RESULTADOS ADICIONALES
EVALUACIÓN DEL INDICADOR DE PROPÓSITO Controlar las Infecciones Intrahospitalarias
11. RECOMENDACIONES Entre las recomendaciones se sugiere:
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Among subjects, the prevalence of H. pylori infection was higher in those with persistent diarrhoea (66.7%) when compared to those with acute watery diarrhoea (34.8%) and dysentery (35.7%), though this difference was not statistically significant (p=0.29) (Table VIb).
Table VIb: Prevalence of H. pylori infection by type of diarrhoea and presence of dysentery (N=112)
Type of Diarrhoea H. pylori
present n (%)
H. pylori
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SECTION THREE: FACTORS ASSOCIATED WITH H. PYLORI INFECTION
The prevalence of H. pylori infection was higher among the children that were 5 years or older (50%), compared with those that were under 5 years of age (38.1%) (p>0.05) (Table VII). There was also no significant difference in prevalence of H. pylori infection comparing male (41.2%) and female (37.6%) children (p>0.05). Father and mother’s occupation as well as father’s level of education did not show significant differences in prevalence of H. pylori infection (p>0.05).
However, there was a higher prevalence of H. pylori infection among those with lower level of maternal education such as primary (61.1%), compared with those with higher level such as tertiary (33.9%). With further analysis, there was a significantly higher prevalence of infection among those with primary or secondary level of maternal education, compared with at least post-secondary level of maternal education (55.2% vs. 34.3%, p=0.00).
Also, prevalence of H. pylori infection was significantly higher among the children in lower compared with higher social class (52.9% vs. 30.1%; p=0.03). Further analysis showed higher statistical prevalence among low compared with high or middle social classes (52.9% vs. 35.8%, p=0.02).
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Table VII: Relationship between socio-demographic characteristics & H. pylori status (N=224)
Variable H. pylori
present n (%)
H. pylori absent
n (%)
Total n (%)
Chi-square
P-value Age groups (years)
<5 74 (38.1) 120 (61.9) 194 (100) 1.53 0.22
>5 15 (50.0) 15 (50.0) 30 (100)
Sex
Male 54 (41.2) 77 (58.8) 131 (100) 0.29 0.59
Female 35 (37.6) 58 (62.4) 93 (100)
Father's occupation
unemployed/student 3 (42.9) 4 (57.1) 7 (100) Fisher’s 0.22
petty trader/business 42 (49.4) 43 (50.6) 85 (100) Exact junior school teacher/servant 3 (27.3) 8 (72.7) 11 (100)
intermediate public servant 35 (34.0) 68 (66.0) 103 (100) senior public servant 6 (33.3) 12 (66.7) 18 (100) Father's educational level
Primary 7 (53.8) 6 (46.2) 13 (100) 1.93 0.59
Secondary 10 (47.6) 11 (52.4) 21 (100)
Post-secondary 21 (38.9) 33 (61.1) 54 (100)
Tertiary 51 (37.5) 85 (62.5) 136 (100)
Mother's occupation
unemployed/student 18 (36.7) 31 (63.3) 49 (100) Fisher’s 0.07
petty trader 44 (45.4) 53 (54.6) 97 (100) Exact
junior school teacher 7 (25.9) 20 (74.1) 27 (100) intermediate public servant 14 (32.6) 29 (67.4) 43 (100)
senior public servant 6 (75.0) 2 (25.0) 8 (100)
Mother's educational level
Primary 11 (61.1) 7 (38.9) 18 (100) 8.2 0.05
Secondary 21 (52.5) 19 (47.5) 40 (100)
Post-secondary 19 (35.2) 35 (64.8) 54 (100)
Tertiary 38 (33.9) 74 (66.1) 112 (100)
Mother's educational level
(regroup)
Primary and/or secondary 32 (55.2) 26 (44.8) 58 (100) 7.80 0.00 At least post-secondary 57 (34.3) 109 (65.7) 166 (100)
Social class division
High 25 (30.1) 58 (69.9) 83 (100) 6.99 0.03
Middle 37 (41.1) 53 (58.9) 90 (100)
Lower 27 (52.9) 24 (47.1) 51 (100)
Social class division (regroup)
Lower class 27 (52.9) 24 (47.1) 51 (100) 5.44 0.02
High or middle class 62 (35.8) 111 (64.2) 173 (100)
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There was significantly higher prevalence of H. pylori infection among children sleeping in the same room with more than two (63.6%) compared with two or less number of persons (63.6% vs.
