INTRODUCTION
An estimated 0.8–1.2 billion people worldwide are infected with the parasite Ascaris lumbricoides,1 and Afghanistan reports the fourth highest national prevalence in the world at 36%.2 Embryos develop in the soil from excreted ova, and are transmitted to new hosts through food or water. Most infections are asymptomatic; however, as prevalence of the disease increases in a community, the intensity of infection becomes greater,3 and individuals may exhibit symptoms such as physical wasting, anemia, intestinal blockage, bowel obstruction, diarrhea, and pneumonitis.4
Because ascariasis is preventable with adequate sanitation systems and regular hand washing, a greater prevalence of ascariasis in an area reflects high poverty and inadequate public health infrastructure.5 These factors are particularly pertinent in Afghanistan, whose Human Development Index is 0.468, the lowest of any country outside of Africa,6 and a poverty rate of 36.5%.7 The infrastructure of Afghanistan’s cities has been stressed by sustained civil conflict and rapid urbanization,8 as economic and educational opportunities in places such as Kabul attract rural migrants.9
Little is known about ascariasis risk factors or the use of anthelminthics in Afghanistan, although a survey conducted in 2003 found that 57.3% of children between 8 and 15 years of age in Kabul were infected (which was higher than other areas, e.g., 27% in Nangarhar).10 Globally, ascariasis prevention focuses on the household as a primary setting for transmission and young children the highest incidence of disease, although older adolescents and young adults maintain a high prevalence of disease.4,11 Not having a latrine and handwashing after defecation were significantly related to ascariasis in studies of children in Delhi, India,12 children in Northern Area, Pakistan,13 and tea workers in Assam, India.14
In a study of university students from Kabul, Afghanistan, we investigated how behaviors and access to sanitary measures differed between students living in different housing conditions and who came from disparate regions of Afghanistan. We also measured the prevalence of ascariasis and identified risk factors for infection.
MATERIALS AND METHODS
Study population.
Established in 1932, Kabul Medical University (KMU) contains a medical school and faculties for allied health fields. The university attracts students from all over Afghanistan, and students either live in a private household (e.g., family in the area) or in a group hostel, which can be crowded and lack proper sanitary and food preparation facilities.
Students attending KMU were selected into this cross-sectional study through a stratified, convenience sampling method. During class, students from seven faculties were approached to participate, to ensure a representative sample of the university. Twenty students were selected from each faculty from each year, so that Curative and Stomatology (5-year programs) had more students than Public Health or Nursing (4-year programs), Technology or Anesthesiology (3-year programs at the time of the study), or Midwifery (2-year programs at the time of the study). An equal number of students living in hostels and living in houses was chosen for each year in each faculty. Our sample size was calculated based on an expected ascariasis prevalence of 24% and a desired confidence interval width of 5%. With an α level of 0.05 and a design effect of 2, 524 participants would be necessary.
Microscopy.
Participants provided researchers with a fresh stool sample in a sterilized specimen container. Approximately 40 mg was uniformly spread over a 20-mm distance on a slide, with a coverslip set on top. Two microbiologists, both trained in medical microbiology and each with over 10 years of laboratory experience, examined slides for the presence of A. lumbricoides ova through simple microscopy using a CH20 Olympus microscope (Olympus Corporation, Tokyo, Japan) at ×40 magnification (0.65 aperture) at laboratories in the KMU Microbiology Department.
Statistical analysis.
Significance of the bivariate associations was assessed using Pearson’s χ2 test or the Cochran–Armitage trend test. We corrected for multiple testing through the sequential Holm–Bonferroni method. A multivariable model was constructed with explanatory variables that had a statistically significant relationship with ascariasis in the bivariate analysis. The model specified a Poisson regression with robust variance estimation, which output estimates of prevalence ratios and 95% confidence intervals (CI). A P value of < 0.05 was considered statistically significant. Analyses were performed in SAS version 9.3 (SAS Institute, Cary, NC).
Ethics statement.
