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. 2019 May 14;10:1017. doi: 10.3389/fmicb.2019.01017

Table 2.

Summary of animal experiments performed to study role of T1F in Salmonella virulence.

No. Serovar Strains Growth conditions Animal Bacteria administration Outcome Source
1. Typhimurium 1566F (T1F+); 1566N (T1F-) Temp: 37°C
Time: 24h
Medium: nutrient broth
O2: ?
Shaking: ?
Mice- LAC Gray Oral Lowest proportion of mice infected and dying; shorter fecal shedding in comparison to oral; more successful infections and deaths with T1F+Non-fimbriated strain rapidly eliminated from the intestine, Darekar and Duguid, 1972
Conjuctival Medium proportion of mice infected and dying; longer fecal shedding in comparison to oral; more successful infections and deaths with T1F+
intraperitoneal Highest proportion of mice infected and dying; more deaths with T1F+
2. Typhimurium 1566F (T1F+); 1566N (T1F-) Temp: 37°C
Time: 24h
Medium: Nutrient broth
O2: Aerobically
Shaking: No
Mice- LAC Gray Oral Higher number of infections and deaths in T1F+ strain than in T1F- strain Duguid et al., 1976
Conjuctival Similar number of infections and deaths for T1F+ and T1F- strain
Intraperitoneal Similar number of infections and deaths for T1F+ and T1F- strain
3. Enteritidis 1981 Temp: 37°C
Time: ?
Medium: Brain heart infusion
O2: Aerated
Shaking: No
The Naval
Aero-Medical
Reserve
Unit (NAMRU) strainmice (12–14 weeks old)
Oral Protective role of antiserum indicates that adherence of S. Enteritidis to the host cells was mediated by type 1 or by type 3 fimbriae Aslanzadeh and Paulissen, 1990
4. Typhimurium SR-11 (T1F+) and x4334- fim transposon mutant (T1F-) Temp: 37°C
Time: ?
Medium: Luria-Bertani or Mueller-Hinton
O2: ?
Shaking: No
BALB/c ♀
Mice (6–8 weeks old)
Oral Higher virulence of T1F- strain (lower LD50 and higher mortality) Lockman and Curtiss, 1992
Intraperitoneal No differences between tested strains
Oral- mixed
bacteria
challenge
Peyer’s patches, intestinal wall – higher amount of T1F- strainSpleen, liver, kidney – 2–3 days – higher amount of T1F- strainSpleen, liver, kidney- 4–5 day- higher amount of T1F+ strainBlood- higher amount of T1F- strain (increasing after each day
5. Enteritidis; Typhimurium 857, phage type 4 (SE)S986 (ST) (T1F+) Temp: ?
Time: 48 h
Medium: Nutrient broth
O2: ?
Shaking: No
Male Hooded Lister rats oral T1F+ bacteria can be detected in ileum after 6 days of infection Ewen et al., 1997
6. Typhimurium AJB3 ( SR11 derivate, T1F+); ABJ4 (T1F-) Temp: 37°C
Time: Overnight
Medium: Luria-Bertani
O2: ?
Shaking: ?
BALB/c ♀
Mice (6–8 weeks old)
oral T1F- strain is 3 times more virulent than T1F+ strain. van der Velden et al., 1998
7. Enteritidis LA5 (T1F+); EAV21 (T1F-) Temp: 37°C
Time: Overnight
Medium: Nutrient broth
O2: Aerobically
Shaking: Yes (Orbital shaking 225rpm)
SPF
White
Leghorn
chicks
(aged 18–24 h)
Collectively, SEF17, SEF21 and flagella fulfill a minor role in the early stages of colonization and invasion in young chicks, but are unnecessary for colonization of birds from the immediate environment Dibb-Fuller and Woodward, 2000
8. Enteritidis phage type 4 Temp: ?
Time: ?
Medium: ?
O2: ?
Shaking: ?
SPF
Chicken (SPAFAS Inc., Roanoke, IL)
No major role for SEF14, SEF17, or SEF21 fimbriae under the conditions tested. Rajashekara et al., 2000
9. Enteritidis LA5 Temp: 37°C
Time: 48 h
Medium: Nutrient broth
O2: ?
Shaking: No
Male Hooded Lister rats (19 days old) The fimbriate strain was preferentially removedfrom the gastrointestinal tract, allowing the mutantstrain to become predominant in the long term.
Lower mount of T1F-strain in spleen after 24h;
Lower mount of T1F-strain in liver after 24h;
Lower mount of T1F-strain in caecum after 24h and 48h
Naughton et al., 2001
10. Typhimurium 798-519’ (pig origin) (T1F+); Mutant 14 (ΔfimA; T1F-) Temp: ?
Time: ?
Medium: ?
O2: ?
Shaking: ?
ICR mice (Harlan) Oral-mixed bacteria challenge Higher amounts of T1F+ strains in caecum, ileum and colon Althouse et al., 2003
BALB/c Oral No statistically significant results
