Submit manuscript...
Journal of
eISSN: 2469 - 2786

Bacteriology & Mycology: Open Access

Research Article Volume 6 Issue 2

Prevalence and intensity of Trichuris trichiura infection and associated determinants in rural tea garden areas of sylhet, Bangladesh

Muhammed Hossain, Jamal Uddin Bhuiyan

Department of Parasitology, Sylhet Agricultural University, Bangladesh

Correspondence: Muhammed Hossain, Department of Parasitology, Faculty of Veterinary, Animal and Biomedical Science, Sylhet Agricultural University, Sylhet-3100, Bangladesh

Received: February 28, 2018 | Published: April 10, 2018

Citation: Hossain M, Bhuiyan JU. Prevalence and intensity of Trichuris trichiura infection and associated determinants in rural tea garden areas of sylhet, Bangladesh J Bacteriol Mycol Open Access. 2018;6(2):130-137. DOI: 10.15406/jbmoa.2018.06.00190

Download PDF

Abstract

The current study of the prevalence, intensity and associated determinants of Trichuris trichiura infection was carried out from June’ 2014 to May’ 2015 among five tea gardens of Sylhet Sadar Upazila of Sylhet district, Bangladesh. Out of 300 participants 42(14.00%); 95% CI 10.28-18.45) were found robustly infected with T. trichiura of the age groups 11-20 years age group showed highest prevalence 31.58% (95% CI 12.58-56.55) than other age groups. Multivariate analysis identified season (OR=6.15; 95% CI 2.27-16.66, P= 0.01), areas, periodic anthelmintic does not taking, unhygienic disposal of the stool (OR=2.79, 95% CI 1.44-5.43, P= 0.02) are as the potential determinants contributing to the intensity of T. trichiura infection. Low income of the family significantly (OR=2.15; 95% CI 1.11-4.15, P=0.02) associated with T. trichiura infection. Low level of education of the parents associated with moderate intensity of T. trichiura infection. Therefore deworming of the tea garden children and worker are warranted. Preventive measures should be emphasized on important determinants like regular taking of anthelmintics, proper disposal of children’s stool, appropriate water management and children should be avoided entering to household dirt.

Keywords: prevalence, trichuris trichiura, intensity, determinants, tea garden community

Introduction

The intestinal parasitic infection particularly T. trichiura causes hundreds of thousands of deaths every year.1 It has been recorded that over one billion people are infected with Ascaris lumbricoides, 800 million with hookworm and 770 million with T. trichiura.2 Trichuriasis prevalent throughout the tropical areas especially the areas associated with the conditions of poverty, unsafe water, sanitation and hygiene particularly in developing nations.3−5 Previous studies have shown the main risk factors for helminths infection are rural residency, low economic status and poor knowledge on hygiene.6,7 There are few data on the epidemiology of helminths infection in tea garden community of Sylhet8 but no data available on risk factors of helminths infections. Negative effects of trichuriases infection include diminished physical fitness, growth retardation, delayed intellectual development and cognition.6,9 To investigate the epidemiology of helminths infection in tea garden children and workers we analyzed collected data during the study period in tropical Sylhet. Current stratagem for controlling helminths infections are primarily based on periodic anthelmintic treatment of community people, and secondarily on education and sanitation improvement. The use of pit latrines and improved drinking water has been associated with reduction of prevalence of helminths infections.10 Treatment based control strategies goal to control rate of mortality through reductions of transmission of helminths infection in the community.11 An understanding of the determinants of infections would assist in designing the most appropriate control measures. The aim of the present study was to determine robustly the prevalence and determinants and clinical features associated with trichuriases infection in tea garden community.

Materials and methods

Study area

The tea garden areas of Sylhet district located 315km north east from capital city Dhaka were selected for this study as it is the poorest area of Bangladesh. Sylhet is located at 24.8917°N and 91.8833°E. It has 86074 units of house hold and total area 323.17 km².12 More than 75% rainfall occurs in the monsoon period. Average temperature of the country ranges from 17 to 20.60°C during winter and 26.90 to 31.10°C during summer. Average relative humidity for the whole year ranges from 70.50% to 78.10% in Bangladesh.13 This district is occupied by high proportion of ethnic minorities, stingy household condition, poor road condition, no prohibition for preventive and curative measures (Figure 1).

