Economic Considerations for Moving beyond the Kato-Katz Technique for Diagnosing Intestinal Parasites As We Move Towards Elimination
2017; Elsevier BV; Volume: 33; Issue: 6 Linguagem: Inglês
10.1016/j.pt.2017.01.007
ISSN1471-5007
AutoresHugo C. Turner, Alison A. Bettis, Julia C. Dunn, Jane M. Whitton, T. Déirdre Hollingsworth, Fiona Fleming, Roy M. Anderson,
Tópico(s)Parasite Biology and Host Interactions
ResumoThe Kato-Katz technique is a widespread tool in intestinal helminth epidemiological surveys. It is used in monitoring and evaluation programmes to investigate the prevalence and geographical distribution of soil-transmitted helminth and Schistosoma mansoni infections – determining the WHO treatment strategy to be used. While the need for more sensitive diagnostic methods for these intestinal parasites has been identified, the cost of developing and employing new and potentially more rapid tests is considered relatively expensive, particularly compared to the Kato-Katz technique (which is often referred to as cheap). Consequently, this area has suffered from a lack of investment. The actual cost of using the Kato-Katz technique is higher and more variable than is often being assumed, and it is difficult to implement at a large scale. While the need for more sensitive diagnostics for intestinal helminths is well known, the cost of developing and implementing new tests is considered relatively high compared to the Kato-Katz technique. Here, we review the reported costs of performing the Kato-Katz technique. We also outline several economic arguments we believe highlight the need for further investment in alternative diagnostics, and considerations that should be made when comparing their costs. In our opinion, we highlight that, without new diagnostic methods, it will be difficult for policy makers to make the most cost-effective decisions and that the potentially higher unit costs of new methods can be outweighed by the long-term programmatic benefits they have (such as the ability to detect the interruption of transmission). While the need for more sensitive diagnostics for intestinal helminths is well known, the cost of developing and implementing new tests is considered relatively high compared to the Kato-Katz technique. Here, we review the reported costs of performing the Kato-Katz technique. We also outline several economic arguments we believe highlight the need for further investment in alternative diagnostics, and considerations that should be made when comparing their costs. In our opinion, we highlight that, without new diagnostic methods, it will be difficult for policy makers to make the most cost-effective decisions and that the potentially higher unit costs of new methods can be outweighed by the long-term programmatic benefits they have (such as the ability to detect the interruption of transmission). The World Health Organization (WHO) recommends using the Kato-Katz technique [1Katz N. et al.A simple device for quantitative stool thick-smear technique in Schistosomiasis mansoni.Rev. Inst. Med. Trop. Sao Paulo. 1972; 14: 397-400PubMed Google Scholar] (see Glossary) for diagnosing and quantifying soil-transmitted helminth (STH) and Schistosoma mansoni infections – as it provides a standardized reading (eggs per gram of faeces (epg)) and the technique can be taught to laboratory microscopists relatively easily. It is performed using a small spatula and a slide template that allows a standardized amount of faeces to be examined under a microscope and the eggs to be counted. Though the technique can be done in the field without sophisticated laboratory techniques or equipment, it is labour intensive and requires expertise in microscopy. The Kato-Katz technique is a widespread tool in intestinal helminth epidemiological surveys. It is used in monitoring and evaluation programmes to determine the geographical distribution of STH and S. mansoni infections which concomitantly defines the endemicity of an area before control (determining the treatment strategy to be used) [2World Health Organization Preventive Chemotherapy in Human Helminthiasis. WHO, 2006Google Scholar, 3World Health Organization Bench Aids for the Diagnosis of Intestinal Parasites. WHO, 1994Google Scholar]. Furthermore, the Kato-Katz technique is used in post-treatment surveys to assess the impact of control by measuring changes in the prevalence and intensity of infection. However, the technique has a poor sensitivity for detecting light intensity infections, and there is substantial variation in the readings (resulting from day-to-day fluctuations of egg excretion, uneven distribution of eggs within a single stool sample, and variation in the ability of the technicians) [4Nikolay B. et al.Sensitivity of diagnostic tests for human soil-transmitted helminth infections: a meta-analysis in the absence of a true gold standard.International J. Parasitol. 2014; 44: 765-774Crossref PubMed Scopus (167) Google Scholar, 5Tarafder M.R. 