37.6%, p=0.02). There was approximately a 3-fold likelihood of H. pylori infection among children sleeping in the same room with greater than two persons compared with those sleeping in the same room with two or less number of persons (OR=2.96; 95% CI: 1.19-7.40).(Table VIII).
Children that had pets in their household had a statistically significantly higher prevalence of H.
pylori infection compared with those that did not have (63.2% vs. 37.6%; p = 0.03).
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Table VIII: Relationship between housing / school environment & H. pylori status (N=224)
Variable H. pylori
present n (%)
H. pylori absent n (%)
Total n (%)
Chi-square
P-value Number of bedrooms
1 32 (38.6) 51 (61.4) 83 (100) 5.53 0.14
2 35 (35.7) 63 (64.3) 98 (100)
3 15 (60.0) 10 (40.0) 25 (100)
>4 7 (50.0) 7 (50.0) 14 (100)
Number of occupants
<5 68 (39.5) 104 (60.5) 172 (100) 0.12 0.91
>5 21 (40.4) 31 (59.6) 52 (100)
Number of siblings
<2 74 (39.8) 112 (60.2) 186 (100) 0.01 0.97
>2 15 (39.5) 23 (60.5) 38 (100)
Number of persons sleeping in the same room with subject/control
0-2 74 (37.6) 123 (62.4) 197 (100) 5.60 0.02
>2 14 (63.6) 8 (36.4) 22 (100)
Presence of pets in household
Yes 12 (63.2) 7 (36.8) 19 (100) 4.68 0.03
No 77 (37.7) 127 (62.3) 204 (100)
Household source of water
Borehole 45 (47.9) 49 (52.1) 94 (100) 4.60 0.10
Pipe borne 34 (34.7) 64 (65.3) 98 (100)
Sachet 10 (31.3) 22 (68.8) 32 (100)
Household waste disposal method
Proper municipal 19 (42.2) 26 (57.8) 45 (100) 0.15 0.70
Improper non-municipal 70 (39.1) 109 (60.9) 179 (100)
Household sewage disposal method
Water closet 79 (39.1) 123 (60.9) 202 (100) 0.33 0.56
Pit latrine 10 (45.5) 12 (54.5) 22 (100)
School type
Public 1 (50.0) 1 (50.0) 2 (100) Fisher’s 0.40
Private 31 (46.3) 36 (53.7) 67 (100) Exact
Under age 57 (36.8) 98 (63.2) 155 (100)
Number in class (N=69)
<20 18 (42.9) 24 (57.1) 42 (100) 0.53 0.47
>20 13 (52.0) 12 (48.0) 25 (100)
School source of water (N=69)
Borehole 16 (64.0) 9 (36.0) 25 (100) Fisher’s 0.14
Pipe borne 13 (34.2) 25 (65.8) 38 (100) Exact
Sachet water 2 (50.0) 2 (50.0) 4 (100)
None 2 (50.0) 2 (50.0) 4 (100)
School waste disposal method (N=69)
Proper municipal 28 (46.7) 32 (53.3) 60 (100) Fisher’s 0.25
Improper non-municipal 2 (25.0) 6 (75.0) 8 (100) Exact
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None of the anthropometric characteristics or clinical features yielded significant differences in prevalence of H. pylori infection between subjects and controls (Table IX).
