Responses to faecal microbiota transplantation in female and male patients with irritable bowel syndrome

doi:10.3748/wjg.v27.i18.2219

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World Journal of Gastroenterology

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1007-9327

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Baishideng Publishing Group Inc, 7041 Koll Center Parkway, Suite 160, Pleasanton, CA 94566, USA

Clinical Trials Study

World J Gastroenterol. May 14, 2021; 27(18): 2219-2237
Published online May 14, 2021. doi: 10.3748/wjg.v27.i18.2219

Table 1 Characteristics of the patients in the placebo and active treated groups

	Placebo			P value	Active treated			P value
	Total	Females	Males		Total	Females	Males
n	55	47	8		109	85	24
Age, yr (median, range)	38.5 (18-75)	38.0 (18-73)	47.0 (20-75)	0.3	39.0 (18-73)	40.0 (18-73)	32.0 (21-65)	0.07
IBS-D	21	19	2	0.7	42	30	12	0.4
IBS-C	22	18	4		40	32	8
IBS-M	12	10	2		27	23	4
IBS duration, yr	15.5 ± 7.9	16.2 ± 8.0	15.0 ± 9.0	0.9	17.3 ± 8.9	16.8 ± 8.2	18.0 ± 9.2	0.9
Age at IBS onset, yr (median, range)	20.0 (15-35)	20.5 (16-35)	19.0 (15-30)	0.4	20.0 (15-36)	20.0 (16-35)	20 (15-33)	0.6
IBS-SSS total score	315.2 ± 77.1	320.1 ± 77.8	286.9 ± 69.3	0.5	312.9 ± 82.0	319.1 ± 77.3	297.7 ± 82.0	0.4
Moderate symptoms¹ (%)	23 (42)	17 (36)	6 (75)	0.06	45 (41)	30 (35)	13 (54)	0.1
Severe symptoms² (%)	32 (58)	30 (64)	2 (25)	0.06	64 (59)	55 (65)	11 (46)	0.1

Data are n, n (%) or mean ± SD values.

¹Irritable bowel syndrome severity scoring system total score between 175 and 300.

²Irritable bowel syndrome severity scoring system total score of ≥ 300. IBS: Irritable bowel syndrome; IBS-D: Irritable bowel syndrome with diarrhoea-predominant; IBS-C: Irritable bowel syndrome with constipation-predominant; IBS-M: Irritable bowel syndrome with mixed diarrhoea and constipation; IBS-SSS: Irritable bowel syndrome severity scoring system.

Table 2 The response rates of females and males in different irritable bowel syndrome-subtypes at different intervals after faecal microbiota transplantation

Time after FMT	IBS-D			IBS-C			IBS-M
Time after FMT	Females	Males	P value	Females	Males	P value	Females	Males	P value
2 wk (%)	73	58	0.3	65	50	0.7	72	55	0.3
1 mo (%)	90	42	0.0003	69	75	0.7	65	60	0.9
3 mo (%)	90	42	0.0003	70	75	0.3	63	80	0.6

IBS-D: Irritable bowel syndrome with diarrhoea-predominant symptom; IBS-C: Irritable bowel syndrome with constipation-predominant symptom; IBS-M: Irritable bowel syndrome with mixed diarrhoea and constipation; FMT: Faecal microbiota transplantation.

Table 3 The response rates in females and males with either moderate or severe irritable bowel syndrome symptoms

Time after FMT	Moderate symptoms¹			Severe symptoms²
Time after FMT	Females	Males	P value	Females	Males	P value
2 wk (%)	58	61	0.999	78	91	0.4
1 mo (%)	61	61	0.999	78	91	0.4
3 mo (%)	63	56	0.778	77	82	0.999

¹Irritable bowel syndrome severity scoring system total score between 175 and 300.

²Irritable bowel syndrome severity scoring system total score of ≥ 300. FMT: Faecal microbiota transplantation.