This study was approved by the Ethics Committee at the KMU. Participants provided a signed informed consent before enrollment. The questionnaire and informed consent documents are in the Supplemental Appendix.
RESULTS
In total, 525 students were asked to participate, and 520 completed the survey. The average age of participants was 20.7 years. Students came from 29 regions of Afghanistan with only 22.9% originally from Kabul. Demographic characteristics and hygienic practices differed by residential place (Table 1). For example, those living in hostels were more likely to eat street food (51.2%) than those living in a house (45.8%).
Differences in demographic characteristics or hygienic practices and residential place, Kabul, Afghanistan, 2014–2015
| Count | Living in hostel, count (%) | Living in house, count (%) | P value* | |
|---|---|---|---|---|
| Overall | 520 | 260 | 260 | |
| Sex | ||||
| Male | 289 | 172 (66.2) | 117 (45.0) | 0.0012 |
| Female | 231 | 88 (33.8) | 143 (55.0) | |
| Province of origin | ||||
| Not Kabul | 401 | 251 (96.5) | 150 (57.7) | 0.0012 |
| Kabul | 119 | 9 (3.5) | 110 (42.3) | |
| Source of water | ||||
| Piped water | 290 | 146 (56.2) | 144 (55.4) | 0.0012 |
| Well water | 159 | 80 (30.8) | 79 (30.4) | |
| Bottled water | 46 | 18 (6.9) | 28 (10.8) | |
| Other | 25 | 16 (6.2) | 9 (3.5) | |
| Eat street food | ||||
| Yes | 252 | 133 (51.2) | 119 (45.8) | 1.00 |
| No | 267 | 127 (48.8) | 140 (53.8) | |
| Eat unwashed vegetables | ||||
| Yes | 66 | 45 (17.3) | 21 (8.1) | 0.0120 |
| No | 453 | 214 (82.3) | 239 (91.9) | |
| Wash hands before eating | ||||
| Yes | 487 | 244 (93.8) | 243 (93.5) | 1.00 |
| No | 33 | 16 (6.2) | 17 (6.5) | |
| Wash hands after using toilet | ||||
| Yes | 437 | 217 (83.5) | 220 (84.6) | 1.00 |
| No | 82 | 43 (16.5) | 39 (15.0) | |
| Need to wash hands before eating and after using toilet | ||||
| Yes | 499 | 248 (95.4) | 251 (96.5) | 1.00 |
| No | 21 | 12 (4.6) | 9 (3.5) | |
| Garbage for solid waste disposal | ||||
| Yes | 380 | 191 (73.5) | 189 (72.7) | 1.00 |
| No | 133 | 64 (24.6) | 69 (26.5) | |
| Clean toilet inside hostel | ||||
| Yes | 182 | 101 (38.8) | 81 (31.2) | 0.4263 |
| No | 335 | 157 (60.4) | 178 (68.5) | |
| Disinfect toilets | ||||
| Yes | 160 | 81 (31.2) | 79 (30.4) | 1.00 |
| No | 359 | 179 (68.8) | 180 (69.2) | |
| Ascaris eggs in stool | ||||
| No | 438 | 205 (78.8) | 233 (89.6) | 0.0072 |
| Yes | 82 | 55 (21.2) | 27 (10.4) |
From Pearson’s χ2 test of independence. Adjusted for multiple testing with the Holm–Bonferroni method.
Approximately 15.8% of the participants had ascariasis (Table 2). Prevalence decreased over the participant’s year of study, with first-year students having higher prevalence of ascariasis (25.0%) than fifth-year students (5.0%) (P = 0.0014). People living in a hostel had greater prevalence of ascariasis (21.2%) than those living in a house (10.4%) (P = 0.008). Students eating street food and eating unwashed vegetables had higher prevalence of ascariasis than those who did not (P = 0.0014 for both variables). Washing hands before eating was protective against ascariasis (P = 0.008). Washing hands after using the toilet was also significantly associated with a lower prevalence of ascariasis (P = 0.008).
