Helicobacter pylori's virulence and infection persistence define pre-eclampsia complicated by fetal growth retardation

doi:10.3748/wjg.v17.i47.5156

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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

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World J Gastroenterol. Dec 21, 2011; 17(47): 5156-5165
Published online Dec 21, 2011. doi: 10.3748/wjg.v17.i47.5156

Table 1 Clinical characteristics of study populations (continuous variables)

Variable	Controls (n = 49) Median (25th-75th)	PE-only (n = 17) Median (25th-75th)	PE FGR (n = 32) Median (25th-75th)	FGR-only (n = 13) Median (25th-75th)	P value¹
Maternal age at delivery (yr)	30 (28-33)⁴	29 (24-32)	30 (26-34)⁷	25 (24-26)⁴⁷	⁴< 0.001; ⁷0.002
Gestational age at delivery (wk)	40 (39-41)²³⁴	30 (28-31)²⁵⁶	32 (31-34)³⁵	34 (32-39)⁴⁶	²³⁴< 0.001; ⁵0.045; ⁶0.009
Neonatal weight (g)	3380 (3170-3700)²³⁴	1140 (1045-1570)²	1278 (920-1668)³	1600 (1060-2730)⁴	²³⁴< 0.001
Placental weight (g)	600 (500-650)²³⁴	300 (240-410)²	280 (215-360)³	345 (300-470)⁴	²³⁴< 0.001
Systolic blood pressure (mmHg)	120 (110-120)²³	160 (150-160)²⁶	150 (148-160)³⁷	120 (120-125)⁶⁷	²³⁶⁷< 0.001
Diastolic blood pressure (mmHg)	75 (70-80)²³	100 (100-100)²⁶	100 (95-105)³⁷	77 (75-80) ⁶⁷	²³⁶⁷< 0.001
Proteinuria (g/24 h)	0 (0-0)²³	2.21 (1.52-3)²⁶	1.34 (0.79-2.38)³⁷	0 (0-0)⁶⁷	²³⁶⁷< 0.001

¹P values were calculated by non-parametric Kruskal-Wallis H test, with post-hoc analysis by Mann-Whitney U test.

²Comparison between controls and PE-only group;

³Comparison between Controls and PE FGR group;

⁴Comparison between controls and FGR-only group;

⁵Comparison between PE-only and PE FGR groups;

⁶Comparison between PE-only and FGR-only groups;

⁷Comparison between PE-only and FGR-only groups. PE: Pre-eclampsia; FGR: Fetal growth retardation.

Table 2 Clinical characteristics of study populations (categorical variables) n (%)

Variable		Controls (n = 49)	PE-only (n = 17)	PE FGR (n = 32)	FGR-only (n = 13)	P value⁵
Cesarean section delivery		15 (30.6)⁶⁷⁸	16 (94.1)⁶	29 (90.6)⁷	9 (69.2)⁸	⁶⁷< 0.001; ⁸0.022
Neonatal sex	Male	19 (38.8)⁷	7 (41.2)	20 (62.5)⁷	6 (46.2)	⁷0.043
	Female	30 (61.2)	10 (58.8)	12 (37.5)	7 (53.8)	NS
Nulliparae		31 (63.3)⁶⁷	16 (94.1)⁶	27 (84.4)⁷	10 (76.9)	⁶0.015; ⁷0.047
Maternal risk factors		4 (8.2)	2 (11.8)¹	8 (25.0)	1 (7.7)	NS
	Autoimmune diseases	1 (2.0)	2 (11.8)	4 (12.5)	0 (0)	NS
	Cardiovascular diseases	3 (6.1)	1 (5.9)	4 (12.5)	1 (7.7)	NS
Family risk factors		20² (40.8)⁶	12³ (70.6)⁶¹⁰	13⁴ (40.6)	2 (15.4)¹⁰	⁶0.049; ¹⁰0.004
	Hypertension	9 (18.4)	8 (47.1)	10 (31.3)	2 (15.4)	NS
	Diabetes	10 (20.4)	3 (17.6)	5 (15.6)	0 (0)	NS
	Cardiovascular diseases	5 (10.2)	2 (11.8)	3 (9.4)	0 (0)	NS
Other complications:	FGR	0 (0.0)⁷⁸	0 (0.0)⁹¹⁰	32 (100)⁷⁹	13 (100)⁸¹⁰	⁷⁸⁹¹⁰< 0.001
	Early onset PE	-	16 (94.1)	29 (90.6)	-	NS
	Severe PE	-	13 (76.5)	19 (59.4)	-	NS
	HELLP syndrome	-	3 (17.6)	2 (6.3)	-	NS

¹One patient presented both maternal risk factors (autoimmune and cardiovascular diseases);

²Four patients presented two family risk factors (3 hypertension and diabetes; 1 diabetes and cardiovascular disease);

³One patient presented two family risk factors (hypertension and diabetes);

⁴Five patients presented two family risk factors (4 hypertension and diabetes; 1 hypertension and cardiovascular disease).