Table IX: Relationship between anthropometric & clinical characteristics and H. pylori infection (N=224)
Variable H. pylori
present n (%)
H. pylori absent
n (%)
Total n (%)
Test Statistic
P-value Mid Arm Circumference (cm)
<11.5cm (severe under-nutrition) 1 (33.3) 2 (66.7) 3 (100) Fisher’s 0.99 11.5-12.5cm (moderate under-nutrition) 7 (41.2) 10 (58.8) 17 (100) Exact
12.6-13.5cm (borderline under-nutrition) 11 (39.3) 17 (60.7) 28 (100)
>13.5cm (well nourished) 70 (39.8) 106 (60.2) 176 (100) Weight-for-age assessment
Severely undernourished 15 (41.7) 21 (58.3) 36 (100) 0.24 0.89
Undernourished 15 (36.6) 26 (63.4) 41 (100)
Normal 59 (40.1) 88 (59.9) 147 (100)
Weight-for-height assessment
Severely wasted 7 (41.2) 10 (58.8) 17 (100) Fisher’s 0.07
Wasted 15 (46.9) 17 (53.1) 32 (100) Exact
Normal 60 (36.1) 106 (63.9) 166 (100)
Overweight / obese 7 (77.8) 2 (22.2) 9 (100)
Height-for-age assessment
Very stunted 19 (32.8) 39 (67.2) 58 (100) Fisher’s 0.16
Stunted 25 (53.2) 22 (46.8) 47 (100) Exact
Normal 44 (38.3) 71 (61.7) 115 (100)
Very tall 1 (25.0) 3 (75.0) 4 (100)
Fever present
Yes 61 (40.4) 90 (59.6) 151 (100) 0.09 0.77
No 28 (38.4) 45 (61.6) 73 (100)
Heart burn present
Yes 0 (0.0) 2 (100) 2 (100) Fisher’s 0.25
No 89 (40.1) 133 (59.9) 222 (100) Exact
Abdominal pain present
Yes 6 (60.0) 4 (40.0) 10 (100) Fisher’s 0.18
No 83 (38.8) 131 (61.2) 214 (100) Exact
Frequent vomiting present
Yes 31 (33.7) 61 (66.3) 92 (100) 2.38 0.12
No 58 (43.9) 74 (56.1) 132 (100)
Irritability present
Yes 3 (75.0) 1 (25.0) 4 (100) Fisher’s 0.15
No 86 (39.1) 134 (60.9) 220 (100) Exact
Previous hospitalization
Yes 27 (50.9) 26 (49.1) 53 (100) 3.64 0.05
No 62 (36.3) 109 (63.7) 171 (100)
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The prevalence of H. pylori infection was highest among the children that had no form of breastfeeding (61.5%). There was a higher prevalence of H. pylori infection among children that were not exclusively breastfed (42.0%) when compared with those that were exclusively breastfed (20.8%). (p=0.05).
Table X: Relationship between infant feeding pattern and H. pylori infection (N=224)
Variable H. pylori
present n (%)
H. pylori absent
n (%)
Total n (%)
Chi-square
P-value Infant feeding pattern
Breastfeeding only for first 6 months 5 (20.8) 19 (79.2) 24 (100) 10.31 0.07 Breastfeeding only for first 4 months 15 (39.5) 23 (60.5) 38 (100)
Breastfeeding only for first 2 months 20 (32.3) 42 (67.7) 62 (100) Breast feeding only for < first 2 months 25 (43.9) 32 (56.1) 57 (100) Breastfeeding with formula from start 16 (53.3) 14 (46.7) 30 (100) No breastfeeding at all 8 (61.5) 5 (38.5) 13 (100)
Six months exclusive breastfeeding
Yes 5 (20.8) 19 (79.2) 24 (100) 3.98 0.05
No 84 (42.0) 116 (58.0) 200 (100)
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MULTIPLE LOGISTIC REGRESSIONS FOR THE PRESENCE OF H. PYLORI INFECTION
Odds ratio and regression analysis was conducted to determine potential predictor variables of presence of H. pylori infection. Only predictor variables that were significantly associated with presence of H. pylori infection (p<0.05) and contributed to model significance (p<0.05) were selected.
The Wald criterion demonstrated that both social class division and presence of pet made significant contribution to prediction (p=0.015, p = 0.03 respectively). Odds ratio indicated that every unit decrease in social class (from high through middle to low classes) yielded a 1.7 times increased likelihood of presence of H. pylori infection. Also, children that had household pet(s) were 1.2 times more likely to have H. pylori infection compared with those that did not (Table XI).
