A Half-Century Studies on Epidemiological Features of Ancylostomiasis in China: A Review Article
-
Rui LI
,
Jie GAO
,
Lingxi GAO
,
Yajun LU
Abstract
Background: Ancylostomiasis is a prevalent and global parasitic disease, including China. A systematic review is significant to understand the epidemiological features of hookworm and provide guidance for prevention and treatment.
Methods: We systematically searched academic databases and assessed 944 papers published from1955-2015 to establish the comprehensive analysis of prevalence of hookworm disease in China. We searched Chinese databases, including CNKI, Wanfang and VIP, for literature with the subject word "Ancylostomiasis and hookworm". The data were analyzed with SPSS 19.0 software using Spearman correlation analysis. Results were statistically significant for a P-value of <0.01.
Results: The search yielded 532,151 cases from epidemiological investigation and 7294 cases based on hospital diagnosis. Hookworm infection was highest (15.83%) in Fujian province, with high rates also found in East China, Southwest China, Central China and Southern China and lower rates in Northwest China, North China and Northeast China. In terms of occupation, farmers had the highest proportion of infections (72.54%). There was no correlation between epidemiological investigations and hospital-diagnosed cases. However, there was significant positive correlation between hospital-diagnosed cases and misdiagnosed cases. The proportion of hospital-misdiagnosed cases was 32.80%.
Conclusion: Ancylostomiasis is a serious public health problem that negatively influences health and hinders socioeconomic development. Positive measures are required by both health services and individuals to prevent and control hookworm disease.
1. Bethony J, Brooker S, Albonico M et al (2006). Soil-transmitted helminth infections: ascariasis, trichuriasis, and hook-worm.Lancet, 367 (9251):1521-1532.
2. Brooker S, Clements AC, Bundy DA (2006). Global epidemiology, ecology and con-trol of soil-transmitted helminth infections. Adv Parasitol, 62:221-261.
3. Humphries D, Nguyen S, Boakye D et al (2012). The promise and pitfalls of mass drug administration to control intestinal helminth infections. Curr Opin Infect Dis, 25 (5): 584-589.
4. Tariq M, Muzammil SM, Shaikh FA et al (2017). Hookworm infestation as a cause of melena and severe anaemia in farmer. J Pak Med Assoc, 67 (2):327-329.
5. Lloyd-Sherlock P (2000). Population ageing in developed and developing regions: implications for health policy. Soc Sci Med, 51 (6):887-895.
6. Jia TW, Melville S, Utzinger J et al (2012). Soil-transmitted helminth hreinfection after drug treatment: a systematic review and meta-analysis. PLoS Negl Trop Dis, 6 (5):e1621.
7. de Silva NR, Brooker S, Hotez PJ et al (2003). Soil-transmitted helminth infections: updating the global picture. Trends Parasi-tol, 19 (12):547-551.
8. Rabelo ÉML, Miranda RRC, Furtado LFV et al (2017). Development of new mi-crosatellites for the hookworm Ancylostoma caninum and analysis of genetic diversity in Brazilian populations. Infect Genet Evol, 51:24-27.
9. Hotez PJ, Feng Z, Xu LQ et al (1997). Emerging and reemerging helminthiases and the public health of China. Emerg In-fect Dis, 3 (3):303-310.
10. Xu LQ, Yu SH, Jin ZX et al (1995). Soil-transmitted helminthiases: nationwide survey in China. Bull World Health Organ, 73 (4):507-513.
11. Xu LQ, Chen YD, Sun FH et al (2005). A National survey on current status of the important parasitic diseases in human population. Chin J Parasitol Parasit Dis, 23 (5):332-340.
12. de Winter JC, Gosling SD, Potter J (2016). Comparing the Pearson and Spearman correlation coefficients across distribu-tions and sample sizes: A tutorial using simulations and empirical data. Psychol Methods, 21 (3):273-290.
13. Bishara AJ, Hittner JB (2012). Testing the significance of a correlation with nonnormal data: comparison of Pearson, Spearman, transformation, and resampling approaches. Psychol Methods, 17 (3):399-417.
14. Artusi R, Verderio P, Marubini E (2002). Bravais-Pearson and Spearman correla-tion coeffici- ents: meaning, test of hy-pothesis and confidence interval. Int J Biol Markers, 17 (2):148-151.
15. Steinmann P, Du ZW, Wang LB et al (2008). Extensive multiparasitism in a village of Yunnan province, People’s Republic of China, revealed by a suite of diagnostic methods. Am J Trop Med Hyg, 78 (5):760-769.
