Abstract
Purpose of Review
This study describes the results obtained by the World Health Organization (WHO) collaborating centre (CC) for the diagnosis of intestinal helminths and protozoa (WHO CC ITA-116) during the first 2 years of its activity on (i) the prevalence of intestinal parasites in migrants in southern Italy and (ii) the development and application of new diagnostic tools for intestinal helminths (e.g. FLOTAC, Mini-FLOTAC Kit 200 tests, Kubic FLOTAC microscope (KFM)).
Recent Findings
Almost 23.3% of migrants examined were positive for at least one intestinal parasite. Moreover, a significant correlation was found between the duration of stay in Italy and positivity for intestinal parasites. The results of the comparison between diagnostic techniques showed a perfect agreement between FLOTAC and Mini-FLOTAC Kit 200 tests whereas no statistically significant differences were found between the count of helminth eggs obtained by Mini-FLOTAC with optical microscope and KFM.
Summary
The results obtained by WHO CC ITA-116 during the first 2 years of its activity provide important information on innovations in parasitological diagnosis and add data to the parasitological scenario of migrants arriving in southern Italy, highlighting the importance of regular parasitological monitoring.
Similar content being viewed by others
Explore related subjects
Find the latest articles, discoveries, and news in related topics.Avoid common mistakes on your manuscript.
Introduction
Over the past decade, the number of migrants and refugees in Europe has increased dramatically due to war, violence, persecution, or poor health in their home countries [1, 2]. According to the United Nations High Commissioner for Refugees (UNHCR), about 200,000 people irregularly crossed European land borders in 2021 (this number has increased by 60% compared to 2020), more than 114,000 by sea, mainly in Italy, Greece, Spain, Cyprus, and Malta. In 2021, asylum seekers in Europe came from about 140 countries, in particular from Syria, Afghanistan, and Iraq (https://ec.europa.eu/info/strategy/priorities-2019-2024/promoting-our-european-way-life/statistics-migration-europe_en#RefugeesinEurope).
Despite the sharp increase in the number of migrants, refugees, and asylum seekers (hereafter “migrants”) worldwide in recent years, insufficient attention has been paid to their health needs as the World Health Organization (WHO) points out [3••]. This entails developing appropriate free health care and comprehensive medical screening, incorporating psychological health care, and breaking down cultural and linguistic barriers [3••, 4]. Knowledge of the health status of migrants is important for a civil reception and a more effective integration process that respects human rights [4]. These people are at very high risk of infection, not only in their countries but also during the travel, due to sub-optimal hygiene standards, malnutrition, and lack of access to health services [5]. Therefore, a full health examination that includes thorough parasitological screening could have far-reaching public health implications and be of great importance in revising the policies and practices applied from the arrival to the final destination of migrants [3••].
Intestinal parasites (helminths and protozoa) are likely to be worth diagnosing through screening strategies. Indeed, many migrants come from countries where parasitic diseases are endemic, e.g. those caused by soil-transmitted helminths (STHs), Schistosoma spp., and other helminths and protozoa [6]. Although these parasites can cause substantial morbidity and mortality, they are seldom diagnosed [7]. As a consequence, data on the prevalence and burden of parasitic diseases among newly arriving migrants in Italy are still scant, with only a few papers published that focused on schistosomiasis and helminthiasis, particularly strongyloidiasis [5, 7,8,9,10]. The Italian guidelines on health assessment for migrants recommend parasitological screening (serology) for Strongyloides stercoralis and Schistosoma spp. when the patients come from endemic areas and copromicroscopy for other intestinal parasites only in presence of symptoms or eosinophilia [11].
To date, the recommended technique for the qualitative diagnosis of intestinal parasites is the formol-ether concentration method (FECM) [12] performed on three different samples. As for quantitative diagnosis, the Kato-Katz technique has been the diagnostic method recommended by WHO since the 1990s for quantifying eggs in stool and then classifying the infection intensity based on faecal egg counts (FECs; expressed as eggs per gram (EPG) of stool) [13]. In the last decade, a variety of new diagnostic methods have been introduced, such as McMaster [14], (Mini-)FLOTAC [15, 16], and FECPAKG2 [17]. More recently, the use of advanced technologies, such as automated methods for copromicroscopy based on artificial intelligence, has begun to offer solutions to overcome gaps and limitations of FEC techniques (i.e. human errors and time for analysis) for the diagnosis of various parasites of public health relevance (e.g. STHs, Schistosoma spp., protozoa, etc.) [18].
For more than 20 years, the Centre for Monitoring of Parasites (CREMOPAR, at the University of Napoli Federico II) has been involved in supporting the diagnosis of protozoa and helminths in endemic populations, using multivalent and accurate diagnostic tools [8, 16, 18, 19]. Moreover, CREMOPAR was designated as collaborating centre of the World Health Organization (WHO) for the diagnosis of intestinal helminths and protozoa (WHO CC ITA-116; https://www.whocc.ita116.unina.it/). Beyond supporting endemic countries in monitoring preventive chemotherapy programmes [20], the WHO CC ITA-116 carries out regular parasitological surveillance and health care for migrants in southern Italy. The present study provides results of two main activities of the WHO CC ITA-116: (i) updating data on the prevalence of intestinal parasites among migrants in southern Italy and (ii) improving diagnostic approaches for intestinal parasites.
