Therapeutic effects of synbiotic on neonates with gestational age over 34 weeks admitted for jaundice

Abstract

BACKGROUND:

Hyperbilirubinemia is a common problem in neonates. The aim of this study was to evaluate the effect of synbiotic in addition to routine phototherapy on the treatment of neonatal jaundice.

METHOD:

This double-blind clinical trial, was performed on 194, 3–14 days old neonates. Neonates were divided into intervention and placebo groups. The intervention group received 5 drops of oral synbiotic daily along with phototherapy and the placebo group underwent phototherapy plus a placebo. Gestational age, age, weight, sex, initial and daily bilirubin level, frequency of defecation, mode of delivery, and length of hospitalization were assessed.

RESULTS:

The rate of bilirubin reduction on the first day of admission was significantly higher in the intervention group (2.9±1.81 vs. 2.06±1.93, p = 0.002). The mean level of bilirubin on the second (9.8±1.92 vs. 10.88±2.26) and third days (8.06±1.54 vs. 9.86±1.7) was lower in the intervention group (p = 0.001). The proportion of discharged patients in the third and fourth days was higher in the intervention group compared to the control (65% vs. 41%, 99% vs. 86.5%, respectively, p = 0.001). However, the duration of hospitalization was shorter in the intervention group compared to the control (2.36±0.5 vs. 2.74±0.74, p = 0.001).

CONCLUSION:

Based on our results, daily treatment with 5 drops of synbiotic along with phototherapy can be a safe and effective modality in faster bilirubin reduction, decreasing the hospitalization period and phototherapy. Therefore, it seems that it can be used as an adjunct therapy for neonates with jaundice.

Keywords

Jaundice neonate synbiotics phototherapy

1 Background

Jaundice is one of the most prevalent clinical conditions during the neonatal period, especially in the first week of life [1]. Phototherapy is the most common intervention used to treat and prevent hyperbilirubinemia, and thus eliminating the need for blood exchange [2]. Although phototherapy is a safe method of treatment, it may also induce complications, such as neonatal hyperthermia, increased imperceptible water excretion, diarrhea, dehydration, maculopapular red skin rash, lethargy, and possible retinal damage [3, 4]. On the other hand, the association between phototherapy, type 1 diabetes mellitus and asthma has been documented [5]. Moreover, it has been reported that phototherapy might be associated with DNA damage and lymphocyte apoptosis in full-term infants [6]. Considering the aforementioned potential harmful effects of phototherapy leads clinicians to find adjuvant therapies in order to decrease the phototherapy period. Prebiotics are non-digestible food ingredients which can stimulate the growth of some beneficial microbiota, such as Bifidobacterium lactis, Lactobacillus acidophilus, and Lactobacillus rhamnosus. On the other hand, probiotics are living micro-organisms that result in better health upon consumption. synbiotics are synergistic combination of prebiotics and probiotics [7]. Probiotics and prebiotics are used to increase immunity by modulating gastrointestinal bacterial colonies. They can form a biological barrier by binding specifically to the epithelial cells of the infant’s gastrointestinal tract via teichoic acid [8]. Microbiological preparations, including probiotics, can reduce enterohepatic circulation by altering the normal intestinal flora and inhibiting beta-glucuronidase activity [9]. Probiotics and prebiotics have been confirmed to have beneficial effects on the enterohepatic cycle, including better gastrointestinal motility, improved stool viscosity, and increasing the frequency of defecation [6]. Although several studies reported a reduction in the duration of phototherapy and the effective therapeutic role of various probiotics in the treatment of neonatal hyperbilirubinemia [6 , 10–12], some did not find a significant relationship [13, 14]. As there were limited studies regarding therapeutic effect of synbiotic on neonatal jaundice, this study aimed to assess the effect of synbiotic on reducing serum bilirubin level in neonates.

