Background
Scabies is a skin condition caused by the microscopic ectoparasite
Sarcoptes scabiei var.
hominis. It affects an estimated 150–200 million people worldwide [
1], with an estimated annual incidence globally in 2019 of 565 (499–634) million cases and disease burden of 4.84 million disability-adjusted life-years [
2]. Infestation with the scabies mite increases the risk of secondary bacterial complications such as impetigo, complicated skin and invasive infections, and immune-mediated conditions such as post-streptococcal glomerulonephritis and acute rheumatic fever [
3]. Scabies is classified as a Neglected Tropical Disease (NTD) by the World Health Organization (WHO) warranting large-scale action for public health control [
4‐
6]. Ivermectin-based mass drug administration (MDA) is effective for disease control in communities with high scabies prevalence (≥10%) [
7‐
9]. Thus, a priority in the strategy for scabies control is establishing standardised diagnostic and survey methods to identify target areas for MDA.
While scabies is definitively diagnosed with direct microscopic visualisation of the mite or its products from skin scrapings, this test is not suitable in field settings due to cost, requirements for training and access to equipment, and low sensitivity [
10,
11]. To standardise diagnosis, the International Alliance for the Control of Scabies (IACS) developed consensus criteria (2020 IACS criteria,
Table S1) encompassing varying levels of diagnostic complexity for use in a variety of research, clinical or public health settings [
12,
13]. For public health settings where direct visualisation techniques are not possible, a diagnosis of ‘Clinical Scabies’ or ‘Suspected Scabies’ using the 2020 IACS criteria requires the examining field worker to take a brief history of itch and contacts and do a skin examination. Initial validation of clinical assessment for non-expert examiners using the 2020 IACS criteria has shown moderate sensitivity and good specificity [
14,
15].
However, assessment of contact history can be time consuming, and may not be reliable [
15]. Simplified criteria defining ‘typical lesions in a typical distribution, with or without itch’ as scabies cases, were proposed by the 2019 WHO Informal Consultation on a Framework for Scabies Control as an alternative, based on the assumption that these criteria would be more efficient and feasible for rapid mapping purposes as they utilised an abbreviated examination and omitted assessment of contact history [
16]. However, the accuracy of prevalence estimates using these simplified criteria is not known, and an evaluation was identified as an operational research priority by the WHO Informal Consultation [
16,
17]. A high scabies prevalence has previously been identified in several Pacific and southeast Asian countries, including Fiji, Solomon Islands and Timor-Leste [
5]. We aimed to evaluate the accuracy of prevalence estimations obtained by simplified criteria compared to the 2020 IACS criteria in surveys completed in these countries. Further, we aimed to investigate whether these estimates differ by country, sex, or age. Lastly, we aimed to explore the accuracy of alternatives to the proposed simplified criteria.
Results
A total of 9632 participants were recruited from the three studies. Following exclusion of 120 participants with incomplete data, a total of 9526 participants were included in the analysis (
Fig. S1). The majority of participants (54.8%) were from the Solomon Islands, with fewer from Fiji (35.2%) and Timor-Leste (10.0%). There were slightly fewer males included (47.6%). The median age of participants was 15 years old (interquartile range 8–38 years old, range 0–98 years old) and the largest proportion of participants ranged from 5 to 14 years old (35.1%, Table
3). There was a higher proportion of participants aged less than 15 years old in the Solomon Islands survey compared to the 2009 national census (48.0% vs 41.0%) [
28]. The age distribution of participants from Timor-Leste was different (median 10 years old; interquartile range 8–11 years old) as that survey only included children. There were no substantial differences in age or sex structure of the sample population in Fiji compared to the overall population reported in the 2017 census.