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Table XI: Multiple regression of presence of H. pylori infection with relevant predictors
Model predictor variables
odds ratio
p-value Intercept
model properties
N
square* HL test**
overall model significance
1
Social Class 1.7 0.015
0.757 0.72 0.257 good
Presence of pet 1.2 0.030
2
Social class 1.08 0.05
-0.036 0.37 0.83 poor***
Presence of pet 0.14 0.20
Maternal education 1.11 0.66
Infant feeding pattern 1.09 0.74
Sharing room 0.28 0.14
* = Nagelkerke’s R square; ** = Hosmer Lemeshow test; *** = considered poor due to low N R square
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DISCUSSION
In this study, the overall prevalence of H. pylori infection was 39.7%. This is similar to the study by Etukudoh et al48 in southern Nigeria who reported a prevalence of 30.9%. However the study by Holcombe et al27 in northern Nigeria reported a higher prevalence of 85%. This disparity in the prevalence of H. pylori infection could be attributed to variations in the standard of living and socioeconomic conditions in these areas.120 Studies have shown that H. pylori prevalence declines with improvement in socioeconomic conditions.24 In addition, the study by Holcombe et al27 was done more than two decades ago so direct comparison with the results of present study is difficult.
Social conditions may have changed, hence the need for a repeat study in northern Nigeria.
The prevalence of H. pylori infection among the subjects and control groups were 46.1% and 53.9%
respectively. There was no significant difference in H. pylori infection status comparing the study groups. There was also no significant difference in the prevalence of acute (27.7%) or chronic (12.1%) H. pylori infection when both study groups were compared. In this study, a higher prevalence of H. pylori infection was seen in the control group without diarrhoeal disease. Thus, the null hypotheses which states that H. pylori infection is not prevalent in children with diarrhoeal diseases in our environment is upheld.
This finding could be explained by the fact that the causative organisms for H. pylori infection and diarrhoeal disease may not always coexist in a particular environment. Hence each can be acquired independently of the other despite the presence of common epidemiologic associations. Some studies have also postulated that colonization with H. pylori may protect from gastrointestinal infections that cause diarrhoea through activation of the immune system and increased IgA production.121,122 The IgA antibodies produced against H. pylori is believed to be fatal to other enteric pathogens that could predispose to the development of diarrhoeal disease. This may also explain the finding of a higher prevalence of H. pylori infection in the control group who presented
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with other clinical conditions other than diarrhoeal disease. It also supports other studies that found lower prevalence of H. pylori infection in those with diarrhoeal disease. Monajemzadeh et al123 investigated the relationship between H. pylori infection and bacterial gastroenteritis due to Salmonella and Shigella, a higher prevalence of H. pylori infection was found in the control group (without diarrhoea) than in the patients with bacterial diarrhoea indicating that the bacterial infected patients were less infected with H. pylori (p = 0.007). H. pylori and bacterial gastroenteritis share common predisposing factors, but a higher prevalence of H. pylori infection was found in the study group that had no bacterial gastroenteritis. A study by Rhaman et al90 to determine the relationship between Helicobacter pylori colonization and morbidity due to diarrhoea found that the median number of diarrhoeal episodes was 1.0 (range 1.0 – 4.0) in the H. pylori positive children and 2 (range 1.0-5.0) in the H. pylori negative children (p=0.19). Bode et al124 in their study also reported less number of diarrhoea episodes for H. pylori infected subjects compared with H. pylori negative subjects (40.2% vs 51.6% p= 0.016) although this study was carried out in the adult population. The studies by Rhaman et al90 and Bode et al124 also show a lower prevalence of diarrhoeal disease in H.
pylori infected patients, thereby supporting the hypothesis that colonization with H. pylori may protect from gastrointestinal infections that cause diarrhoea through activation of the immune system and increased IgA production.
Among the subjects infected with H. pylori, the prevalence of H. pylori was higher in those with persistent diarrhoea compared with those with acute diarrhoea and dysentery, though this difference was not statistically significant (p=0.29). Castro-Rodriguez et al92 also found a higher prevalence of H. pylori infection in children with persistent diarrhoea when compared with those with acute diarrhoea and without diarrhoea. The study by Etukudoh et al48 showed a positive association between H. pylori IgG seropositivity and diarrhoea. However the more prevalent form of diarrhoea was not specified in their study population. The reason for a higher prevalence of H. pylori infection in the children with persistent diarrhoea is however unclear.
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The prevalence of H. pylori infection was higher among children that were 5 years or older (50%), compared with those that were under five years of age (38.1%). Although this difference was not statistically significant (p>0.05), it may be clinically significant and represents a cumulative effect.
