Biology:Lacticaseibacillus paracasei

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Short description: Species of bacterium

Lacticaseibacillus paracasei
Lactobacillus paracasei.jpg
Scientific classification edit
Domain: Bacteria
Phylum: Bacillota
Class: Bacilli
Order: Lactobacillales
Family: Lactobacillaceae
Genus: Lacticaseibacillus
Species:
L. paracasei
Binomial name
Lacticaseibacillus paracasei
(Collins et al. 1989) Zheng et al. 2020
Subspecies
  • Lacticaseibacillus paracasei subsp. paracasei
  • Lacticaseibacillus paracasei subsp. tolerans
Synonyms
  • Lactobacillus paracasei Collins et al. 1989

Lacticaseibacillus paracasei (commonly abbreviated as Lc. paracasei) is a gram-positive, homofermentative species of lactic acid bacteria that are commonly used in dairy product fermentation and as probiotic cultures. Lc. paracasei is a bacterium that operates by commensalism. It is commonly found in many human habitats such as human intestinal tracts and mouths as well as sewages, silages, and previously mentioned dairy products.[1] The name includes morphology, a rod-shaped (bacillus shape) bacterium with a width of 2.0 to 4.0μm and length of 0.8 to 1.0μm.

Strains of L. paracasei have been isolated from a variety of environments including dairy products, plants or plant fermentations, and from the human and animal gastrointestinal tracts.[2][3] A protracted refrigeration period before in vitro gastrointestinal transit (GIT) did not affect or influenced very weakly cell resistance.[4]

Lacticaseibacillus paracasei is genotypically and phenotypically closely related from other members of the Lacticaseibacillus casei group which also includes Lacticaseibacillus casei, Lacticaseibacillus zeae[5] and Lacticaseibacillus rhamnosus.[6] However, these species are readily differentiated from each other by Multi-Locus-Sequence-Typing, core genome phylogeny, or Average Nucleotide Identity.[5][3][7] Its fermentative properties allows it to be used as biological food processors and supplements for diets and medical disorders, especially in the gastrointestinal tract.[8]

Although probiotics are considered safe, they may cause bacteria-host interactions and adverse health consequences. In certain cases there is a risk of bacteremia when probiotics are used.[9][10] Currently, the probiotic strain, frequency, dose and duration of the probiotic therapies are not established.[9]

Physiology

Lacticaseibacillus paracasei is a gram-positive, homofermentative, non-spore forming microorganism.[11] As Lc. paracasei is homofermentative, lactic acid is produced as the main product of hexose metabolism while lactate and acetate are produced from pentoses. The cells of Lc. paracasei are typically rod shaped, with a size range of 2.0μm to 4.0μm in width, and 0.8 to 1.0μm in length.[6] The organism is nonmotile. Lc. paracasei cells often have square ends, and may exist either in single form or in chains.[6]

Lacticaseibacillus paracasei grows optimally in a temperature range between 10 and 37 °C.[12] No growth takes place above 40 °C. The organism is able to survive for approximately 40 seconds in a maximum temperature of 72 °C.[6] The survivability of Lc. paracasei was remarkably higher when stored under refrigeration (4 °C). In contrast, the lowest survival was observed during non-refrigerated storage(22 °C)[13] Freezing at -20 degrees C and -70 degrees C had much less adverse effect on viability than did storage at 7 degrees C[14]

Lacticaseibacillus paracasei temporarily exists as a common inhabitant of the human gastrointestinal tract as part of the normal microbiota.[11] Naturally fermented vegetables, milk, and meat may also contain strains of L. paracasei.[15]

Phylogeny

Lacticaseibacillus paracasei belongs to kingdom Bacteria. Lc. paracasei is part of the phylum Bacillota, the class Bacilli,[6] the order Lactobacillales and the family Lactobacillaceae respectively.[6][7] The argument on the nomenclature of L. paracasei versus L. casei was intensely debated as many strains of L. casei or L. paracasei for which sequence data is available in the databases are mis-labeled.[2] In 1989, it was proposed that L. paracasei be designated a subspecies (paracasei) to account for the species that it shares DNA homology with.[6] It has been shown their names have been used interchangeably in scientific literature.[2] 16S RNA sequence homology has confirmed the relatedness between these species[6] but core genome phylogeny confirmed that the closely related species Lc. casei, Lc. paracasei, Lc. rhamnosus and Lc. zeae are separate species.[7][5]