2 Methods

2.1 Study design

The present study is a double-blinded clinical trial. The study population included hospitalized infants due to jaundice in the neonatal ward of 17 Shahrivar children’s Hospital in Rasht, Iran, from July 2018 until August 2019. The inclusion criteria were as followed; 3–14 days of age, weight > 2500 gm, serum bilirubin level of 15 to 22mg/dl, direct bilirubin level < 1.5mg/dL, exclusive breastfeeding, healthy neonates, and no specific diseases. The patients acquiring any of the following factors were excluded; gestational age < 35 weeks, sepsis and underlying disease, cephalohematomas, ABO incompatibility, RH incompatibility, glucose 6 phosphate dehydrogenase deficiency, parental dissatisfaction during hospitalization, diabetic mother, evidence of bleeding, polycythemia, feeding with formula, treated with phenobarbital or Bilineaster drop, down syndrome, family history of immunodeficiency, blood exchange, antibiotic therapy, evidence of hemolysis, and serum intake. In this study, 194 neonates were included. The neonates were divided into intervention and placebo groups consisting of 97 neonates in each one. They were randomly assigned based on quadruple random blocks. Both groups received phototherapy, based on the American Academy of Pediatrics (AAP) guideline [15]. The intervention group received 5 drops of PediLact as a type of synbiotic once daily until the day of discharge along with phototherapy and the placebo group received placebo and phototherapy. PediLact is in the form of oral drops made by Iran Bio-Fermentation Zisttakhmir Company and contains three types of probiotics (Lactobacillus reuteri, lactobacillus rhamnosus, and bifidobacterium infantis) as well as fructo oligosaccharide as a prebiotic [14]. For appropriate efficacy, PediLact should be stored in the refrigerator. In the placebo group, 5 drops of diluted formula that were similar in appearance and shape to PediLact drops were given. The glass containers containing PediLact were emptied and the diluted formula was poured into them, so that the placebo was indistinguishable from PediLact. Neonates received PediLact or placebo once daily before breastfeeding until the day of discharge. The researcher and parents were unaware of the group and type of prescription. For double blind status of this research, an experienced neonatal nurse was aware of the process of classifying patients and the type of substance prescribed to the neonates. Blood sampling was performed daily for serum bilirubin measurement. The laboratory bilirubin measurement method was by BT 3500 device (Italy). Patients were discharged when their serum bilirubin level fell below 11 mg/dl. Neonates were evaluated daily for synbiotic complications (diarrhea and bloating), symptoms of sepsis, and vomiting during hospitalization. Data were gathered by a form including gestational age, age, type of delivery, weight, sex, initial and daily bilirubin level during hospitalization until discharge, frequency of defecation, and duration of hospitalization and phototherapy.

2.2 Ethical consideration

Written consent was obtained from the parents of the neonates. This study was approved by the Vice Chancellor of Research at Guilan University of Medical Sciences (Number: IR.GUMS.REC.1397.196, date: 2018.08.18). The IRCT code was IRCT2018.228.38895N1 (date: 2018.09.26).

2.3 Statistical analysis

After collecting the data, they were entered into SPSS software version 21. Data were reported by frequency, percent, mean, and standard deviation. To compare the number of changes in bilirubin level and frequency of defecation and duration of hospitalization in two groups, the independent T-test was used. In the case of abnormal distribution of bilirubin, Mann Whitney U-test was used. Repeated Measured ANOVA was used to compare the trend of bilirubin changes in the two groups. A Chi-square test was performed to compare the complications in the two groups. P value < 0.05 noted significant difference.

3 Results

In this study, 194 neonates were assessed including 97 patients in intervention and placebo group. Results showed that there was no significant difference between groups regarding demographic and pregnancy-related characteristics including gestational age (week), term or preterm status, infant age, infant weight, and type of delivery (Table 1).