Duration of the study

The study was conducted for a period of 12 months starting from June’ 2014 to May’ 2015.

Ethical approval

The study was approved by the Ethical Committee for public health research, Sylhet Agricultural University, Sylhet-3100. Verbal consent was obtained from the parents or legal caretakers of the children. Children positive with intestinal parasites were treated with appropriate drugs by physicians from Upazila Hospitals free of cost.

Data collection

Demographic and socio-economic information of the participant and other member of the family were collected using standard questionnaire. The probable potential determinants like age, sex, participants schooling, Parent’s occupation, taking anthelmintic, type of latrine, toilet floor, how often toilet clean, washing hand and feet coming from toilet, access to safe drinking water, and work in bare foot. The parents were also asked for if any ill health condition last six month as itching, abdominal pain, diarrhea, weight loss, fatigue and weakness, and blood in stool etc. Household socio-economic status like monthly income of family, education of the house head, household floor, ownership of the animal cattle, sheep, goat, dog, cat and pigs.

Sample collection

Labeled stool containers were provided to the parents of each child. The filled containers were collected in the following morning and were carried in a cool ice-box to the Laboratory and examination was performed within 24 hour of collection.

Study design and selection of the tea garden

In first step, the heads of respective tea garden from all five tea garden were asked for community outreach activities in June’ 2014 to prepare a list of all primary schools in their respective tea garden including the number of children attending grades 2 and 3. All interested participants of the selected household were also enlisted for the study with making proper consent of the household head.

Analysis of collected stool sample

Direct smear method and Kato Katz Techniques

The collected stool samples were examined by direct saline smear for the presence of parasitic ova and the same sample also were subjected to Kato Katz thick smear14 and in every slide egg of each parasite species evaluated and recorded (Figure 2). The intensity of infection [egg per gram (EPG)] was determined. Based on the criteria of the [15]: A. lumbricoides: light, 0–4999 EPG; moderate, 5000-49999 EPG; and heavy, ≥50 000 EPG; T. trichiura: light, 0–999 EPG; moderate, 1000–9999 EPG; and heavy, ≥10 000 EPG; and hookworm: light, 0–399 EPG; moderate, 400–2999 EPG; and heavy, ≥3000 EPG.

Data analysis

Statistical analysis was performed by Logistic Regression procedure using STATA 13 (College Station, Texas 77845 USA) and the level of significance was considered as P<0.05. In the univariable analysis, λ2 test done for determinants associated with infection. In the multivariable logistic regressions, variables with a P-value of ≤0.20 in the univariable analysis were included as predictors. ORs and 95% CI were reported. P-values <0.05 were regarded as significant.

Figure 1 Location of tea garden in Sylhet Sadar Upazilla

Figure 2 Preparation of Kato Katz slides (Step 1: All the required tools are accommodated; Step 2: Setting up the slide and plastic strip with pit; Step 3: Placement of required quantity of stool in the pit; Step 4: Removal of the plastic strip and desired amount of stool remained in the glass slide; Step 5: Placing the nylon screen over the stool sample; Step 6: Slide prepared and ready for ova counting under microscope).

Results

Household, education and income of the family

Of the participants 91.67% live in the house floor made up of mud, 08.00% concrete made and 0.33% in semi cemented floor house. In the tea garden community 34.67% had primary education, 05.33% secondary education and 60% Illiterate. The participant’s father possesses higher literacy than mother. Primary education 28.67% and 21.00%; Secondary 24.00% and 01.00%; Illiteracy 47.33% and 78.00% respectively for male and female (Table 1). Occupation and family income of the participants playing a crucial role in trichuris infection (Table 2) (Table 3).

