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Can ivermectin mass drug administrations to control scabies also reduce skin and soft tissue infections? Hospitalizations and primary care presentations lower after a large-scale trial in Fiji

2022; Elsevier BV; Volume: 22; Linguagem: Inglês

10.1016/j.lanwpc.2022.100454

2666-6065

Jo Middleton,

Cultural Competency in Health Care

Evaluations of Mass Drug Administrations (MDAs) targeting scabies have generally not assessed their secondary impacts on skin and soft tissue infections. These are major health burdens in the global south, with sequelae including glomerulonephritis, rheumatic fever and chronic kidney disease.1Engelman D. Marks M. Steer A.C. et al.A framework for scabies control.PLoS Negl Trop Dis. 2021; 15e0009661https://doi.org/10.1371/journal.pntd.0009661Crossref Scopus (4) Google Scholar, 2Romani L. Steer A.C. Whitfeld M.J. Kaldor J.M. Prevalence of scabies and impetigo worldwide: a systematic review.Lancet Infect Dis. 2015; 15: 960-967https://doi.org/10.1016/S1473-3099(15)00132-2Summary Full Text Full Text PDF PubMed Scopus (210) Google Scholar, 3Chung S.D. Wang K.H. Huang C.C. Lin H.C. Scabies increased the risk of chronic kidney disease: a 5-year follow-up study.JEADV. 2014; 28: 286-292https://doi.org/10.1111/jdv.12099Crossref Scopus (29) Google Scholar In a major step forward Li Jun Thean and colleagues4Thean L.J. Romani L. Engelman D. et al.Prevention of bacterial complications of scabies using mass drug administration, a population-based, before-after trial in Fiji, 2018–2020.Lancet Reg Health West Pac. 2022; 22100433PubMed Google Scholar report in The Lancet Regional Health Western Pacific on the impact on skin infections of an oral ivermectin MDA targeting scabies in Fiji. Importantly, they show in the largest before-after trial of its kind that not only did scabies and impetigo prevalence reduce, but so too did hospitalisations with severe skin and soft tissue infections and attendance at primary care with scabies and skin infections. Scabies is a highly irritant skin infestation with the mite Sarcoptes scabiei and is primarily transmitted by touch. It is classed by WHO as a Neglected Tropical Disease (NTD) in recognition of its high burden and the health risks associated with secondary infections of impetigo (i.e., cellulitis, necrotising fascittis, skin abscesses, rheumatic fever, chronic kidney disease).1Engelman D. Marks M. Steer A.C. et al.A framework for scabies control.PLoS Negl Trop Dis. 2021; 15e0009661https://doi.org/10.1371/journal.pntd.0009661Crossref Scopus (4) Google Scholar, 2Romani L. Steer A.C. Whitfeld M.J. Kaldor J.M. Prevalence of scabies and impetigo worldwide: a systematic review.Lancet Infect Dis. 2015; 15: 960-967https://doi.org/10.1016/S1473-3099(15)00132-2Summary Full Text Full Text PDF PubMed Scopus (210) Google Scholar, 3Chung S.D. Wang K.H. Huang C.C. Lin H.C. Scabies increased the risk of chronic kidney disease: a 5-year follow-up study.JEADV. 2014; 28: 286-292https://doi.org/10.1111/jdv.12099Crossref Scopus (29) Google Scholar Evidence indicates prevalence is not influenced by personal washing.5Middleton J. Cassell J.A. Jones C.I. Lanza S. Head M.G. Walker S.L. Scabies control the forgotten role of personal hygiene – authors reply.Lancet Infect Dis. 2018; 18: 1068-1069https://doi.org/10.1016/S1473-3099(18)30558-9Summary Full Text Full Text PDF PubMed Scopus (6) Google Scholar Neglected tropical skin diseases are significant health problems across Oceania.6Kline K. McCarthy J.S. Pearson M. Loukas A. Hotez P.J. Neglected tropical diseases of Oceania: review of their prevalence, distribution, and opportunities for control.PLoS Negl Trop Dis. 2013; 7: e1755https://doi.org/10.1371/journal.pntd.0001755Crossref PubMed Scopus (69) Google Scholar,7Middleton J. Cassell J.A. Colthart G. et al.Rationale, experience and ethical considerations underpinning integrated actions to further global goals for health and land biodiversity in Papua New Guinea.Sustain Sci. 2020; 15: 1653-1664https://doi.org/10.1007/s11625-020-00805-xCrossref Scopus (4) Google Scholar Some of the world's highest prevalence rates of scabies have been measured in the region (e.g., Papua New Guinea, 71%; Fiji, 32%).2Romani L. Steer