Helicobacter pylori: A foodborne pathogen?

Table 1 Studies evaluating the survival of Helicobacter pylori in artificially contaminated foods

Year	Food	Method	Observations	Ref.
1998	Sterilized milk	Bacterial count on chocolate agar	10 d at 4 °C	Fan et al[54]
			3 d at 25 °C
2001	Pasteurized milk water tofu, tofu, yogurt, lettuce and chicken	Bacterial count on tryptic soy agar, non-selective Wilkins-Chalgren Anaerobe blood agar and selective Wilkins-Chalgren Anaerobe blood agar	from 5 to 7 d in pasteurized milk, tofu and water tofu at 4 °C	Poms et al[26]
			for up to 2 d in lettuce and raw chicken at 4 °C
			for up to 1 d in yogurt at 4 °C
2000	Ground beef packaged in vacuum and air	Bacterial count on H. pylori special peptone agar	6 d in ground beef packaged in air at 4 °C	Stevenson et al[55]
			3-6 d in ground beef packaged in vacuum at 4 °C
			3 d in ground beef packaged in air and in vacuum at -18 °C
2002	Ground beef, sterile milk, and apple and orange juices	Bacterial count on brain heart infusion agar and horse serum	7 d in ground beef at 4 °C	Jiang et al[56]
			11 d in irradiated ground beef at 4 °C
			6 d in sterile milk at 4 °C
			1 d in apple and orange juice at 4 °C and 25 °C
2004	Lettuce and carrots	Bacterial count on Helicobacter special peptone agar and Columbia blood agar	3 d in lettuce at 8 °C	Gomes et al[57]
			5 d in sterilized carrot at 8 °C
			3 d in sanitized carrot at 8 °C
2007	Sterile milk and pasteurized milk	Bacterial count on Wilkins-Chalgren anaerobe agar	12 d in sterile milk at 4 °C	Quaglia et al[53]
			9 d in pasteurized milk at 4 °C
2010	Spinach	Bacterial count on brucella blood agar, Wilkins-Chalgren anaerobe blood agar	6 d at 8 °C	Buck et al[58]
2011	Traditional Turkish fermented sausage (sucuk)	Bacterial count on Wilkins-Chalgren anaerobe blood agar	7 d	Guner et al[59]
2017	Spring onion, cabbage, lettuce and spinach	Bacterial count on non-selective Blood base agar with 5% horse blood	3 d in spring onion, lettuce and spinach	Ng et al[60]
			4 d in cabbage stored at 4 °C