Table 4 Irritable bowel syndrome severity scoring system total scores of females and males in the two study groups at different times after faecal microbiota transplantation

Time	Placebo		P value	Active treated		P value
Time	Females	Males	P value	Females	Males	P value
0	320 ± 78	287 ± 69	0.2	319 ± 77	297 ± 82	0.3
2 wk	254 ± 106	256 ± 90	0.9	199 ± 102	205 ± 95	0.6
1 mo	277 ± 98	272 ± 89	0.8	196 ± 108	193 ± 94	0.9
3 mo	288 ± 90	266 ± 100	0.6	173 ± 116	183 ± 105	0.5

Data are mean ± SD values.

Table 5 The irritable bowel syndrome severity scoring system total scores in females and males belonging to different irritable bowel syndrome-sub-types

Time after FMT	IBS-D			IBS-C			IBS-M
Time after FMT	Females	Males	P value	Females	Males	P value	Females	Males	P value
2 wk	190.5 ± 191.4	204.0 ± 92.2	0.6	228.1 ± 116.2	239.2 ± 113.8	0.5	202.8 ± 121.3	225.0 ± 65.8	0.5
1 mo	177.8 ± 94.9	226.9 ± 73.3	0.02	228.8 ± 118.1	215.8 ± 115.7	0.6	219.9 ± 136.6	197.0 ± 65.2	0.8
3 mo	157.8 ± 102.9	212.3 ± 96.9	0.03	212.8 ± 124.0	234.6 ± 131.8	0.5	219.2 ± 146.3	149.0 ± 36.0	0.5

Data are mean ± SD values. IBS-D: Irritable bowel syndrome with diarrhoea-predominant symptom; IBS-C: Irritable bowel syndrome with constipation-predominant symptom; IBS-M: Irritable bowel syndrome with mixed diarrhoea and constipation; FMT: Faecal microbiota transplantation.

Table 6 Irritable bowel syndrome severity scoring system total scores in females and males with moderate or severe irritable bowel syndrome symptoms

Time after FMT	Moderate symptoms¹			Severe symptoms²
Time after FMT	Females	Males	P value	Females	Males	P value
2 wk	166.5 ± 70.0	167.2 ± 55.8	0.8	225.1 ± 114.0	259.5 ± 102.3	0.3
1 mo	162.1 ± 73.1	179.4 ± 63.8	0.5	229.2 ± 120.2	214.1 ± 118.1	0.7
3 mo	155.3 ± 76.9	175.3 ± 100.2	0.5	214.6 ± 131.8	202.3 ± 120.6	0.8

Data are mean ± SD values.

¹Irritable bowel syndrome severity scoring system total score between 175 and 300.

²Irritable bowel syndrome severity scoring system total score of ≥ 300. FMT: Faecal microbiota transplantation.

Table 7 Fatigue Assessment Scale total scores of females and males in the two study groups at different times after faecal microbiota transplantation

Time	Placebo			Active treated
Time	Females	Males	P value	Females	Males	P value
0	31 ± 5	29 ± 4	0.3	32 ± 5	30 ± 5	0.09
2 wk	31 ± 6	29 ± 6	0.2	28 ± 6	28 ± 5	0.5
1 mo	31 ± 6	27 ± 7	0.1	27 ± 7	29 ± 5	0.5
3 mo	30 ± 4	26 ± 4	0.01	29 ± 6	27 ± 5	0.7

Data mean ± SD values.

Table 8 Fatigue Assessment Scale total scores of females and males irritable bowel syndrome patients belonging to different irritable bowel syndrome-subtypes

Time after FMT	IBS-D			IBS-C			IBS-M
Time after FMT	Females	Males	P value	Females	Males	P value	Females	Males	P value
2 wk	30.1 ± 3.6	27.0 ± 3.6	0.04	28.0 ± 6.3	29.3 ± 7.4	0.5	26.7 ± 5.4	26.3 ± 2.1	0.9
1 mo	27.1 ± 5.2	26.6 ± 4.6	0.6	27.1 ± 6.7	31.3 ± 6.1	0.1	28.3 ± 8.3	28.3 ± 4.0	0.9
3 mo	27.5 ± 5.7	27.8 ± 5.0	0.4	26.0 ± 6.2	29.2 ± 5.0	0.2	26.8 ± 7.6	24.8 ± 2.2	0.7