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: 399-404Crossref PubMed Scopus (135) Google Scholar, 6Lamberton P.H. et al.Sensitivity and specificity of multiple Kato-Katz thick smears and a circulating cathodic antigen test for Schistosoma mansoni diagnosis pre- and post-repeated-praziquantel treatment.PLoS Negl. Trop. Dis. 2014; 8: e3139Crossref PubMed Scopus (111) Google Scholar, 7Kongs A. et al.The unreliability of the Kato-Katz technique limits its usefulness for evaluating S. mansoni infections.Trop. Med. Int. Health. 2001; 6: 163-169Crossref PubMed Scopus (122) Google Scholar, 8Engels D. et al.Day-to-day egg count fluctuation in Schistosoma mansoni infection and its operational implications.Am. J. Trop. Med. Hyg. 1996; 54: 319-324Crossref PubMed Scopus (180) Google Scholar, 9Lamberton P.H. Jourdan P.M. Human ascariasis: diagnostics update.Curr. Trop. Med. Rep. 2015; 2: 189-200Crossref PubMed Scopus (41) Google Scholar, 10Krauth S.J. et al.An in-depth analysis of a piece of shit: distribution of Schistosoma mansoni and hookworm eggs in human stool.PLoS Negl. Trop. Dis. 2012; 6: e1969Crossref PubMed Scopus (71) Google Scholar, 11Anderson R.M. Schad G.A. Hookworm burdens and faecal egg counts: an analysis of the biological basis of variation.Trans. R. Soc. Trop. Med. Hyg. 1985; 79: 812-825Abstract Full Text PDF PubMed Scopus (156) Google Scholar]. Consequently, it is recommended that the test be performed in duplicate, with two slides prepared and read per sample [12World Health Organization Prevention and control of schistosomiasis and soil-transmitted helminthiasis.Wld Hlth Organ. Tech. Rep. Ser. 2002; (back cover): 1-57PubMed Google Scholar]. Additional challenges involved with STH include the need to collect and process fresh stool samples within a limited timeframe (as hookworm eggs start to degrade rapidly within 30min of sample preparation [3World Health Organization Bench Aids for the Diagnosis of Intestinal Parasites. WHO, 1994Google Scholar, 13Dacombe R.J. et al.Time delays between patient and laboratory selectively affect accuracy of helminth diagnosis.Trans. R. Soc. Trop. Med. Hyg. 2007; 101: 140-145Abstract Full Text Full Text PDF PubMed Scopus (88) Google Scholar]), which adds logistical constraints to Kato-Katz-based surveys. In this paper, we review the published costs of performing the Kato-Katz technique, and examine the variation in the reported values. We also outline several economic arguments that, in our opinion, support further investment in alternative diagnostic tools, particularly as the overarching policy for these diseases shifts from morbidity control to transmission elimination. A single Kato-Katz kit, which includes the template and plastic spatula, only costs between 0.1 and 0.3 US$ [14Speich B. et al.Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys.Parasit. Vectors. 2010; 3: 71Crossref PubMed Scopus (105) Google Scholar]. These kits are typically washed and then re-used over multiple collection sites and surveys. Consequently, other than the initial investment in a microscope, the Kato-Katz technique is a cheap test in terms of the required materials and equipment. However, because the technique requires stool samples to be collected and processed, it is associated with a significant personnel cost. This is due to the time required to collect and prepare stool samples as well as the number of staff needed to conduct the survey due to the logistical demands of the technique. As a result, personnel-related costs are often the largest contribution to the total cost of performing the Kato-Katz technique (for example, Speich et al. [14Speich B. et al.Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys.Parasit. Vectors. 2010; 3: 71Crossref PubMed Scopus (105) Google Scholar] found that personnel constituted 74% of the cost of performing a duplicate Kato-Katz test in a costing study). The reported cost of performing a duplicate Kato-Katz test varies between 2.67 and 12.48 US$ [adjusted to 2014 prices (https://www.imf.org/external/pubs/ft/weo/2016/02/weodata/index.aspx)] in the published literature [14Speich B. et al.Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys.Parasit. Vectors. 2010; 3: 71Crossref PubMed Scopus (105) Google Scholar, 15Assefa L.M. et al.Diagnostic accuracy and cost-effectiveness of alternative methods for detection of soil-transmitted helminths in a post-treatment setting in western Kenya.PLoS Negl. Trop. Dis. 2014; 8: e2843Crossref PubMed Scopus (32) Google Scholar, 16Sturrock H.J. et al.Optimal survey designs for targeting chemotherapy against soil-transmitted helminths: effect of spatial heterogeneity and cost-efficiency of sampling.Am. J. Trop. Med. Hyg. 2010; 82: 1079-1087Crossref PubMed Scopus (29) Google Scholar, 17Sturrock H.J.W. et al.Planning schistosomiasis control: investigation of alternative sampling strategies for Schistosoma mansoni to target mass drug administration of praziquantel in East Africa.International Health. 