Table 2 Studies evaluating the occurrence of Helicobacter pylori in foods

Year	Food	Method	Number of samples n	Observations	Ref.
2001	Raw sheep milk	Culture and PCR	63 raw sheep milk	60% PCR positive samples	Dore et al[65]
				2.6% culture positive samples
2002	Raw and pasteurized cow milk	Semi nested PCR, culture method and electron microscopy	18 raw cow milk	Raw milk: 72.2% semi-nested PCR positive samples; 1 culture positive sample	Fujimura et al[66]
			20 pasteurized milk	Pasteurized milk: 55% semi-nested PCR positive samples
2002	Raw sheep milk	Culture	440 raw sheep milk	0% positive samples	Turutoglu et al[74]
2008	Raw goat, sheep, and cow milks	Nested-PCR	160 raw goat milk	25.6% positive goat milk	Quaglia et al[71]
			130 raw sheep milk	33% positive sheep milk
			110 raw cow milk	50% positive cow milk
2008	Raw chicken and ready- to- eat raw tuna	Multiplex PCR	11 raw chicken	36% positive raw chicken	Meng et al[77]
			18 ready-to-eat raw tuna	44% positive ready-to-eat raw tuna
2011	Raw cow milk	FISH	20	20% positive samples	Angelidis et al[67]
2012	Raw cow, sheep, goat, buffalo and camel milks	PCR	75 raw cow milk	16.00% positive cow milk	Rahimi et al[68]
			58 raw sheep milk	13.79% positive sheep milk
			42 raw goat milk	4.76% positive goat milk
			20 raw buffalo milk	13.33% positive camel milk
			15 raw camel milk	20.00% positive buffalo milk
2014	Milk and traditional dairy products	Culture and PCR	120 raw cow milk	16.6% positive cow milk	Mousavi et al[69]
			100 raw goat milk	28% positive goat milk
			100 raw sheep milk	35% positive sheep milk
			80 raw buffalo milk	15% positive buffalo milk
			60 raw camel milk	13.3% positive camel milk
			60 raw donkey milk	0% positive donkey milk
			100 cheese	30% positive cheese
			100 butter	15% positive cream
			100 cream	5% positive butter
			100 ice cream	27% positive ice cream
2014	Vegetables and salad	Culture and PCR	60 salad	16.6% positive salad	Atapoor et al[81]
			40 basil	12.5% positive basil
			40 radish	7.5% positive radish
			40 leek	20% positive leek
			80 spinach	6.25% positive spinach
			80 lettuce	13.75% positive lettuce
			120 parsley	6.6% positive parsley
2014	Washed and unwashed vegetables	Culture and PCR	430 washed and unwashed vegetable	13.72% positive vegetables and salads	Yahaghi et al[80]
2015	Raw cow, sheep, goat, buffalo and camel milks	PCR	75 raw cow milk	16.00% positive cow milk	Talaei et al[72]
			58 raw sheep milk	13.79% positive sheep milk
			42 raw goat milk	4.76% positive goat milk
			20 raw buffalo milk	13.33% positive camel milk
			15 raw camel milk	20.00% positive buffalo milk
2015	Raw cow milk	Culture and nested PCR	50 raw cow milk	22% positive cow milk	Osman et al[73]
2015	Raw cow milk	Culture and nested PCR	163 raw cow milk	0% positive cow milk	Bianchini et al[75]
2016	Raw cow, sheep, goat, buffalo and camel milks and meats	Culture and PCR	420 raw milk	21.90% positive raw milk	Saedi et al[70]
			400 raw meat	26.25% positive meat
2016	Ready-to-eat food	Culture and PCR	550 ready-to-eat food	13.45% positive ready-to-eat food	Hemmatinezhad et al[78]
2016	Ready-to-eat food and minced meat	Culture and PCR	60 ready-to-eat fish	15% positive ready-to-eat fish	Ghorbani et al[79]
			60 ham	8.33% positive ham
			40 chicken sandwich	5% positive chicken sandwich
			40 vegetable sandwich	45% positive vegetable sandwich
			50 meat sandwich	20% positive meat sandwich
			50 minced meat	32% positive minced meat
2017	Hamburger and minced meat	Culture and nested PCR	80 hamburger	1.42% positive hamburger	Gilani et al[76]
			70 minced-meat	12.5% positive minced-meat

Table 3 Studies evaluating the occurrence and survival of Helicobacter pylori in water