Table 9 Irritable bowel syndrome quality of life scale total scores of females and males in the two study groups at different times after faecal microbiota transplantation

Time	Placebo			Active treated
Time	Females	Males	P value	Females	Males	P value
0	116 ± 20	130 ± 11	0.03	111 ± 23	114 ± 21	0.9
2 wk	123 ± 29	120 ± 23	0.7	122 ± 24	118 ± 27	0.6
1 mo	123 ± 26	121 ± 26	0.8	126 ± 24	119 ± 29	0.4
3 mo	112 ± 24	118 ± 26	0.2	132 ± 23	131 ± 25	0.9

Data are mean ± SD values.

Table 10 Irritable bowel syndrome quality of life scale total scores of females and males irritable bowel syndrome patients belonging to different irritable bowel syndrome-subtypes

Time after FMT	IBS-D			IBS-C			IBS-M
Time after FMT	Females	Males	P value	Females	Males	P value	Females	Males	P value
2 wk	123.3 ± 98	123.7 ± 25.5	0.8	120.5 ± 23.1	102.4 ± 28.0	0.06	123.1 ± 24.6	131.5 ± 13.0	0.4
1 mo	131.3 ± 20.8	129.6 ± 28.2	0.9	121.9 ± 24.4	111.4 ± 29.1	01	125.4 ± 25.2	130.5 ± 11.3	0.8
3 mo	136.4 ± 16.6	134.5 ± 22.7	0.9	128.7 ± 24.4	129.1 ± 31.3	0.6	129.5 ± 28.6	124.8 ± 22.0	0.5

Table 11 Faecal bacteria levels in the female and male irritable bowel syndrome patients in the placebo group at the baseline and 1 mo after faecal microbiota transplantation

