Atalabi and Adubi BMC Infectious Diseases (2019) 19:73 https://doi.org/10.1186/s12879-018-3647-y

RESEARCHARTICLE Open Access The epidemiology and chemotherapeutic approaches to the control of urinary schistosomiasis in school-age children (SAC): a systematic review Tolulope Ebenezer Atalabi1* and Taiwo Oluwakemi Adubi2

Abstract Background: Human schistosomiases are acute and chronic infectious diseases of poverty. Currently, epidemiological data of urinary schistosomiasis (US) in school-age children (SAC) and adults are often reported together making it difficult to ascertain the true status of the disease. Based on this premise, we set out to carry out this review. Method: To achieve this aim, we carried out a computer-aided search of PubMed, Web of Science, Science Direct, African Journals OnLine (AJOL) and the database of World Health Organization. However, the information obtained from these sources was supplemented with additional literatures from Mendeley,ARTICLE Research Gate, and Google. Results: The search yielded 183 literatures of which 93 full text research, review and online articles were deemed fit for inclusion. Our key findings showed that: (1) of all World Health Organization (WHO) Regions, Africa is the most endemic zone for US, with Kenya and Senegal recording the highest prevalence and mean intensity respectively; (2) SAC within the range of 5–16 years contribute most significantly to the transmission cycle of US globally; (3) gender is a factor to watch out for, with male often recording the highest prevalence and intensity of infection; (4) contact with open, potentially infested water sources contribute significantly to transmission; (5) parental factors (occupation and education status) predispose SAC to US; (6) economic vis a vis ecological factors play a key role in infection transmission; and (7) in the last decade, a treatment coverage of 45% was never achieved globally for SAC or non-SAC treatment category for urinary schistosomiasis. Conclusion: In view of the WHO strategic plan to eliminate schistosomiasis by 2020 and the findings from this review, it is obvious that this goal, in the face of realities, might not be achieved. It is imperative that annual control programmes be scaled up marginally, particularly in the African region of WHO. While US-based researches should be sponsored at the grass-root level to unveil hidden endemic foci, adequate facilities for Water, Sanitation, and Hygiene (WASH) should be put in place in all schools globally. Keywords: Prevalence, Control, Urinary, Schistosomiasis, School, Children

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* Correspondence: [email protected] 1Department of Biological Sciences, Federal University, Dutsin-Ma, Km 65, P.M.B. 5001, Dutsin-Ma, , Full list of author information is available at the end of the article

© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Atalabi and Adubi BMC Infectious Diseases (2019) 19:73 Page 2 of 12