Pigs; Oral Faster clearance of T1F- strain from ileocecal junction and mid-ileum.
T1F+ strain was recovered in increasing numbers after 2 weeks in comparison to 1 week after challenge
11. Enteritidis S1400/94 (T1F+); ΔfimD of S1400/94 (T1F-) Temp: 37°C
Time: 20 h
Medium: Brain Heart Infusion
O2: ?
Shaking: Yes
non-Salmonella-vaccinated laying hens (ISA Warren Brown) (19 weeks old) Intravenous Higher amounts of T1F- strains in spleen after 14 and 21 daysHigher amounts of birds positive for T1F- strains in swabs: from vagina and isthmus after 21 days.
Higher amounts of egg shells contaminated with T1F+.
De Buck et al., 2004
12. Enteritidis ?? Temp: ?
Time: ?
Medium: ?
O2: ?
Shaking: ?
SHAVER 579 hens
(5 weeks old)
1 group was immunized twice with FimA protein
Oral significant reduction of duodenum colonization and persistence of Salmonella Enteritidis Kuczkowski et al., 2004
13. Enteritidis phage type 4, strain S1400/94; strain MB 1454 Temp: 37°C
Time: 20 h
Medium: Brain Heart Infusion
O2: ?
Shaking: Yes
non-Salmonella-vaccinated laying hens (ISA Warren Brown) (18 weeks old); 1 group was vaccinated with twice with purified T1F Intravenous Higher amounts of egg shells contaminated in non-vaccinated chickens.
Higher and longer colonization of oviducts in non-vaccinated chickens.
De Buck et al., 2005
14. Typhimurium 1402/84 (ClinicalIsolate) Temp: 37 °C
Time: 60 h
Medium: Colonizationfactor antigen (CFA) agar
O2: ?
Shaking: ?
Male albino Wistar rats (50–60 g);
One group of rats was immunized with purified T1F
Oral Immunization prevents from: Na+, Cl-, Ca2+ fluxes in intestines; cAMP, Prostaglandin E2 concentration changes in intestines; NADPH, G-6-PDH 6-PGDH changes in gut macrophages Verma et al., 2005
15. Enteritidis phage type 4, strain P125109 (T1F+); ΔfimA of P125109 (T1F-) Temp: ?
Time: ?
Medium: LB
O2: ?
Shaking: ?
SPF out-bred Rhode
Island Red chickens, 18-day-old
Oral No significant changes in caecal load after 3, 7, 10 days post-infection Clayton et al., 2008
16. Gallinarum isolate no. 589/02 (1,T1F+); ΔfimH of 589/02 (2, T1F-); 589/02 with fimH gene from S. Enteritidis (3, T1F+) Temp: 37°C
Time: five passages
Medium: Luria-Bertani
O2: ?
Shaking: No
Salmonella-free chicks (1-day-old) Oral FimH-dependent interactions of S. Gallinarum with chicken leukocytes are responsible for the increased virulence in chicksT1F- strain (2) had weak and delayed colonization of caecal tonsils, liver and spleen, didn’t colonize bursa of Fabricius.
T1F+ strain (3) didn’t colonize caecal tonsils, bursa of Fabricius, liver had weak and delayed colonization of spleen.
Kuźmińska-Bajor et al., 2012
17. Typhimurium SL1344 expressing various FimH variants Temp: ?
Time: Overnight
Medium: SB broth supplemented with 30 mg/ml chloramphenicol
O2: ?
Shaking: No
BALB/c mice
(6–8 week-old)
Oral No effect of FimH mutations on bacterial burdens inthe liver and spleen. Kisiela et al., 2012
18. Enteritidis JL12 Temp: 37°C
Time: 72h
Medium: Colonization factor antigen broth
O2: ?
Shaking: No
Salmonella-free Hy-Line white leghorn chickens; (1 day old); one group was immunized twice orally with liposome associated SEF21 gene Lower amounts of Salmonella in cecum and rectum after 4 weeks in immunized bacteria Pang et al., 2012
19. Enteritidis SD-2 Temp: ?
Time: ?
Medium: ?
O2: ?
Shaking: ?
BALB/c mice; Groups of mice were immunized with FimA protein and it’s derivates with mC3d extenstions Intraperitoneal Lower infection of mice immunized with FimA proteins constructs Musa et al., 2014
20. Enteritidis isolate no. 327 (T1F+); ΔfimH of 327 (T1F-) Temp: 37°C
Time: Five passages
Medium: Luria- Bertani broth
O2: ?
Shaking: No
BALB/c ♀
Mice (6–8 weeks old)
oral Fimbriated wild-type S. Enteritidis is less virulent than the non-fimbriated S. Enteritidis mutant strain Kuźmińska-Bajor et al., 2015

Temp., Temperature; O2, presence of oxygen during growth; T1F, type 1 fimbriae; “T1F+”, type 1 fimbriae expressing; “T1F-”, type 1 fimbriae non-expressing; “SPF”, specific pathogen free.