Table 1
Demographic and pregnancy-related characteristics of neonates

Studied group P-value

Synbiotics and phototherapy recipients Phototherapy treatment Total

Sex Boy Number 51 57 108 0.386

Percent 52.6% 58.8% 55.7%

Girl Number 46 40 86

Percent 47.4% 41.2% 44.3%

Gestational age (Week) Mean 37.93 37.83 37.88 0.538

Standard deviation 1.15 1.14 1.14

Minimum 35.00 35.00 35.00

Maximum 40.00 41.00 41.00

Term or preterm status Under 37 Weeks Number 21 25 46 0.749

Percent 21.6% 25.8% 23.7%

Over 37 Weeks Number 76 72 148

Percent 78.3% 74.2% 76.3%

Infant age Mean 5.80 6.30 6.05 0.116

Standard deviation 2.13 2.33 2.24

Minimum 3.00 3.00 2.50

Maximum 14.00 14.00 14.00

Infant weight Mean 3050.67 3036.44 3043.56 0.778

Standard deviation 387.02 310.09 349.83

Minimum 2500.00 2500.00 2500.00

Maximum 3900.00 3850.00 3900.00

Type Of delivery Normal Number 33 31 64 0.760

Percent 34.0% 32.0% 33.0%

Cesarean section Number 64 66 130

Percent 66.0% 68.0% 67.0%

Total Number 97 97 194

Percent 100.0% 100.0% 100.0%

			Studied group	P-value
Sex	Boy	Number	51	57	108	0.386
		Percent	52.6%	58.8%	55.7%
	Girl	Number	46	40	86
		Percent	47.4%	41.2%	44.3%
Gestational age (Week)	Mean		37.93	37.83	37.88	0.538
	Standard deviation		1.15	1.14	1.14
	Minimum		35.00	35.00	35.00
	Maximum		40.00	41.00	41.00
Term or preterm status	Under 37 Weeks	Number	21	25	46	0.749
		Percent	21.6%	25.8%	23.7%
	Over 37 Weeks	Number	76	72	148
		Percent	78.3%	74.2%	76.3%
Infant age	Mean		5.80	6.30	6.05	0.116
	Standard deviation		2.13	2.33	2.24
	Minimum		3.00	3.00	2.50
	Maximum		14.00	14.00	14.00
Infant weight	Mean		3050.67	3036.44	3043.56	0.778
	Standard deviation		387.02	310.09	349.83
	Minimum		2500.00	2500.00	2500.00
	Maximum		3900.00	3850.00	3900.00
Type Of delivery	Normal	Number	33	31	64	0.760
		Percent	34.0%	32.0%	33.0%
	Cesarean section	Number	64	66	130
		Percent	66.0%	68.0%	67.0%
	Total	Number	97	97	194
		Percent	100.0%	100.0%	100.0%

Table 2 compared the bilirubin level at hospitalization days and its changes by independent t-test and paired t-test. Mean bilirubin level on the first day after phototherapy was not statistically different between the two groups (p = 0.057) but despite the significant decrease of bilirubin in both groups (p < 0.001), the rate of reduction in the intervention group was significantly greater than the placebo group (p = 0.002). There was a significant difference between the two groups regarding bilirubin level on the second and third days (p < 0.001). The rate of bilirubin reduction in the intervention group was significantly higher than placebo group. On the fourth day, only one patient in the intervention group and 13 patients in the placebo group were still in the neonatal ward (p = 0.335). The comparison of changes between two groups, on the fourth day, was not significant due to the small number of samples remained in the intervention group (p = 0.088). On the fifth day, 100% of the intervention group were discharged, but two of the neonates in the placebo group were still hospitalized. Therefore, comparing bilirubin level was not possible (Table 2).

Table 2

Comparison of serum bilirubin level during hospitalization in 2 groups

		Groups
		No	Synbiotic and phototherapy	No	Phototherapy	Total	P
Basic bilirubin	Mean	97	16.93	97	16.73	16.83	0.342
	Standard deviation		1.43		1.53	1.48
The first day bilirubin	Mean	97	14.03	97	14.67	14.35	0.057
	Standard deviation		2.39		2.23	2.33
First day bilirubin decrease	Mean	97	2.90	97	2.06	2.48	0.002
	Standard deviation		1.81		1.93	1.91
P			0.001 >		0.001 >
The second day bilirubin	Mean	96	9.80	97	10.88	10.35	0.001
	Standard deviation		1.92		2.26	2.16
Bilirubin level decrease until the second day	Mean	96	7.15	97	5.85	6.50	0.001
	Standard deviation		1.64		2.36	2.13
P			0.001 >		0.001 >
The third day bilirubin	Mean	34	8.06	57	9.86	9.19	0.001
	Standard deviation		1.54		1.70	1.86
Bilirubin level decrease	Changes until	34	9.83	57	7.18	8.17	0.001
until the third day	the second day
	Standard deviation		2.55		2.37	2.74
P			0.001 >		0.001 >
The fourth day bilirubin	Mean	1	8.60	13	10.02	9.92	0.335
	Standard deviation		.		1.37	1.37
Bilirubin level decrease	Mean	1	11.40	13	7.20	7.50	0.088
until the fourth day	Standard deviation		.		2.18	2.38
P			–		0.001 >
The fifth day bilirubin	Mean	0	.	2	10.20	10.20	–
	Standard deviation		.		0.42	0.42
Changes until the fifth day	Mean	0	.	2	9.15	9.15	–
	Standard deviation		.		3.32	3.32
P			–		0.160

Table 3 compared the distribution of discharge time in the two groups. Results showed that at the end of the third day, the frequency of discharged patients in the intervention group was 65.7%; but in the placebo group, it was 40.6%. This difference was statistically significant (p < 0.001). At the end of the fourth day, 99% of the neonates in the intervention group were discharged. This frequency was 86.5% in the placebo group, which was also statistically significant (p = 0.001).