Background Currently, epidemiological data on prevalence, inten- Human schistosomiases are acute and chronic infectious sity and control of US in SAC and adults are often diseases associated with abject poverty in 78 low and reported together, thus making information peculiar to middle-income countries in the sub-tropical and tropical SAC to be insufficient in the literature. The implication parts of the world where there is negligible access to of this is that it is difficult to ascertain the epidemio- potable water and adequate sanitation. The agents of logical status of the disease in this group to enhance the etiology of these diseases are “blood-thirsty” digenetic success of control programmes targeting this group. trematodes in the genus Schistosoma [1, 2]. Based on this premise, the aim of this review article was Freshwater gastropod snails in the genus Bulinus are to study the epidemiology and chemotherapeutic strat- suitable intermediate hosts to Schistosoma haematobium egies to the control of US in SAC. which causes urinary schistosomiasis. The transmission gap of the disease is bridged when people come into Methods contact with unwholesome water sources [3–5] infested Search strategy with the cercariae (infective larval form) which mechan- We carried out a computer-aided search of PubMed, ically penetrates the skin of their human definitive hosts. Web of Science, Science Direct, African Journals OnLine A transmission cycle is consolidated when infected (AJOL) and the database of World Health Organization humans, due to lack of modern waste disposal facilities, (WHO). However, the information obtained from these indiscriminately pass urine-infested eggs in close prox- sources was supplemented with additional literatures imity to water bodies where they hatch into larval form from Mendeley, Research Gate, and Google. The (called miracidia) which infect Bulinus. In humans, cer- searches were performed independently by the authors cariae undergo series of larval migration before maturing using the key words: “urinary/urinary schistosomiasis” in into adults which migrate to the veins of the urinary combination with “prevalence”, “intensity”, “morbidity”, tract where gravid females lay a large number of eggs “control/praziquantel”, “school” and “children”. which are responsible for the various signs, symptoms ARTICLE and morbidity associated with the disease. The classical Selection criteria sign of urinary schistosomiasis is haematuria, a term Literatures that address prevalence, intensity, morbidity, coined to describe the presence of blood in urine. indicators or risk factors as well as the control of US, Genital schistosomiais causes pathological damage in without restriction to year of publication, were included both sexes, with females being more at risk of contract- in this review article. Besides, such papers addressed ing Human Immuno-Deficiency Virus (HIV) [6, 7]. school children specifically. The implication of this is Nonetheless, a review of the burden of schistosomiasis that articles exclusively addressing intestinal schistosom- has shown that over 200, 000 people die from the com- iasis or other Neglected Tropical Diseases were not plications due to the disease in Sub-Saharan Africa considered eligible for inclusion. (SSA) annually while children suffer anaemia, stunted growth [8, 9], urinary tract damage [10] and reduced Analysis and presentation of data mental ability to cope with academics. In advanced The secondary data presented in this manuscript were cases, hydronephrosis, [11] ureteral and bladder fibrosis/ manually extracted from the articles included in this cancer commonly occur [6]. review paper. Data imported into Microsoft Excel As a follow up to the 2001 World Health Assembly Spreadsheet were used to generate Bar Charts. resolution WHA54.19, many endemic countries in Af- rica launched national control programmes largely based Results on preventive chemotherapeutic intervention with prazi- The search quantel (PZQ) targeting at least 75% of school-age The search yielded 183 literatures. After proper scrutiny children-SAC (5─14 years old) and adults at risk of of the retrieved literatures, 93 full text research, review schistosomiasis [12, 13] by 2010. This resolution aligns and online articles were deemed fit for inclusion. Conse- properly with earlier report that SAC, adolescent and quently, this review is a product of the findings from youngRETRACTED adults usually recorded the highest prevalence these articles. The flow chart in Fig. 1 shows the result and intensities of schistosomiasis [14]. Meanwhile, the of our search. guideline of World Health Organization required that treatment of SAC (enrolled and not enrolled) be Characteristics of the included articles done: once every year for high-risk communities, once Of the 93 literatures included in this review, majority, 46 every two years for moderate-risk communities and (49.46%), were products of researches/reviews carried out twice during their Primary School Age in low-risk in African WHO Region, with Nigeria recording the sec- communities [13, 15]. ond largest number of articles, 19 (20.43%). Switzerland in Atalabi and Adubi BMC Infectious Diseases (2019) 19:73 Page 3 of 12