There was no statistically significant difference in prevalence of H. pylori infection comparing male (41.5%) and female (38.0%) children (p>0.05). The difference may however be clinically significant and may be explained by the more adventurous nature of males.
There was a higher prevalence of H. pylori infection among children with lower levels of maternal education compared with those with higher levels. A significantly higher prevalence of infection was found among the children whose mothers had primary or secondary level of education compared with at least post-secondary level of education.
The higher prevalence of H. pylori infection in the study population with low level of maternal education may imply poor hygiene and low income status. Children from the low social class had a statistically higher prevalence of H. pylori infection. This agrees with other studies that postulate poor hygiene and low socioeconomic conditions as predisposing factors in the acquisition of H.
pylori infection.21 In this study, social class was found to be a good predictor of infection with H.
pylori.
The number of bedrooms, occupants and siblings in the childrens’ houses, were not found to significantly affect the prevalence of H. pylori infection. However, there was significantly higher prevalence of H. pylori infection among children that slept in the same with more than two compared with two or less number of persons.
Webb et al25 in their study found that subjects from large families, whose childhood homes were crowded or who regularly shared a bed in childhood, were significantly more likely to be seropositive for H. pylori infection. Although a retrospective study in the adult population, it showed that close person to person contact in childhood was an important determinant of
lxix
seroprevalence of H. pylori infection. The precise mode of transmission however still remains unclear.
Children that had pets in their household had a significantly higher prevalence of H. pylori infection compared with those that did not have. This finding supports the possibility of zoonotic transmission of H. pylori infection. The recent isolation of H. pylori from the inflamed gastric mucosa of commercially reared cats, and the ability to experimentally infect cats with H. pylori, raises the possibility of zoonotic H. pylori transmission from infected animals that have close human contact.125 In this study, the presence of household pets was also a good predictor of infection with H. pylori.
The difference in the prevalence of H. pylori infection was not significant comparing household sources of water, waste and sewage disposal. This is similar to the study by Fiedorex et al28 done in a developed country. In their study, there was no significant difference in H. pylori infection in relation to gender, type of housing, location of housing or source of water supply. In our study, the prevalent source of water for household use was pipe borne (43.8%) and borehole (42.0%). Most household (80.0%) utilized municipal waste bins as means of waste disposal. Also, most household (90.2%) utilized water closet for sewage disposal. The wide availability of pipe borne water supply and a proper means of waste disposal system in Calabar may have a positive impact on the hygiene status of our study population. These are similar to conditions in the developed world and may explain the similarity in findings.
None of the anthropometric characteristics significantly influenced the prevalence of H. pylori infection. Although studies have shown that H. pylori infection may predispose to malnutrition in children,96 malnutrition was not a significant finding in this study. Castro-Rodriguez et al92 in their study reported that H. pylori was not associated with malnutrition in Peruvian children. The
lxx
children were aged between three to 36 months. Nalficy et al126 in a cohort study of children less than 36 months of age reported that H. pylori was not associated with malnutrition.
Thomas et al127 reported differently. A birth cohort study done showed that H. pylori colonization in early infancy predisposes to the development of malnutrition and growth faltering. In a study by Richter et al128 H. pylori infection was associated with growth delay, growth retardation or both in affected children. The study population consisted of children aged five to seven years.
The disparity noted in the various studies could be as a result of the presence of socioeconomic or demographic confounding variables in the various studies. In addition, it has been established that though acquisition of H. pylori usually occurs in early infancy, the sequellae such as gastritis and peptic ulceration which can predispose to malnutrition usually occur in the older age group. This could possibly explain the absence of malnutrition in this study populations consisting of infants and preschool aged children. More than 80% of the study population were less than 5 years of age.
More research studies to establish the presence of malnutrition in the older age group is advocated.
