Risk factor profiles for gastric cancer prediction with respect to Helicobacter pylori: A study of a tertiary care hospital in Pakistan

Table 1 Score response categories of Likert scale questionnaire

Study variables/risk factors	Category	Consumption/behavior frequency in d/wk
Tooth brushing and miswak usage	Always	7
	Often	4-6
	Seldom	1-3
	Never	0
Consumption of chili, dairy products, rice, potatoes, red and processed meat, sweets, junk food	No	0
	Rarely	1-2
	Moderately	2-4
	Frequently	5-6
		Servings per day
Drinking black and green tea	Normal	1-2
	Moderate	3-4
	High	5-7
		Habits per day
Washing hands with soap before meal and after use of toilet	Always	7
	Often	4-6
	Seldom	1-3
	Never	0
Addiction and passive smoking	No	< 10 (In Pakistan smoking is common practice.)
	Yes	> 10
		Consumption of cooked food
Salt/sodium chloride consumption; Normal: 2300 mg/d; Low: 140 mg/serving; High: > 3400 mg/d[38]	No	Without salt (Patients with high blood pressure did not use salt in their food)
	Normal	Without adding salt
	Low	With additional pinch of salt/serving; 1 Pinch = 0.36 g or 360 mg
	High	After addition of several pinches of salt/serving

Table 2 Descriptive characteristics of the proband cohort groups and results of χ²/Fisher’s exact test (P value)