Table 3
Demographics of participants
Sex |
Male | 2473 (47.3%) | 1625 (48.5%) | 439 (46.2%) | 4537 (47.6%) |
Female | 2751 (52.7%) | 1726 (51.5%) | 512 (53.8%) | 4989 (52.4%) |
Age (years) |
0–1 | 263 (5.0%) | 171 (5.1%) | 4 (0.4%) | 438 (4.6%) |
2–4 | 541 (10.4%) | 258 (7.7%) | 19 (2.0%) | 818 (8.6%) |
5–9 | 900 (17.2%) | 403 (12.0%) | 438 (46.1%) | 1741 (18.3%) |
10–14 | 804 (15.4%) | 310 (9.3%) | 482 (50.7%) | 1596 (16.8%) |
15–29 | 990 (19.0%) | 719 (21.5%) | 8 (0.8%) | 1717 (18.0%) |
30–49 | 1051 (20.1%) | 809 (24.1%) | 0 | 1860 (19.5%) |
≥ 50 | 675 (12.9%) | 681 (20.3%) | 0 | 1356 (14.2%) |
Total | 5224 (54.8%) | 3351 (35.2%) | 951 (10.0%) | 9526 (100.0%) |
Prevalence by 2020 IACS criteria
Using the 2020 IACS criteria, 1577 individuals (16.6%, [95% CI 15.8, 17.3], Table
4) were classified as cases of scabies. This included 880 cases (55.8% of cases) of ‘Clinical Scabies’, and 697 cases (44.2% of cases) of ‘Suspected Scabies’ (C1: 418 cases, 26.5% of cases; and C2: 279 cases, 17.7% of cases, Table
5). The prevalence of ‘Suspected Scabies subcategory C2’ in Timor-Leste was 8.9% (26.5% of cases), 2.7% in Solomon Islands (18.2% of cases) and 1.5% in Fiji (10.9% of cases, Table
5). Itch was present in 1470 cases (93.2% of cases), and contact history in 1266 (80.3% of cases, Table
5) [
23].
Table 4
Comparison of prevalence estimates between 2020 IACS criteria and simplified criteria
Total (n = 9526) | 1577 | 16.6 (15.8, 17.3) | 1490 | 15.6 (14.9, 16.4) | 0.9 (−0.1, 2.0) | 0.82 (0.80–0.83) |
Country |
Solomon Islands (n = 5224) | 786 | 15.0 (14.1, 16.0) | 788 | 15.1 (14.1, 16.1) | −0.0 (−1.4, 1.3) | 0.79 (0.77–0.80) |
Fiji (n = 3351) | 470 | 14.0 (12.9, 15.2) | 450 | 13.4 (12.3, 14.6) | 0.6 (−1.15, 2.2) | 0.90 (0.88–0.91) |
Timor-Leste (n = 951) | 321 | 33.8 (30.8, 36.8) | 252 | 26.5 (23.8, 29.4) | 7.3 (3.1, 11.4) | 0.75 (0.73–0.77) |
Sex |
Male (n = 4537) | 804 | 17.7 (16.6, 18.9) | 772 | 17.0 (15.9, 18.1) | 0.7 (−0.9, 2.3) | 0.82 (0.81–0.84) |
Female (n = 4989) | 773 | 15.5 (14.5, 16.5) | 718 | 14.4 (13.4, 15.4) | 1.1 (−0.3, 2.5) | 0.81 (0.80–0.83) |
Age (years) |
0–1 (n = 438) | 124 | 28.3 (24.3, 32.7) | 135 | 30.8 (26.7, 35.3) | −2.5 (−8.6, 3.5) | 0.84 (0.83–0.86) |
2–4 (n = 818) | 212 | 25.9 (23.0, 29.0) | 220 | 26.9 (24.0, 30.0) | −1.0 (−5.3, 3.3) | 0.81 (0.80–0.83) |
5–9 (n = 1741) | 450 | 25.8 (23.8, 28.0) | 440 | 25.3 (23.3, 27.4) | 0.6 (−2.3, 3.5) | 0.81 (0.79–0.82) |
10–14 (n = 1596) | 336 | 21.1 (19.1, 23.1) | 319 | 20.0 (18.1, 22.0) | 1.1 (−1.7, 3.9) | 0.78 (0.77–0.80) |
15–29 (n = 1717) | 180 | 10.5 (9.1, 12.0) | 163 | 9.5 (8.2, 11.0) | 1.0 (−1.0, 3.0) | 0.80 (0.79–0.82) |
30–49 (n = 1860) | 158 | 8.5 (7.3, 9.9) | 123 | 6.6 (5.6, 7.8) | 1.9 (0.2, 3.6) | 0.83 (0.81–0.84) |
≥ 50 (n = 1356) | 117 | 8.6 (7.2, 10.2) | 90 | 6.6 (5.4, 8.1) | 2.0 (−0.0, 4.0) | 0.82 (0.80–0.83) |
Table 5
Breakdown of scabies cases by 2020 IACS Criteria
Country |
Solomon Islands | 706 (89.8%) | 662 (84.2%) | 644 (81.9%) | 785 (99.9%) | 786 | 439 (55.9%) | 204 (26.0%) | 143 (18.2%) |
Fiji | 454 (96.6%) | 325 (69.1%) | 423 (90.0%) | 466 (99.1%) | 470 | 258 (54.9%) | 161 (34.3%) | 51 (10.9%) |
Timor-Leste | 310 (96.6%) | 279 (86.9%) | 236 (73.5%) | 321 (100.0%) | 321 | 183 (55.8%) | 53 (16.5%) | 85 (26.5%) |