16. Booth M, Vounatsou P, N’Goran EK et al (2003). The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma man-soni and hookworm co-infections in rural Coˆted’Ivoire. Parasitology, 127 (6):525-531.
17. Yu SH, Xu LQ, Jiang ZX et al (1994). Na-tionwide survey of human parasites in China. Southeast Asian J Trop Med Public Health, 25 (1):4-10.
18. Truscott JE, Turner HC, Farrell SH et al (2016). Soil-Transmitted Helminths: mathe-matical models of transmission, the im-pact of mass drug administration and transmission elimination criteria. Adv Par-asitol, 94:133-198.
19. Richards JC, Behnke JM, Duce IR (1995). In vitro studies on the relative sensitivity to ivermectin of Necator americanus and Ancylostoma ceylanicum. Int J Parasitol, 25 (10):1185-91.
20. Chu D, Bungiro RD, Ibanez M et al (2004). Molecular characterization of Ancylostoma ceylanicum Kunitz-type serine prote-ase inhibitor: evidence for a role in hook-worm associated growth delay. Infect Immun, 72 (4):2214-2221.
21. Kotze AC, Coleman GT, Mai A et al (2005). Field evaluation of anthelmintic drug sen-sitivity using in vitro egg hatch and larval motility assays with Necator americanus re-covered from human clinical isolates. Int J Parasitol, 35 (4):445-453.
22. Kumar S, Pritchard DI (1992). Secretion of metalloproteases by living infective larvae of Necator americanus. J Parasitol, 78 (5):917-919.
23. Heukelbach J, Feldmeier H (2008). Epidemi-ological and clinical characteristics of hookworm-related cutaneous larva migrans. Lancet Infect Dis, 8 (5):302-309.
24. Yong W, Guangjin S, Weitu W, Shuhua X et al (1999). Epidemiology of human ancylos-tomiasis among rural villagers in Nanlin County (Zhongzhou village), Anhui Prov-ince, China: age-associated prevalence, in-tensity and hookworm species identifica-tion. Southeast Asian J Trop Med Public Health, 30 (4):692-7.
25. Torgerson PR, Devleesschauwer B, Praet N et al (2015). World Health Organization estimates of the global and regional dis-ease burden of 11 foodborne parasitic diseases, 2010: a data synthesis. PLoS Med, 12 (12):e1001920.
26. Hotez PJ, Brindley PJ, Bethony JM et al (2008). Helminth infections: the great ne-glected tropical diseases. J Clin Invest, 118 (4):1311-21.
27. Verweij JJ, Brienen EA, Ziem J et al (2007). Simultaneous detection and quantification of Ancylostoma duodenale, Necator americanus, and Oesophagostomum bifurcum in fecal sam-ples using multiplex real-time PCR. Am J Trop Med Hyg, 77 (4):685-690.
28. Humphries DL, Stephenson LS, Pearce EJ et al (1997). The use of human faeces for fertilizer is associated with increased in-tensity of hookworm infection in Viet-namese women. Trans R Soc Trop Med Hyg, 91 (5):518-20.
29. Brooker S, Clements AC, Hotez PJ et al (2006). The co-distribution of Plasmodi-um falciparum and hookworm among African school children. Mal J, 3;5:99.
30. Hotez PJ, Brooker S, Bethony JM et al (2004). Hookworm Infection. Ne Engl J Med, 351 (8):799-807.
31. Haas W, Haberl B, Syafruddin et al (2005). Infective larvae of the human hookworms Necator americanus and Ancy-lostoma duodenale differ in their orienta-tion behavior when crawling on surfaces. Parasitol Res, 95 (1):25-29.
32. Staudacher O, Heimer J, Steiner F et al (2014). Soil-transmitted helminths in southern highland Rwanda: associated factors and effectiveness of school-based preventive chemotherapy. Trop Med Int Health, 19 (7):812-824.
33. Bottazzi ME (2015). The human hookworm vaccine: recent updates and prospects for success. J Helminthol, 89 (5):540-544.
34. Brooker S, Hotez PJ, Bundy DA (2008). Hookworm-related anemia among preg-nant women: a systematic review. PLoS Negl Trop Dis, 2 (9):e291.
35. Hotez PJ, Bethony JM, Diemert DJ et al (2010). Developing vaccines to combat hookworm infection and intestinal schis-tosomiasis. Nat Rev Microbiol, 8 (11):814-826.
36. Croese J, Giacomin P, Navarro S et al (2015). Experimental hookworm infec-tion and gluten microchallenge promote tolerance in celiac disease. J Allergy Clin Immunol, 135 (2):508-516.