2011; 3: 165-175Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar, 18Worrell C.M. et al.Cost analysis of tests for the detection of Schistosoma mansoni infection in children in western Kenya.Am. J. Trop. Med. Hyg. 2015; 92: 1233-1239Crossref PubMed Scopus (30) Google Scholar]. This variation is can be attributed to several key factors:(i)Method of collection. In some settings sample pots are left overnight, and then taken to a local laboratory facility for processing the next day [14Speich B. et al.Comparative cost assessment of the Kato-Katz and FLOTAC techniques for soil-transmitted helminth diagnosis in epidemiological surveys.Parasit. Vectors. 2010; 3: 71Crossref PubMed Scopus (105) Google Scholar], whereas others use a mobile team of technicians which collect and process the samples at each survey site [16Sturrock H.J. et al.Optimal survey designs for targeting chemotherapy against soil-transmitted helminths: effect of spatial heterogeneity and cost-efficiency of sampling.Am. J. Trop. Med. Hyg. 2010; 82: 1079-1087Crossref PubMed Scopus (29) Google Scholar, 17Sturrock H.J.W. et al.Planning schistosomiasis control: investigation of alternative sampling strategies for Schistosoma mansoni to target mass drug administration of praziquantel in East Africa.International Health. 2011; 3: 165-175Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar].(ii)Number of sites sampled per day (Figure 1) and the distance between them.(iii)Variation in personnel costs. There is variation in the reported country-specific daily per diems for laboratory technicians {e.g., 14.29 US$ in Kenya versus 37.23 US$ in Ethiopia (2009 prices) [17Sturrock H.J.W. et al.Planning schistosomiasis control: investigation of alternative sampling strategies for Schistosoma mansoni to target mass drug administration of praziquantel in East Africa.International Health. 2011; 3: 165-175Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar]}. The personnel costs are often the main driver in the cost of performing the Kato-Katz technique, and can cause substantial variation in the test's costs between different settings. The majority of the identified studies reported only the financial costs of personnel (i.e., the staff's per diems). If the opportunity cost (economic value) of the staff's time is included in the analysis [15Assefa L.M. et al.Diagnostic accuracy and cost-effectiveness of alternative methods for detection of soil-transmitted helminths in a post-treatment setting in western Kenya.PLoS Negl. Trop. Dis. 2014; 8: e2843Crossref PubMed Scopus (32) Google Scholar], the costs associated with personnel would be even larger (economic costs).(iv)Adjustment of microscope costs. If the microscope is also used for other activities, only a percentage of the total cost would be applied to the Kato-Katz-based survey, thus, reducing the cost per test. Furthermore, the cost of a microscope is often annualized (meaning the cost is spread over its useful lifetime). If this is not performed, the cost per test would be higher.(v)Number of samples taken. There are economies of scale associated with Kato-Katz-based surveys (as the sample size is increased, the cost per test typically decreases) (Figure 1). Consequently, the sample size should be considered when comparing the cost per test reported from different studies/settings [17Sturrock H.J.W. et al.Planning schistosomiasis control: investigation of alternative sampling strategies for Schistosoma mansoni to target mass drug administration of praziquantel in East Africa.International Health. 2011; 3: 165-175Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar]. A further source of potential variation in the reported costs is the level of community sensitization that has been performed. It should be noted that though performing community sensitization is an extra cost, it can make it easier and quicker to obtain the samples. This will be particularly important for studies/settings that are also sampling from adults (as opposed to only children in schools) and the amount needed (and its cost) will depend on the local culture. Within a Kato-Katz-based survey, increasing the number of study participants sampled per site results in economies of scale (Figure 1), as many of the costs are fixed/step-fixed and incurred regardless of the number of samples processed at each site. Consequently, the cost per test is not constant. We illustrate this based on cost data collected in Ethiopia [16Sturrock H.J. et al.Optimal survey designs for targeting chemotherapy against soil-transmitted helminths: effect of spatial heterogeneity and cost-efficiency of sampling.Am. J. Trop. Med. Hyg. 2010; 82: 1079-1087Crossref PubMed Scopus (29) Google Scholar, 17Sturrock H.J.W. et al.Planning schistosomiasis control: investigation of alternative sampling strategies for Schistosoma mansoni to target mass drug administration of praziquantel in East Africa.International Health. 2011; 3: 165-175Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar]. However, the reduction in the cost per test approaches a limit (Figure 1). This is because, as the sample size increases, there are thresholds above which more technicians would need to be employed in order to process all samples collected that day [16Sturrock H.J. et al.Optimal survey designs for targeting chemotherapy against soil-transmitted helminths: effect of spatial heterogeneity and cost-efficiency of sampling.Am. J. Trop. Med. Hyg. 2010; 82: 1079-1087Crossref PubMed Scopus (29) Google Scholar, 17Sturrock H.J.W. et al.Planning schistosomiasis control: investigation of alternative sampling strategies for Schistosoma mansoni to target mass drug administration of praziquantel in East Africa.International Health. 