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The Impacts of Fecal Microbiota Transplantation from Same Sex on the Symptoms of Ulcerative Colitis Patients

Shu Shang
Shu Shang
, 
Jian Zhu
Jian Zhu
, 
Xi Liu
Xi Liu
, 
Wei Wang
Wei Wang
, 
Tingting Dai
Tingting Dai
, 
Li Wang
Li Wang
 oraz 
Baojun Li
Baojun Li
   | 20 wrz 2023
Polish Journal of Microbiology's Cover Image
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Article Category: Original Paper
Data publikacji: 20 wrz 2023
Zakres stron: 247 - 268
Otrzymano: 13 mar 2023
Przyjęty: 08 cze 2023
DOI: https://doi.org/10.33073/pjm-2023-025
Słowa kluczowe
© 2023 Shu Shang et al., published by Sciendo
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Fig. 1.

Overview of the retrospective cohort study design.This flow chart presents the study's framework, focusing on a retrospective cohort of hospitalized ulcerative colitis patients, categorized upon admission and subsequent fecal microbiota transplantation (FMT) treatment. The study also includes placebo groups partitioned by gender. Four categories were devised: male and female patients receiving FMT and male and female patients receiving a placebo.
Overview of the retrospective cohort study design.This flow chart presents the study's framework, focusing on a retrospective cohort of hospitalized ulcerative colitis patients, categorized upon admission and subsequent fecal microbiota transplantation (FMT) treatment. The study also includes placebo groups partitioned by gender. Four categories were devised: male and female patients receiving FMT and male and female patients receiving a placebo.

Fig. 2 A, B.

Comparative analysis of microbiota characteristics among patient cohorts.A – via a Venn diagram, represents the unique and shared operational taxonomic units (OTUs) for male patients in both experimental and placebo groups. B – similarly represents female patients. Overlapping circles demonstrate shared OTUs.AFP represents female ulcerative colitis patients post-placebo treatment; AM signifies male ulcerative colitis patients post-fecal microbiota transplantation (FMT); AMP indicates male patients post-placebo treatment. AS refers to a subgroup of 20 male ulcerative colitis patients post-FMT, while AU represents a similar subgroup of 20 female patients post-FMT. BF shows data from female ulcerative colitis patients’ pre-FMT, and BFP is for those same female patients pre-placebo treatment. BM and BMP correspond to male ulcerative colitis patients’ pre-FMT and pre-placebo treatment. BS and BU denote subgroups of 20 male and female patients pre-FMT. Finally, FD and MD represent female and male fecal donors, respectively.
Comparative analysis of microbiota characteristics among patient cohorts.A – via a Venn diagram, represents the unique and shared operational taxonomic units (OTUs) for male patients in both experimental and placebo groups. B – similarly represents female patients. Overlapping circles demonstrate shared OTUs.AFP represents female ulcerative colitis patients post-placebo treatment; AM signifies male ulcerative colitis patients post-fecal microbiota transplantation (FMT); AMP indicates male patients post-placebo treatment. AS refers to a subgroup of 20 male ulcerative colitis patients post-FMT, while AU represents a similar subgroup of 20 female patients post-FMT. BF shows data from female ulcerative colitis patients’ pre-FMT, and BFP is for those same female patients pre-placebo treatment. BM and BMP correspond to male ulcerative colitis patients’ pre-FMT and pre-placebo treatment. BS and BU denote subgroups of 20 male and female patients pre-FMT. Finally, FD and MD represent female and male fecal donors, respectively.

Fig. 2 C, D, E, F, G.