Demographic information (Table 4)

Prevalence of Trichuris infection

The T. trichiura organism has been identified from stool specimens with the overall prevalence 14.00% (95% CI 10.28-18.45). The prevalence of trichuriases is higher in male 14.69% (95% CI 09.83-20.78) than female 13.01% (95% CI 07.62-20.26). Highest infection occurred during Rainy season and which is 24.62% (95% CI 14.77-36.87) then the infection gradually decreases from 17.24% (95% CI 10.86-25.36) to 05.04% (95% CI 01.87-10.65) respectively for Winter and Summer. The highest infection recorded in the age group 11-20 years 31.58% (95% CI 12.58-56.55) and lowest infection in ≥41 age groups 07.14% (95% CI 0.18-33.87) (Table 4). Interesting finding of our work was no T. trichiura infection in Daldali tea garden, it is most likely because of the geographical and hygienic condition of this area. People of this area are quietly abided by the hygienic health regulations rules.

Intensity of trichiura infection in tea garden community of Sylhet (Table 5)

Determinants for trichiura infection

The univariable analysis disclosed season, areas, participant’s schooling, receiving anthelmintic periodically, family income and disposal of the stool were significantly P<0.05 associated with Trichuris infection (Table 6). The rural slum of the tea garden poorly arranged and the unhygienic condition of the areas favor the transmission cycle of the infection.

The multivariable logistic regression shows that season are keenly associated with T. trichiura infection and the Rainy season revealed OR=6.15(95% CI 2.27-16.66) than the Winter OR=3.92(95% CI 1.51-10.17). Periodic anthelmintic taking reduces the chance of infection than those are not taking anthelmintics OR=2.07(95% CI 1.07-4.01). The tea garden location also favors the transmission cycle of T. trichiura due to poor hygiene maintenance in the rural slums (Table 7).

Characteristics

Frequency

Percentage

Participants schooling

Primary

104

34.67

Secondary

16

5.33

No schooling

180

60

Mother’s schooling

Primary

63

21

Secondary

3

1

No schooling

234

78

Father’s schooling

Primary

86

28.67

Secondary

72

24

No schooling

142

47.33

Table 1 Educational status of the 300 participants and their parents in tea garden community

Level of occupation

Frequency

Percentage

Father’s occupation

Unemployed

11

3.67

Day labourer

182

60.67

Service

80

26.67

Tea garden worker

9

3

Business

18

6

Mother’s occupation

Housewife

167

53.33

Service

1

0.33

Business

132

44

Table 2 Occupational status of the parents of 300 participants in tea garden community

Other demographic information

Frequency

Percentage

Age group

≤10

242

80.67

20-Nov

19

6.33

21-30

13

4.33

31-40

12

4

41-up

14

4.67

Sex

Male

177

59

Female

123

41

Name of the areas

Khadim tea estate

47

15.67

Burjan tea estate

79

26.33

Lakkatora tea estate

65

21

Malnichara tea esstate

63

21.67

Daldali tea estate

46

15.33

Category of weight (kg)

≤20

186

62

21-40

65

21.67

41-up

49

16.33

Income of house (Taka)

≤5000

103

34.33

>5000

197

65.67

No of people living in house

≤4

145

48.33

≥5

155

51.67

Name of the season

Rainy

65

21.67

Winter

116

38.67

Summer

119

39.67

Table 3 Other demographic information of the 300 participants of tea garden community

Points

Total no. of tested

Total no. of positive

Prevalence (95% confidence Intervals)

Season

Rainy

65

16

24.62% (14.77-36.87)

Winter

116

20

17.24% (10.86-25.36)

Summer

119

6

05.04% (01.87-10.65)

Age

≤10

242

30

12.39% (08.52-17.22)

20-Nov

19

6

31.58% (12.58-56.55)

21-30

13

3

23.08% (05.04-53.81)

31-40

12

2

16.67% (02.09-48.41)

≥41

14

1

07.14% (0.18-33.87)

Areas

Khadim tea estate

47

14

29.79% (17.34-44.90)

Burjan tea estate

79

18

22.78% (14.10-33.60)