Fig. 1 Flowchart of the article search and selection process

European Region, however, accounted for the largest, 22 tested positive for US, resulting in a prevalence rate of (23.66%), which were all technical reports/review articles 0.31%. (see Table 1). In Cameroon,ARTICLE out of the 1346 school children inter- The sampling years reported by the 61 research arti- viewed and examined as reported by two articles, 446 cles included in this review ranged from 1984 to 2017, were found to be suffering from the menace of US, with the studies executed between 2004 and 2017 being giving a prevalence rate of 33.14%. 11 times more in number than those carried out in each Furthermore, a prevalence of 67.16% was computed of 1984–1993 and 1994–2003. Sixty-Five point from a total sample size of 539 reported by two Fifty-Eight percent (40), 63.93% (39), and 60.66% (37) of papers which showed that 362 school children were the studies were cross-sectional in nature, carried out in infected. school settings and rural areas respectively (see Table 1). Finally, each research paper obtained from Malawi, However, it is worthy of note that sample size deter- Niger, Ghana, Burkina Faso, Yemen, Zimbabwe, Zambia mination, sampling method, and intensity of US were and Angola reported prevalence rates (sample size) of: not reported by 49.18% (30), 54.09% (33) and 46.34% 14.20% (1642), 75.40% (1642), 50% (100), 8.76% (3514), (19) of the studies included in this review (see Table 1). 23.80% (400), 60% (551), 9.60% (2040) and 61.80% (785) respectively. Table 2 also presents the extracted data on the inten- Prevalence and intensity of urinary schistosomiasis sity of US. It is obvious that only 17 research articles Data on the prevalence of US in different endemic (48.57%) reported the intensity of infection due to the settings are presented in Table 2 below. In Nigeria, the disease in question. Of this figure, 12 (70.59%) presented prevalent rates obtained from 14 research articles with a mean intensity of infection as Arithmetic Mean while total sample size of 5675 ranged from 2.07%–78.43%. only 5 (29.41%) presented it as Geometric Mean. They showed that 2116 school children were infected, By Arithmetic format of reporting mean intensity, giving an overall prevalence rate of 37.29%. Coinciden- the highest value, 154.7 eggs per 10 ml of urine sam- tally, these articles represent the six (6) geopolitical ple, was reported in a survey carried out in Magba zonesRETRACTED of Nigeria. Region, Cameroon while the runner up value, 107.30 However, six studies from Kenya reported that of the eggs per 10 ml of urine sample, was reported from 25, 809 respondents sampled, 11,728 were infected with , Nigeria. The overall highest mean inten- the infective stage of S. haematobium, giving a preva- sity of infection was reported in Fatick Region, lence rate of 45.44%. The prevalence of US obtained Senegal as a Geometric Mean Intensity of 356.1 eggs from Kenya-based literatures ranged from 8.90%–94%. per 10 ml of urine sample. The same location re- Moreover, two Ethiopia-based research articles retrieved corded the second highest mean egg count of 185 showed that of the 100,030 respondents examined, 310 eggs per 10ml of urine sample. Atalabi and Adubi BMC Infectious Diseases (2019) 19:73 Page 4 of 12