Comparative analysis of microbiota characteristics among patient cohorts.C and D – exhibit the rank abundance curves based on relative species abundance and biodiversity components for male and female patients, respectively. E, F, and G – demonstrate the top 10 bacterial families for male and female donors and male and female patients in both experimental and placebo groups, respectively.AFP represents female ulcerative colitis patients post-placebo treatment; AM signifies male ulcerative colitis patients post-fecal microbiota transplantation (FMT); AMP indicates male patients post-placebo treatment. AS refers to a subgroup of 20 male ulcerative colitis patients post-FMT, while AU represents a similar subgroup of 20 female patients post-FMT. BF shows data from female ulcerative colitis patients’ pre-FMT, and BFP is for those same female patients pre-placebo treatment. BM and BMP correspond to male ulcerative colitis patients’ pre-FMT and pre-placebo treatment. BS and BU denote subgroups of 20 male and female patients pre-FMT. Finally, FD and MD represent female and male fecal donors, respectively.
Comparative analysis of microbiota characteristics among patient cohorts.C and D – exhibit the rank abundance curves based on relative species abundance and biodiversity components for male and female patients, respectively. E, F, and G – demonstrate the top 10 bacterial families for male and female donors and male and female patients in both experimental and placebo groups, respectively.AFP represents female ulcerative colitis patients post-placebo treatment; AM signifies male ulcerative colitis patients post-fecal microbiota transplantation (FMT); AMP indicates male patients post-placebo treatment. AS refers to a subgroup of 20 male ulcerative colitis patients post-FMT, while AU represents a similar subgroup of 20 female patients post-FMT. BF shows data from female ulcerative colitis patients’ pre-FMT, and BFP is for those same female patients pre-placebo treatment. BM and BMP correspond to male ulcerative colitis patients’ pre-FMT and pre-placebo treatment. BS and BU denote subgroups of 20 male and female patients pre-FMT. Finally, FD and MD represent female and male fecal donors, respectively.

Fig. 3A, B.

Alpha and beta diversity analysis of gut microbiota among patient cohorts.This figure depicts various indices measuring microbial diversity within and between cohorts. A–D represent diversity indices (Shannon, Simpson, ACE, Chao1) for male patients across experimental and placebo groups. E–H mirror these indices for female patients. I–L illustrate Principal Component Analysis (PCA) and Principal Coordinate Analysis (PCoA) for male and female patients, respectively, comparing overall gut microbiota structure with FMT or placebo treatments. Ellipses represent an 80% confidence level, with color/shape indicating the specific cohort. AM and AF denote male and female ulcerative colitis patients, post-FMT; BF and BM are used to indicate female and male ulcerative colitis patients, respectively, pre-FMT. AFP and AMP represent female and male patients, respectively, post-placebo treatment, while BFP and BMP signify female and male patients, respectively, pre-placebo treatment.
Alpha and beta diversity analysis of gut microbiota among patient cohorts.This figure depicts various indices measuring microbial diversity within and between cohorts. A–D represent diversity indices (Shannon, Simpson, ACE, Chao1) for male patients across experimental and placebo groups. E–H mirror these indices for female patients. I–L illustrate Principal Component Analysis (PCA) and Principal Coordinate Analysis (PCoA) for male and female patients, respectively, comparing overall gut microbiota structure with FMT or placebo treatments. Ellipses represent an 80% confidence level, with color/shape indicating the specific cohort. AM and AF denote male and female ulcerative colitis patients, post-FMT; BF and BM are used to indicate female and male ulcerative colitis patients, respectively, pre-FMT. AFP and AMP represent female and male patients, respectively, post-placebo treatment, while BFP and BMP signify female and male patients, respectively, pre-placebo treatment.

Fig. 3C, D, E, F, G, H.

Alpha and beta diversity analysis of gut microbiota among patient cohorts.
Alpha and beta diversity analysis of gut microbiota among patient cohorts.

Fig. 3I, J, K, L.