Sex |
Male | 745 (92.7%) | 645 (80.2%) | 674 (83.8%) | 802 (99.8%) | 804 | 454 (56.5%) | 218 (27.1%) | 132 (16.4%) |
Female | 725 (93.8%) | 621 (80.3%) | 629 (81.4%) | 770 (99.6%) | 773 | 426 (55.1%) | 200 (25.9%) | 147 (19.0%) |
Age (years) |
0–1 | 110 (88.7%) | 94 (75.8%) | 115 (92.7%) | 124 (100.0%) | 124 | 71 (57.3%) | 44 (35.5%) | 9 (7.3%) |
2–4 | 205 (96.7%) | 164 (77.4%) | 186 (87.7%) | 212 (100.0%) | 212 | 131 (61.8%) | 55 (25.9%) | 26 (12.3%) |
5–9 | 423 (94.0%) | 369 (82.0%) | 381 (84.7%) | 450 (100.0%) | 450 | 273 (60.7%) | 108 (24.0%) | 69 (15.3%) |
10–14 | 307 (91.4%) | 281 (83.6%) | 271 (80.7%) | 336 (100.0%) | 336 | 187 (55.7%) | 84 (25.0%) | 65 (19.3%) |
15–29 | 167 (92.8%) | 134 (74.4%) | 142 (78.9%) | 179 (99.4%) | 180 | 82 (45.6%) | 59 (32.8%) | 39 (21.7%) |
30–49 | 146 (92.4%) | 137 (86.7%) | 121 (76.6%) | 155 (98.1%) | 158 | 85 (53.8%) | 33 (20.9%) | 40 (25.3%) |
≥ 50 | 112 (95.7%) | 87 (74.4%) | 87 (74.4%) | 116 (99.1%) | 117 | 51 (43.6%) | 35 (29.9%) | 31 (26.5%) |
Total | 1470 (93.2%) | 1266 (80.3%) | 1303 (82.6%) | 1572 (99.7%) | 1577 | 880 (55.8%) | 418 (26.5%) | 279 (17.7%) |
The prevalence of scabies (either ‘Clinical Scabies’ or ‘Suspected Scabies’) was 33.8% in Timor-Leste, 15% in Solomon Islands, and 14% in Fiji (Table
4). A higher proportion of males (17.7%) were classified as having scabies compared to females (15.5%, relative risk (RR) 1.1, [95% CI 1.0, 1.3]). Scabies was more commonly diagnosed in younger age groups, with a prevalence of 24.4% in children aged less than 15 years, compared to those aged 15 years or older (prevalence 9.2%; RR 2.6, [95% CI 2.4, 2.9]).
Prevalence by simplified criteria
The differences in the prevalence estimates obtained by the 2020 IACS criteria and the simplified criteria were not significant overall (16.6% vs 15.6%, difference 0.9, [95% CI -0.1, 2.0], Table
4) or in Solomon Islands or Fiji. In Timor-Leste, the 2020 IACS criteria prevalence was higher than the simplified criteria prevalence (33.8% vs 26.5%, difference 7.3, [95% CI 3.1, 11.4], Table
4). There was very strong agreement between the two prevalence estimates overall (κ = 0.82, [95% CI 0.80, 0.83], Table
4). In Timor-Leste the agreement was moderately strong (κ = 0.75, [95% CI 0.73, 0.77]). There were no statistical differences between the estimates using the two methods by sex or age groups.
Sensitivity and specificity of simplified criteria
Overall, simplified criteria had a sensitivity of 82.3% (95% CI 80.2, 84.2) and specificity of 97.6% (95% CI 97.2, 97.9, Table
6) compared to the 2020 IACS criteria. There were 279 false negative cases (2.9% of all participants), all of whom had itch and a positive contact history but atypical features in either lesion appearance or distribution (2020 IACS criteria subcategory C2), thus failing to meet the simplified criteria definition. As contact history is not included in the simplified criteria, these cases were categorised as negative. The 192 false positives (2.0% of all participants) had typical lesions in a typical distribution but neither itch nor contact history (at least one of which is required by the 2020 IACS criteria).
