Probiotics Improve Gastrointestinal Function and Life Quality in Pregnancy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Design
2.2. Data and Specimen Collection
2.3. Quantification of Bacteria Genes
2.4. Shotgun Metagenomic Sequencing
2.5. Bioinformatic Analysis
2.6. Untargeted Metabolomic Analysis
2.7. Statistical Analysis
3. Results
3.1. The Effect of Probiotics on Symptoms
3.2. The Effect of Probiotics on Fecal Metabolites
3.3. The Effect of Probiotics on Fecal Microbiota
3.4. The Effect of Probiotics on the Butyric Acid and Bile Acid-Generating Bacteria
3.5. The Relationships between Biomarkers and Symptoms
4. Discussion
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Koretz, R.L.; Rotblatt, M. Complementary and alternative medicine in gastroenterology: The good, the bad, and the ugly. Clin. Gastroenterol. Hepatol. 2004, 2, 957–967. [Google Scholar] [CrossRef]
- McParlin, C.; O’Donnell, A.; Robson, S.C.; Beyer, F.; Moloney, E.; Bryant, A.; Bradley, J.; Muirhead, C.R.; Nelson-Piercy, C.; Newbury-Birch, D.; et al. Treatments for Hyperemesis Gravidarum and Nausea and Vomiting in Pregnancy: A Systematic Review. JAMA 2016, 316, 1392–1401. [Google Scholar] [CrossRef] [Green Version]
- Black, C.J.; Drossman, D.A.; Talley, N.J.; Ruddy, J.; Ford, A.C. Functional gastrointestinal disorders: Advances in understanding and management. Lancet 2020, 396, 1664–1674. [Google Scholar] [CrossRef]
- Edwards, S.M.; Cunningham, S.A.; Dunlop, A.L.; Corwin, E.J. The Maternal Gut Microbiome During Pregnancy. MCN Am. J. Matern Child Nurs. 2017, 42, 310–317. [Google Scholar] [CrossRef]
- Li, T.; Chiang, J.Y.L. Bile acid-based therapies for non-alcoholic steatohepatitis and alcoholic liver disease. Hepatobiliary Surg. Nutr. 2020, 9, 152–169. [Google Scholar] [CrossRef]
- Wan, Y.-J.; Sheng, L. Regulation of bile acid receptor activity(☆). Liver Res. 2018, 2, 180–185. [Google Scholar] [CrossRef]
- Duboc, H.; Taché, Y.; Hofmann, A.F. The bile acid TGR5 membrane receptor: From basic research to clinical application. Dig. Liver Dis. 2014, 46, 302–312. [Google Scholar] [CrossRef] [Green Version]
- Alemi, F.; Poole, D.P.; Chiu, J.; Schoonjans, K.; Cattaruzza, F.; Grider, J.R.; Bunnett, N.W.; Corvera, C.U. The receptor TGR5 mediates the prokinetic actions of intestinal bile acids and is required for normal defecation in mice. Gastroenterology 2013, 144, 145–154. [Google Scholar] [CrossRef]
- Housset, C.; Chrétien, Y.; Debray, D.; Chignard, N. Functions of the Gallbladder. Compr. Physiol. 2016, 6, 1549–1577. [Google Scholar] [CrossRef] [PubMed]
- Yu, H.; Zhao, T.; Liu, S.; Wu, Q.; Johnson, O.; Wu, Z.; Zhuang, Z.; Shi, Y.; Peng, L.; He, R.; et al. MRGPRX4 is a bile acid receptor for human cholestatic itch. Elife 2019, 8. [Google Scholar] [CrossRef]
- Settles, M.; Streett, D.; Angell, J.; Hunter, S. HTStream. 2016. Available online: https://s4hts.github.io/HTStream/ (accessed on 26 October 2021).