⁵P values were calculated by chi-square test (χ²).

⁶Comparison between controls and PE-only group;

⁷Comparison between controls and PE FGR group;

⁸Comparison between controls and FGR-only group;

⁹Comparison between PE-only and PE FGR groups;

¹⁰Comparison between PE-only and FGR-only groups. NS: Non significant; PE: Pre-eclampsia; FGR: Fetal growth retardation; HELLP: Hemolysis-elevated liver enzymes-low platelets.

Table 3 Leukocytes, platelets and liver enzymes in normal and pathological pregnancies

Variable	Normal values in Italian female population range	Controls (n = 49) Median (25th-75th)	All PE (n = 49) Median (25th-75th)	PE-only (n = 17) Median (25th-75th)	PE FGR (n = 32) Median (25th-75th)	FGR-only (n = 13) Median (25th-75th)	P value²
Total leukocyte count (1 × 10³/μL)	4.00-11.00	10.56 (9.21-11.65)³⁷⁵⁶	12.03 (10.69-14.1)³	12.34 (10.71-13.83)⁵	11.83 (10.2-14.51)⁶	12.27 (11.21-13.47)⁷	³0.004; ⁷0.045
							⁵0.007; ⁶0.024
Neutrophils (1 × 10³/μL)		8.27 (7.45-9.19)	10.09 (7.30-11.6)	10.15 (7.81-12.10)	9.92 (7.30-11.51)	9.34 (6.27-9.48)	NS
(%)	45.0-73.0	75.8 (68.1-78.8)	76.7 (68.37-87.1)	80 (72.5-90.1)	72.1 (68.2-83.6)	64.4 (57.3-77.3)	NS
Lymphocytes (1 × 10³/μL)		2.02 (1.68-2.26)	2.08 (1.3-3.06)	1.86 (1.22-2.34)	2.08 (1.31-3.07)	3.15 (2.13-3.79)	NS
(%)	19.0-47.0	18.7 (14-23.5)	17.4 (10.8-22.43)	14.55 (8.9-18.15)⁸	18.8 (11.1-23.2)	25.9 (17.4-34.3)⁸	⁸0.047
Monocytes (1 × 10³/μL)		0.54 (0.47-0.74)	0.59 (0.3-0.85)	0.61 (0.25-0.81)	0.58 (0.3-0.88)	0.89 (0.54-1.05)	NS
(%)	3.0-9.0	5.4 (4.5-6)	5.3 (3-7.3)	4.15 (2.15-7.75)	5.4 (3.5-7.3)	6.1 (4.9-7.9)	NS
Eosinophils (1 × 10³/μL)		0.15 (0.09-0.19)³	0.05 (0.02-0.1)³	0.04 (0.02-0.11)	0.05 (0.03-0.1)	0.17 (0.03-0.33)	³0.028
(%)	0.2-4.4	1.2 (0.9-1.8)³	0.5 (0.2-0.8)³	0.35 (0.1-0.8)	0.5 (0.2-0.8)	1.7 (0.2-2.4)	³0.020
Basophils (1 × 10³/μL)		0.02 (0.01-0.03)	0.02 (0.01-0.03)	0.03 (0.01-0.03)	0.02 (0.01-0.03)	0.01 (0-0.04)	NS
(%)	0.1-1.3	0.2 (0.1-0.3)	0.2 (0.1-0.3)	0.2 (0.15-0.25)	0.2 (0.1-0.3)	0.1 (0-0.3)	NS
Platelets (1 × 10³/μL)	150-400	219 (170-240)⁵	187 (126-228)	170 (111-214)⁵⁸	191 (143-234)	235 (177-285)⁸	⁵0.024; ⁸0.031
Platelets¹ (1 × 10³/μL)	150-400	219 (170-240)	191 (161-234)	180.5 (154-228)	191 (165-242)	235 (177-285)	NS
ALT (U/L)	< 34	15 (10-19)³⁵	23 (14-46)³	26 (19-150)⁵⁸	19.5 (13.5-35)	14 (10-21.5)⁸	³0.006; ⁵0.002; ⁸0.026
ALT¹ (U/L)	< 34	15 (10-19)³	20 (14-31)³	25 (15-46)	18 (13-27)	14 (10-21.5)	³0.023
AST (U/L)	< 31	17.5 (14-19)³	21 (16-39)³⁴	25 (16-123)⁸	20 (16-35.5)⁹	14 (12-18)⁴⁸⁹	³0.029; ⁴0.018; ⁸0.031; ⁹0.026
AST¹ (U/L)	< 31	17.5 (14-19)	19 (15.5-33)	19 (15-39)	18.5 (16-32)	14 (12-18)	NS

¹Hemolysis-elevated liver enzymes-low platelets cases excluded;

²P values were calculated by non-parametric Kruskal-Wallis H test, with post-hoc analysis by Mann-Whitney U test.