2011; 3: 165-175Abstract Full Text Full Text PDF PubMed Scopus (20) Google Scholar]. Consequently, there is a limit to what degree economies of scale can reduce the cost of Kato-Katz-based surveys (Figure 1). These sample size thresholds may vary depending on the expertise of the technicians, and the distance between the collection sites. In contrast to increasing the number sampled per sample site, increasing the number of sites sampled within a Kato-Katz-based survey is not associated with the same degree of economies of scale (Figure 1). This is because sampling more sites takes longer, and therefore increases the total personnel and transportation costs of the survey. In other words, many of the costs do not change (i.e., they are fixed) with regard to the number sampled at each site (generating economies of scale when increasing the number sampled within each school), but do change in relation to the number of sites sampled (stepped-fixed costs). The degree of economies of scale will vary in different settings (Figure 1). For example, there may be greater economies of scale in settings where the samples are brought to a local laboratory facility rather than processed at each school or in settings that have lower per diems for the technicians. It should be noted that these costs could be reduced by integrating the Kato-Katz technique within another survey (such as transmission assessment surveys (TAS) for lymphatic filariasis [19Smith J.L. et al.Factors associated with the performance and cost-effectiveness of using lymphatic filariasis transmission assessment surveys for monitoring soil-transmitted helminths: a case study in Kenya.Am. J. Trop. Med. Hyg. 2015; 92: 342-353Crossref PubMed Scopus (12) Google Scholar, 20Kolaczinski J.H. et al.Integrated surveys of neglected tropical diseases in Southern Sudan: how much do they cost and can they be refined?.PLoS Negl. Trop. Dis. 2010; 4: e745Crossref PubMed Scopus (12) Google Scholar]), resulting in so-called economies of scope. This analysis highlights that the unit cost of performing the Kato-Katz technique will vary depending on sample size and number of sample sites. Therefore, the cost per test should be not be considered to be constant for different study designs and study sites. The need for more sensitive diagnostic methods for the STH and schistosomes (SCH) has been frequently identified in recent years [21Stothard J.R. et al.Diagnostics for schistosomiasis in Africa and Arabia: a review of present options in control and future needs for elimination.Parasitology. 2014; 141: 1947-1961Crossref PubMed Scopus (0) Google Scholar, 22Utzinger J. et al.New diagnostic tools in schistosomiasis.Clin. Microbiol. Infect. 2015; 21: 529-542Abstract Full Text Full Text PDF PubMed Scopus (162) Google Scholar, 23McCarthy J.S. et al.A research agenda for helminth diseases of humans: diagnostics for control and elimination programmes.PLoS Negl. Trop. Dis. 2012; 6: e1601Crossref PubMed Scopus (132) Google Scholar, 24Lammie P.J. et al.A14 Diagnostic Needs for NTD programs. 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In the following section, we outline several economic arguments we believe highlight the need for further investment in alternative diagnostic methods to the Kato-Katz technique, particularly as the overarching goal for these diseases shifts from morbidity control to transmission interruption and elimination. It is important to highlight that the requirements/ideal features of a test are dependent on the stage of the programme (for example, the features of a test ideal for conducting pre-control mapping are not the same as those ideal for certifying elimination/post-mass drug administration (MDA) surveillance [21Stothard J.R. et al.Diagnostics for schistosomiasis in Africa and Arabia: a review of present options in control and future needs for elimination.Parasitology. 2014; 141: 1947-1961Crossref PubMed Scopus (0) Google Scholar, 22Utzinger J. et al.New diagnostic tools in schistosomiasis.Clin. Microbiol. Infect. 2015; 21: 529-542Abstract Full Text Full Text PDF PubMed Scopus (162) Google Scholar, 26Bergquist R. et al.Diagnostic dilemmas in helminthology: what tools to use and when?.Trends Parasitol. 2009; 25: 151-156Abstract Full Text Full Text PDF PubMed Scopus (294) Google Scholar]). We therefore focus our economic arguments on two key areas (i) more rapid and convenient tests, and (ii) more sensitive tests (though these should not be treated as mutually exclusive as it is possible that a test could have both of these qualities). Though it is likely that a new test or method will be more expensive in terms of the required materials, they can, in some cases, be faster to process and prepare – particularly if they do not require a stool sample. For example, the unit cost of a urine-based point-of-contact circulating cathodic antigen (CCA) test alone is now around 1.46 to 1.76 US$ [18Worrell C.M. et al.Cost analysis of tests for the detection of Schistosoma mansoni infection in children in western Kenya.Am. J. Trop. Med. Hyg. 2015; 92: 1233-1239Crossref PubMed Scopus (30) Google Scholar] (which is higher than the unit cost of a Kato-Katz kit), but the test is much faster and less labour intensive to implement [32Stothard J.R. et al.Use of circulating cathodic antigen (CCA) dipsticks for detection of intestinal and urinary schistosomiasis.Acta Tropica. 