Table 1 Descriptive statistics (estimates) of the features of the Table 1 Descriptive statistics (estimates) of the features of the articles included in the systematic review articles included in the systematic review (Continued) Variable Category A Category B Number % Variable Category A Category B Number % (who region) of articles (who region) of articles Countries Nigeria Africa 19 20.43 *Sample size Yes 11 18.03 determination Cameroon Africa 3 3.23 Not reported 30 49.18 Cote d’Ivoire Africa 1 1.08 Could not be 20 32.78 ascertained Mali Africa 1 1.08 *Setting School 39 63.93 Kenya Africa 8 8.60 Community 9 14.75 Senegal Africa 4 4.30 Others 13 21.31 United State of The Americas 3 3.23 America *Population Rural 37 60.66 area South Africa Africa 2 2.15 Peri-urban 7 11.48 Switzerland Europe 22 23.66 Others 17 27.87 Netherlands Europe 1 1.08 **Mode of Microscope only 18 43.90 diagnosis Swaziland Africa 1 1.08 Real time PCR Assays 1 2.44 + Reagent strip + United Kingdom Europe 3 3.23 Test for cSEA + Yemen Eastern 1 1.08 microscopy Mediterranean Reagent strip only 1 2.44 Malawi Africa 1 1.08 Microscopy and 21 51.22 Niger Africa 1 1.08 Reagent strip Ghana Africa 1 1.08 **Format of Arithmetic mean only 5 12.19 intensity ARTICLE Burkina Faso Africa 1 1.08 Geometric mean only 3 7.32 Zimbabwe Africa 1 1.08 WHO categories only 13 31.71 Zambia Africa 1 1.08 Geometric+ WHO 1 2.44 categories Angola Africa 1 1.08 Not reported/Not 19 46.34 Tanzania Africa 1 1.08 specified Ethiopia Africa 2 2.15 *Only applicable to research articles; **Only applicable to prevalence/ intensity Others 14 15.05 studies on humans; cSEA, Circulating Soluble Egg Antigen Type of Research 61 65.59 Article Review 6 6.45 As it stands, Kenya has the highest prevalence while Senegal has the highest mean intensity of infection with Technical report 22 23.66 US among SAC. Online article 4 4.30 Of the 41 research articles included in this review *Sample year 1984─1993 4 6.56 paper, 35 reported a total number of 144,755 partici- 1994─2003 4 6.56 pants with prevalence/intensity records. As far as S. hae- 2004─2017 44 72.13 matobium egg concentration technique was concerned, Not reported 9 14.75 11, 18 and 4 articles recorded centrifugation, filtration, and sedimentation as means of preparing sample for *Sampling Cluster 2 3.28 method viewing under the microscope. However, 2 articles from Random 19 31.15 Angola and Zimbabwe did not report technique of egg Universal/census 4 6.56 concentration. Stratified 2 3.28 RETRACTEDNot reported 33 54.09 Risk factors of urinary schistosomiasis in school Fish bowl/ systematic 1 1.64 children Table 3 presents the factors that are considered *Study type Cross-sectional 40 65.58 pertinent to the transmission of US in school children. Longitudinal 5 8.19 Findings from this review reveal that SAC within the Not reported 16 26.23 range of 5–16 years of age were consistently and unanimously reported as the group with the highest prevalence and association with US. Atalabi and Adubi BMC Infectious Diseases (2019) 19:73 Page 5 of 12

Table 2 Urine Processing Technique, Prevalence, and intensity of urinary schistosomiasis by country’s subarea Ref Country Subarea Eggs concentration Sample size Prevalence (%) Mean Intensity Age group (Years) technique [45] Nigeria Kwara State Centrifugation 551 35.20 N.R 9─16 [46] Cameroon Northern Province Sedimentation 964 36 N.R 9─17 [47] Nigeria Plateau State Sedimentation 242 2.07 27.8** 5─14 [48] Nigeria Kano State Centrifugation 493 44.20 107.30** 5─16 [49] Kenya Migori County Filtration 1768 8.90 N.R 7─14 [50] Nigeria Centrifugation 232 47.80 8.30** 4─15 [51] Kenya Coast Province Filtration 12,541 41.50 45* 5─19 [52] Kenya Coast Province Filtration 7093 66 20** 5─21 [53] Senegal Fatick Region Filtration 329 73.20 356.1* 5─15 [54] Nigeria Katsina State Centrifugation 611 21.11 26.98** 10─15 [55] Kenya North Coast Filtration 262 94 N.R 5─12 [56] Nigeria Centrifugation 487 57.1 45** 6─14 [57] Malawi Chikhwawa district Centrifugation 1642 14.20 N.R N.R [58] Niger Tillabery /Tahoua Filtration 1642 75.40 15.50* 7,8 & 11 [59] Kenya Coast Province Filtration 4031 35 N.R N.R [60] Ghana Brong Ahafo Region Centrifugation 100 50 N.R 6─15 [61] Senegal Fatick Region Filtration 682 57.6 N.R 5─15 [62] Cameroon Magba Region Filtration 382ARTICLE 41.10 154.7** 7─14 [63] Senegal Fatick Region Filtration 210 57.6 185* 7─15 [64] Nigeria Lagos State Sedimentation 102 78.43 N.R 5─15 [65] Burkina Faso Ouagadougou Filtration 3514 8.76 6** 7─11 [66] Zimbabwe Chikwaka Communal Land N.R 551 60 N.R 9─16 [67] Nigeria Katsina State Centrifugation 436 27.98 35.29** 12─17 [68] Zambia Lusaka Province Filtration 2040 9.60 31.40** 6─15 [69] Nigeria Ogun State Centrifugation 187 64.7 0.95* 5─15 [70] Kenya Coast Province Filtration 114 22.8 N.R N.R [71] Angola Cubal District N.R 785 61.80 N.R 9─10 [72] Yemen Taiz, Ibb, Dhamar, Sana’a Filtration 400 23.80 N.R † and Hodiedah Provinces [73] Nigeria Kaduna State Centrifugation 505 12.30 2.69** 4─15 [74] Nigeria Rivers State Sedimentation 130 23.10 N.R 5─16 [75] Ethiopia Gambella Regional State Filtration 304 35.90 8.76** 7─14 [76] Ethiopia Almost all regions Filtration 99,726 0.20 N.R 10─15 [77] Nigeria Adamawa State Centrifugation 346 32.40 N.R 5─15 [78] Nigeria Taraba State Filtration 1153 53.08 N.R 6─15 [79] Nigeria Filtration 200 21 N.R 5─15 TOTAL 144,755 *GeometricRETRACTED Mean Intensity; N. R, Not reported; **Arithmetic Mean Intensity; † Not clearly defined