Bacteria	Baseline		1 mo after FMT
Bacteria	Females	Males	Females	Males
Actinobacteria	-0.235 ± 0.763	-0.365 ± 0.768	-0.250 ± 0.954	-0.375 ± 0.838
Actinomycetales	0.118 ± 0.382	-0.212 ± 0.536	0.175 ± 0.594	0.100 ± 0.496
Bifidobacterium spp.	-0.020 ± 0.607	-0.154 ± 0.539	0.025 ± 0.660	-0.075 ± 0.572
Alistipes	-0.863 ± 0.895	-0.885 ± 0.900	-0.875 ± 0.853	-0.800 ± 0.709
Alistipes onderdonkii	-0.667 ± 0.792	-0.615 ± 0.718	-0.650 ± 0.834	-0.550 ± 0.783
Bacteroides fragilis	-0.255 ± 0.689	-0.212 ± 0.637	0.175 ± 0.501	0.050 ± 0.221
Bacteroides spp. and Prevotella spp.	-0.980 ± 1.157	-0.885 ± 1.182	-0.750 ± 1.032	-0.900 ± 0.687
Bacteroides stercoris	-0.137 ± 0.448	-0.154 ± 0.415	0.025 ± 0.158	0.100 ± 0.304
Bacteroides zoogleoformans	0.078 ± 0.272	0.038 ± 0.194	0.025 ± 0.158	0 ± 0
Parabacteroides johnsonii	0.039 ± 0.196	0.077 ± 0.269	0.050 ± 0.221	0.100 ± 0.304
Parabacteroides spp.	-0.451 ± 0.642	-0.327 ± 0.706	-0.425 ± 0.747	-0.225 ± 0.480
Firmicutes	-0.431 ± 0.575	-0.385 ± 0.566	-0.325 ± 0.526	-0.400 ± 0.591
Bacilli	0.235 ± 1.124	0.192 ± 0.991	0.271 ± 1.132	0.150 ± 1.001
Catenibacterium mitsuokai	0.000 ± 0.400	0.135 ± 0.525	0.050 ± 0.289	0.100 ± 0.441
Clostridia	-0.020 ± 0.244	-0.077 ± 0.269	-0.025 ± 0.276	0.0 ± 0.036
Clostridium spp.	0.039 ± 0.196	0.038 ± 0.194	0.0 ± 0.0	0.050 ± 0.316
Dialister invisus	0.118 ± 0.381	-0.173 ± 0.474	0.200 ± 0.405	0.225 ± 0.158
Dialister invisus and Megasphaera micronuciformis	0.059 ± 0.238	0.173 ± 0.474	0.125 ± 0.335	0.025 ± 0.158
Dorea spp.	0.569 ± 0.700	0.500 ± 0.700	0.625 ± 0.628	0.667 ± 0.806
Eubacterium biforme	0.412 ± 0.753	0.269 ± 0.598	0.275 ± 0.640	0.400 ± 0.633
Eubacterium hallii	0.804 ± 0.939	0.673 ± 0.879	0.655 ± 0.730	0.650 ± 0.597
Eubacterium rectale	0.078 ± 0.337	0.058 ± 0.235	0.050 ± 0.221	0.025 ± 0.158
Eubacterium siraeum	-1.412 ± 0.963	-1.288 ± 0.161	-1.475 ± 1.086	-1.200 ± 1.265
Faecalibacterium prausnitzii	-0.431 ± 0.671	-0.500 ± 0.804	-0.550 ± 0.745	-0.500 ± 0.599
Lachnospiraceae	0.196 ± 0.566	0.269 ± 0.630	0.325 ± 0.730	0.275 ± 0.640
Lactobacillus ruminis and Pediococcus acidilactici	0.059 ± 0.311	0.077 ± 0.334	0.0 ± 0.0	0.025 ± 0.158
Lactobacillus spp.	0.353 ± 0.594	0.269 ± 0.528	0.325 ± 0.616	0.475 ± 0.680
Phascolarctobacterium spp.	0.078 ± 0337	0.077 ± 0.337	0.125 ± 0.404	0.075 ± 0.350
Ruminococcus albus and Ruminococcus bromii	0.353 ± 0.658	0.404 ± 0.721	0.325 ± 0.616	0.450 ± 0.749
Ruminococcus gnavus	0.431 ± 0.878	0.577 ± 0.878	0.450 ± 0.815	0.325 ± 0.764
Streptococcus agalactiae & Eubacterium rectale	0.157 ± 0.367	0.250 ± 0.480	0.110 ± 0.304	0.125 ± 0.345
Streptococcus salivarius ssp. Thermophilus and Streptococcus sanguinis	0.412 ± 0.606	0.346 ± 0.556	0.675 ± 0.888	0.475 ± 0.751
Streptococcus salivarius ssp. thermophilus	0.628 ± 0.871	0.577 ± 0.915	0.500 ± 0.934	0.600 ± 0.928
Streptococcus spp.	0.471 ± 0.833	0.423 ± 0.696	0.400 ± 0.709	0.450 ± 0.815
Veillonella spp.	-0.177 ± 0.518	-0.173 ± 0.648	-0.175 ± 0.385	-0.150 ± 0.534
Proteobacteria	0.294 ± 0.576	0.289 ± 0.499	0.275 ± 0.599	0.325 ± 0.616
Shigella spp. and Escherichia spp.	-0.275 ± 0.940	-0.212 ± 0.893	-0.200 ± 0.853	-0.335 ± 0.920
Mycoplasma hominis	-0.451 ± 0.503	-0.404 ± 0.496	-0.450 ± 0.504	-0.450 ± 0.503
Akkermansia muciniphila	0.471 ± 0.644	0.365 ± 0.627	0.450 ± 0.714	0.650 ± 0.802

The bacterial levels are mean ± SD relative values to a normobiotic microbiota profile of 165 healthy subjects. FMT: Faecal microbiota transplantation.