37. Utzinger J, Rinaldi L, Lohourignon LK et al (2008). FLOTAC: a new sensitive tech-nique for the diagnosis of hookworm in-fections in humans. Trans R Soc Trop Med Hyg, 102 (1): 84-90.
38. Keiser J, Utzinger J (2008). Efficacy of cur-rent drugs against soil-transmitted hel-minth infections: systematic review and meta-analysis. JAMA, 299 (16):1937-1948.
39. Horton J (2002). Albendazole: a broad spec-trum anthelminthic for treatment of indi-viduals and populations. Curr Opin Infect Dis, 15 (6):599-608.
40. Labianoabello N, Canese J, Velazquez ME et al (1999). Epidemiology of hookworm infection in Itagua, Paraguay: a cross sec-tional study. Mem Inst Oswaldo Cruz, 94 (5):583-586.
41. Makhoul Z, Taren D, Duncan B et al (2012). Risk factors associated with anemia, iron deficiency and iron deficiency anemia in rural Nepali pregnant women. Southwest Asian J Trop Med Public Health, 43 (3):735-746.
42. Brunet J, Lemoine J P, Lefebvre N et al (2015). Bloody diarrhea associated with Hookworm infection in Traveler return-ing to France from Myanmar. Emerg Infect Dis, 21 (10): 1878-1879.
43. Bergquist, R, Johansen MV, Utzinger J (2009). Diagnostic dilemmas in helmin-thology: what tools to use and when? Trends Parasitol, 25 (4):151-156.
44. Albonico, M, Ame, SM, Vercruysse J et al (2012). Comparison of the Kato-Katz thick smear and McMaster egg counting techniques for monitoring drug efficacy against soil-transmitted helminths in schoolchildren on Pemba Is-land,Tanzania. Trans R Soc Trop Med Hyg, 106 (3):199-201.
45. Midzi N, Mtapuri-Zinyowera S, Mapingure MP et al (2011). Knowledge attitudes and practices of grade three primary school-children in relation to schistosomiasis, soil transmitted helminthiasis and malaria in Zimbabwe. BMC Infect Dis, 11:169.
46. Howson CP (2000). Perspectives and needs for health in the 21st century: 20th-century paradigms in 21st-century sci-ence. J Hum Virol, 3 (2):94-103.
47. Pullan R, Brooker S (2008). The health im-pact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases? Parasitology, 135 (7):783-794.
48. Hotez PJ, Molyneux DH, Fenwick A et al (2007). Control of neglected tropical dis-eases. N Engl J Med, 357 (10):1018-1027.
49. Hotez PJ, Fenwick A, Savioli L et al (2009). Rescuing the bottom billion through con-trol of neglected tropical diseases. Lancet, 373 (9674):1570-1575.
2. Brooker S, Clements AC, Bundy DA (2006). Global epidemiology, ecology and con-trol of soil-transmitted helminth infections. Adv Parasitol, 62:221-261.
3. Humphries D, Nguyen S, Boakye D et al (2012). The promise and pitfalls of mass drug administration to control intestinal helminth infections. Curr Opin Infect Dis, 25 (5): 584-589.
4. Tariq M, Muzammil SM, Shaikh FA et al (2017). Hookworm infestation as a cause of melena and severe anaemia in farmer. J Pak Med Assoc, 67 (2):327-329.
5. Lloyd-Sherlock P (2000). Population ageing in developed and developing regions: implications for health policy. Soc Sci Med, 51 (6):887-895.
6. Jia TW, Melville S, Utzinger J et al (2012). Soil-transmitted helminth hreinfection after drug treatment: a systematic review and meta-analysis. PLoS Negl Trop Dis, 6 (5):e1621.
7. de Silva NR, Brooker S, Hotez PJ et al (2003). Soil-transmitted helminth infections: updating the global picture. Trends Parasi-tol, 19 (12):547-551.
8. Rabelo ÉML, Miranda RRC, Furtado LFV et al (2017). Development of new mi-crosatellites for the hookworm Ancylostoma caninum and analysis of genetic diversity in Brazilian populations. Infect Genet Evol, 51:24-27.
9. Hotez PJ, Feng Z, Xu LQ et al (1997). Emerging and reemerging helminthiases and the public health of China. Emerg In-fect Dis, 3 (3):303-310.
10. Xu LQ, Yu SH, Jin ZX et al (1995). Soil-transmitted helminthiases: nationwide survey in China. Bull World Health Organ, 73 (4):507-513.