Alpha and beta diversity analysis of gut microbiota among patient cohorts.This figure depicts various indices measuring microbial diversity within and between cohorts. A–D represent diversity indices (Shannon, Simpson, ACE, Chao1) for male patients across experimental and placebo groups. E–H mirror these indices for female patients. I–L illustrate Principal Component Analysis (PCA) and Principal Coordinate Analysis (PCoA) for male and female patients, respectively, comparing overall gut microbiota structure with FMT or placebo treatments. Ellipses represent an 80% confidence level, with color/shape indicating the specific cohort.AM and AF denote male and female ulcerative colitis patients, post-FMT; BF and BM are used to indicate female and male ulcerative colitis patients, respectively, pre-FMT. AFP and AMP represent female and male patients, respectively, post-placebo treatment, while BFP and BMP signify female and male patients, respectively, pre-placebo treatment.
Alpha and beta diversity analysis of gut microbiota among patient cohorts.This figure depicts various indices measuring microbial diversity within and between cohorts. A–D represent diversity indices (Shannon, Simpson, ACE, Chao1) for male patients across experimental and placebo groups. E–H mirror these indices for female patients. I–L illustrate Principal Component Analysis (PCA) and Principal Coordinate Analysis (PCoA) for male and female patients, respectively, comparing overall gut microbiota structure with FMT or placebo treatments. Ellipses represent an 80% confidence level, with color/shape indicating the specific cohort.AM and AF denote male and female ulcerative colitis patients, post-FMT; BF and BM are used to indicate female and male ulcerative colitis patients, respectively, pre-FMT. AFP and AMP represent female and male patients, respectively, post-placebo treatment, while BFP and BMP signify female and male patients, respectively, pre-placebo treatment.

Fig. 4A.

Heatmaps illustrating microbiome analysis results.This figure showcases heatmaps of the top-ranking gut microbiota OTUs among patients before and after FMT or placebo treatments.A – the top 35 OTUs in male patients before and after FMT.AM and AF denote male and female ulcerative colitis patients, respectively, post-FMT; AS refers to a subgroup of 20 male ulcerative colitis patients post-FMT, while AU represents a similar subgroup of 20 female patients post-FMT. BU and BS are used to indicate female and male ulcerative colitis patients, respectively, pre-FMT. AFP and AMP represent female and male patients, respectively, post-placebo treatment, while BFP and BMP signify female and male patients, respectively, pre-placebo treatment.
Heatmaps illustrating microbiome analysis results.This figure showcases heatmaps of the top-ranking gut microbiota OTUs among patients before and after FMT or placebo treatments.A – the top 35 OTUs in male patients before and after FMT.AM and AF denote male and female ulcerative colitis patients, respectively, post-FMT; AS refers to a subgroup of 20 male ulcerative colitis patients post-FMT, while AU represents a similar subgroup of 20 female patients post-FMT. BU and BS are used to indicate female and male ulcerative colitis patients, respectively, pre-FMT. AFP and AMP represent female and male patients, respectively, post-placebo treatment, while BFP and BMP signify female and male patients, respectively, pre-placebo treatment.

Fig. 4B, C.

Heatmaps illustrating microbiome analysis results.This figure showcases heatmaps of the top-ranking gut microbiota OTUs among patients before and after FMT or placebo treatments.B – the male group pre- and post-placebo.C – the female patients with the top 45 OTUs before and after FMT.AM and AF denote male and female ulcerative colitis patients, respectively, post-FMT; AS refers to a subgroup of 20 male ulcerative colitis patients post-FMT, while AU represents a similar subgroup of 20 female patients post-FMT. BU and BS are used to indicate female and male ulcerative colitis patients, respectively, pre-FMT. AFP and AMP represent female and male patients, respectively, post-placebo treatment, while BFP and BMP signify female and male patients, respectively, pre-placebo treatment.
Heatmaps illustrating microbiome analysis results.This figure showcases heatmaps of the top-ranking gut microbiota OTUs among patients before and after FMT or placebo treatments.B – the male group pre- and post-placebo.C – the female patients with the top 45 OTUs before and after FMT.AM and AF denote male and female ulcerative colitis patients, respectively, post-FMT; AS refers to a subgroup of 20 male ulcerative colitis patients post-FMT, while AU represents a similar subgroup of 20 female patients post-FMT. BU and BS are used to indicate female and male ulcerative colitis patients, respectively, pre-FMT. AFP and AMP represent female and male patients, respectively, post-placebo treatment, while BFP and BMP signify female and male patients, respectively, pre-placebo treatment.