By the findings in this review paper, gender played Water-related factors like swimming, playing in shal- a significant role in the transmission of US, with low waters, fetching water for domestic uses in open and males recording higher prevalence of infection and potentially infested water bodies like lakes, rivers, ponds, significant association more often over their female streams, etc. vis a vis proximity of residence to sources counterparts. of unwholesome water sources have all been reported by Atalabi and Adubi BMC Infectious Diseases (2019) 19:73 Page 6 of 12

Table 3 Risk factors of urinary schistosomiasis peculiar to school Table 4 Reported morbidities by infection phases of urinary children schistosomiasis Risk factor Category References Infection Phase Morbidity/Pathological References Consequences Age 7─9[62] Larval Invasion Swimmers itch [54] 5─10 [79] Acute Eosinophilia [55] 10─12 [55] (Maturation) ─ 12 14 [56] Chronic Terminal haematuria [46, 52, 54–56, 11─15 [53] (Establishment) 58, 62] 5─15 [69] Proteinuria [52, 56, 66] 6─15 [78] Dysuria [46, 54, 62, 66] 13─16 [74] Pseudopolyps [55, 66] Gender Male [49, 53, 54, 62, 63, 65, Bladder papillomas/lesion [52, 58] 67, 75, 78–80] Bladder wall calcification [20] Female [64, 73, 74] Ureteric fibrosis [52] Recreational activities Swimming/play in [54, 73] Kidney pyelon dilatation [55, 58, 66] shallow water Ureter dilatation [16, 55, 58] Water sourcing for *Unwholesome [54, 62, 67, 72, 73, 81] domestic use water sources Intravesical mass formation [16] Parental occupation/Farm- Farming [54, 57, 73, 75] Hydronephrosis [52, 66] related activities Fishing [54, 57, 62, 67, 73] Genital discharge/itching/burning [69, 82] sensation Brown collar jobs [54, 67] Genital lesions [16] House wives [54] ARTICLEGenital swelling/lump [69] Irrigation [20] Parental educational Illiteracy [72, 73] status system as shown in Table 4 below. They are majorly Proximity of residence to [71, 72, 81] associated with the chronic phase of the disease. infested water Table 5 presents a list of drugs of intervention for US. Altitude Valley [68] It shows PZQ as having the highest cure rate and Lack of sewage disposal Toilet [72] Niridazole as the least. facilities Generally, the global population treated for schisto- Changing global climate [20] somiasis increased from 2008 to 2016 with the exception *Rivers, streams, ponds, and dams of 2011 and 2013 when a decline was experienced (Fig. 2). The same applied to the number of SAC treated researchers as key factors in the transmission of the as well as their treatment coverage within the same disease. period. The highest distribution coverage for PZQ was In addition, parental factors such as educational and achieved in 2016 (see Fig. 3). However, the SAC requir- occupational status have been reported by researchers ing chemotherapeutic intervention with PZQ kept from various endemic settings of US. increasing till 2014 (see Table 6 and Fig. 2). Finally, economic and ecological factors like lack of sewage disposal facilities and climate change were re- Discussion ported as determinant factors of the disease. Results summary In summary, the overall findings in this review showed that: (1) of all WHO Regions, Africa is the most en- Pathology and morbidity markers of urinary demic zone for US, with Kenya and Senegal recording schistosomiasisRETRACTEDthe highest prevalence and mean intensity respectively; Table 4 presents the pathological consequences and (2) SAC within the range of 5–16 years contribute most morbidity markers of US by infection phases as reported significantly to the transmission cycle of the disease by the research articles included in this review. globally; (3) gender is a factor to watch out for, with Morbidity markers identified include swimmer’sitch, male often recording the highest prevalence and eosinophilia, terminal haematuria, proteinuria, and dys- intensity of infection; (4) contact with open, potentially uria. On a broad note, the morbidities/pathological conse- infested water sources contribute significantly to its quences reported obviously revolve around the urogenital transmission; (5) parental factors (occupation and Atalabi and Adubi BMC Infectious Diseases (2019) 19:73 Page 7 of 12