Lakkatora tea estate

65

2

03.08% (00.38-10.68)

Malnichara tea estate

63

8

12.70% (05.65-23.50)

Daldali tea estate

46

-

Sex

Male

177

26

14.69% (09.83-20.78)

Female

123

16

13.01% (07.62-20.26)

Table 4 Prevalence of Trichuris trichiura infection in tea garden community of Sylhet

Trichuris trichiura

Percentage of infection

No infection

258(86.00)

Light

30(10.00)

Moderate

08(02.67)

Heavy

04(01.33)

Total

300(100.0)

Table 5 Intensity of T. trichiura infection in tea garden community of Sylhet

The epg (egg per gram) counting by Kato Katz revealed light, moderate and heavy infection of T. trichiura and which were 10.00%, 02.67% and 01.33% respectively (Table 5)

Characteristics

Positive
n=42(%)

Negative
n=258(%)

P-value

Season

Rainy

16(69.23)

49(30.77)

Winter

20(26.05)

96(73.95)

Summer

06(42.40)

113(57.76)

<0.01***

Areas

Khadim tea estate

14(63.83)

33(36.17)

Burjan tea estate

18(55.70)

61(44.30)

Lakkatora tea estate

02(29.23)

63(70.77)

Malnichara tea esstate

08(39.68)

55(60.32)

Daldali tea estate

0

46(84.78)

<0.01***

Participant’s schooling

Primary

22(50.96)

82(49.04)

Secondary

03(18.75)

13(81.25)

No schooling

17(38.33)

163(61.67)

0.02

Father’s occupation

Unemployed

03(63.64)

08(36.36)

Day labourer

24(46.70)

158(53.30)

Service

11(28.75)

69(71.25)

Tea garden worker

02(33.33)

07(66.67)

Other

02(38.89)

16(61.11)

0.67

Monthly family income (Taka/Month)

≤5000

21(50.49)

82(49.51)

>5000

21(37.06)

176(62.94)

0.02

Receive treatment

No

24(65.60)

101(34.40)

Yes

18(24.57)

157(75.43)

0.03

Treatment 4 month interval

No

33(62.29)

142(37.71)

Yes

09(12.80)

116(87.20)

0.04

Toilet floor

Mud

26(58.59)

175(41.41)

Bamboo

16(33.33)

83(66.67)

0.45

Where dispose stool

Around house

21(34.12)

190(65.88)

Jungle/Tea garden

21(59.55)

68(40.45)

0.02

Rub hand after toilet

No

35(39.84)

221(60.16)

Yes

07(52.27)

37(47.73)

0.69

Use disinfectant toilet cleaning

No

13(56.76)

61(43.24)

Yes

29(36.73)

197(63.27)

0.31

Have foot ware

No

02(04.76)

05(01.94)

Yes

40(95.24)

253(98.06)

0.26

Use shoe inside home

Always

04(09.52)

24(09.30)

Most time

11(26.19)

117(45.35)

Rarely

25(59.52)

112(43.41)

Never

01(02.38)

04(01.55)

Not applicable

01(02.38)

01(0.04)

0.17

Activity outside home

Always

07(16.67)

37(14.34)

Most time

14(33.33)

147(56.98)

Rarely

20(47.62)

71(27.52)

Never

00(0.00)

02(0.07)

Not applicable

01(02.38)

01(0.04)

<0.01***

Work in bare foot

No

09(21.43)

46(17.83)

yes

33(78.57)

212(82.17)

0.58

Wash feet coming from out

Not always

23(54.76)

149(57.75)

Always

19(45.24)

109(42.25)

0.72

Table 6 Univariable analysis by λ2 test of the factors associated with T. trichuria infection in tea garden community of Sylhet

*P<0.05 Significant association with positive sample, ***= highly significant

Name of variable

Odds ratio (95% confidence Intervals)

P-value

Season

Rainy

6.15(2.27-16.66)

<0.01***

Winter

3.92(1.51-10.17)

Summer

1

Areas

Khadim tea estate

2.92(1.11-7.69)