Factor	Categories	NGM	GDD	GC	P value	Significant
		% (number of patients/total number of patients)
Infection status	Negative	28 (14/50)	39 (100/260)	26 (8/31)	0.176	> 0.05
	Positive	72 (36/50)	62 (160/260)	74 (23/31)
Gender	Male	46 (23/50)	52 (136/260)	58 (18/31)	0.553	> 0.05
	Female	54 (27/50)	48 (124/260)	42 (13/31)
BMI	Normal, underweight	58 (29/50)	63 (163/260)	78 (24/31)	0.191	> 0.05
	Overweight, obese	42 (21/50)	37 (97/260)	23 (7/31)
Marital status	Married	78 (39/50)	80 (208/260)	87 (27/31)	0.580	> 0.05
	Single	22 (11/50)	20 (52/260)	13 (4/31)
Age	< 46	82 (41/50)	65 (170/260)	29 (9/31)	0.000	< 0.01
	> 45	18 (9/50)	35 (90/260)	71 (22/31)
Ethnic background	Federal	6 (3/50)	6 (16/260)	3 (1/31)	0.291f	> 0.05
	Lower punjab	16 (8/50)	15 (40/260)	13 (4/31)
	Kashmir	12 (6/50)	5 (14/260)	3 (1/31)
	Upper punjab	60 (30/50)	62 (161/260)	81 (25/31)
	Khyber pakhtunkhwa	6 (3/50)	11 (29/260)	0 (0/31)
Education level	Illiterate	18 (9/50)	35 (90/260)	48 (15/31)	0.013	< 0.05
	Literate	82 (41/50)	65 (170/260)	52 (16/31)
Medication	Antibiotics	44 (22/50)	33 (86/260)	32 (10/31)	0.132f	> 0.05
	PPI	22 (11/50)	36 (93/260)	45 (14/31)
	NSAID	12 (6/50)	4 (9/260)	3 (1/31)
	Others	8 (4/50)	10 (27/260)	3 (1/31)
	NIL	14 (7/50)	17 (45/260)	16 (5/31)
Income level	10.000	6 (3/50)	7 (19/260)	3 (1/31)	0.007f	< 0.05
	11.000-30.000	48 (24/50)	69 (178/260)	84 (26/31)
	> 30.000	46 (23/50)	24 (63/260)	13 (4/31)
Acid reflux	No	66 (33/50)	45 (116/260)	39 (12/31)	0.013	< 0.05
	Yes	34 (17/50)	55 (144/260)	61 (19/31)
Abdominal pain	No	54 (27/50)	25 (64/260)	10 (3/31)	0.000	< 0.01
	Yes	46 (23/50)	75 (196/260)	90 (28/31)
Heartburn	No	56 (28/50)	46 (119/260)	45 (14/31)	0.403	> 0.05
	Yes	44 (22/50)	54 (141/260)	55 (17/31)
Vomiting	No	64 (32/50)	41 (107/260)	16 (5/31)	0.000	< 0.01
	Yes	36 (18/50)	59 (153/260)	84 (26/31)
Bloating	No	74 (37/50)	41 (106/260)	39 (12/31)	0.000	< 0.01
	Yes	26 (13/50)	59 (154/260)	61 (19/31)
Black tea	Low	80 (40/50)	69 (178/260)	71 (22/31)	0.261	> 0.05
	High	20 (10/50)	32 (82/260)	29 (9/31)
Green tea	Low	70 (35/50)	70 (181/260)	65 (20/31)	0.837	> 0.05
	High	30 (15/50)	30 (79/260)	36 (11/31)
Chili consumption	Low	30 (15/50)	39 (102/260)	48 (15/31)	0.240	> 0.05
	High	70 (35/50)	61 (158/260)	52 (16/31)
Dairy product consumption	Low	36 (18/50)	32 (83/260)	32 (10/31)	0.853	> 0.05
	High	64 (32/50)	68 (177/260)	68 (21/31)
Fresh fruit & vegetable consumption	Low	28 (14/50)	18 (46/260)	23 (7/31)	0.222	> 0.05
	High	72 (36/50)	82 (214/260)	77 (24/31)
Rice consumption	Low	26 (13/50)	37 (94/260)	23 (7/31)	0.154	> 0.05
	High	74 (37/50)	64 (166/260)	77 (24/31)
Potato consumption	Low	32 (16/50)	40 (104/260)	32 (10/31)	0.422	> 0.05
	High	68 (34/50)	60 (156/260)	68 (21/31)
Red meat consumption	Low	54 (27/50)	47 (123/260)	55 (17/31)	0.543	> 0.05
	High	46 (23/50)	53 (137/260)	45 (14/31)
Processed meat consumption	Low	70 (35/50)	77 (199/260)	77 (24/31)	0.597	> 0.05
	High	30 (15/50)	24 (61/260)	23 (7/31)
Junk food consumption	Low	78 (39/50)	84 (218/260)	84 (26/31)	0.596	> 0.05
	High	22 (11/50)	16 (42/260)	16 (5/31)
Sweets consumption	Low	62 (31/50)	69 (178/260)	68 (21/31)	0.671	> 0.05
	High	38 (19/50)	32 (82/260)	32 (10/31)
High salt intake	No	16 (8/50)	31 (80/260)	23 (7/31)	0.081	> 0.05
	Yes	84 (42/50)	69 (180/260)	77 (24/31)
Overcrowding	Yes	54 (27/50)	42 (108/260)	55 (17/31)	0.129	> 0.05
	No	46 (23/50)	59 (152/260)	45 (14/31)
Oral hygiene	Yes	84 (42/50)	87 (226/260)	77 (24/31)	0.340	> 0.05
	No	16 (8/50)	13 (34/260)	23 (7/31)
Hand hygiene	Yes	98 (49/50)	99 (256/260)	97 (30/31)	0.437f	> 0.05
	No	2 (1/50)	2 (4/260)	3 (1/31)
House insects	No	0 (0/50)	2 (4/260)	0 (0/31)	1.00f	> 0.05
	Yes	100 (50/50)	99 (256/260)	100 (31/31)
Household animals	No	62 (31/50)	69 (180/260)	22/31 (71)	0.570	> 0.05
	Yes	38 (19/50)	31 (80/260)	29 (9/31)
Potable water source	In	4 (2/50)	14 (37/260)	13 (4/31)	0.136	> 0.05
	Out	96 (48/50)	86 (223/260)	87 (27/31)
Sewage system	Proper	0 (0/50)	3 (7/260)	7 (2/31)	0.196f	> 0.05
	Damaged	100 (50/50)	97 (253/260)	94 (29/31)
Addiction	No	66 (33/50)	68 (176/260)	71 (22/31)	0.897	> 0.05
	Yes	34 (17/50)	32 (84/260)	29 (9/31)
Passive smoking	No	58 (29/50)	62 (162/260)	65 (20/31)	0.806	> 0.05
	Yes	42 (21/50)	38 (98/260)	36 (11/31)
Physical activity	Low	80 (40/50)	80 (208/260)	77 (24/31)	0.944	> 0.05
	High	20 (10/50)	20 (52/260)	23 (7/31)
Family history of stomach disease	No	74 (37/50)	72 (187/260)	84 (26/31)	0.361	> 0.05
	Yes	26 (13/50)	28 (73/260)	16 (5/31)
Type 2 diabetes	No	94 (47/50)	92 (238/260)	97 (30/31)	0.680f	> 0.05
	Yes	6 (3/50)	9 (22/260)	3 (1/31)

^fFor the expected counts less than 5, P values were obtained from Fisher’s exact test. Significant discriminators are marked in bold. BMI: Body mass index; NGM: Normal gastric mucosa, GC: Gastric cancer; GDD: Gastroduodenal diseases; NSAIDS: Non-steroidal anti-inflammatory drugs; PPI: Proton pump inhibitors.