Table 5 Mode of administration, dosage and cure rate of selected drugs for adult S. haematobium control Drugs Mode of administration Dosage Cure rate References Antimonials Intravenous 30 mg/15 kg (12 injections) 82% [83] Niridazole Oral 100 mg/kg 36% [84] Metrifonate 10 mg/kg (single) 50.8% [85] Praziquantel 40 mg/kg (single) 75%–85% [86] education status) predispose SAC to US; (6) economic Scientific and Cultural Organization (UNESCO), United vis a vis ecological factors play a key role in infection Nations Children’s Fund (UNICEF), and other inter- transmission; and (7) in the last decade, a treatment national agencies since the 1950s [21]. SAC are a target coverage of 45% was never achieved globally for SAC or group for Mass Drug Administration (MDA) since non-SAC treatment category for US. WHO expert committee on schistosomiasis met for the first time 64 years ago [18, 22]. The need to treat school-age children (SAC) This is ascertained by the projected budget of about Meanwhile, schistosomiasis, an infectious disease of USD 116 million for 2009 to 2013 global procure- poverty, is easily contracted through poor hygiene and ment and delivery of drug to endemic countries by play habits of school children. In majority of areas en- WHO and the UN systems without custom fees and demic for US, a peak of morbidity is usually observed in clearance charges due to existing agreements [23, 24]. school children within age range 7–14 years [16]. On the In Central Nigeria, study on the epidemiology of US long run, it prolongs squalor and as a result, blocks in SAC using the WHO paradigm of ≥50% prevalence cognitive academic performance and normal growth of has been used as a benchmark for the treatment of children. This culminates in suffering and sometimes, the disease in adults [25]. death [17]. The extent of morbidity due to US is strongly ARTICLE linked with the intensity and the length of infection Management strategies of urinary schistosomiasis in SAC period. Because US is more prevalent in SAC, control and associated challenges programme is directed at them so that the duration Various strategies have been applied in the control of of heavy infection intensity could be reduced mark- US. These include indiscriminate mass treatment, active edly [18, 19]. case finding and treatment of particular risk groups such Unfortunately, as our findings revealed, majority of as school-aged children [26]. However, before the advent SAC are from Africa which had previously been reported of PZQ, other drugs effective against different species to have accounted for an estimate of over 85% of all and stages of development were used (see Table 5). cases of schistosomiasis globally [20]. Therefore, pro- Drugs of intervention for schistosomiasis progressed moting the health of SAC has been an integral part of from antimonial compounds to PZQ which is the drug the programme of WHO, United Nations Educational, of choice today [27]. Metrifonate and Hycathone