2006; 97: 219-228Crossref PubMed Scopus (122) Google Scholar]. Consequently, a survey using the CCA test instead of the Kato-Katz technique could potentially be performed faster and with fewer staff, reducing the personnel cost required to implement the survey. Furthermore, if the staff do not require training in microscopy to perform the diagnostic test, scaling-up implementation would be more programmatically feasible and cheaper (it is important to note that the number of trained parasitologists can be limited in some endemic areas). This is illustrated by the study by Worrell et al. [18Worrell C.M. et al.Cost analysis of tests for the detection of Schistosoma mansoni infection in children in western Kenya.Am. J. Trop. Med. Hyg. 2015; 92: 1233-1239Crossref PubMed Scopus (30) Google Scholar] who found that the labour costs associated with using the point-of-contact CCA test were less than that of the Kato-Katz test. Ideally, a new diagnostic method could be performed by community health workers and teachers, and therefore integrated within the distribution of treatment, at a much lower cost than if trained laboratory personnel were required (though the opportunity cost of this should be evaluated). It should be noted that a recent study found that pooling of stool samples may be a way of increasing the speed of the Kato-Katz technique [33Kure A. et al.Comparison of individual and pooled stool samples for the assessment of intensity of Schistosoma mansoni and soil-transmitted helminth infections using the Kato-Katz technique.Parasit. Vectors. 2015; 8: 489Crossref PubMed Scopus (22) Google Scholar]. However, how this method affects the cost of performing the Kato-Katz technique and its sensitivity at low infection levels requires further investigation. Past research has shown that it is more effective and accurate to increase the number of schools sampled within a pre-control mapping survey compared to sampling more children per school [16Sturrock H.J. et al.Optimal survey designs for targeting chemotherapy against soil-transmitted helminths: effect of spatial heterogeneity and cost-efficiency of sampling.Am. J. Trop. Med. Hyg. 2010; 82: 1079-1087Crossref PubMed Scopus (29) Google Scholar]. Point-of-contact rapid diagnostics would make this more feasible and achievable at a potentially lower cost. Furthermore, if the method had a greater sensitivity than the standard Kato-Katz technique, a smaller sample size would be required to have the equivalent statistical power – again bringing down the costs. When considering potential samples sizes, it is important to recognise that, as we progress towards elimination, the decrease in infection prevalence will necessitate a larger sample size than previously used to retain statistical power. Furthermore, if a new test had a higher sensitivity than the Kato-Katz technique, it would result in an increase in the reported prevalence of infection. Calibration will be essential to allow measurements from new methods to be equated to past Kato-Katz (epg) measures [31Easton A.V. et al.Multi-parallel qPCR provides increased sensitivity and diagnostic breadth for gastrointestinal parasites of humans: field-based inferences on the impact of mass deworming.Parasit. Vectors. 2016; 9: 1-12Crossref PubMed Scopus (111) Google Scholar]. This is particularly important when interpreting WHO's treatment guidelines (which are based on prevalence estimates obtained using the Kato-Katz technique). Due to financial and programmatic constraints, the majority of Kato-Katz-based surveys for STH and S. mansoni currently focus on sampling children in schools. However, this provides a misleading picture regarding the impact of treatment on the overall rate of transmission and infection levels in the community as a whole [34Anderson R.M. et al.Should the goal for the treatment of soil transmitted helminth (STH) infections be changed from morbidity control in children to community-wide transmission elimination?.PLoS Negl. Trop. Dis. 2015; 9: e0003897Crossref PubMed Scopus (88) Google Scholar]. Mathematical modelling studies have indicated that, in many settings, we need to consider expanding interventions beyond the school to include the community as a whole (or for Trichuris trichiura, to increase the treatment frequency and/or use combination therapy) [34Anderson R.M. et al.Should the goal for the treatment of soil transmitted helminth (STH) infections be changed from morbidity control in children to community-wide transmission elimination?.PLoS Negl. Trop. 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