Historically, the difference between Lacticaseibacillus paracasei and other lactobacilli has been based on biochemical characteristics. There is an approximately 90% sequence identity between casei, paracasei, and rhamnosus.[2] However, there are some differential criteria that are commonly used to differentiate between them. These differential criteria include nutritional requirements and growth environment.[2] L. paracasei has been found to show specific differences with other lactobacilli in that it is somewhat heat resistant, grows well in ripening cheese, and it has high proteolytic activity.[16]

Genomics

Lacticaseibacillus paracasei's genome contains circular DNA and varies slightly among the different strains isolated. On average, the genomes are 2.9 to 3.0 million base pairs (commonly abbreviated Mb). It has a GC-content between 46.2 and 46.6% and is predicted to encode about 2800 to 3100 proteins.[3] The difference in the genomes of these strains lies in variant cell envelopes, secretory proteins, and polysaccharides. Many of the commonly coded proteins are cell-surface associated cell-wall hydrolases that protect the cell against apoptosis. These enzymes have been shown to provide cellular protection to human epithelial cells.[2]

Genetic diversity for the different L. paracasei genomes was assessed using multilocus sequence typing (MLST) and amplified fragment length polymorphism (AFLP). MLST is a technique used for classifying microbes by the use of DNA fragments from essential genes of the organism.[17] AFLP is a Polymerase Chain Reaction (PCR) tool used in DNA profiling to amplify a desired DNA fragment with the use of restriction enzymes and ligands.[18]

Clinical and research applications

Lacticaseibacillus paracasei has been identified as a bacterium that has probiotic properties.[1]

Allergic respiratory disease

A systematic review provided significant evidence of beneficial clinical and immunologic effects of Lc. paracasei LP-33 strains in the treatment of Allergic rhinitis.[19]

Ingestion of LP-33(Lactobacillus paracasei 33 )-fortified fermented milk for 30 days can effectively and safely improve the quality of life of patients with allergic rhinitis, and may serve as an alternative treatment for allergic rhinitis.[20]

Lacticaseibacillus paracasei BRAP01 are the dominant strains inducing IFN-γ/IL-10 production in Taiwanese individuals.[21]

Lacticaseibacillus paracasei HB89 mitigates respiratory tract allergies stimulated by PM2.5.[22]

For allergic rhinitis (AR), oral administration of Lactobacillus paracasei (all stored at 4°C before consumption) with more than 10 billion bacteria (1x1010CFU) per day for 8 weeks can improve nasal itching (AR’s key clinical features) and reduced secretion of the pro-inflammatory mediator IL-5. [23]

Atopic dermatitis, Urticaria

Oral administration of L. paracasei KBL382 significantly reduced atopic dermatitis(AD)-associated skin lesions, epidermal thickening, serum levels of immunoglobulin E, and immune cell infiltration. [24]

Influenza

Oral administration of heat-killed Lactobacillus paracasei MoLac-1 increased the proportion of NK cells in spleen, and ameliorated the symptoms of influenza virus(IFV) infection in mice. [25]

Common cold

L. paracasei MCC1849 has the potential to improve resistance to common cold infections in susceptible subjects and maintain a desirable mood state, even under mental stress conditions. [26]

Coronavirus disease (COVID-19)

The Lacticaseibacillus paracasei DG strain significantly induced the expression of genes involved in protective antiviral immunity and prevented the expression of proinflammatory genes triggered by SARS-CoV-2 infection. [27]

Inflammatory bowel disease

A formulation of live bacteria including Lc. paracasei may be used in combination with conventional therapies to treat ulcerative colitis.[28] Lipoteichoic acid from the cell wall of a heat killed Lacticaseibacillus paracasei D3-5 ameliorates aging-related leaky gut, inflammation and improves physical and cognitive functions in mice[29]

Diarrhea

Lactobacillus paracasei has been shown to inhibit the bacterial activity of Escherichia coli, a common strain of diarrhea-causing bacteria, so Lactobacillus paracasei is used in the treatment of diarrhea. [30]。

Helicobacter pylori Infection

Lacticaseibacillus paracasei showed bacteriostatic and bactericidal activity vs. H. pylori. [31]