11. Xu LQ, Chen YD, Sun FH et al (2005). A National survey on current status of the important parasitic diseases in human population. Chin J Parasitol Parasit Dis, 23 (5):332-340.
12. de Winter JC, Gosling SD, Potter J (2016). Comparing the Pearson and Spearman correlation coefficients across distribu-tions and sample sizes: A tutorial using simulations and empirical data. Psychol Methods, 21 (3):273-290.
13. Bishara AJ, Hittner JB (2012). Testing the significance of a correlation with nonnormal data: comparison of Pearson, Spearman, transformation, and resampling approaches. Psychol Methods, 17 (3):399-417.
14. Artusi R, Verderio P, Marubini E (2002). Bravais-Pearson and Spearman correla-tion coeffici- ents: meaning, test of hy-pothesis and confidence interval. Int J Biol Markers, 17 (2):148-151.
15. Steinmann P, Du ZW, Wang LB et al (2008). Extensive multiparasitism in a village of Yunnan province, People’s Republic of China, revealed by a suite of diagnostic methods. Am J Trop Med Hyg, 78 (5):760-769.
16. Booth M, Vounatsou P, N’Goran EK et al (2003). The influence of sampling effort and the performance of the Kato-Katz technique in diagnosing Schistosoma man-soni and hookworm co-infections in rural Coˆted’Ivoire. Parasitology, 127 (6):525-531.
17. Yu SH, Xu LQ, Jiang ZX et al (1994). Na-tionwide survey of human parasites in China. Southeast Asian J Trop Med Public Health, 25 (1):4-10.
18. Truscott JE, Turner HC, Farrell SH et al (2016). Soil-Transmitted Helminths: mathe-matical models of transmission, the im-pact of mass drug administration and transmission elimination criteria. Adv Par-asitol, 94:133-198.
19. Richards JC, Behnke JM, Duce IR (1995). In vitro studies on the relative sensitivity to ivermectin of Necator americanus and Ancylostoma ceylanicum. Int J Parasitol, 25 (10):1185-91.
20. Chu D, Bungiro RD, Ibanez M et al (2004). Molecular characterization of Ancylostoma ceylanicum Kunitz-type serine prote-ase inhibitor: evidence for a role in hook-worm associated growth delay. Infect Immun, 72 (4):2214-2221.
21. Kotze AC, Coleman GT, Mai A et al (2005). Field evaluation of anthelmintic drug sen-sitivity using in vitro egg hatch and larval motility assays with Necator americanus re-covered from human clinical isolates. Int J Parasitol, 35 (4):445-453.
22. Kumar S, Pritchard DI (1992). Secretion of metalloproteases by living infective larvae of Necator americanus. J Parasitol, 78 (5):917-919.
23. Heukelbach J, Feldmeier H (2008). Epidemi-ological and clinical characteristics of hookworm-related cutaneous larva migrans. Lancet Infect Dis, 8 (5):302-309.
24. Yong W, Guangjin S, Weitu W, Shuhua X et al (1999). Epidemiology of human ancylos-tomiasis among rural villagers in Nanlin County (Zhongzhou village), Anhui Prov-ince, China: age-associated prevalence, in-tensity and hookworm species identifica-tion. Southeast Asian J Trop Med Public Health, 30 (4):692-7.
25. Torgerson PR, Devleesschauwer B, Praet N et al (2015). World Health Organization estimates of the global and regional dis-ease burden of 11 foodborne parasitic diseases, 2010: a data synthesis. PLoS Med, 12 (12):e1001920.
26. Hotez PJ, Brindley PJ, Bethony JM et al (2008). Helminth infections: the great ne-glected tropical diseases. J Clin Invest, 118 (4):1311-21.
27. Verweij JJ, Brienen EA, Ziem J et al (2007). Simultaneous detection and quantification of Ancylostoma duodenale, Necator americanus, and Oesophagostomum bifurcum in fecal sam-ples using multiplex real-time PCR. Am J Trop Med Hyg, 77 (4):685-690.
28. Humphries DL, Stephenson LS, Pearce EJ et al (1997). The use of human faeces for fertilizer is associated with increased in-tensity of hookworm infection in Viet-namese women. Trans R Soc Trop Med Hyg, 91 (5):518-20.
29. Brooker S, Clements AC, Hotez PJ et al (2006). The co-distribution of Plasmodi-um falciparum and hookworm among African school children. Mal J, 3;5:99.
