE grades I and II at baseline, 15 out of 19 treated with Enterococcus SF68 and 14 out of 19 treated with lactulose were improved (HE normalized or reduced); in only one patient, treated with Enterococcus SF68, did HE change from grade I to grade II. After the 10 days' post-treatment followup the improvement in HE was maintained in 4.85% of patients given lactulose and in 6()o,.-b of those given Enterococcus SF68 (Table 5). Two patients showed serious HE a few days after the end of lactulose treatment; this did not occur in patients given Enterococcus SF68. DISCUSSION The results of this investigation show that the administration of Enterococcus SF68 is useful in the treatment of nonadvanced HE, probably due to modification of the intestinal microflora. A 10 day administration of Enterococcus SF68 induced a marked decrease of blood ammonia levels and improved mental state and psychometric performance. Previous observations in patients with liver cirrhosis showed decreased ammonia levels -3 weeks after administration of Bifidobacterium and Lactobacillus acidophilus, while during the first 7-10 days of treatment ammonia levels were unchanged or even increased.' The more rapid onset of the effect of administering Enterococcus SF68 is likely to be due to more rapid intestinal development and reproduction of these bacteria.vs There appear to be no reports of clinical studies comparing the use of lactic acid producers and drugs useful in the treatment of HE, apart from our preliminary observations," Conn and Floch,'! however, have compared the effects of lactulose and L. acidophilis on the composition of the faecal flora. In the present study, the results obtained with Enterococcus SF68 appeared to be similar to those obtained with lactulose, whose effectiveness in treating HE is well documented.v!' Data from the present study are of practical relevance since sometimes the effectiveness of lactulose is reduced by low compliance by patients. In this study five patients reported diarrhoea and abdominal pain, and one required a reduction in the dosage of lactulose. Treatment with Enterococcus SF68 was virtually free of side-effects indicating that it can be used safely for long-term treatment. The follow-up data after cessation of treatment show that the effectiveness of lactulose is closely related to its intake, as proved by increased blood ammonia levels after drug withdrawal in all patients given lactulose. On the contrary, 10 days after withdrawal from Enterococcus SF68 therapy no increase in blood ammonia levels was observed. The evaluation of mental conditions also suggests a more Table 5 Overall evaluation oftherapeutic response Treatment Improvement at day 10 Improvement at day 0 Enterococcus SF68 Lactulose 15/19 (78.95%) 14/19 (73.68%) 9/15 (600!o)* 6/14 (4.85%)* * In patients who completed the follow-up period. 34

9 Enterococcus LAB SF68 favourable persistent effect in patients treated with Enterococcus SF68. A possible explanation may be that Enterococcus SF68-induced changes in the intestinal flora are maintained for longer after treatment is stopped.' As Enterococcus SF68 is resistant to various antibiotics it can also be used with contact antibiotics, such as neomycin and paromomycin. The chronic HE occurring in a cirrhotic patient and the presence of a surgical shunt, often require long-term treatment. When antibiotics and/or lactulose are used for this, either alone or combined with reduced levels of dietary protein, side-effects often occur. Although not directly demonstrated in the present study, combined treatment with Enterococcus SF68, lactulose and neomycin/paromomycin may allow dosage reduction and, hence, reduce the sideeffects of such drugs. It is important to note that the present study showed a marked improvement in HE, without using a low protein diet which may have exacerbated the disease. In conclusion, this study indicates that the administration of Enterococcus LAB strain SF68 is effective and free of side-effects in the management of chronic non-advanced HE. ACKNOWLEDGEMENTS We should like to thank Dr G. Frigerio and Dr G. Brunetti of Gipharmex, Milan, Italy for advice throughout the study and Dr Mariella Pozzoli for the statistical analysis. REFERENCES I. Fraser CL, Arieff A: Hepatic encephalopathy. N Engl J Med 1985; 313: Hansen BA, Vilstrup H: Increased intestinal hydrolysis of urea in patients with alcoholic cirrhosis. Scand J Gastroenterol 1985; 0: Read AE, McCarthy CF, Heaton KW, et al: Lactobacillus acidophilus (enpac) in the treatment of hepatic encephalopathy. Br Med J 1966; 1: Passaretti S, Fesce E, Testoni PA, et al: Trattamento sperimentale dell'iperarnmoniemia con una associazione di bifidobacterium e Lactobacillus acidophilus somministrata per via orale. CUn Ter 198; 100: Carbone M, Bonina L, Fera M: Microbiological properties of Streptococcus faecium SF68-strain and relationship with other microorganisms. Boll 1st Sieroter Milan 1980; 59: Lewenstein A, Frigerio G, Moroni M: Biological properties ofsf68, a new approach for the treatment of diarrheal diseases. Curr Ther Res 1979; 6: Del Vecchio Blanco C, Ambrogio G, Mattera D, et al: Influence du traitment par Streptococcus faecium (SF68) sur la courbe ammoniemique de charge proteique chez des sujets atteints de cirrhose hepatique. Med Hyg 1981; 39: Del Vecchio Blanco C, Ambrogio G, Coltorti M: Studio pilota sull-effetto di trattamento "short term" con Streptococcus faecium (SF68) sull-ammoniogenesi intestinale in pazienti cirrotici, Continuing Education in Gastroenterology 1983; suppl I: Conn HO, Lieberthal MM: The Hepatic Coma Syndromes and Lactulose. Baltimore: Williams & Wilkins, 1979; pp Loguercio C, Del Vecchio Blanco C, Coltorti M: Psychometric tests and "latent" portal systemic encephalopathy. Br J CUn Pharmaco11984; 38: I. 11. Conn HO, Floch MH: Effects of lactulose and Lactobacillus acidophilus in the fecal flora Am J CUn Nutr 1970; 3:

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