The prevalence of H. pylori infection was highest among children that had no form of breastfeeding. The lowest prevalence of H. pylori infection was found among the children that had exclusive breastfeeding for six months. The practice of six months exclusive breastfeeding was also found to be significantly commoner among controls compared with subjects (70.8% vs. 29.2%, p=0.03)
Studies have shown that breastfeeding protects against the acquisition of H. pylori infection. The possible mechanism of this protection may be the lactoferrin in human milk which binds to H.
pylori liposaccharide and inactivates the organism. H. pylori-specific IgA present in breast milk also offers protection against infection with H. pylori. IgA is fatal to enteric pathogens.129,130 Lactoferrin and H. pylori specific IgA are not present in infant formula hence the highest prevalence of H. pylori infection in our study was found in those that had no form of breastfeeding and the
lxxi
lowest prevalence was found in those that had exclusive breastfeeding for six months. The practice of exclusive breastfeeding was higher in the controls without diarrhoeal disease. This may also be explained by the protective effect of lactoferrin and IgA in breast milk against enteric pathogens that may cause diarrhoeal disease.
lxxii
CONCLUSION
The prevalence of H. pylori infection in children with diarrhoeal disease was not statistically significant when compared with children without diarrhoeal disease. `
Poor socioeconomic conditions such as overcrowding and low level of maternal education increases the risk of acquisition of H. pylori infection. Transmission of H. pylori infection is associated with contact with infected household pets.
Exclusive breastfeeding for the first six months of life is associated with a lower prevalence of H.
pylori infection amongst the study population.
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RECOMMENDATIONS
i. Post-secondary education for all, including the girl child is highly advocated.
ii. The practice of exclusive breastfeeding for the first six months of life is highly
recommended. This will not only protect against the acquisition of H. pylori infection but also a variety of other known childhood illnesses.
lxxiv
LIMITATION OF THE STUDY
The 13C-Urea Breath Test (UBT) is more sensitive and specific than the antibody tests. However, UBT is very expensive. Furthermore, it would be difficult to use UBT in the presence of vomiting which often accompanies diarrhoea in children. It could also interfere with the use of oral rehydration salt. The use of questionnaire also has the limitation that the response may not always be accurate.
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REFERENCES
1. Blecker U. Helicobacter pylori- associated gastroduodenal disease in childhood. South Med J 1997;90:570-6.
2. Adrienne ZA, Simon I, Emily RM. Update on Helicobacter pylori treatment. Am Fam Physician 2007;75:351-358.
3. Amir E, Ali M, Nader A, Ardeshir L. Detection of H. pylori using PCR in dental plaque of patients with and without gastritis. Med Oral Patol Oral Buccal 2010;15:28-31.
4. Burstein M, Monge E, Leon-Barua R, Lozano R, Berendson R, Gilman RH et al. Low peptic ulcer and high gastric cancer prevalence in a developing country with a high prevalence of infection by Helicobacter pylori. J Clin Gastroenterol 1991;13:154-156.
5. Blaser MJ, Chyou PH, Nomura A. Age at establishment of Helicobacter pylori infection and gastric carcinoma, gastric ulcer and duodenal ulcer risk. Cancer Res 1995;55:562-565.
6. Macarthur C, Saunders N, Feldman W. Helicobacter pylori, gastroduodenal disease, and recurrent abdominal pain in children. JAMA 1995;273:729-734.
7. Beales IL. H. pylori-associated hypochlohydria. Gastroenterology 1999;104:216-221.
8. Harford WV, Barnette C, Lee E, Perez-Perez G, Blaser MJ, Peterson WL. Acute gastritis with hypochlorhydria: report of 35 cases with long term follow up. Gut 2000;47:467-472.
9. IARC Working Group. Monographs on the Evaluation of Carcinogenic Risks to Humans.
Schistosomes, Liver Flukes and Helicobacter pylori. Lyon, France: International Agency for Research on Cancer, 1994;61:177-241.
lxxvi
10. Tanih NF, Dube C, Green E, Mkewtshana N, Clarke AM, Ndip LM et al. An African perspective of Helicobacter pylori: Prevalence of human infection, drug resistance and alternative approaches to treatment. Am J Trop Med Hyg 2009;103:189-204.
11. Graham DY. Helicobacter pylori, its epidemiology and its role in duodenal ulcer disease. J Gastroenterol Hepatol 1991;6:105-113.
12. Balaban DH, Peura DA. Helicobacter pylori-associated peptic ulcer and gastritis. In: LaMont JJ (ed). Gastrointestinal Infections Diagnosis and Management. New York, Marcel Dekker, Inc. 1997;29-56.
13. Goh KL, Chan WK, Shiota S, Yamaoka Y. Epidemiology of Helicobacter pylori infection and public health implication. Helicobacter 2011;16:1-9.