Bivariate associations between demographic characteristics or hygienic practices and prevalence of Ascaris, Kabul, Afghanistan, 2014–2015
| Ascaris eggs in stool | |||
|---|---|---|---|
| Count | Count (%) | P value* | |
| Overall | 520 | 82 (15.8) | |
| Sex | |||
| Male | 289 | 47 (16.3) | 1.00 |
| Female | 231 | 35 (15.2) | |
| Year of study | |||
| 1 | 140 | 35 (25.0) | 0.0014 |
| 2 | 140 | 23 (16.4) | |
| 3 | 120 | 15 (12.5) | |
| 4 | 80 | 7 (8.8) | |
| 5 | 40 | 2 (5.0) | |
| Faculty | |||
| Curative | 100 | 12 (12.0) | 0.33 |
| Stomatology | 100 | 8 (8.0) | |
| Public Health | 80 | 15 (18.8) | |
| Nursing | 80 | 15 (18.8) | |
| Midwifery | 40 | 7 (17.5) | |
| Technology | 60 | 10 (16.7) | |
| Anesthesiology | 60 | 15 (25.0) | |
| Province of origin | |||
| Not Kabul | 401 | 71 (17.7) | 0.17 |
| Kabul | 119 | 11 (9.2) | |
| Residential place | |||
| Hostel | 260 | 55 (21.2) | 0.0080 |
| House | 260 | 27 (10.4) | |
| Source of water | |||
| Piped water | 290 | 28 (9.7) | 0.0014 |
| Well water | 159 | 44 (27.7) | |
| Bottled water | 46 | 3 (6.5) | |
| Other | 25 | 7 (28.0) | |
| Eat street food | |||
| Yes | 252 | 74 (29.4) | 0.0014 |
| No | 267 | 8 (3.0) | |
| Eat unwashed vegetables | |||
| Yes | 66 | 42 (63.6) | 0.0014 |
| No | 453 | 40 (8.8) | |
| Wash hands before eating | |||
| Yes | 487 | 70 (14.4) | 0.0080 |
| No | 33 | 12 (36.4) | |
| Wash hands after using toilet | |||
| Yes | 437 | 59 (13.5) | 0.0080 |
| No | 82 | 23 (28.0) | |
| Need to wash hands before eating and after using toilet | |||
| Yes | 499 | 75 (15.0) | 0.17 |
| No | 21 | 7 (33.3) | |
| Garbage for solid waste disposal | |||
| Yes | 380 | 52 (13.7) | 0.34 |
| No | 133 | 27 (20.3) | |
| Clean toilet inside residence | |||
| Yes | 182 | 22 (12.1) | 0.34 |
| No | 335 | 60 (17.9) | |
| Disinfect toilets | |||
| Yes | 160 | 24 (15.0) | 1.00 |
| No | 359 | 58 (16.2) | |
From Pearson’s χ2 test of independence for all variables except year of study, which used the Cochran–Armitage trend test. Adjusted for multiple testing with the Holm–Bonferroni method.
Table 3 shows the multivariable regression. Each additional year of study in Kabul was associated with 0.73 times the prevalence of ascariasis compared with the previous year (95% CI: 0.61, 0.88), and residing in a hostel was associated with 1.61 times higher prevalence of ascariasis compared with those living in a house (95% CI: 1.13, 2.30). Using well water, eating street food, and eating unwashed vegetables were all associated with higher prevalence of ascariasis. Washing hands before eating was associated with decreased prevalence of ascariasis.
Multivariable associations between demographic characteristics or hygienic practices and prevalence of Ascaris eggs in stool, Kabul, Afghanistan, 2014–2015
| Prevalence ratio* (95% confidence interval) | P value | |
|---|---|---|
| Year of study (continuous) | 0.73 (0.61, 0.88) | 0.0009 |
| Live in hostel vs. house | 1.61 (1.13, 2.30) | 0.0089 |
| Use well water vs. use piped water | 2.18 (1.47, 3.22) | < 0.0001 |
| Use other water vs. use piped water | 1.22 (0.71, 2.09) | 0.47 |
| Eat street food (yes vs. no) | 7.56 (3.73, 15.33) | < 0.0001 |
| Eat unwashed vegetables (yes vs. no) | 3.22 (2.15, 4.82) | < 0.0001 |
| Wash hands before eating (yes vs. no) | 0.38 (0.23, 0.63) | 0.0002 |
| Wash hands after using the toilet (yes vs. no) | 2.08 (1.31, 3.32) | 0.0021 |
From Poisson regression with robust variance estimation.