Table 3

Comparison of discharge in two groups

			Groups					P
		Recipient of synbiotics and phototherapy		Phototherapy treatment		Total
		No	Percent	No	Percent	No	Percent
The first day	(No discharge)Bilirubin above 11	97	100.0%	97	100.0%	194	100.0%	0.999
of hospitalization	(Discharge)Bilirubin below 11	0	0.0%	0	0.0%	0	0.0%
The second day	(No discharge)Bilirubin above 11	96	99.0%	97	100.0%	193	99.5%	0.508
of hospitalization	(Discharge)Bilirubin below 11	1	1.0%	0	0.0%	1	0.5%
The third day	(No discharge)Bilirubin above 11	34	35.0%	57	59.0%	91	46.9%	0.001
of hospitalization	(Discharge)Bilirubin below 11	63	65.0%	40	41.0%	103	53.1%
The fourth day	(No discharge)Bilirubin above 11	1	1.0%	13	13.5%	14	7.2%	0.001
of hospitalization	(Discharge)Bilirubin below 11	96	99.0%	84	86.5%	183	92.8%
The fifth day	(No discharge)Bilirubin above 11	0	0.0%	2	2.0%	2	1.0%	0.241
of hospitalization	(Discharge)Bilirubin below 11	97	100.0%	95	98.0%	195	99.0%

Comparing groups, there was no statistically significant difference in terms of defecation on the first day (p = 0.169), second day (p = 0.122), third day (p = 0.429) and on the fourth day (p = 0.544). As all neonates in intervention group were discharged upon the fifth day, no comparison was possible to be performed between groups.

The duration of hospitalization in the intervention group was shorter than the placebo group (2.36±0.50 vs. 2.74±0.74, p = 0.001). However, there was no significant difference between two groups regarding the rate of bilirubin reduction until the day of discharge, in association with neonatal sex and mode of delivery (p > 0.05). But in neonates delivered by cesarean section, reduction in bilirubin of the intervention group was significantly higher than the placebo group (p = 0.028). In intergroup comparison, changes in bilirubin levels in preterm neonates (<37 weeks of gestation) were not significant (p = 0.854), and in term neonates, the rate of bilirubin reduction was significantly greater in intervention vs. placebo group (p = 0.002). The mean reduction of bilirubin until the day of discharge in the intervention group was 8.45±2.2 with a median of 8,and in the placebo group was 7.53±1.9 with a median of 7.2, which was statistically significant (p = 0.003). No complication was seen in none of the neonates.

4 Discussion

It has been confirmed that the intestinal probiotics affect the level of bilirubin in the enterohepatic circulation by reducing the degradation of bound bilirubin, as well as stimulating the intestinal peristalsis [16, 17].The present study attempted to evaluate the therapeutic effects of a particular probiotic called synbiotic on neonates admitted for jaundice. Our results a significant difference in the amount of decrease in bilirubin level among two groups from the second day of treatment. Synbiotic was used in a study conducted by Ahmadi et al., who reported significantly lower bilirubin levels, higher stool and urine frequency and faster discharge among neonates treated by synbiotic [18]. On the other hand, Liu et al. in their study examining the effects of probiotic therapy on jaundice in term neonates reported that the difference in the numerical level of bilirubin became apparent from the fourth day [8]. Meanwhile, in studies conducted by Secre et al., Ling et al., and Zahed Pasha using saccharomyces boulardii, Mami Ai, and Pedi-Lact respectively as probiotic, no association was found between probiotic consumption and reducing the duration of phototherapy and decreasing the bilirubin level [14 , 19]. These differences can be explained by the different types of probiotic prescribed in studies. On the other hand, since some formulas may contain some prebiotics or probiotics that can affect the outcome of the study, formula-fed patients were excluded from this study.

The current study showed that the proportion of discharged patients at the third and fourth days was significantly higher in the intervention group. In the study of Turkaman et al., most neonates receiving probiotics and phototherapy (84.7%) were discharged within two days after the intervention while 69.5% in the control group were still receiving treatment on the third day [11]. In other studies, the frequency of discharge has not been evaluated.