³Comparison between controls and all PE group;

⁴Comparison between all PE and FGR-only groups;

⁵Comparison between controls and PE-only group;

⁶Comparison between controls and PE FGR group;

⁷Comparison between controls and FGR-only group;

⁸Comparison between PE-only and FGR-only groups;

⁹Comparison between PE-only and FGR-only groups. ALT: Alanine aminotransferase; AST: Aspartate aminotransferase; NS: Non significant; PE: Pre-eclampsia; FGR: Fetal growth retardation.

Table 4 Seropositivity against Helicobacter pylori, cytotoxin-associated antigen A, vacuolating cytotoxin A, ureases A, C, E and H, heat shock protein B and flagellin A n (%)

	Controls (n = 49)	All PE (n = 49)	PE-only (n = 17)	PE FGR (n = 32)	FGR-only (n = 13)	P value¹²	Odds ratio¹ (95% CI)
Helicobacter pylori	21 (42.9)³⁵	42 (85.7)³	12 (70.6)	30 (93.8)⁵	6 (46.2)	³⁵< 0.001	³9.22 (2.83-30.04)
							⁵35.56 (5.22-242.43)
CagA	11 (22.4)³⁴⁵	40 (81.6)³	11 (64.7)⁴	29 (90.6)⁵	5 (38.5)	³⁵< 0.001	³17.66 (5.25-59.49)
						⁴0.038	⁴5.20 (1.09-24.69)
							⁵54.97 (9.24-326.88)
VacA	20 (40.8)³⁵	37 (75.5)³	9 (52.9)	28 (87.5)⁵	6 (46.2)	³0.005	³4.89 (1.62-14.73)
						⁵< 0.001	⁵19.64 (3.75-102.98)
HspB	15 (30.6)	21 (42.9)	5 (29.4)	16 (50.0)	6 (46.2)	NS
FlagA	13 (26.5)	22 (44.9)	6 (35.3)	16 (50.0)	5 (38.5)	NS
UreA	10 (20.4)	13 (26.5)	4 (23.5)	9 (28.1)	3 (23.1)	NS
UreC	13 (26.5)³⁵	19 (38.8)³	4 (23.5)	15 (46.9)⁵	4 (30.8)	³0.042	³2.84 (1.04-7.75)
						⁵0.018	⁵4.02 (1.27-12.80)
UreE	12 (24.5)³⁵	26 (53.1)³	8 (47.1)	18 (56.3)⁵	3 (23.1)	³0.004	³4.41 (1.59-12.26)
						⁵0.003	⁵6.29 (1.88-21.04)
UreH	8 (16.3)	13 (26.5)	5 (29.4)	8 (25.0)	4 (30.8)	NS

¹Adjusted for maternal age at delivery, pre-pregnancy body mass index, parity, and presence of maternal and family risk factors;

²P values were calculated by χ² test;

³Comparison between controls and all PE group;

⁴Comparison between controls and PE-only group;

⁵Comparison between controls and PE FGR group. CI: Confidence intervals; NS: Non significant; PE: Pre-eclampsia; FGR: Fetal growth retardation; CagA: Cytotoxin-associated antigen A; VacA: Vacuolating cytotoxin A; HspB: Heat shock protein B; FlagA: Flagellin A; Ure: Ureases.

Table 5 Cytotoxin-associated antigen A/vacuolating cytotoxin A dual seropositivity n (%)

	Controls (n = 49)	All PE (n = 49)	PE-only (n = 17)	PE FGR (n = 32)	FGR-only (n = 13)	P value¹²	Odds ratio¹ (95% CI)
CagA+VacA+	11 (22.4)³⁴	37 (75.5)³	9 (52.9)	28 (87.5)⁴	5 (38.5)	³< 0.001	12.10 (3.76-38.91)
						⁴0.001	45.44 (7.79-265.18)
CagA-VacA+	9 (18.4)	0 (0)	0 (0)	0 (0)	1 (7.7)	NS
CagA+VacA-	0 (0.0)	3 (6.1)	2 (11.8)	1 (3.1)	0 (0.0)	NS
CagA-VacA-	29 (59.2)³⁴	9 (18.4)³	6 (35.3)	3 (9.4)⁴	7 (53.8)	³0.001	0.13 (0.04-0.42)
						⁴< 0.001	0.04 (0.01-0.22)

¹Adjusted for maternal age at delivery, pre-pregnancy body mass index, parity, and presence of maternal and family risk factors;

²P values were calculated by chi-square test (χ²);

³Comparison between controls and all PE group;

⁴Comparison between controls and PE FGR group. CI: Confidence intervals; NS: Non significant; CagA: Cytotoxin-associated antigen A; VacA: Vacuolating cytotoxin A; PE: Pre-eclampsia; FGR: Fetal growth retardation.