- Wood, D.E.; Lu, J.; Langmead, B. Improved metagenomic analysis with Kraken 2. Genome Biol. 2019, 20, 257. [Google Scholar] [CrossRef] [Green Version]
- Lu, J.; Thielen, P.; Salzberg, S.L. Bracken: Estimating species abundance in metagenomics data. PeerJ Comput. Sci. 2017, 3, e104. [Google Scholar] [CrossRef]
- Fitzmaurice, G.M.; Laird, N.M.; Ware, J.H. Applied Longitudinal Analysis; John Wiley & Sons: Hoboken, NJ, USA, 2012. [Google Scholar]
- Li, G.; Taljaard, M.; Van den Heuvel, E.R.; Levine, M.A.; Cook, D.J.; Wells, G.A.; Devereaux, P.J.; Thabane, L. An introduction to multiplicity issues in clinical trials: The what, why, when and how. Int. J. Epidemiol. 2017, 46, 746–755. [Google Scholar] [CrossRef]
- Body, C.; Christie, J.A. Gastrointestinal Diseases in Pregnancy: Nausea, Vomiting, Hyperemesis Gravidarum, Gastroesophageal Reflux Disease, Constipation, and Diarrhea. Gastroenterol. Clin. N. Am. 2016, 45, 267–283. [Google Scholar] [CrossRef]
- Sheng, L.; Jena, P.K.; Liu, H.X.; Kalanetra, K.M.; Gonzalez, F.J.; French, S.W.; Krishnan, V.V.; Mills, D.A.; Wan, Y.Y. Gender Differences in Bile Acids and Microbiota in Relationship with Gender Dissimilarity in Steatosis Induced by Diet and FXR Inactivation. Sci. Rep. 2017, 7, 1748. [Google Scholar] [CrossRef]
- Kulkarni, S.; Ganz, J.; Bayrer, J.; Becker, L.; Bogunovic, M.; Rao, M. Advances in Enteric Neurobiology: The "Brain" in the Gut in Health and Disease. J. Neurosci. 2018, 38, 9346–9354. [Google Scholar] [CrossRef] [Green Version]
- Wei, P.; Keller, C.; Li, L. Neuropeptides in gut-brain axis and their influence on host immunity and stress. Comput. Struct. Biotechnol. J. 2020, 18, 843–851. [Google Scholar] [CrossRef]
- Liu, J.; Zhan, S.; Jia, Y.; Li, Y.; Liu, Y.; Dong, Y.; Tang, G.; Li, L.; Zhai, Y.; Cao, Z. Retinol and α-tocopherol in pregnancy: Establishment of reference intervals and associations with CBC. Matern. Child. Nutr. 2020, 16, e12975. [Google Scholar] [CrossRef]
- Geerlings, S.Y.; Kostopoulos, I.; de Vos, W.M.; Belzer, C. Akkermansia muciniphila in the Human Gastrointestinal Tract: When, Where, and How? Microorganisms 2018, 6, 75. [Google Scholar] [CrossRef] [Green Version]
- Sheng, L.; Jena, P.K.; Hu, Y.; Liu, H.X.; Nagar, N.; Kalanetra, K.M.; French, S.W.; French, S.W.; Mills, D.A.; Wan, Y.Y. Hepatic inflammation caused by dysregulated bile acid synthesis is reversible by butyrate supplementation. J. Pathol. 2017, 243, 431–441. [Google Scholar] [CrossRef] [Green Version]
- Traczyk, W.Z. Neuropeptides--the present state of research work. Mater. Med. Pol. 1987, 19, 3–6. [Google Scholar]
- Ridlon, J.M.; Wolf, P.G.; Gaskins, H.R. Taurocholic acid metabolism by gut microbes and colon cancer. Gut. Microbes. 2016, 7, 201–215. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Begley, M.; Hill, C.; Gahan, C.G. Bile salt hydrolase activity in probiotics. Appl. Environ. Microbiol. 2006, 72, 1729–1738. [Google Scholar] [CrossRef] [Green Version]
Characteristics | n (%) or Mean ± SD |
---|---|
Non-Hispanic White | |
No | 19 (59.4%) |
Yes | 13 (40.6%) |
Education | |
High school diploma or equivalent | 1 (3.1%) |
Some college | 3 (9.4%) |
College degree or higher | 28 (87.5%) |
Age | 31.6 ± 3.9 years |
BMI | 27.5 ± 6.4 |
Gestational age | 72.3 ± 15.6 days |
Constipation a, b | |
No | 2 (13.3%) |
Yes | 13 (86.7%) |
Nausea times per day | 7.0 ± 5.5 |
Nausea hours per day b | 10.3 ± 6.6 |
Nausea score (1–5) | 3.6 ± 0.9 |