Burjan tea estate

2.03(0.82-5.04)

0.03

Lakkatora tea estate

0.22(0.04-1.07)

Malnichara tea estate

0.15(0.07-.03)

Daldali tea estate

1

Income (Taka/Month)

2.15(1.11-4.15)

≤5000

1

0.02

>5000

Receive anthelmintic

No

2.07(1.07-4.01)

0.03

Yes

1

Receive anthelmintic 4 month interval

No

2.99(1.38-6.51)

0.01

Yes

1

Disposal of stool

Jungle/garden

2.79(1.44-5.43)

0.02

Around house

1

Table 7 Multi-variable logistic regression analysis of Trichuris trichiura infection in Tea garden community of Sylhet

*P<0.05 Significant association with positive sample, ***= highly significant

Discussion

This cross sectional study included 300 participants in rural slum of tea garden community in Sylhet district. These numbers of participants are representative of the local population in this poor remote setting as previous study.16 The overall prevalence of T. trichiura infection was 14.00% (95% CI 10.28-18.45). This finding was higher than the reports from other study of Bangladesh.7,16 The variation of prevalence of T. trichiura infection in different studies would be due to differences in climate and geographical location of the areas. What’s more, socio-economic condition as well as environmental, household, personal hygiene plays a pivotal role for the variation in the prevalence of infection.17 There is a paucity of information in the prevalence of T. trichiura because at the best of my knowledge this is the first time reporting the age category. Previous study targeted the overall infection of the regular female tea pluckers.16 Prevalence of Trichuris infection in the slums of urban areas was 03.43%1,7 which is lower than the rural slum areas 31.58% (95% CI 12.58-56.55). Exposure of older children to the infection is higher as they show different way of behaviors. However, older children accumulate infection during their lifetime.18 The existence of this parasite higher among the children might be due to the resistant nature of the eggs against different environmental factors.19 Trichuris infection is higher in older children which was consistent to other researchers.20,21 Trichuris infection is comparatively higher in male than female which is contradictory to7,18 but similar to.22

It is known that a single Kao Katz thick smear done on a single sample has a relatively lower sensitivity.23 Therefore it could be assumed that the true prevalence of infection is higher than which documented here. In addition the Kato Katz technique does not allow detection of a broader range of parasite species.

In this study the infection intensity of T. trichiura measured as an indirect tool of morbidity. T. trichiura infection was identified as light, moderate and heavy infection but in study of18 only light and moderate infection found. However, there was prevalence of malnutrition and anemia in the study subjects but no association with the Trichuris infection although T. trichiura were associated with higher level of anemia.24

Determinants analysis showed that the areas were significantly associated with T. trichiura infection which is similar to the findings of.22 This might be due to the climatic condition like humid and warm weather, poor hygiene of the rural slum, lack of provision for potable water.

In the multivariate analysis, T. trichiura is best predicted by season. Rainy season contributed significantly the infection because children spend more time outside of the house and eat frequently unwashed fruit from the gardens. OR=6.15(95% CI 2.27-16.66; P=<0.01) than winter OR=3.92(95% CI 1.51-10.17; P=<0.01). This study is slight contradictory by the Matthys B & Gungoren B et al.25,26 that speculated parasitic infection might be higher in summer.

We identified periodic anthelmintic taking reduces the parasitic infection significantly. The participants who does not take anthelmintic four month interval they had opportunity of getting infection OR=2.99(95% CI 1.38-6.51; P<0.01). Unhygienic disposal of human stool significantly associated with Trichuris infection because disposal of stool in jungle or tea garden canal showed OR=2.79(95% CI 1.44-5.43; P<0.02), where children and workers regularly enter in stool conveying canal which ultimately promotes the transmission cycle (Figure 3).27

The economic condition of the household is significantly associated with T. trichiura infection because with low family income the rate of infection increases as we found in our study 2.15 (95% CI 1.11-4.15; P<0.02) which is similar to the findings of28 when the family income increases then they had privileges to maintain all hygienic measures.