A.C. Whitfeld M.J. Kaldor J.M. Prevalence of scabies and impetigo worldwide: a systematic review.Lancet Infect Dis. 2015; 15: 960-967https://doi.org/10.1016/S1473-3099(15)00132-2Summary Full Text Full Text PDF PubMed Scopus (210) Google Scholar The situation is similar for impetigo, particularly in children (e.g., Samoa, 57%; Solomon Islands, 52%; Fiji, 36%; Vanuatu, 16%).2Romani L. Steer A.C. Whitfeld M.J. Kaldor J.M. Prevalence of scabies and impetigo worldwide: a systematic review.Lancet Infect Dis. 2015; 15: 960-967https://doi.org/10.1016/S1473-3099(15)00132-2Summary Full Text Full Text PDF PubMed Scopus (210) Google Scholar,8Taiaroa G. Matalavea B. Tafuna'i M. et al.Scabies and impetigo in Samoa: a school-based clinical and molecular epidemiological study.Lancet Reg Health West Pac. 2021; 6100081https://doi.org/10.1016/j.lanwpc.2020.100081Summary Full Text Full Text PDF PubMed Scopus (3) Google Scholar The first trial in Oceania of an ivermectin MDA for scabies (outside of institutional outbreaks) was carried out in a Papua New Guinea village in 1996,9Bockarie M.J. Alexander N.D.E. Kazura J.W. Bockarie F. Griffin L. Alpers M.P. Treatment with ivermectin reduces the high prevlance of scabies in a village in Papua New Guinea.Acta Trop. 2000; 75: 127-130https://doi.org/10.1016/S0001-706X(99)00087-XCrossref PubMed Scopus (50) Google Scholar followed on a greater scale in the Solomon Islands 1997–2000,10Marks M. Taotao-Wini B. Satorara L. et al.Long term control of scabies fifteen years after an intensive treatment programme.PLoS Negl Trop Dis. 2015; 9e0004246https://doi.org/10.1371/journal.pntd.0004246Crossref Scopus (24) Google Scholar Fiji in 2004,11Haar K. Romani L. Filimone R. Scabies community prevalence and mass drug administration in two Fijian villages.Int J Dermatol. 2014; 53: 739-745https://doi.org/10.1111/ijd.12353Crossref PubMed Scopus (42) Google Scholar and in aboriginal communities in Australia.12Kearns T.M. Speare R. Cheng A.C. et al.Impact of an Ivermectin mass drug administration on scabies prevalence in a remote Australian aboriginal community.PLoS Negl Trop Dis. 2015; 9e0004151https://doi.org/10.1371/journal.pntd.0004151Crossref PubMed Scopus (59) Google Scholar A 15-year follow-up of the first Solomon Islands MDA found very low scabies prevalence, in fact just one case. Marks et al.10Marks M. Taotao-Wini B. Satorara L. et al.Long term control of scabies fifteen years after an intensive treatment programme.PLoS Negl Trop Dis. 2015; 9e0004246https://doi.org/10.1371/journal.pntd.0004246Crossref Scopus (24) Google Scholar attributed this to MDA and an associated period of active case finding. Subsequently, in the Solomon Islands13Marks M. Lucia Romani L. Oliver Sokana O. et al.Prevalence of scabies and impetigo 3 years after mass drug administration with ivermectin and azithromycin.Clin Infect Dis. 2020; 70: 1591-1595https://doi.org/10.1093/cid/ciz444Crossref PubMed Scopus (13) Google Scholar and Fiji14Romani L. Whitfeld M.J. Koroiveuta J. et al.Mass drug administration for scabies control in a population with endemic disease.N Engl J Med. 2015; 373: 2305-2313https://doi.org/10.1056/NEJMoa1500987Crossref PubMed Scopus (156) Google Scholar MDAs targeting scabies have been associated with decreased impetigo prevalence (respectively: from 24.7% to 9.6%; 24.6% to 8.0%). Influenced by these developments in Oceania, similar interventions are increasingly being conducted elsewhere.1Engelman D. Marks M. Steer A.C. et al.A framework for scabies control.PLoS Negl Trop Dis. 2021; 15e0009661https://doi.org/10.1371/journal.pntd.0009661Crossref Scopus (4) Google Scholar The largest adoption of this approach has been in Ethiopia where a 2018 scabies MDA involved over nine million people,15Enbiale W. Bayniem T.B. Ayalew A. et al.Stopping the itch": mass drug administration for scabies outbreak control covered for over nine million people in Ethiopia.J Infect Dev Ctries. 2020; 14: 28S-35Shttps://doi.org/10.3855/jidc.11701Crossref PubMed Scopus (4) Google Scholar and the secondary impacts on scabies of an ivermectin MDA targeting onchocerciasis is also being assessed.16Yirgu R. Middleton J. Fekadu A. et al.The secondary impact of ivermectin MDA for the control of onchocerciasis on the prevalence of scabies in the Amhara region of northern Ethiopia.in: In: International Alliance for the Control of Scabies Annual Scientific Meeting. 