Table 6
Diagnostic accuracy of simplified diagnostic compared to 2020 IACS criteria
Country |
Solomon Islands (n = 5224) | 643 | 4293 | 145 | 143 | 81.8 (78.9, 84.4) | 96.7 (96.2, 97.2) |
Fiji (n = 3351) | 419 | 2850 | 31 | 51 | 89.1 (86.0, 91.8) | 98.9 (98.5, 99.3) |
Timor-Leste (n = 951) | 236 | 614 | 16 | 85 | 73.5 (68.3, 78.3) | 97.5 (95.9, 98.5) |
Sex |
Male (n = 4537) | 672 | 3633 | 100 | 132 | 83.6 (80.8, 86.1) | 97.3 (96.7, 97.8) |
Female (n = 4989) | 626 | 4124 | 92 | 147 | 81.0 (78.0, 83.7) | 97.8 (97.3, 98.2) |
Age (years) |
0–1 (n = 438) | 115 | 294 | 20 | 9 | 92.7 (86.7, 96.6) | 93.6 (90.3, 96.1) |
2–4 (n = 818) | 186 | 572 | 34 | 26 | 87.7 (82.5, 91.8) | 94.4 (92.2, 96.1) |
5–9 (n = 1741) | 381 | 1232 | 59 | 69 | 84.7 (81.0, 87.9) | 95.4 (94.1, 96.5) |
10–14 (n = 1596) | 271 | 1212 | 48 | 65 | 80.7 (76.0, 84.7) | 96.2 (95.0, 97.2) |
15–29 (n = 1717) | 141 | 1515 | 22 | 39 | 78.3 (71.6, 84.1) | 98.6 (97.8, 99.1) |
30–49 (n = 1860) | 118 | 1697 | 5 | 40 | 74.7 (67.2, 81.3) | 99.7 (99.3, 99.9) |
≥ 50 (n = 1356) | 86 | 1235 | 4 | 31 | 73.5 (64.5, 81.2) | 99.7 (99.2, 99.9) |
Total (n = 9526) | 1298 | 7757 | 192 | 279 | 82.3 (80.2, 84.2) | 97.6 (97.2, 97.9) |
Sensitivity and specificity did not vary between males and females. The sensitivity was highest in children aged less than two years (92.7%) and decreased with age (73.5% in those ≥50 years). Specificity increased with age (93.6% in children aged less than two years to 99.7% in those aged ≥30 years, Table
6).
Alternative simplified criteria
The proportion of individuals classified as having scabies estimated by alternative simplified criteria ASC1, ASC2 and ASC3 were significantly higher than estimates using 2020 IACS criteria (ASC1: 20.3%, difference = − 3.7% [95% CI −4.8, − 2.6], ASC2: 23.8%, difference = − 7.2% [95% CI −8.3, − 6.1], ASC3: 27.8%, difference = − 11.2% [95% CI −12.4, − 10.0],
Table S2). ASC4 produced the most similar prevalence estimate overall of 16.7% (difference = − 0.1%, [95% CI −1.2, 0.9]) however greatly overestimated scabies prevalence in those younger than five years old (difference = 6.1%, [95% CI 2.7, 9.4]). Use of the alternate criteria led to an increase in sensitivity for ASC1 (99.7%, [95% CI 99.3, 99.9]), ASC2 (99.7%, [95% CI 99.3, 99.9]) and ASC3 (93.2%, [95% CI 91.9, 94.4]), however all four alternative criteria had lower specificity (
Table S3).
Discussion
Our results suggest that the simplified criteria proposed by the WHO Informal Consultation can be used to accurately estimate the prevalence of scabies during rapid mapping and surveys, with a similar prevalence estimate when compared to assessment using the 2020 IACS criteria. The simplified criteria had a sensitivity of 82% and specificity of 98%. We believe this accuracy is acceptable for the purposes of surveys, where public health decisions are made based on community prevalence, rather than treatment decisions based on individual diagnoses.
Rapid mapping aims to identify areas where the community prevalence of scabies is ≥10% (or ≥ 15% in school-aged children, if a school-survey method is used) for implementation of MDA programs [
16]. Based on our data in these three countries where scabies prevalence was > 10%, use of simplified criteria as opposed to 2020 IACS criteria would not lead to a different recommendation for where MDA should be implemented. This study demonstrates that the simplified criteria may be useful in regions with a high scabies prevalence. This is an important finding as these are the regions where the public health control of scabies using MDA is being prioritised, but where there are currently very little or no estimates of prevalence. However, it is possible that in populations where scabies prevalence is close to the recommended MDA starting threshold, choice of criteria may impact public health decision making.