Vomiting times c | 2.0 ± 1.3 |
Vomiting score (1–5) c | 2.8 ± 1.0 |
Symptoms | Number of Participants (Observation Days) | Incidence Rate Ratio a (95% CI) | p-Value | Odds Ratio b (95% CI) | p-Value |
---|---|---|---|---|---|
Nausea and Vomiting: | |||||
Daily nausea score (1–5) | 32 (535) | 0.46 (0.31, 0.67) ** | <0.001 | ||
Daily vomit score (1–5) c | 12 (187) | 0.31 (0.15, 0.65) ** | 0.002 | ||
Nausea hours per day | 15 (255) | ||||
Daily nausea times | 32 (534) | 0.84 (0.75, 0.95) ** | 0.005 | ||
Daily vomiting times c | 12 (200) | 0.84 (0.77, 0.92) ** | <0.001 | ||
Nausea and Vomiting: | 32 (535) | 0.67 (0.50, 0.90) ** | 0.008 | ||
Mood/Life Quality: | |||||
| 32 (534) | 0.41 (0.27, 0.61) ** | <0.001 | ||
| 32 (534) | 0.70 (0.45, 1.07) | 0.10 | ||
| 32 (532) | 0.47 (0.30, 0.75) ** | 0.001 | ||
| 32 (535) | 0.37 (0.25, 0.57) ** | <0.001 | ||
| 32 (535) | 0.59 (0.36, 0.97) * | 0.04 | ||
| 32 (533) | 0.42 (0.28, 0.63) ** | <0.001 | ||
| 32 (535) | 0.44 (0.28, 0.67) ** | <0.001 | ||
| 32 (535) | 0.46 (0.31, 0.69) ** | <0.001 | ||
| 32 (535) | 0.50 (0.33, 0.76) ** | 0.001 | ||
| 32 (535) | 0.68 (0.42, 1.08) | 0.10 | ||
| 32 (535) | 0.60 (0.38, 0.93) * | 0.02 | ||
| 32 (535) | 0.43 (0.28, 0.65) ** | <0.001 | ||
| 32 (535) | 0.38 (0.25, 0.57) ** | <0.001 | ||
| 32 (535) | 0.42 (0.27, 0.65) ** | <0.001 | ||
| 32 (534) | 0.43 (0.27, 0.67) ** | <0.001 | ||
| 32 (535) | 0.29 (0.18, 0.46) ** | <0.001 | ||
| 32 (533) | 0.42 (0.27, 0.66) ** | <0.001 | ||
Constipation: | |||||
Bowel movement (yes/no) | 15 (255) | 0.93 (0.45, 1.93) | 0.85 | ||
Number of Bowel movement | 15 (255) | 0.94 (0.73, 1.20) | 0.605 | ||
Stools are difficult to pass (yes/no) | 15 (255) | 0.54 (0.26, 1.12) | 0.10 | ||
Stools are hard (yes/no) | 15 (255) | 0.23 (0.10, 0.50) ** | <0.001 | ||
Not all stools passed (yes/no) | 15 (254) | 0.47 (0.22, 1.02) | 0.06 | ||
Constipation (yes/no) d | 15 (255) | 0.37 (0.18, 0.79) * | 0.010 |
Genes | Number of Participants (Observation Days) | Fold Change a (95% CI) | p-Value |
---|---|---|---|
Butyric acid-producing genes | |||
bcoA | 25 (155) | 0.94 (0.74, 1.18) | 0.57 |
buk | 25 (155) | 0.96 (0.71, 1.31) | 0.81 |
Bile acid-producing genes | |||
bsh | 25 (155) | 5.41 (3.13, 9.34) ** | <0.001 |
baiJ | 25 (155) | 0.79 (0.49, 1.26) | 0.31 |
Biomarker = Log-Transformed Bsh Copy Number | |||||
---|---|---|---|---|---|
Symptoms | Number of Participants (Observation Days) | Incidence Rate Ratio a (95% CI) | p-Value | Odds Ratio b (95% CI) | p-Value |
Daily nausea score (1–5) | 25 (416) | 0.71 (0.34, 1.48) | 0.36 | ||
Daily vomit score (1–5) b | 10 (166) | 0.20 (0.06, 0.72) * | 0.02 | ||
Daily nausea times | 25 (415) | 0.94 (0.75, 1.18) | 0.60 | ||
Daily vomiting times c | 10 (166) | 0.50 (0.31, 0.81) ** | 0.005 |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Liu, A.T.; Chen, S.; Jena, P.K.; Sheng, L.; Hu, Y.; Wan, Y.-J.Y. Probiotics Improve Gastrointestinal Function and Life Quality in Pregnancy. Nutrients 2021, 13, 3931. https://doi.org/10.3390/nu13113931
Liu AT, Chen S, Jena PK, Sheng L, Hu Y, Wan Y-JY. Probiotics Improve Gastrointestinal Function and Life Quality in Pregnancy. Nutrients. 2021; 13(11):3931. https://doi.org/10.3390/nu13113931
Chicago/Turabian StyleLiu, Albert T., Shuai Chen, Prasant Kumar Jena, Lili Sheng, Ying Hu, and Yu-Jui Yvonne Wan. 2021. "Probiotics Improve Gastrointestinal Function and Life Quality in Pregnancy" Nutrients 13, no. 11: 3931. https://doi.org/10.3390/nu13113931