Irritable bowel syndrome

The Lactobacillus paracasei may reduce GI symptom severity and improve the psychological well-being of individuals with certain IBS subtypes. [32]

Cancer

L. paracasei IMPC2.1 may be a chemoprophylactic in gastrointestinal cells.[33] Gastrointestinal cells are susceptible to apoptosis and cell growth from both heat-killed and viable IMPC2.1 strains.[1]

Lc. paracasei 8700:2 has been isolated from healthy human gastrointestinal mucosa and human feces.[16] Strain 8700:2 was also found to inhibit Salmonella enterica and Helicobacter pylori, two pathogens commonly found in the gastrointestinal tract. Strain 8700:2 breaks down oligofructose and inulin, while also growing rapidly on both and producing lactic acid as the end product.[34]

Health concerns

The manipulation of the gut microbiota is complex and may cause bacteria-host interactions. Although probiotics are considered safe, when they are used by oral administration there is a risk of passage of viable bacteria from the gastrointestinal tract to the internal organs (bacterial translocation) and subsequent bacteremia, which can cause adverse health consequences.[9] Some people, such as those with immune compromise, short bowel syndrome, central venous catheters, cardiac valve disease and premature infants, may be at higher risk for adverse events.[10]

Currently, the probiotic strain, frequency, dose and duration of the probiotic therapy are not established.[9] Live bacteria might not be essential because of beneficial effects of probiotics seems to be mediated by their DNA and by secreted soluble factors, and their therapeutic effects may be obtained by systemic administration rather than oral administration.[9][35]

History

LAB (Lactic Acid Bacteria) were classified and grouped in the early 1900s after gaining scientists' attention after observing the bacteria's interactions in different foods, especially dairy products. In 1991, Martinus Beijerinck, a Dutch microbiologist, separated Lactobacillus as gram positive bacteria from the previously known LAB group.[36] L. paracasei has been recently classified as a part of the Lacticaseibacillus casei group of probiotics.[1] The name Lc. paracasei was proposed for rejection in 1996 by Dicks, Duplessis, Dellaglio, and Lauer[6] but subsequent work confirmed the validity of the species.[3][7]