Accurate mapping strategies are important to identify and prioritise areas for scabies control and MDA, but these methods need to be feasible at large scale. Rapid mapping strategies, using simplified criteria, have been successfully used for the control of other NTDs including trachoma, schistosomiasis, lymphatic filariasis and onchocerciasis [
29,
30]. Similarly, in 1994, a UK working party developed simplified diagnostic criteria for atopic dermatitis to be used in epidemiological studies [
31‐
34]. The simplified criteria for scabies comprise a brief examination of frequently exposed skin, which may facilitate implementation at large scale with limited resources by using less specialised local healthcare workers and reducing the number of interpreters required. Studies comparing the accuracy of examination of exposed areas of the skin to examination of the whole body found that examination of exposed areas had close to 90% sensitivity [
14,
35]. Omitting contact history and consideration of atypical lesions should further simplify training and assessment in the field. In addition, it may increase recruitment rates by omitting examination of sensitive body areas and reducing the time burden placed on participants. Our exploration of alternatives to the simplified criteria showed that it is possible to improve sensitivity by including cases with atypical lesions. However, three of the four of these alternative methods (ASC1, ASC2, ASC3) overestimated the prevalence of scabies. Therefore, our data support the current recommendations for the simplified criteria. Prevalence estimates using ASC4 (presence of itch and contact history) were similar to those using 2020 IACS criteria. However, itch is a highly non-specific symptom which is caused by many common conditions, and is variably reported, including in young children. Further studies would be required to investigate whether an assessment method that omits examination of the skin could be a feasible alternative to the proposed simplified criteria.
The simple, brief nature of scabies assessment may facilitate integration with surveys for other NTDs and other health programmes [
36,
37]. Epidemiological mapping of onchocerciasis (REMO) integrates geographical and environmental risk factors with mapping data to establish zones of endemicity [
38]. Although no such risk factors have been established for scabies, and scabies is not a vector-borne disease, this could be explored through future research.
Our study has limitations. First, the three surveys we included are from tropical, island countries with a very high scabies prevalence. Our results may not be generalisable to other settings such as temperate climates, mainland populations, highly urbanised environments or to lower-prevalence settings. Second, the Timor-Leste survey only enrolled school-aged children and their siblings. Scabies is more prevalent in children, which may have contributed to the difference in results between surveys. There is also a high prevalence of secondary impetiginized scabies in this population [
19,
39,
40]. These cases may have lesions of atypical appearance or distribution, which are not classified as scabies using the simplified criteria. Similarly, scabies can present in more atypical forms in the elderly population, which may have contributed to the lower sensitivity seen in those aged 50 years and older [
41]. Third, the current recommended threshold to cease MDA is a prevalence of < 2% [
16], and further evidence is needed to compare the accuracy of simplified criteria in lower-prevalence settings. Fourth, we were only able to compare simplified criteria with the ‘Clinical and Suspected Scabies’ levels of the 2020 IACS criteria, as the ‘Confirmed Scabies’ level, which requires direct mite visualisation was not feasible to include in these surveys. The absence of an appropriate reference standard is a limitation for all studies of diagnostic accuracy for scabies, and further development of objective diagnostic tests that can be feasibly used in the field is required. Fifth, we compared the accuracy of the criteria based on an analysis of the components collected during a single assessment in the field, in which health workers were trained to assess participants according to 2020 IACS clinical criteria. It is possible that knowledge of contact history may have influenced the classification of skin lesions in some cases, and it is not known how a different training program and survey method, based on the simplified criteria, would affect the recording of scabies lesions. Finally, examination was conducted by healthcare workers with limited experience, and the sensitivity of scabies diagnosis may be lower, particularly for mild forms of scabies [
15].
Conclusions
There was no significant difference between the prevalence of scabies using simplified diagnostic criteria, as recommended in the informal WHO Framework, compared with the 2020 IACS criteria in the pooled survey results from these three tropical island populations. Implementation of simplified criteria may be an efficient and accurate way to facilitate rapid mapping to determine high prevalence areas for scabies control. Further work is needed to investigate the accuracy in urbanised and lower-prevalence populations, and to evaluate the implementation of simplified criteria in the field setting.
Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit
http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.