Factors like education, occupation, toilet floor and work in bare foot did not correlate with T. trichiura infection which seems to have an association with infection. Steenhard NR et al.22 reported illiterate mother is significantly associated with infection.

Chemotherapy on regular basis for prevention has been shown to reduce parasitic infection in a cost effective way.29,30 Hygienic practices needed additionally to ensure a long term benefits.31 To keep the children free from parasite for longer period, treatment should be started in early life. The ahead challenges is how best we can reach to the tea garden communities and identify innovative approaches for delivery of anthelmintic to the vulnerable age groups.

Figure 3 House yard of rural tea garden community of Sylhet, Bangladesh, early 2014.

Study limitations

Financial constraints made it difficult to check for false negatives using a more sensitive method like formal-ether concentration technique as it is known that Kato- Katz technique tends to have low sensitivity in the diagnosis of intestinal helminths particularly in areas with high proportions of low intensity of infections.31,32 Therefore, there could be some false negative, thus underestimating the prevalence.

Conclusion

T. trichiura infection is prevalent both in the children and adult. The determinants of the infections suggest proper disposal of human stool, anthelmintic taking four month intervals in the slum rural areas to reduce the worms’ burden in the community.

Acknowledgements

The Authors thankful to International Center for Diarrhoeal Disease Research Bangladesh (icddr’b), Dhaka, Bangladesh for their logistic supports and providing laboratory facilities. We also thank the Department of Parasitology, Sylhet Agricultural University, Sylhet. We also acknowledge the contribution of the study participants.

Conflict of interest

There is no conflict to publish the article in this Journal.