References

  1. ↑ 1.0 1.1 1.2 1.3 Orlando, A.; Refolo, M. G.; Messa, C.; Amati, L.; Lavermicocca, P.; Guerra, V.; Russo, F. (October 2012). "Antiproliferative and Proapoptotic Effects of Viable or Heat-Killed IMPC2.1 and GG in HGC-27 Gastric and DLD-1 Colon Cell Lines". Nutrition and Cancer 64 (7): 1103–1111. doi:10.1080/01635581.2012.717676. PMID 23061912. 
  2. ↑ 2.0 2.1 2.2 2.3 2.4 2.5 Smokvina, Tamara; Wels, Michiel; Polka, Justyna; Chervaux, Christian; Brisse, Sylvain; Boekhorst, Jos; Vlieg, Johan E. T. van Hylckama; Siezen, Roland J. et al. (19 July 2013). "Lactobacillus paracasei Comparative Genomics: Towards Species Pan-Genome Definition and Exploitation of Diversity". PLOS ONE 8 (7): e68731. doi:10.1371/journal.pone.0068731. PMID 23894338. Bibcode: 2013PLoSO...868731S. 
  3. ↑ 3.0 3.1 3.2 3.3 Wuyts, Sander; Wittouck, Stijn; De Boeck, Ilke; Allonsius, Camille N.; Pasolli, Edoardo; Segata, Nicola; Lebeer, Sarah (2017). "Large-Scale Phylogenomics of the Lactobacillus casei Group Highlights Taxonomic Inconsistencies and Reveals Novel Clade-Associated Features" (in en). mSystems 2 (4). doi:10.1128/msystems.00061-17. PMID 28845461. 
  4. ↑ José Fernandes Lemos Junior, Wilson; Fioravante Guerra, André; Tarrah, Armin; Silva Duarte, Vinícius da; Giacomini, Alessio; Luchese, Rosa Helena; Corich, Viviana (June 2020). "Safety and Stability of Two Potentially Probiotic Lactobacillus Strains After In Vitro Gastrointestinal Transit" (in en). Probiotics and Antimicrobial Proteins 12 (2): 657–666. doi:10.1007/s12602-019-09565-2. ISSN 1867-1306. PMID 31214943. 
  5. ↑ 5.0 5.1 5.2 Huang, Chien-Hsun; Chen, Chih-Chieh; Liou, Jong-Shian; Lee, Ai-Yun; Blom, Jochen; Lin, Yu-Chun; Huang, Lina; Watanabe, KoichiYR 2020 (2020). "Genome-based reclassification of Lactobacillus casei: emended classification and description of the species Lactobacillus zeae". International Journal of Systematic and Evolutionary Microbiology 70 (6): 3755–3762. doi:10.1099/ijsem.0.003969. ISSN 1466-5034. PMID 32421490. 
  6. ↑ 6.0 6.1 6.2 6.3 6.4 6.5 6.6 6.7 6.8 COLLINS, M. D.; PHILLIPS, B. A.; ZANONI, P. (1 April 1989). "Deoxyribonucleic Acid Homology Studies of Lactobacillus casei, Lactobacillus paracasei sp. nov., subsp. paracasei and subsp. tolerans, and Lactobacillus rhamnosus sp. nov., comb. nov.". International Journal of Systematic Bacteriology 39 (2): 105–108. doi:10.1099/00207713-39-2-105. 
  7. ↑ 7.0 7.1 7.2 7.3 Zheng, Jinshui; Wittouck, Stijn; Salvetti, Elisa; Franz, Charles M.A.P.; Harris, Hugh M.B.; Mattarelli, Paola; O’Toole, Paul W.; Pot, Bruno et al. (2020). "A taxonomic note on the genus Lactobacillus: Description of 23 novel genera, emended description of the genus Lactobacillus Beijerinck 1901, and union of Lactobacillaceae and Leuconostocaceae". International Journal of Systematic and Evolutionary Microbiology 70 (4): 2782–2858. doi:10.1099/ijsem.0.004107. ISSN 1466-5034. PMID 32293557. 
  8. ↑ Felten, A; Barreau, C; Bizet, C; Lagrange, PH; Philippon, A (Mar 1999). "Lactobacillus species identification, H2O2 production, and antibiotic resistance and correlation with human clinical status.". Journal of Clinical Microbiology 37 (3): 729–33. doi:10.1128/JCM.37.3.729-733.1999. PMID 9986841. 
  9. ↑ 9.0 9.1 9.2 9.3 9.4 "Diet therapy for inflammatory bowel diseases: The established and the new.". World J Gastroenterol 22 (7): 2179–94. 2016. doi:10.3748/wjg.v22.i7.2179. PMID 26900283. 
  10. ↑ 10.0 10.1 "Risk and safety of probiotics.". Clin Infect Dis 60 (Suppl 2): S129–34. 2015. doi:10.1093/cid/civ085. PMID 25922398. 
  11. ↑ 11.0 11.1 HESSLE; HANSON; WOLD (May 1999). "Lactobacilli from human gastrointestinal mucosa are strong stimulators of IL-12 production". Clinical and Experimental Immunology 116 (2): 276–282. doi:10.1046/j.1365-2249.1999.00885.x. PMID 10337019. 