Table 3 Factors associated with gastroduodenal diseases and gastric cancer vs normal gastric mucosa

Variable	Category	GDD/NGM		GC/GDD		GC/NGM
		Significant	Odds ratio (95%CI)	Significant	Odds ratio (95%CI)	Significant	Odds ratio (95%CI)
Age	< 46	0.078	0.45 (0.18-1.09)	0.00	0.19 (0.08-0.46)	0.000	0.08 (0.02-0.29)
	> 45		Reference		Reference		Reference
Education level	Illiterate	0.404	1.44 (0.61-3.43)	0.609	1.25 (0.53-2.95)	0.325	1.81 (0.56-5.86)
	Literate		Reference		Reference		Reference
Income level	Low	0.767	1.25 (0.29-5.44)	0.847	0.79 (0.07-8.61)	0.992	0.99 (0.06-15.29)
	Middle	0.028	2.32 (1.09-4.91)	0.218	2.1 (0.65-6.8)	0.022	4.86 (1.25-18.84)
	Upper		Reference		Reference		Reference
Vomiting	No	0.088	0.54 (0.27-1.09)	0.599	1.26 (0.53-3.01)	0.003	0.16 (0.05-0.53)
	Yes		Reference		Reference		Reference
Bloating	No	0.012	0.37 (0.17-0.8)	0.019	0.29 (0.1-0.81)	0.184	0.47 (0.15-1.44)
	Yes		Reference		Reference		Reference
Abdominal pain	No	0.075	0.52 (0.25-1.07)	0.092	0.32 (0.09-1.2)	0.016	0.17 (0.04-0.72)
	Yes		Reference		Reference		Reference
Acid reflux	No	0.220	0.63 (0.3-1.32)	0.944	0.97 (0.41-2.3)	0.379	0.61 (0.2-1.83)
	Yes		Reference		Reference		Reference
Medication	Antibiotics	0.686	0.81 (0.29-2.25)	0.519	1.51 (0.43-5.24)	0.803	1.22 (0.25-5.85)
	PPI	0.520	1.45 (0.47-4.44)	0.139	2.48 (0.74-8.26)	0.118	3.58 (0.72-17.76)
	NSAIDS	0.020	0.16 (0.03-0.75)	0.936	1.1(0.1-11.93)	0.212	0.18 (0.01-2.68)
	Others	0.512	1.64 (0.38-7.12)	0.598	0.54 (0.06-5.3)	0.928	0.88 (0.06-12.75)
	Nil		Reference		Reference		Reference
High salt intake	No	0.215	1.77 (0.72-4.37)	0.215	0.55 (0.21-1.42)	0.965	0.97 (0.27-3.49)
	Yes		Reference		Reference		Reference

Nine variables were added to the multinomial logistic regression analysis with P < 0.05 (marked in bold). GDD: Gastroduodenal diseases; NGM: Normal gastric mucosa; NSAIDS: Non-steroidal anti-inflammatory drugs; PPI: Proton pump inhibitors; Sign.: Significant.

Table 4 Correlation of histopathological variables, antral vs corpus biopsies (P < 0.01)

Variable	Spearman correlation coefficient
Helicobacter pylori load	0.991
Neutrophil infiltration	1.000
Mononuclear cell infiltration	0.942
Atrophy	0.969
Atypia	0.881
Metaplasia	1.000
Dysplasia	0.786
Atrophic score (OLGA)	0.951
Metaplasia score (OLGIM)	1.000
Inflammation	0.930
Gastritis	0.921
Ulceration	1.000
Eosinophilia	1.000

OLGA: Operative link for gastritis assessment; OLGIM: Operative link on gastric intestinal metaplasia.

Table 5 Gastric cancer associated risk factors chosen for prediction model building

Risk factors	Ref.
H. pylori infection	[1]
Family history	[4]
PPI	[8,20,21]
Addiction (smoking)	[13]
Passive smoking	[44,64]
Sewage system (cockroaches/H. pylori)	[31]
Potable water source (H. pylori)	[30]
Exercise/fruits and vegetables	[7,8]
BMI	[16]
Gender (male)	[12]
Age	[11]
High salt intake/green and black tea	[7,58]
Chili consumption	[24]
Processed food (meat) consumption	[19,40]
Sugar intake	[17]
Excess of rice and potatoes	[18]
Miswak usage	[23]

BMI: Body mass index; PPI: Proton pump inhibitors; H. pylori: Helicobacter pylori.

Table 6 Dataset used to train the gastric cancer prediction model

Clinical findings	Total samples	Training dataset	Test dataset
NGM	50	35	15
Gastritis	232	162	70
Ulcer	30	21	9
GC	29	20	8
Total	341	239	102

GC: Gastric cancer; NGM: Normal gastric mucosa.