Table 12 Gut bacteria levels in female and male irritable bowel syndrome patients in the active treated group at the baseline and 1 mo after faecal microbiota transplantation

Bacteria	Baseline		1 mo after FMT
Bacteria	Females	Males	Females	Males
Actinobacteria	-0.250 ± 0.954	-0.375 ± 0.838	-0.250 ± 0.719	-0.2350 ± 0.636
Actinomycetales	0.175 ± 0.594	0.100 ± 0.496	0.068 ± 0255	0.145 ± 0.412
Bifidobacterium spp.	0.025 ± 0.660	-0.075 ± 0.572	-0.045 ± 0.526	-0.063 ± 0.433
Alistipes	-0.875 ± 0.853	-0.800 ± 0.709	-0.886 ± 0.869	-0.783 ± 0.821
Alistipes onderdonkii	-0.650 ± 0.834	-0.550 ± 0.783	-0.523 ± 0.699	-0.354 ± 0.565
Bacteroides fragilis	0.175 ± 0.501	0.050 ± 0.221	0.159 ± 0.480	0.104 ± 0.371
Bacteroides spp. and Prevotella spp.	-0.750 ± 1.032	-0.800 ± 0.687	-1.091 ± 1.996	-0.708 ± 0.967
Bacteroides stercoris	0.025 ± 0.158	0.100 ± 0.304	0.023 ± 0.151	0.146 ± 0.357
Bacteroides zoogleoformans	0.025 ± 0.158	0 ± 0	0.091 ± 0.291	0.083 ± 0.347
Parabacteroides johnsonii	0.050 ± 0.221	0.100 ± 0.304	0.045 ± 0.302	0.021 ± 0.144
Parabacteroides spp.	-0.425 ± 0.747	-0.225 ± 0.480	-0.455 ± 0.504	-0.313 ± 0.468
Firmicutes	-0.325 ± 0.526	-0.400 ± 0.591	-0.546 ± 0.627	-0.454 ± 0.483
Bacilli	0.271 ± 1.132	0.150 ± 1.001	0.205 ± 1.047	0.042 ± 0.824
Catenibacterium mitsuokai	0.050 ± 0.289	0.100 ± 0.441	0.023 ± 0.151	0.104 ± 0.515
Clostridia	-0.025 ± 0.276	0.0 ± 0.036	0.068 ± 0.255	0.021 ± 252
Clostridium spp.	0.0 ± 0.0	0.050 ± 0.316	0.223 ± 0.151	0.063 ± 0.245
Dialister invisus	0.200 ± 0.405	0.225 ± 0.158	0.091 ± 0.362	0.146 ± 0.505
Dialister invisus and Megasphaera micronuciformis	0.125 ± 0.335	0.025 ± 0.158	0.068 ± 0.034	0.104 ± 0.308
Dorea spp.	0.625 ± 0.628	0.667 ± 0.806	0.727 ± 0.758	0.663 ± 0.796
Eubacterium biforme	0.275 ± 0.640	0.400 ± 0.633	0.477 ± 0.791	0.563 ± 0.769
Eubacterium hallii	0.655 ± 0.730	0.550 ± 0.597	0.886 ± 0.993	0.979 ± 1.021
Eubacterium rectale	0.050 ± 0.221	0.025 ± 0.158	0-068 ± 0.255	0.042 ± 0.202
Eubacterium siraeum	-1.475 ± 1.086	-1.200 ± 1.265	-1.295 ± 0.930	-1.208 ± 0.988
Faecalibacterium prausnitzii	-0.550 ± 0.745	-0.500 ± 0.599	-0.568 ± 0.759	-0.521 ± 0.825
Lachnospiraceae	0.325 ± 0.730	0.275 ± 0.640	0.205 ± 0.553	0.125 ± 0.489
Lactobacillus ruminis and Pediococcus acidilactici	0.0 ± 0.0	0.025 ± 0.158	0.021 ± 0.146	0.188 ± 0.571
Lactobacillus spp.	0.325 ± 0.616	0.475 ± 0.680	0.500 ± 0.731	0.583 ± 0.679
Phascolarctobacterium spp.	0.125 ± 0.404	0.075 ± 0.350	0.091 ± 0.362	0.083 ± 0.347
Ruminococcus albus and Ruminococcus bromii	0.325 ± 0.616	0.450 ± 0.749	0.205 ± 0.553	0.271 ± 0.574
Ruminococcus gnavus	0.450 ± 0.815	0.325 ± 0.764	0.364 ± 0.810	0.250 ± 0.636
Streptococcus agalactiae & Eubacterium rectale	0.110 ± 0.304	0.125 ± 0.345	0.267 ± 0.495	0.083 ± 0.279
Streptococcus salivarius ssp. thermophilus and Streptococcus sanguinis	0.675 ± 0.888	0.475 ± 0.751	0.455 ± 0.504	0.292 ± 0.459
Streptococcus salivarius ssp. thermophilus	0.500 ± 0.934	0.600 ± 0.928	0.523 ± 0.821	0.604 ± 0.844
Streptococcus spp.	0.400 ± 709	0.450 ± 0.815	0.444 ± 0.841	0.396 ± 0.610
Veillonella spp.	-0.175 ± 0.385	-0.150 ± 0.534	-0.273 ± 0.544	-0.208 ± 0.504
Proteobacteria	0.275 ± 0.599	0.325 ± 0.616	0.717 ± 0.750	0.583 ± 0.498
Shigella spp. and Escherichia spp.	-0.200 ± 0.853	-0.335 ± 0.920	-0.151 ± 1.077	-0.188 ± 0.790
Mycoplasma hominis	-0.450 ± 0.504	-0.450 ± 0.503	-0.500 ± 0.506	-0.479 ± 0.505
Akkermansia muciniphila	0.450 ± 0.714	0.650 ± 0.802	0.741 ± 0.713	0.813 ± 0.915