2021Google Scholar Against this regional and global background Thean and colleagues4Thean L.J. Romani L. Engelman D. et al.Prevention of bacterial complications of scabies using mass drug administration, a population-based, before-after trial in Fiji, 2018–2020.Lancet Reg Health West Pac. 2022; 22100433PubMed Google Scholar report a 2018–2020 before-after MDA trial covering Fiji's Northern Division: first dose, 135,744 people (97% coverage); second dose, 121,760 people (87%). The prior MDA in Fiji had 716 participants enrolled in the ivermectin arm,14Romani L. Whitfeld M.J. Koroiveuta J. et al.Mass drug administration for scabies control in a population with endemic disease.N Engl J Med. 2015; 373: 2305-2313https://doi.org/10.1056/NEJMoa1500987Crossref PubMed Scopus (156) Google Scholar in the Solomon Islands 26,188.13Marks M. Lucia Romani L. Oliver Sokana O. et al.Prevalence of scabies and impetigo 3 years after mass drug administration with ivermectin and azithromycin.Clin Infect Dis. 2020; 70: 1591-1595https://doi.org/10.1093/cid/ciz444Crossref PubMed Scopus (13) Google Scholar This then is by far the largest study to date to report the impact of a scabies MDA on impetigo. Scabies prevalence decreased from 14.2% to 7.7%, and impetigo from 15.3% to 6.1%. Whilst this valuably supports the conclusions of the earlier smaller trials, what is most important in this study is the observed reductions in primary and secondary care burdens. Incidence of childhood invasive infections and post-streptococcal sequelae were unchanged. However, hospitalisations with severe skin and soft tissue infections reduced 17%, attendance at primary care with scabies and skin infections 21%. Thean and colleagues note the reduction in scabies prevalence was lower than expected compared to other in-region studies. They are likely correct in linking this in part to the intervention not being distributed and overseen directly by the study team, as many smaller scabies MDA trials have been, but instead by the national health system. A similar reduction in expected effectiveness has been observed in a non-researcher run MDA in Ethiopia.16Yirgu R. Middleton J. Fekadu A. et al.The secondary impact of ivermectin MDA for the control of onchocerciasis on the prevalence of scabies in the Amhara region of northern Ethiopia.in: In: International Alliance for the Control of Scabies Annual Scientific Meeting. 2021Google Scholar Rather than a weakness of the study, this underlines its value as the important effects shown may more realistically indicate benefits to be expected when operationalising MDAs at large-scales beyond smaller researcher-run trials. These results strongly support (1) expansion of ivermectin MDAs targeting scabies and impetigo, (2) collection of similar hospitalisation and primary care data as MDAs expand, and (3) development of further research and interventions that capitalise on how NTD control can secondarily reduce wider burdens to health systems. Given resource scarcity such synergistic integrations are important clinically not only in Oceania6Kline K. McCarthy J.S. Pearson M. Loukas A. Hotez P.J. Neglected tropical diseases of Oceania: review of their prevalence, distribution, and opportunities for control.PLoS Negl Trop Dis. 2013; 7: e1755https://doi.org/10.1371/journal.pntd.0001755Crossref PubMed Scopus (69) Google Scholar, but worldwide.1Engelman D. Marks M. Steer A.C. et al.A framework for scabies control.PLoS Negl Trop Dis. 2021; 15e0009661https://doi.org/10.1371/journal.pntd.0009661Crossref Scopus (4) Google Scholar The author is a co-investigator of SURFACES Papua New Guinea, which is funded by Sussex Sustainability Research Project (University of Sussex, UK), and the Darwin Initiative (Department for Environment, Food & Rural Affairs, UK government). Their work on scabies in Ethiopia is funded by the National Institute for Health Research (NIHR) Global Health Research Unit on Neglected Tropical Diseases. The views expressed are those of the author and not necessarily those of the NHS, the NIHR or the UK government Department of Health and Social Care.