DISCUSSION
A high prevalence of ascariasis is common in low-income countries; poor public health and municipal infrastructure result in limited access to sanitation and clean water, inadequate hygienic practices, and greater infectious morbidity in the presence of greater population density.4 This study found a high prevalence of ascariasis in a university student population in Kabul, Afghanistan. Kabul is one of the five fastest growing cities in the world, and in 2015 was home to approximately 3.7 million people.15 As the population has rapidly expanded, the city has faced housing shortages and a decaying sanitary infrastructure.16,17 Ascariasis was particularly high among those living in hostels, or group homes, and could be explained in part through differences in hygienic behaviors: for instance, students in hostels more commonly consumed well water and unwashed vegetables. Location characteristics have been previously identified as a strong predictors of ascariasis.13 In Assam, India, people living in crowded households (≥ ;6 people), not dissimilar to the crowded hostels we encountered, had higher prevalence of ascariasis (48.0%) than those in less crowded households (29.2%).14
About half of all students in this study regularly consumed street food—the strongest predictor of ascariasis. A study among schoolchildren in Ethiopia also found an association between eating street food and helminth infections,18 and eating or preparing street food has been linked to risk of other gastrointestinal infections, such as Salmonella.19 Encouraging students to prepare their own food, including lunch brought to the university, could be one simple method to reduce infections.
Limitations.
This study was cross-sectional, and we were unable to evaluate temporality of these associations, including if students from outside Kabul were infected in Kabul or their home province. We also focused on university students, who as an age group are at high risk for infection, but who are likely to be economically privileged compared with young adults who are not attending university. Additionally, ascertainment of ascariasis was through microscopy, other methods such as the Kato–Katz technique and polymerase chain reaction are more sensitive and have higher negative predictive value,20 and we cannot discount the possibility of miscategorizing other parasitic infections as ascariasis. The Kato–Katz stain was not available at KMU during the study period. Our outcome did not quantify the intensity of infection, which is an important predictor of the degree of illness. Our study was also limited by not collecting additional information on socioeconomic status, previous helminth infections, concurrent parasite infections, or history of receiving anthelminthic therapy.
Conclusions.
Ascariasis leads to chronic malnutrition and other serious health outcomes. In this study of university students in Kabul, Afghanistan, most of whom were recent migrants into the city, many engaged in unhygienic practices, like eating unwashed vegetables and not washing hands. Because the prevalence of positive hygienic behaviors was lower among students who lived in hostels than in houses, these dwellings can be targeted for future interventions. Encouraging students to prepare their own food, to regularly wash hands, and to not use street vendors would be important steps in reducing risk of this infection in Afghanistan. This study may also be a call to routinely screen matriculants for parasites and/or provide mass treatment with anthelminthic therapy on admission.
Acknowledgments:
We would like to thank the study team from Kabul Medical University who diligently carried out the survey and the microbiologists who evaluated the samples. We are thankful to Alexander Rickard for his comments and intellectual contributions to the paper.
REFERENCES
- 1.↑
Centers for Disease Control and Prevention, 2016. Parasites—Ascariasis. Available at: http://www.cdc.gov/parasites/ascariasis/index.html. Accessed September 29, 2016.
- 2.↑
Pullan RL, Smith JL, Jasrasaria R, Brooker SJ, 2014. Global numbers of infection and disease burden of soil transmitted helminth infections in 2010. Parasit Vectors 7: 37.