  12. ↑ Rogan, WJ; Gladen, BC; Hung, KL; Koong, SL; Shih, LY; Taylor, JS; Wu, YC; Yang, D et al. (Jul 15, 1988). "Congenital poisoning by polychlorinated biphenyls and their contaminants in Taiwan". Science 241 (4863): 334–6. doi:10.1126/science.3133768. PMID 3133768. Bibcode: 1988Sci...241..334R. https://semanticscholar.org/paper/0dc1c74d7ce9db84ae38214d1a95e416dfa5b730. 
  13. ↑ Jofré, A.; Aymerich, T.; Garriga, M. (2014-11-06). "Impact of different cryoprotectants on the survival of freeze-dried Lactobacillus rhamnosus and Lactobacillus casei/paracasei during long-term storage" (in en). Beneficial Microbes 6 (3): 381–6. doi:10.3920/BM2014.0038. ISSN 1876-2883. PMID 25380798. 
  14. ↑ Juárez Tomás, María Silvina; Soledad Ocaña, Virginia; Nader-Macías, María Elena (February 2004). "Viability of vaginal probiotic lactobacilli during refrigerated and frozen storage" (in en). Anaerobe 10 (1): 1–5. doi:10.1016/j.anaerobe.2004.01.002. ISSN 1075-9964. PMID 16701493. 
  15. ↑ Lavermicocca, P (2015). Lactobacillus paracasei-enriched vegetables containing health promoting molecules.. Elsevier Inc.. pp. 361–370. ISBN 9780128023716. 
  16. ↑ 16.0 16.1 Molin, G.; Jeppsson, B.; Johansson, M.-L.; Ahrné, S.; Nobaek, S.; Ståhl, M.; Bengmark, S. (March 1993). "Numerical taxonomy of Lactobacillus spp. associated with healthy and diseased mucosa of the human intestines". Journal of Applied Bacteriology 74 (3): 314–323. doi:10.1111/j.1365-2672.1993.tb03031.x. PMID 8468264. 
  17. ↑ Maiden, Martin; Jane Bygraves; Edward Feil (January 6, 1998). "Multilocus sequence typing: A portable approach to the identification of clones within populations of pathogenic microorganisms". Proceedings of the National Academy of Sciences of the United States of America 95 (6): 3140–3145. doi:10.1073/pnas.95.6.3140. PMID 9501229. Bibcode: 1998PNAS...95.3140M. 
  18. ↑ Kumar, Awanish; Anuradha Dube (February 2013). "Amplified fragment length polymorphism: an adept technique for genome mapping, genetic differentiation, and intraspecific variation in protozoan parasites [electronic resource]". Parasitology Research 112 (2): 457–466. doi:10.1007/s00436-012-3238-6. PMID 23254590. 
  19. ↑ Guvenc, I. A.; Muluk, N. Bayar; Mutlu, F. S.; Eski, E.; Altintoprak, N.; Oktemer, T.; Cingi, C. (2016-07-20). "Do probiotics have a role in the treatment of allergic rhinitis?: A comprehensive systematic review and meta analysis". American Journal of Rhinology & Allergy 30 (5): 157–175. doi:10.2500/ajra.2016.30.4354. ISSN 1945-8932. PMID 27442711. 
  20. ↑ Wang, Ming-Fuu; Lin, Hsiao-Chuan; Wang, Ying-Yu; Hsu, Ching-Hsiang (2004-03-30). "Treatment of perennial allergic rhinitis with lactic acid bacteria" (in en). Pediatric Allergy and Immunology 15 (2): 152–8. doi:10.7025/HEJ.200409.0005. ISSN 0905-6157. PMID 15059192. 
  21. ↑ Ho, Y-H; Huang, Y-T; Lu, Y-C; Lee, S-Y; Tsai, M-F; Hung, S-P; Hsu, T-Y (2016-10-11). "Effects of gender and age on immune responses of human peripheral blood mononuclear cells to probiotics: A large scale pilot study" (in en). The Journal of Nutrition, Health & Aging 21 (5): 521–526. doi:10.1007/s12603-016-0818-7. ISSN 1279-7707. PMID 28448082. 
  22. ↑ Lin, Ching-Hung; Tseng, Chia-Yi; Chao, Ming-Wei (2020-12-07). "Administration of Lactobacillus paracasei HB89 mitigates PM2.5-induced enhancement of inflammation and allergic airway response in murine asthma model" (in en). PLOS ONE 15 (12): e0243062. doi:10.1371/journal.pone.0243062. ISSN 1932-6203. PMID 33284823. Bibcode: 2020PLoSO..1543062L. 
  23. ↑ Perrin, YExpression error: Unrecognized word "et". (2014-01-06). "Comparison of two oral probiotic preparations in a randomized crossover trial highlights a potentially beneficial effect of Lactobacillus paracasei NCC2461 in patients with allergic rhinitis". Clinical and Translational Allergy 4 (1): 1. doi:10.1186/2045-7022-4-1. PMID 24393277. 