Table 6 Hematological values and cytotoxin-associated antigen A/vacuolating cytotoxin A antigens

Variables	Normal values in Italian female population range	CagA-VacA- (n = 45) Median (25th-75th)	CagA-VacA+ (n =10) Median (25th-75th)	CagA+VacA- (n = 3) Median (25th-75th)	CagA+VacA+ (n = 53) Median (25th-75th)	P value²
Total leukocyte count (1 × 10³/μL)	4.00-11.00	12.02 (10.6-13.13)³	8.95 (7.75-10.5)³⁵⁶	14.1 (12.4-16.34)⁵	11.27 (9.62-13.64)⁶	³0.003; ⁶0.012; ⁵0.014
Neutrophils (1 × 10³/μL)		10.02 (8.88-11.40)	7.45 (4.87-9.48)	12.75 (11.03-14.48)	8.43 (6.9-10.5)	NS
(%)	45.0-73.0	78.8 (67.05-88.85)	71.9 (68.1-77.3)	83.4 (78.2-88.6)	72.05 (67.4-80)	NS
Lymphocytes (1 × 10³/μL)		1.72 (1.11-2.85)	2.13 (1.68-2.13)	1.61 (0.93-2.28)	2.34 (1.63-3.07)	NS
(%)	19.0-47.0	15.3 (8.9-23.2)	20.6 (17.4-23.5)	10.95 (5.7-16.2)	18.75 (14-23.3)	NS
Monocytes (1 × 10³/μL)		0.57 (0.26-0.89)	0.54 (0.43-0.6)	0.78 (0.68-0.88)	0.6 (0.44-0.84)	NS
(%)	3.0-9.0	4.75 (2.15-6.85)	5.2 (4.9-6)	5.1 (4.8-5.4)	5.81 (4.3-7.4)	NS
Eosinophils (1 × 10³/μL)		0.05 (0.02-0.18)	0.09 (0.03-0.21)	0.06 (0.03-0.08)	0.06 (0.03-0.15)	NS
(%)	0.2-4.4	0.55 (0.1-1.45)	1.2 (0.2-2)	0.4 (0.2-0.6)	0.58 (0.3-1.17)	NS
Basophils (1 × 10³/μL)		0.01 (0-0.02)	0.03 (0.01-0.03)	0.02 (0.02-0.03)	0.03 (0.01-0.04)	NS
(%)	0.1-1.3	0.1 (0-0.2)	0.2 (0.2-0.3)	0.15 (0.1-0.2)	0.2 (0.2-0.3)	0.002
Platelets¹ (1 × 10³/μL)	150-400	222 (169-249)	175 (154-209.5)	214 (210-228)	191 (166-242)	NS
ALT¹ (U/L)	< 34	16 (12.5-26)⁴	11 (9-12)⁵	32 (30-178)⁴⁵⁷	17 (11.5-24)⁷	⁴0.020; ⁵0.025; ⁷0.023
AST¹ (U/L)	< 31	18 (15.5-23.5)	13 (12-19)	58 (15-143)	18 (14.5-26)	NS

¹Hemolysis-elevated liver enzymes-low platelets cases excluded;

²P values were calculated by non-parametric Kruskal-Wallis H test, with post-hoc analysis by Mann-Whitney U test;

³Comparison between CagA-VacA- and CagA-VacA+ groups;

⁴Comparison between CagA-VacA- and CagA+VacA- groups;

⁵Comparison between CagA-VacA+ and CagA+VacA- groups;

⁶Comparison between CagA-VacA+ and CagA+VacA+ groups;

⁷Comparison between CagA+VacA- and CagA+VacA+ groups. CagA: Cytotoxin-associated antigen A; VacA: Vacuolating cytotoxin A; ALT: Alanine aminotransferase; AST: Aspartate aminotransferase; NS: Non significant.

Citation: Cardaropoli S, Rolfo A, Piazzese A, Ponzetto A, Todros T. Helicobacter pylori's virulence and infection persistence define pre-eclampsia complicated by fetal growth retardation. World J Gastroenterol 2011; 17(47): 5156-5165
URL: https://www.wjgnet.com/1007-9327/full/v17/i47/5156.htm
DOI: https://dx.doi.org/10.3748/wjg.v17.i47.5156