References

  1. Tadesse G. The prevalence of intestinal helminthic infections and associated risk factors among school children in Babile town, eastern Ethiopia. Ethiopian Journal of Health Development. 2005;19(2):140−147.
  2. Ogbe MG, Edet E, Isichel M. Intestinal helminth infection in primary school children in areas of operation of Shell Petroleum Development Company of Nigeria (SPDC), Western Division in Delta State. Nigerian Journal of Parasitology. 2006;23(1):3−10.
  3. Chan MS. The global burden of intestinal nematode infections-fifty years on. Parasitol today. 1997;13(11):438−443.
  4. WHO technical report series. 2002;912:57.
  5. Cairncross S, Bartram J, Cumming O, et al. Hygiene, sanitation, and water: what needs to be done? PLoS medicine. 2010;7(11):1366.
  6. Bethony J, Brooker S, Albonico M, et al. Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet. 2006;367(9521):1521−1532.
  7. Khanum H, Rahman F, Zaman RF. Occurrence of intestinal parasites among the teachers, students and staffs of Dhaka University. Journal of the Asiatic Society of Bangladesh, Science. 2014;39(2):239−246.
  8. Bangladesh Medical Research Council Bulletin. 1985;11(2):69−74.
  9. Hotez PJ, Brindley PJ, Bethony JM, et al. Helminth infections: the great neglected tropical diseases. J Clin Invest. 2008;118(118 (4):1311−1321.
  10. Wang X, Zhang L, Luo R, et al. Soil-transmitted helminth infections and correlated risk factors in preschool and school-aged children in rural southwest China. PLoS One. 2012;7(9):e45939.
  11. WHO. Soil-transmitted helminthiases: number of children treated in 2012. WHO Weekly Epidemiological Record No, 2014. 13: p. 89.
  12. www.banglapedia.org/HT/S_0739.htm
  13. Islam S. Banglapedia: national encyclopedia of Bangladesh/chief editor, Sirajul Islam; managing editor, Sajahan Miah. Asiatic society of Bangladesh; 2003.
  14. Katz N, Chaves A, Pellegrino JA. A simple device for quantitative stool thick-smear technique in schistosomiasis mansoni. Rev Inst Med Trop Sao Paulo. 1972;14(6):397−400.  
  15. WHO. Cellophane faecal thick smear examination technique (Kato) for diagnosis of intestinal schistosomiasis and gastrointestinal helminth infections. PDP/83.3, WHO, Geneva: 1983.
  16. Gilgen DD, Mascie-Taylor CG, Rosetta LL. Intestinal helminth infections, anaemia and labour productivity of female tea pluckers in Bangladesh. Trop Med Int Health. 2001;6(6):449−457.
  17. Sultana Y, Gilbert GL, Ahmed BN, et al. Strongyloidiasis in a high risk community of Dhaka, Bangladesh. Trans R Soc Trop Med Hyg. 2012;106(12):756−762.
  18. Kounnavong S, Vonglokham M, Houamboun K, et al. Soil-transmitted helminth infections and risk factors in preschool children in southern rural Lao People's Democratic Republic. Trans R Soc Trop Med Hyg. 2011;105(3):160−166.
  19. Amare B, Ali J, Moges B, et al. Nutritional status, intestinal parasite infection and allergy among school children in Northwest Ethiopia. BMC pediatr. 2013;13(1):7.
  20. Escobedo AA, Cañete R, Núñez FA. Prevalence, risk factors and clinical features associated with intestinal parasitic infections in children from San Juan y Martínez, Pinar del Río, Cuba. West Indian Med J. 2008;57(4):378−382.
  21. Michael E. This wormy world: Fifty years on. The challenge of controlling common helminthiases of humans today. Parasit Today. 1997;13(11):407−408.
  22. Steenhard NR, Ørnbjerg N, Mølbak K. Concurrent infections and socioeconomic determinants of geohelminth infection: a community study of schoolchildren in periurban Guinea-Bissau. Trans R Soc Trop Med H. 2009;103(8):839−845.
  23. Tarafder MR, Carabin H, Joseph L, et al. Estimating the sensitivity and specificity of Kato-Katz stool examination technique for detection of hookworms, Ascaris lumbricoides and Trichuris trichiura infections in humans in the absence of a ‘gold standard’. Int J Parasitol. 2010;40(4):399−404.
  24. Ezeamama AE, McGarvey ST, Acosta LP, et al. The synergistic effect of concomitant schistosomiasis, hookworm, and trichuris infections on children’s anemia burden. PLoS Negl Trop Dis. 2008;2(6):e245.
  25. Matthys B, Bobieva M, Karimova G, et al. Prevalence and risk factors of helminths and intestinal protozoa infections among children from primary schools in western Tajikistan. Parasit Vectors. 2011;4(1):195.
  26. Gungoren B. Effect of hygiene promotion on the risk of reinfection rate of intestinal parasites in children in rural Uzbekistan. Transactions of the Royal Society of Tropical Medicine and Hygiene. 2007;101(6):564−569.
  27. Zheng Q, Ying C, Hao-Bing z, et al. The control of hookworm infection in China. Parasit Vectors. 2009;2(1):44.
  28. Ngui R, Ishak S, Chuen CS, et al. Prevalence and risk factors of intestinal parasitism in rural and remote West Malaysia. PLoS Negl Trop Dis. 2011;5(3):e974.
  29. Phommasack B, Saklokham K, Chanthavisouk C, et al. Coverage and costs of a school deworming programme in 2007 targeting all primary schools in Lao PDR. Trans R Soc Trop Med Hyg.2008;102(12):1201−1206.
  30. Kojima S, Yoshiki A, Nobuo O, et al. School-health-based parasite control initiatives: extending successful Japanese policies to Asia and Africa. Trends in parasitology. 2007;23(2):54−57.
  31. Knopp S, Mgeni AF, Khamis IS, et al. Diagnosis of soil-transmitted helminths in the era of preventive chemotherapy: effect of multiple stool sampling and use of different diagnostic techniques. PLoS Negl Trop Dis. 2008;2(11):e331.
  32. Hossain M. et al. Prevalence and determinants of trichuris trichiura infection in tea garden community of sylhet, Bangladesh. 21th BSVER Annual Scientific Conference, BAU, Bangladesh, 2016; 63.
Creative Commons Attribution License

©2018 Hossain, et al. This is an open access article distributed under the terms of the, which permits unrestricted use, distribution, and build upon your work non-commercially.

Citations