  24. ↑ Kim, WKExpression error: Unrecognized word "et". (2020-11-09). "Lactobacillus paracasei KBL382 administration attenuates atopic dermatitis by modulating immune response and gut microbiota". Gut Microbes 12 (1): 1–14. doi:10.1080/19490976.2020.1819156. ISSN 1949-0976. PMID 33016202. 
  25. ↑ Iwabuchi, NoriyukiExpression error: Unrecognized word "et". (November 2012). "Immunomodulating and anti-infective effects of a novel strain of Lactobacillus paracasei that strongly induces interleukin-12". FEMS Immunology & Medical Microbiology 66 (2): 230–9. doi:10.1111/j.1574-695X.2012.01003.x. ISSN 0928-8244. PMID 22775119. 
  26. ↑ Murata, MExpression error: Unrecognized word "et". (December 2018). "Effects of paraprobiotic Lactobacillus paracasei MCC1849 supplementation on symptoms of the common cold and mood states in healthy adults". Beneficial Microbes 9 (6): 855–864. doi:10.3920/BM2017.0197. ISSN 1876-2883. PMID 30099891. 
  27. ↑ Salaris, ClaudioExpression error: Unrecognized word "et". (Jan–Dec 2021). "Lacticaseibacillus paracasei DG enhances the lactoferrin anti-SARS-CoV-2 response in Caco-2 cells". Gut Microbes 13 (1): 19490976. doi:10.1080/19490976.2021.1961970. ISSN 1949-0976. PMID 34365895. 
  28. ↑ Ghouri, Yezaz A; Richards, David M; Rahimi, Erik F; Krill, Joseph T; Jelinek, Katherine A; DuPont, Andrew W (9 December 2014). "Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease". Clin Exp Gastroenterol 7: 473–487. doi:10.2147/CEG.S27530. PMID 25525379. 
  29. ↑ Wang, Shaohua; Ahmadi, Shokouh; Nagpal, Ravinder; Jain, Shalini; Mishra, Sidharth P.; Kavanagh, Kylie; Zhu, Xuewei; Wang, Zhan et al. (2019-12-08). "Lipoteichoic acid from the cell wall of a heat killed Lactobacillus paracasei D3-5 ameliorates aging-related leaky gut, inflammation and improves physical and cognitive functions: from C. elegans to mice" (in en). GeroScience 42 (1): 333–352. doi:10.1007/s11357-019-00137-4. ISSN 2509-2723. PMID 31814084. 
  30. ↑ Caridi, A. (2002). "Selection of Escherichia coli-inhibiting strains of Lactobacillus paracasei subsp. paracasei" (in en). Journal of Industrial Microbiology & Biotechnology 29 (6): 303–308. doi:10.1038/sj.jim.7000300. ISSN 1367-5435. PMID 12483469. 
  31. ↑ Saracino, IMExpression error: Unrecognized word "et". (2020-05-01). "Antimicrobial Efficacy of Five Probiotic Strains Against Helicobacter pylori". Antibiotics 9 (5): 244. doi:10.3390/antibiotics9050244. ISSN 2079-6382. PMID 32403331. 
  32. ↑ Lewis, Erin DExpression error: Unrecognized word "et". (2020-04-21). "Efficacy of Lactobacillus paracasei HA-196 and Bifidobacterium longum R0175 in Alleviating Symptoms of Irritable Bowel Syndrome (IBS): A Randomized, Placebo-Controlled Study". Nutrients 12 (4): 1159. doi:10.3390/nu12041159. ISSN 2072-6643. PMID 32326347. 
  33. ↑ Bernstein, Charles N; Nugent, Zoann; Blanchard, James F (15 March 2011). "5-Aminosalicylate Is Not Chemoprophylactic for Colorectal Cancer in IBD: A Population Based Study". The American Journal of Gastroenterology 106 (4): 731–736. doi:10.1038/ajg.2011.50. PMID 21407180. 
  34. ↑ Makras, L.; Van Acker, G.; De Vuyst, L. (3 November 2005). "Lactobacillus paracasei subsp. paracasei 8700:2 Degrades Inulin-Type Fructans Exhibiting Different Degrees of Polymerization". Applied and Environmental Microbiology 71 (11): 6531–6537. doi:10.1128/AEM.71.11.6531-6537.2005. PMID 16269678. Bibcode: 2005ApEnM..71.6531M. 
  35. ↑ "Probiotics in inflammatory bowel disease: possible mechanisms of action". Curr Opin Gastroenterol 21 (4): 426–30. 2005. PMID 15930982. 
  36. ↑ Stiles, ME; Holzapfel, WH (Apr 29, 1997). "Lactic acid bacteria of foods and their current taxonomy.". International Journal of Food Microbiology 36 (1): 1–29. doi:10.1016/s0168-1605(96)01233-0. PMID 9168311. 

External links

Wikidata ☰ Q1799829 entry



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