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Fig. 2 A clustered column chart showing the population categories of School-Age Children (SAC) treated with Praziquantel between 2008 and 2016 intervention period Atalabi and Adubi BMC Infectious Diseases (2019) 19:73 Page 8 of 12

Fig. 3 A clustered column chart showing the distribution coverage of Praziquantel in the last decade mesylate are effective for the treatment of US. Albendazole can, however, be administered together Lucanthone hydrochloride was used from 1948 to safely where there is co-endemicity of schistosomiasis mid-sixties. When given a short treatment from 3 to 6 and Soil-Transmitted Helminthiasis (STH) [32]. It is days, it had moderate activity against S. haematobium. already well known that after chemotherapy, cessation of Niridazole is used against S. mansoni, S. japonicum and symptoms isARTICLE evidenced in the reduction of egg excretion, S. haematobium [28]. Corticosteroids and anticonvul- proteinuria, haematuria, urinary iron loss, leucocyturia, sants are used to treat katayama fever in order to and few remaining schistosomes which cannot multiply suppress the hypersensitivity reaction and with PZQ to [17, 18, 33–36]. Consequently, they pose little or no eliminate the already mature adult. PZQ should be ad- threat to their hosts. Therefore, control programmes ministered with great caution in the case or concurrent should focus on the achievement of a sharp decline in neurocysticercosis [29]. The use of Artemisinin deriva- the intensity of infection [17]. Based on this premise, in tives as prophylaxis for acute schistosomiasis, possibly in 2001, the World Health Assembly adopted resolution combination with PZQ, has been investigated. However, 54.19 which set a target for all endemic countries to Artemisinin use in malaria-endemic areas is not encour- regularly treat over 75% of all SAC at risk of morbid- aged because of anticipated drug resistance [30]. ity due to schistosomiasis and STH by 2010 [37, 38]. However, the most rapid and cost-effective way to It is pertinent to state that the result of this review control morbidity due to schistosomiasis is through a clearly showed that this aim was not achieved (see chemotherapeutic intervention with PZQ [31]. PZQ and Table 6).

Table 6 Proportion of school-age children requiring treatment and the number treated for schistosomiasis in the past decade Period of Global population SAC requiring Reported SAC Coverage (%) References intervention (Year) treated (Millions) treatment (Millions) treated (Millions) 2008 17.5 N.R 9.6 N.R [87] 2009 19.6 N.R 10.8 N.R [88] 2010 33.5 108.9 21.7 19.9 [89] 2011 28.1 111.5 16.5 14.8 [90] 2012RETRACTED 42.1 114.7 29.7 25.9 [91] 2013 39.5 121.2 26.8 22.1 [92] 2014 61.6 123.3 49.2 34.6 [92] 2015 66.5 118.5 53.2 42.2 [32] 2016 89.2 111.2 70.9 53.7 [93] 2017 ** ** ** ** N.A **Data not available yet; SAC School-age Children, NR Not reported, NA Not applicable Atalabi and Adubi BMC Infectious Diseases (2019) 19:73 Page 9 of 12