The bacterial levels are relative values to a normobiotic microbiota profile of 165 healthy subjects (mean ± SD). FMT: Faecal microbiota transplantation.

Table 13 The short-chain fatty acids concentration in the faeces of the placebo group and the patients that received donor’s faecs (faecal microbiota transplantation) at the baseline and 1 mo after faecal microbiota transplantation

Acids	Placebo				Active treated
	Baseline		1 mo after FMT		Baseline		1 mo after FMT
	Females	Males	Females	Males	Females	Males	Females	Males
Total SCFAs	72 ± 37	69 ± 23.	73 ± 37	69 ± 23	77 ± 40	72 ± 40	87 ± 42	89 ± 26
Acetic acid	42 ± 18	40 ± 15	41 ± 17	40 ± 14	44 ± 21	44 ± 20	46 ± 13	40.2 ± 15.0
Propionic acid	12 ± 8	11 ± 5	12 ± 8	11 ± 5	13 ± 10	13 ± 8	14 ± 4	11 ± 7
Iso-butyric acid	2 ± 2	1 ± 1	1 ± 2	1 ± 1	1 ± 1	1 ± 1	2 ± 2	1 ± 1
Butyric acid	14 ± 9	12 ± 6	13 ± 8	12 ± 6	11 ± 8	12 ± 9	18 ± 14	16 ± 10
Iso-valeric acid	2 ± 2	2 ± 1	2 ± 2	2 ± 1	2 ± 1	2 ± 2	2 ± 2	2 ± 1
Valeric acid	2 ± 2	1 ± 1	2 ± 2	1 ± 1	2 ± 2	2 ± 2	2 ± 1	2 ± 1
Iso-capronic acid	0.1 ± 0.04	0.01 ± 0.07	0.5 ± 0.7	0.4 ± 0.7	0.0 ± 0.0	0.02 ± 0.08	0.01 ± 0.04	0.0 ± 0.0
Capronic acid	0.5 ± 0.7	0.5 ± 0.7	0.01 ± 0.04	0.1 ± 0.08	0.7 ± 1.3	0.6 ± 0.8	0.6 ± 0.9	0.5 ± 0.9

The values were expressed as mmol/kg wet weight (mean ± SD). FMT: Faecal microbiota transplantation; SCFAs: Short-chain fatty acids.

Citation: El-Salhy M, Casen C, Valeur J, Hausken T, Hatlebakk JG. Responses to faecal microbiota transplantation in female and male patients with irritable bowel syndrome. World J Gastroenterol 2021; 27(18): 2219-2237
URL: https://www.wjgnet.com/1007-9327/full/v27/i18/2219.htm
DOI: https://dx.doi.org/10.3748/wjg.v27.i18.2219