Although our study showed an earlier discharge among patients in synbiotic group, we found no significant difference between two groups regarding the frequency of defecation which was consistent with the results of Suganti et al. using Saccharomyces boulardii as the probiotic [12]. However, a study by Bisceglia et al. showed that infants receiving probiotics had more frequent defecation than those receiving placebo [20]. Also, in the study of Armenian et al., the frequency of defecation in the prebiotic group was significantly increased compared to the placebo group (p = 0.003). Armenian et al. used two types of prebiotics on premature neonates to prevent jaundice [6]. Preterm neonates lack intestinal motor complex [13] therefore it seems that administering pre or probiotics in preterm neonates may be more effective on defecation compared to term neonates [13]. Regarding the gestational age in this study, the decrease in bilirubin were not significant in preterm neonates and was significant in term infants. Other studies did not compare the rate of bilirubin reduction, considering gestational age.

In the current study, the length of hospital stay in the intervention group was significantly shorter, which can greatly reduce hospital costs as well as the separation of mothers and neonate. In several studies, including the studies of Turkaman, Liu, Chandrasekhar, and Demirel, a reduction in the course and duration of phototherapy were observed in the group receiving probiotics and phototherapy compared to phototherapy [8 , 21] and in some studies, including the studies of Zahed Pasha and Secre, no reduction was found [13, 14].

Comparing the reduction of bilirubin according to the type of delivery, in cesarean delivered neonates, the reduction of bilirubin in the intervention group was significantly higher compared to the placebo group. It seems that the lack of contact of the baby with maternal vaginal secretions during cesarean labor, can affect the neonatal intestinal bacterial colonization and justify this result. In several studies, the type of delivery was evaluated as a variable in icteric neonates. However, the relationship between bilirubin reduction in neonates born of different types of deliveries was not investigated [11, 14].

In the current study like other studies [8 , 11] no complication was seen in any neonates of two groups [8 , 11]. The present study had some limitations. The first limitation was the small sample size. The other limitation was that investigators did not study the colonization of neonatal fecal bacteria before and after synbiotic prescriptions. Based on the current findings, it is suggested to perform larger studies with different types of probiotics and prebiotics, in order to use these compounds safely and effectively as an adjuvant treatment of neonatal jaundice.

5 Conclusion

Ethical approval

This study was approved by the Vice Chancellor of Research at Guilan University of Medical Sciences (Number: IR.GUMS.REC.1397.196, date: 2018.08.18). The IRCT code was IRCT2018.228.38895N1 (date: 2018.09.26).

Consent for publication

Written consent was obtained from the parents of the neonates.

Availability of data and supporting materials section

Please contact the corresponding author for data requests.

Conflict of interest

None of the authors have any conflict of interest to disclose.

Funding

This study was financially supported by the Vice chancellor of Research of Guilan University of Medical Sciences.

Footnotes

Acknowledgments

The authors would like to deeply appreciate the cooperation of all colleagues and participants. This study was the thesis of the third author (Dr Yalda Navidi Moghaddam).

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			Studied group			P-value
			Synbiotics and phototherapy recipients	Phototherapy treatment	Total
Sex	Boy	Number	51	57	108	0.386
		Percent	52.6%	58.8%	55.7%
	Girl	Number	46	40	86
		Percent	47.4%	41.2%	44.3%
Gestational age (Week)	Mean		37.93	37.83	37.88	0.538
	Standard deviation		1.15	1.14	1.14
	Minimum		35.00	35.00	35.00
	Maximum		40.00	41.00	41.00
Term or preterm status	Under 37 Weeks	Number	21	25	46	0.749
		Percent	21.6%	25.8%	23.7%
	Over 37 Weeks	Number	76	72	148
		Percent	78.3%	74.2%	76.3%
Infant age	Mean		5.80	6.30	6.05	0.116
	Standard deviation		2.13	2.33	2.24
	Minimum		3.00	3.00	2.50
	Maximum		14.00	14.00	14.00
Infant weight	Mean		3050.67	3036.44	3043.56	0.778
	Standard deviation		387.02	310.09	349.83
	Minimum		2500.00	2500.00	2500.00
	Maximum		3900.00	3850.00	3900.00
Type Of delivery	Normal	Number	33	31	64	0.760
		Percent	34.0%	32.0%	33.0%
	Cesarean section	Number	64	66	130
		Percent	66.0%	68.0%	67.0%
	Total	Number	97	97	194
		Percent	100.0%	100.0%	100.0%