Fig. 4C.

Heatmaps illustrating microbiome analysis results.C – the female patients with the top 45 OTUs before and after FMT.
Heatmaps illustrating microbiome analysis results.C – the female patients with the top 45 OTUs before and after FMT.

Fig. 4D.

Heatmaps illustrating microbiome analysis results.This figure showcases heatmaps of the top-ranking gut microbiota OTUs among patients before and after FMT or placebo treatments.D – the female group pre- and post-placebo.AM and AF denote male and female ulcerative colitis patients, respectively, post-FMT; AS refers to a subgroup of 20 male ulcerative colitis patients post-FMT, while AU represents a similar subgroup of 20 female patients post-FMT. BU and BS are used to indicate female and male ulcerative colitis patients, respectively, pre-FMT. AFP and AMP represent female and male patients, respectively, post-placebo treatment, while BFP and BMP signify female and male patients, respectively, pre-placebo treatment.
Heatmaps illustrating microbiome analysis results.This figure showcases heatmaps of the top-ranking gut microbiota OTUs among patients before and after FMT or placebo treatments.D – the female group pre- and post-placebo.AM and AF denote male and female ulcerative colitis patients, respectively, post-FMT; AS refers to a subgroup of 20 male ulcerative colitis patients post-FMT, while AU represents a similar subgroup of 20 female patients post-FMT. BU and BS are used to indicate female and male ulcerative colitis patients, respectively, pre-FMT. AFP and AMP represent female and male patients, respectively, post-placebo treatment, while BFP and BMP signify female and male patients, respectively, pre-placebo treatment.

Self-rating depression scale (SDS) and self-rating anxiety scale (SAS) before and after FMT (± SD).

Time Experimental group Placebo group
SDS SAS SDS SAS
Males
Before FMT 55.29 ± 7.393 44.16 ± 5.929 57.829 ± 9.209 43.377 ± 4.004
3 weeks 49.55 ± 6.093 ***### 41.01 ± 5.287 # 55.113 ± 5.801 41.958 ± 7.969
6 weeks 45.98 ± 5.4 ****#### 37.5 ± 4.275 ***### 58.437 ± 8.857 42.09 ± 7.982
9 weeks 42.84 ± 4.051 ****#### 33.99 ± 3.623 ****#### 55.386 ± 11.322 45.402 ± 6.562
Females
Before FMT 54.76 ± 7.411 45.09 ± 5.935 55.217 ± 9.891 44.784 ± 5.301
3 weeks 46.79 ± 5.752 ****### 39.08 ± 5.17 ***## 54.6 ± 10.427 44.177 ± 8.28
6 weeks 43.41 ± 5.362 ****### 34.29 ± 3.909 ****## 53.23 ± 6.527 46.833 ± 7.012
9 weeks 37.66 ± 4.091 ****#### 28.5 ± 3.781 ****#### 56.04 ± 5.384 49.115 ± 4.044

UC scores before and after FMT (± SD).