30. Hotez PJ, Brooker S, Bethony JM et al (2004). Hookworm Infection. Ne Engl J Med, 351 (8):799-807.
31. Haas W, Haberl B, Syafruddin et al (2005). Infective larvae of the human hookworms Necator americanus and Ancy-lostoma duodenale differ in their orienta-tion behavior when crawling on surfaces. Parasitol Res, 95 (1):25-29.
32. Staudacher O, Heimer J, Steiner F et al (2014). Soil-transmitted helminths in southern highland Rwanda: associated factors and effectiveness of school-based preventive chemotherapy. Trop Med Int Health, 19 (7):812-824.
33. Bottazzi ME (2015). The human hookworm vaccine: recent updates and prospects for success. J Helminthol, 89 (5):540-544.
34. Brooker S, Hotez PJ, Bundy DA (2008). Hookworm-related anemia among preg-nant women: a systematic review. PLoS Negl Trop Dis, 2 (9):e291.
35. Hotez PJ, Bethony JM, Diemert DJ et al (2010). Developing vaccines to combat hookworm infection and intestinal schis-tosomiasis. Nat Rev Microbiol, 8 (11):814-826.
36. Croese J, Giacomin P, Navarro S et al (2015). Experimental hookworm infec-tion and gluten microchallenge promote tolerance in celiac disease. J Allergy Clin Immunol, 135 (2):508-516.
37. Utzinger J, Rinaldi L, Lohourignon LK et al (2008). FLOTAC: a new sensitive tech-nique for the diagnosis of hookworm in-fections in humans. Trans R Soc Trop Med Hyg, 102 (1): 84-90.
38. Keiser J, Utzinger J (2008). Efficacy of cur-rent drugs against soil-transmitted hel-minth infections: systematic review and meta-analysis. JAMA, 299 (16):1937-1948.
39. Horton J (2002). Albendazole: a broad spec-trum anthelminthic for treatment of indi-viduals and populations. Curr Opin Infect Dis, 15 (6):599-608.
40. Labianoabello N, Canese J, Velazquez ME et al (1999). Epidemiology of hookworm infection in Itagua, Paraguay: a cross sec-tional study. Mem Inst Oswaldo Cruz, 94 (5):583-586.
41. Makhoul Z, Taren D, Duncan B et al (2012). Risk factors associated with anemia, iron deficiency and iron deficiency anemia in rural Nepali pregnant women. Southwest Asian J Trop Med Public Health, 43 (3):735-746.
42. Brunet J, Lemoine J P, Lefebvre N et al (2015). Bloody diarrhea associated with Hookworm infection in Traveler return-ing to France from Myanmar. Emerg Infect Dis, 21 (10): 1878-1879.
43. Bergquist, R, Johansen MV, Utzinger J (2009). Diagnostic dilemmas in helmin-thology: what tools to use and when? Trends Parasitol, 25 (4):151-156.
44. Albonico, M, Ame, SM, Vercruysse J et al (2012). Comparison of the Kato-Katz thick smear and McMaster egg counting techniques for monitoring drug efficacy against soil-transmitted helminths in schoolchildren on Pemba Is-land,Tanzania. Trans R Soc Trop Med Hyg, 106 (3):199-201.
45. Midzi N, Mtapuri-Zinyowera S, Mapingure MP et al (2011). Knowledge attitudes and practices of grade three primary school-children in relation to schistosomiasis, soil transmitted helminthiasis and malaria in Zimbabwe. BMC Infect Dis, 11:169.
46. Howson CP (2000). Perspectives and needs for health in the 21st century: 20th-century paradigms in 21st-century sci-ence. J Hum Virol, 3 (2):94-103.
47. Pullan R, Brooker S (2008). The health im-pact of polyparasitism in humans: are we under-estimating the burden of parasitic diseases? Parasitology, 135 (7):783-794.
48. Hotez PJ, Molyneux DH, Fenwick A et al (2007). Control of neglected tropical dis-eases. N Engl J Med, 357 (10):1018-1027.
49. Hotez PJ, Fenwick A, Savioli L et al (2009). Rescuing the bottom billion through con-trol of neglected tropical diseases. Lancet, 373 (9674):1570-1575.
| Files | ||
| Issue | Vol 48 No 9 (2019) | |
| Section | Review Article(s) | |
| DOI | https://doi.org/10.18502/ijph.v48i9.3011 | |
| Keywords | ||
| Hookworm Epidemiological features Hospital cases Misdiagnosis | ||
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How to Cite
1.
LI R, GAO J, GAO L, LU Y. A Half-Century Studies on Epidemiological Features of Ancylostomiasis in China: A Review Article. Iran J Public Health. 2019;48(9):1555-1565.