14. Sinha SK, Martin B, Sargent M, McConnell JP, Bernstein CN. Age at acquisition of Helicobacter pylori in a Pediatric Canadian First Nation Population. Helicobacter 2002;7:76-85.
15. Holcombe C, Tsimiri S, Eldridge J, Jones DM. Prevalence of antibody to Helicobacter pylori in children in northern Nigeria. Trans R Soc Trop Med Hyg 1993;87:19-24.
16. Sullivan PB, Thomas JE, Wight DG. Helicobacter pylori in the Gambian children with chronic diarrhoea and malnutrition. Arch Dis Child 1990;65:189-191.
17. Graham DY, Qureshi WA. Markers of infection. In: Mobley HLT, Mendz GL, Flazell SL, (eds). Helicobacter pylori: Physiology and Genetics. Washington(DC). ASM Press. 2001.
18. Breslin NP, O’Morain CA. Noninvasive diagnosis of Helicobacter pylori infection: A Review. Helicobacter 1997;2 suppl 3.
lxxvii
19. Alem M, Alem N, Cohen H, England T, Hamedi N, Moussazadeh M et al. Diagnostic value of detection of IgM antibodies to Helicobacter pylori. Exp Mol Pathol 2002;72:77-83.
20. Gold BD, Khanna B, Huang LM, Lee CY, Banatvala N. Helicobacter pylori acquisition in infancy after decline of maternal passive immunity. Pediatr Res 1997;41:641-646.
21. Malaty HM, Graham DY. Importance of childhood socioeconomic status on the current prevalence of Helicobacter pylori infection. Gut 1994;35:742-745.
22. Ertem D, Harmanii H, Pehlivannoglu E. Helicobacter pylori infection in Turkish preschool and school children: role of socioeconomic factors and breastfeeding. Turk J Pediatr 2003;45: 114-122.
23. Malaty HM, Logan ND, Graham DY. Helicobacter pylori infection in preschool and school aged minority children: effect of socioeconomic indicators and breastfeeding practices. Clin Infec Dis 2001;32:138-192.
24. Mendell MA, Goggin PM, Molineaux N, Levy J, Toosy T, Strachan D et al. Childhood living conditions and Helicobacter pylori seropositivity in adult life. Lancet 1992;339:896-897.
25. Webb PM, Knight T, Greaves S, Wilson A, Newell DG, Elder J et al. Relation between infection with Helicobacter pylori and living conditions in childhood: evidence for person to person transmission in early life. Brit Med J 1994;308:750-753.
26. Sathar MA, Gouws E, Simjee AE, Mayat AM. Seroepidemiological study of Helicobacter pylori infection in South African children. Trans R Soc Trop Med Hyg 1997;91:393-395.
lxxviii
27. Holcombe C, Omotara BA, Eldrige J, Jones DM. H. pylori, the most common bacterial infection in Africa: a random serologic study. Am J Gastroenterol 1992;87:28-30.
28. Fiedorek SC, Malaty HM, Evans DL. Factors influencing the epidemiology of Helicobacter pylori infection in children. Pediatrics 1991;88 :578-582.
29. Epplein M, Signorello LB, Zheng W, Peek RM, Michel A, Williams SM et al. Race, African ancestry and Helicobacter pylori infection in a low-income United States population. Cancer Epidemol Biomarkers Prev 2011;20:826-834.
30. Marion Rowland, Brendan Drumm. Clinical significance of Helicobacter infection in children. Brit Med Bull 1998;54:95-103.
31. Mitchell H, Megraud F. Epidemiology and diagnosing of Helicobacter pylori infection.
Helicobacter 2002;1:8-16.
32. WHO. Diarrhoeal diseases. Fact sheet N°330. April 2013.
33. Readings on diarrhoe (students’ manual). Adapted manual of WHO for the control of diarrhoea diseases. 1990:2.
34. Pulak Sahay, Anthony TR Axon. Reserviors of Helicobacter pylori and Modes of Transmission. Helicobacter 1996;1:3.
35. Freedburg AS, Baron LE. The presence of spirochaetes in human gastric mucosa. Am J Dig Dis 1940;7:443-445.
36. Palmer ED. Investigation of the gastric spirochaetes of the human. Gastroenterology 1954;27:218-220.