Time Diarrhea score Abdominal pain score Bloody stool Mucosa score Mayo score
Males (experimental group)
Before FMT 5.294 ± 1.658 5.091 ± 1.696 5.358 ± 1.579 1.772 ± 0.516 5.357 ± 1.724
3 weeks 4.719 ± 1.612 *## 4.598 ± 1.378 *## 3.956 ± 1.428 *****#### 1.533 ± 0.478 *# 5.066 ± 1.651
6 weeks 4.267 ± 1.457 ***### 4.269 ± 1.428 ***### 3.932 ± 1.195 *****#### 1.416 ± 0.441 ***### 4.317 ± 1.806 ***###
9 weeks 3.965 ± 1.163 ****#### 4.116 ± 1.053 ****#### 3.524 ± 0.895 *****#### 1.259 ± 0.385 ****#### 4.443 ± 1.242 **##
Males (placebo group)
Before FMT 5.511 ± 1.605 5.089 ± 2.126 5.464 ± 1.217 1.837 ± 0.772 5.360 ± 1.565
3 weeks 5.430 ± 1.937 5.246 ± 1.725 5.815 ± 1.391 1.960 ± 0.681 5.405 ± 2.220
6 weeks 5.504 ± 1.351 5.305 ± 1.892 5.194 ± 1.432 1.859 ± 0.546 5.483 ± 2.218
9 weeks 5.566 ± 2.071 5.188 ± 1.762 5.073 ± 1.229 1.772 ± 0.508 4.957 ± 1.361
Females (experimental group)
Before FMT 4.979 ± 1.741 4.812 ± 1.606 5.086 ± 1.696 1.721 ± 0.501 5.665 ± 1.808
3 weeks 4.005 ± 1.282 ****### 3.381 ± 1.327 ****#### 3.520 ± 1.254 ****#### 1.442 ± 0.457 **## 4.730 ± 1.473 ***###
6 weeks 3.523 ± 1.087 ****### 3.12 ± 1.009 ****#### 3.034 ± 0.925 ****#### 1.24 ± 0.349 ****#### 4.503 ± 1.643 ****####
9 weeks 2.933 ± 0.787 ****#### 2.924 ± 0.835 ****#### 2.396 ± 0.535 ****#### 1.098 ± 0.309 ****#### 3.978 ± 1.096 ****####
Females (placebo group)
Before FMT 5.318 ± 2.286 5.060 ± 1.895 5.009 ± 1.574 1.653 ± 0.752 5.711 ± 1.858
3 weeks 5.095 ± 1.952 4.512 ± 1.217 5.587 ± 2.193 1.958 ± 0.363 5.287 ± 2.241
6 weeks 4.640 ± 1.970 5.282 ± 1.496 5.079 ± 1.563 1.867 ± 0.743 5.533 ± 2.010
9 weeks 5.459 ± 1.997 5.062 ± 1.390 5.048 ± 2.109 1.713 ± 0.654 5.542 ± 1.831

Baseline characteristics of adolescent donors.

Parameters Males (n = 68) Females (n = 68) t-values p-values
Age 13.91 ± 2.22 13.91 ± 2.563 0.010 0.992
BMI 22.59 ± 1.468 22.38 ± 1.416 0.001 0.999
hsCRP (mg/dl) 0.487 ± 0.253 0.4856 ± 0.299 1.232 0.999
Triglyceride (mg/dl) 73.24 ± 14.41 75.41 ± 14.96 0.821 0.771
Total cholesterol (mg/dl) 169.6 ± 14.09 171.1 ± 13.43 0.268 0.958
HDL-c (mg/dl) 64.91 ± 3.155 65.38 ± 2.962 0.513 0.999
LDL-c (mg/dl) 94.8 ± 15.2 95.7 ± 13.67 0.002 0.996

hsCRP levels in ulcerative colitis (UC) patients before and after FMT (± SD).

Time Experimental group Placebo group t-values p-values
Males
Before FMT 3.707 ± 1.209 3.634 ± 1.262 0.288 0.294
3 weeks 3.521 ± 1.312 4.127 ± 1.374 3.279 0.001
6 weeks 3.511 ± 1.091 3.493 ± 0.966 0.134 0.894
9 weeks 3.033 ± 1.184** 3.577 ± 1.581 1.753 0.008
Females
Before FMT 3.776 ± 1.379 3.426 ± 1.295 1.941 0.054
3 weeks 3.219 ± 1.219* 3.791 ± 1.275 2.035 0.044
6 weeks 2.821 ± 1.023**** 3.474 ± 1.091 3.911 0.000
9 weeks 2.35 ± 0.8592**** 3.526 ± 1.365 6.359 0.000

Baseline characteristics of ulcerative colitis (UC) patients.