Nevertheless, the greatest challenge of MDA is to be achieved just like the strategic plan for 2010. Our extend regular drug coverage to reach all the children at view is in agreement with the report that if WHO sus- risk of morbidity due to infection by helminths [23]. tains the current treatment trend, elimination is achiev- There are two perspectives to this. One, each School-age able in 2030 [44]. It is imperative that annual control Child (SAC) treated may not have access to enough programmes be scaled up marginally, particularly in the PZQ that would clear all the parasites. Two, the distri- African region of the WHO. While US-based researches bution coverage may not cater for the whole population should be sponsored at the grass-root level to unveil of infected SAC. Consequently, symptoms of chronic in- hidden endemic foci, adequate facilities for Water, fection may show up after 5–15 years in children who Sanitation, and Hygiene (WASH) should be put in place were partially treated as a result of poor coverage of in all schools globally. PZQ [20]. However, the report of a School-Based Treat- Acknowledgements ment carried out in Zanzibar Island, Tanzania, where We express our profound gratitude to the authors of the research papers, 8000 pupils were treated showed amazing coverage of review articles and online materials used in the course of preparing the 85.2 and 86.9% in Pemba and Unguja Districts respect- manuscript of this review article. Without their meritorious contribution to knowledge about schistosomiasis, this paper would have been written with ively [39]. scanty references. PZQ is not without its adverse reactions like abdom- inal pain, dizziness, headache, vomiting, diarrhea, round, Funding Not applicable. swollen and itching skin rashes, and fever [40]. These are usually mild and last for 24 h. These are reactions Availability of data and materials from dying worms. Not applicable. In addition, studies have shown that false negative Authors’ contributions results cause infected SAC to escape treatment, lead- TEA conceived the review. TEA and TOA searched for relevant literatures and ing to chronic condition and if such case occurs after wrote the manuscript. Both authors read and approved the final version of the manuscript. MDA, cure rate may be overestimated and this may ARTICLE be a prelude to drug resistance and further transmis- Ethics approval and consent to participate sion of US [41]. Not applicable. It is hoped that in the nearest future, global schisto- Consent for publication somiasis control programmes will receive a boost when Not applicable. the current “evolutionary” process of vaccine-linked Competing interests chemotherapy culminates in approval by WHO. A good The authors declare that they have no competing interests. number of these vaccines undergoing preclinical and clinical trials on the field are particularly made for Publisher’sNote children [42]. Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Limitations of the review Author details This review took articles reported in English into consid- 1Department of Biological Sciences, Federal University, Dutsin-Ma, Km 65, 2 eration instead of including those reported in other P.M.B. 5001, Dutsin-Ma, Katsina State, Nigeria. Department of Biological Sciences and Biotechnology, College of Pure and Applied Sciences, Caleb languages. Besides, we noticed that mean intensity of University, Imota, Lagos State, Nigeria. infection with US was either underreported or not reported by some authors of articles included in this Received: 8 January 2018 Accepted: 21 December 2018 review article. Consequently, the report of the mean in- tensity reported here may not be an accurate reflection References of what is obtainable among SAC globally. 1. Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. Lancet. 2014;383(9936):2253–64. 2. World Health Organization. Schistosomiasis. Fact sheet 115 updated January Conclusion 2017. Available at: http://www.who.int/mediacentre/factsheets/fs115/en/. The prevalence rates and intensities of US vis a vis its Accessed on 8 June 2017. 3. Steinman P, Keiser J, Bos R, Tanner M, Utzinger J. Schistosomiasis and water impactRETRACTED on SAC, keep increasing from year to year, resources development: systematic review, meta-analysis and estimates of leading to increase in the global population requiring people at risk. Lancet Infect Dis. 2006;6:411–25. chemotherapeutic intervention with PZQ. In view of the 4. Atalabi TE, Lawal U, Ipinlaye SJ. Prevalence and intensity of genito-urinary schistosomiasis and associated risk factors among junior high school WHO strategic ambitious plan to eliminate schistosom- students in two local government areas around Zobe Dam in Katsina state, iasis by 2020 [43] and the findings from this review Nigeria. Parasit Vectors 2016a; 9:388. stipulating that in the last decade, a PZQ distribution 5. Atalabi TE, Lawal U, Akinluyi FO. Urogenital schistosomiasis and associated determinant factors among senior high school students in the Dutsin-ma coverage of 45% has never been achieved for SAC, it is and Safana local government areas of Katsina state, Nigeria. Infect Dis obvious that this goal, in the face of realities, might not Poverty 2016b; 5:69. Atalabi and Adubi BMC Infectious Diseases (2019) 19:73 Page 10 of 12

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