Year	Water and study type	Method	Observations	Ref.
1993	Survival of H. pylori in artificially contaminated sterile river water	Culture	Culture up to 48 h	Shahamat et al[118]
		Autoradiography
1996	Occurrence of H. pylori in 48 water samples: 30 from municipal water system, 14 from community taps, 4 from brick tanks or plastic barrels of different households	IMS and PCR	50% PCR positive samples	Hulten et al[101]
1997	Study on H. pylori resistance to chlorination	Culture	H. pylori were readily inactivated by free chlorine	Johnson et al[117]
1999	Occurrence of H. pylori in water from rivers and ponds	IMS and nested PCR	H. pylori-specific DNA was detected in samples	Sasaki et al[103]
1999	Occurrence of H. pylori in water from delivery truck and two lakes	Nested PCR and Southern blot hybridization	PCR positive samples from truck	McKeown et al[105]
			PCR positive samples from two lakes
2001	Occurrence of H. pylori in 10 seawater samples, 10 river water samples, 10 tap water samples, 6 well water samples	IMS, real-time PCR and nested PCR	2 PCR positive samples of well water	Horiuchi et al[127]
2001	Occurrence of H. pylori in 139 ground water samples	PCR and Southern blot hybridization	69% positive samples	Mazari-Hiriart et al[104]
2002	Occurrence of H. pylori in raw municipal wastewater	IMS, culture and PCR	23 out of 37 isolated strains were confirmed to be H. pylori	Lu et al[106]
			11 out of 23 strains of H. pylori demonstrated vacA gene heterogeneity
2002	Study on the susceptibility of H. pylori to chlorine, monochloramine, and ozone compared to that of Escherichia coli	Culture	H. pylori was more resistant than E. coli to chlorine and ozone but not monochloramine	Baker et al[116]
2004	Occurrence of H. pylori in water and biofilms: 11 samples from domestic proprieties, 7 samples from educational properties and from hydrants, and samples from reservoirs and water meters of 3 water utilities	Culture, IMS and PCR	All cultures were negative 26% PCR positive sample with the highest frequency in biofilm	Watson et al[120]
2004	Occurrence of H. pylori in seawater	Nested-PCR	H. pylori DNA only detected in fractionated water samples containing zooplanktonic organisms	Cellini et al[130]
2005	Occurrence of H. pylori in seawater	Filtration (200 mm, filter), culture and PCR	H. pylori was only isolated from fractionated water samples containing large zooplanktonic organisms	Cellini et al[131]
2005	Occurrence of H. pylori in 36 seawater samples	Culture and PCR	30 positive samples	Carbone et al[132]
2006	Study on the ability of H. pylori to adhere on different water-exposed abiotic surfaces	Scanning electron microscope	H. pylori was able to adhere to all substrates tested	Azevedo et al[123]
2007	Study on the ability of H. pylori to adhere to stainless steel 304 in different environmental conditions	Epifluorescence microscopy	H. pylori was able to adhere to stainless steel 304	Azevedo et al[124]
2007	Study on the resistance of H. pylori to chlorination	Culture, FISH, PCR and RT-PCR	Culture until 5 min	Moreno et al[115]
			FISH viable cells until 3 h
			PCR samples positive after 24 h
			RT-PCR positive after 24 h
2007	Survival of H. pylori in spiked bottled mineral water (drinking water)	Culture epifluorescence microscopy and PCR	Culture until 5 d	Queralt et al[114]
			Cell viability until 14 d
2007	Survival of H. pylori in spiked chlorinated filtered water (drinking water)	Culture, FISH and PCR	Culture until 5 min	Monero-Mesonero et al[115]
			FISH viable cells until 3 h
			PCR positive after 24 h
			RT-PCR after 24 h
2009	Occurrence of H. pylori in 75 drinking and environmental water samples and 21 natural water biofilms samples	Real-time PCR	0% positive samples	Janzon et al [129]
2010	Occurrence of H. pylori in 198 drinking water samples	Culture	10 out of 469 isolated strains were confirmed H. pylori	Al-Sulami et al[109]
2011	Occurrence of H. pylori in 137 seawater samples	PCR	21% of the samples were positive for H. pylori	Twing et al[134]
2013	Occurrence of H. pylori in 50 tap water samples, 35 dental units’ water samples, and 40 bottled mineral water samples	Culture and PCR	2 positive tap water samples	Bahrami et al[110]
			2 positive water from dental unit samples
			1 positive water coolers sample
2013	Occurrence of H. pylori in 31 seawater samples	Culture and PCR	4 positive samples	Holman et al[135]
2016	Occurrence of H. pylori in 450 bottled mineral water samples	Culture and PCR	8 positive samples	Ranjbar et al[111]
2018	Occurrence of H. pylori in 241 drinking water samples	PCR	49 positive samples	Boehnke et al[102]

H. pylori: Helicobacter pylori.