Parameters Experimental group (n = 68) Placebo group (n = 68) χ2 or t-values p-values
Males
Age 45.2 ± 13.6 47.1 ± 11.4 0.402 0.688
BMI 22.5 ± 2.16 21.5 ± 3.4 1.484 0.141
Smoker, n (%) 18 (43.9%) 17 (25.0%) 0.038 0.844
Drinker, n (%) 12 (17.6%) 11 (16.2%) 0.052 0.819
Protein intake (g/day) 79.252 ± 14.791 82.543 ± 27.594 0.456 0.377
Fat intake (g/day) 89.618 ± 33.173 92.609 ± 38.641 0.158 0.623
Carbohydrate intake (g/day) 258.167 ± 70.847 264.875 ± 74.136 0.568 0.326
Vitamin A intake (μg/day) 817.949 ± 190.225 839.24 ± 196.633 0.479 0.354
Vitamin C intake (mg/day) 99.564 ± 37.648 108.344 ± 11.862 0.984 0.102
Vitamin D intake (μg/day) 28.134 ± 14.025 30.848 ± 10.064 1.033 0.096
Calcium intake (mg/day) 997.56 ± 202.16 1018.256 ± 310.141 1.527 0.058
Iron intake (mg/day) 41.123 ± 25.249 38.897 ± 35.102 1.320 0.079
hsCRP (mg/dl) 3.707 ± 1.209 4.034 ± 1.25 0.135 0.893
Triglyceride (mg/dl) 98.2 ± 33.0 95.4 ± 33.9 1.375 0.172
Total cholesterol (mg/dl) 188 ± 21.4 191.6 ± 14.3 0.841 0.402
HDL-c (mg/dl) 49.7 ± 6.11 46.04 ± 7.44 1.951 0.064
LDL-c (mg/dl) 123 ± 18 129.9 ± 21.3 1.152 0.133
Females
Age 40.6 ± 12.9 36.7 ± 14.0 1.220 0.225
BMI 21.6 ± 1.94 20.55 ± 1.62 1.861 0.056
Smoker, n (%) 20 (48.78%) 18 (26.5%) 0.146 0.702
Drinker, n (%) 11 (16.17%) 13 (19.12%) 0.202 0.653
Menopausal status
Premenopausal, n (%) 41 (60.29) 48 (70.59)
Perimenopausal, n (%) 20 (29.41) 17 (25) 2.394 0.302
Postmenopausal, n (%) 7 (10.29) 3 (4.41)
Protein intake (g/day) 75.252 ± 28.791 70.543 ± 15.594 1.632 0.053
Fat intake (g/day) 73.618 ± 32.173 77.609 ± 16.641 0.105 0.647
Carbohydrate intake (g/day) 247.167 ± 74.847 259.875 ± 85.136 0.258 0.394
Vitamin A intake (μg/day) 830.949 ± 184.225 870.24 ± 220.633 0.752 0.214
Vitamin C intake (mg/day) 115.564 ± 35.648 112.344 ± 32.862 0.121 0.698
Vitamin D intake (μg/day) 12.134 ± 4.975 10.848 ± 5.064 0.097 0.876
Calcium intake (mg/day) 1000.56 ± 222.16 1096.256 ± 307.141 0.118 0.7063
Iron intake (mg/day) 12.123 ± 10.249 13.897 ± 6.102 0.237 0.425
hsCRP (mg/dl) 3.776 ± 1.379 3.694 ± 1.663 0.023 0.982
Triglyceride (mg/dl) 99.9 ± 31.2 99.4 ± 33.8 0.453 0.651
Total cholesterol (mg/dl) 193 ± 19.3 186.4 ± 26.8 0.781 0.436
HDL-c (mg/dl) 50.7 ± 5 49.7 ± 1.5 0.504 0.616
LDL-c (mg/dl) 119 ± 18.1 119.5 ± 19.8 0.753 0.453
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