- 3.↑
Hall A, Anwar KS, Tomkins A, Rahman L, 1999. The distribution of Ascaris lumbricoides in human hosts: a study of 1765 people in Bangladesh. Trans R Soc Trop Med Hyg 93: 503–510.
- 4.↑
Hall A, Hewitt G, Tuffrey V, De Silva N, 2008. A review and meta-analysis of the impact of intestinal worms on child growth and nutrition. Matern Child Nutr 4 (Suppl 1): 118–236.
- 5.↑
Bethony J, Brooker S, Albonico M, Geiger SM, Loukas A, Diemert D, Hotez PJ, 2006. Soil-transmitted helminth infections: ascariasis, trichuriasis and hookworm. Lancet 367: 1521–1532.
- 6.↑
United Nations High Commissioner for Refugees, 2015. UNHCR—Afghanistan. Available at: http://www.unhcr.org/pages/49e486eb6.html. Accessed November 12, 2015.
- 7.↑
Varkey S, Higgins-Steele A, Mashal T, Hamid BA, Bhutta ZA, 2015. Afghanistan in transition: call for investment in nutrition. Lancet Glob Health 3: e13–e14.
- 8.↑
United Nations Department of Economic and Social Affairs, 2014. Afghanistan. Available at: http://esa.un.org/unpd/wup/Country-Profiles/. Accessed October 15, 2015.
- 10.↑
Gabrielli AF, Ramsan M, Naumann C, Tsogzolmaa D, 2005. Soil-transmitted helminths and haemoglobin status among Afghan children in World Food Programme assisted schools. J Helminthol 79: 381–384.
- 11.↑
Cairncross S, Blumenthal U, Kolsky P, Moraes L, Tayeh A, 1996. The public and domestic domains in the transmission of disease. Trop Med Int Health 1: 27–34.
- 12.↑
Ranjan S, Passi SJ, Singh SN, 2013. Prevalence and risk factors associated with the presence of soil-transmitted helminths in children studying in Municipal Corporation of Delhi Schools of Delhi, India. J Parasit Dis 39: 377–384.
- 13.↑
Nishiura H, Imai H, Nakao H, Tsukino H, 2002. Ascaris lumbricoides among children in rural communities in the northern area, Pakistan: prevalence, intensity, and associated socio-cultural and behavioral risk factors. Acta Trop 83: 223–231.
- 14.↑
Traub RJ, Robertson ID, Irwin P, Mencke N, Thompson RCA, 2004. The prevalence, intensities and risk factors associated with geohelminth infection in tea-growing communities of Assam, India. Trop Med Int Health 9: 688–701.
- 15.↑
GeoHive, 2016. Afghanistan: Administrative Units, Extended. Available at: http://www.geohive.com/cntry/afghanistan_ext.aspx. Accessed June 27, 2016.
- 16.↑
Setchell CA, Luther CN, 2009. Kabul, Afghanistan: a case study in responding to urban displacement. Humanit Exch Mag 45: 33–36.
- 17.↑
Mubarak MY, Wagner AL, Asami M, Carlson BF, Boulton ML, 2016. Hygienic practices and diarrheal illness among persons living in at-risk settings in Kabul, Afghanistan: a cross-sectional study. BMC Infect Dis 16: 459.
- 18.↑
Tadesse G, 2005. The prevalence of intestinal helminthic infections and associated risk factors among school children in Babile town, eastern Ethiopia. Ethiop J Health Dev 19: 140–147.
- 19.↑
Vollaard A, Ali S, van Asten HAGH, Ismid IS, Widjaja S, Visser LG, Surjadi C, van Dissel JT, 2004. Risk factors for transmission of foodborne illness in restaurants and street vendors in Jakarta, Indonesia. Epidemiol Infect 132: 863–872.
- 20.↑
Periago MV, Diniz RC, Pinto SA, Yakovleva A, Correa- R, Diemert DJ, Bethony JM, 2015. The right tool for the job : detection of soil-transmitted helminths in areas co-endemic for other helminths. PLoS Negl Trop Dis 9: e0003967.