Materials and Methods
From July 2020 to March 2022, 373 migrants who arrived in the Campania region (southern Italy) were screened for intestinal parasites. The spokes for the stool collection were set in three different migrant assistance centres in the region: (i) extraordinary reception centres (CAS), (ii) Protection System for Beneficiaries of International Protection and for Unaccompanied Foreign Minors (SIPROIMI)/Reception and Integration System (SAI), and (iii) Medical Centre for the Health Protection of migrants (ASL-NA1). At the time of stool collection, patients were not taking drugs or other substances that could affect the results of the parasitological examination. The samples were collected after the signature of an informed consent document by the participants indicating that they understood the purpose and the procedures required for the study and that they were willing to let their child participate in the study (in the case of parents of children). This study was approved by the ethics committee of the University of Naples Federico II.
All samples were analysed in the laboratories of the WHO CC ITA-116 as described in the study design (Fig. 1), and all individuals resulted positive for intestinal parasites (helminths and protozoa) received targeted antiparasitic treatment.
First, one aliquot of two grams of stool sample was analysed by the FLOTAC dual technique, using two flotation solutions (FS), i.e. FS2 (sodium chloride-based; specific gravity, s.g. = 1200) and FS7 (zinc sulphate-based; s.g. = 1350), according to the protocol described by Cringoli et al. [15].
Second, a sub-sample of 90 stool samples was used to validate for the first time the Mini-FLOTAC Kit 200 tests (Fig. 2) for field diagnosis of helminth infections. Each sample was homogenized and analysed by Mini-FLOTAC using FS2 and FS7, according to the protocol described by Cringoli et al. [16] and recommended by the WHO Bench Aids [21].
Finally, the first validation of the Kubic FLOTAC microscope (KFM) [18] was performed on 23 stools resulted positive for STHs (16 for hookworms and 7 for Trichuris trichiura) using the Mini-FLOTAC technique. The performance of the Mini-FLOTAC was evaluated using either a traditional optical microscope (OM) or KFM.
For each positive subject, the number of cysts/oocysts/eggs and larvae per gram (CPG/OPG/EPG/LPG) of faeces was calculated. Furthermore, a questionnaire was filled out for each patient, reporting age, sex, country of origin, alimentary habits, health status, and duration of stay in Italy. The country of origin of each migrant was geo-referenced in a geographical information system (GIS) using ArcGIS Pro 2.7 (Environmental Systems Research Institute, Inc., Redlands, California, USA).
Statistical Analyses
The overall positivity was analysed in correlation with the variables: gender, age class, geographic origin of migrants, and duration of stay in Italy using Pearson’s chi-squared test. The association was considered significant at P < 0.05.
The performance comparison (i.e. sensitivity and negative predictive value, NPV) of the diagnostic methods used for the detection of intestinal parasitic infections was calculated considering the combined results as a “Gold standard” [22]. The agreement between the diagnostic techniques (FLOTAC and Mini-FLOTAC) for detecting intestinal parasites was calculated using Cohen’s κ statistic [23]. The κ measure was interpreted as follows: 0, no agreement; 0.01–0.20, poor agreement; 0.21–0.40, fair agreement; 0.41–0.60, moderate agreement; 0.61–0.80, substantial agreement; and 0.81–1.0, nearly perfect agreement.
All statistical analyses were performed using version 23 of SPSS software for Windows (SPSS Inc., Chicago, IL, USA).
Results
The 373 migrants, refugees, and asylum seekers who underwent parasitological examinations came from 32 countries. They were 46 females and 327 males, aged between 2 and 69 years (mean = 29; median = 28). Concerning the country of origin, 184 subjects (49.3%; 95% confidence interval [CI] = 44.2–54.5) came from Asia, 177 (47.4%; 95%CI = 42.3–52.6) from Africa, 6 from Eastern Europe (1.6%; 95%CI = 0.6–3.6), and 6 from Southern America (1.6%; 95%CI = 0.6–3.6) (Fig. 3).
A total of 87 migrants resulted positive for at least one intestinal parasite with an overall prevalence of 23.3% (95%CI = 19.2–28.0); of these 19 subjects (21.8%; 95%CI = 14.0–32.2) were co-infected with two or more helminth and/or protozoa species. Positivity to intestinal parasites according to the country of origin is summarized in Table 1.
Table 2 reports the number of positives, the prevalence (%), and EPG/LPG/OPG/CPG (min–max or single value in case of one positive sample) for each helminth/protozoa detected. No significant association (P > 0.05) was found between the positivity to parasites and the following independent variables: age, sex, country of origin, alimentary habits, and health status. However, a statistically significant difference was found between the duration of stay in Italy and the presence of intestinal parasites (63.6% of migrants resulted positive for intestinal parasites stayed in Italy for less than 1 year; P = 0.0076).
Table 3 shows the results of the comparison between the diagnostic techniques. Out of the 90 subsamples, the number of samples that resulted positive for helminths using each technique was as follows: 52 (57.8%, 95%CI = 46.9–68.0) with FLOTAC, 49 (54.4%, 95%CI = 43.6–64.9) with Mini-FLOTAC Kit 200 tests. Table 4 shows the performance of each technique. A nearly perfect agreement (κ = 0.93; P < 0.01) was observed between FLOTAC and Mini-FLOTAC Kit 200 tests.
No statistically significant differences (P > 0.05) were found between the total STH eggs (only hookworms and T. trichiura, since any sample was positive for Ascaris lumbricoides), counted by the Mini-FLOTAC with OM and with KFM (320 EPG vs 320 EPG). The time for counting helminth eggs in the Mini-FLOTAC chambers under the OM was ∼1–5 min, whereas the time for reading the Mini-FLOTAC with KFM was ∼3–8 min. Finally, 1185 images were acquired for the development of artificial intelligence (AI) and deep learning (DL) software for the automatic detection of hookworms and T. trichiura (Fig. 4) (a paper on validation of KFM and AI and DL software training in the human field is in preparation).
Discussion
The present study showed an overall prevalence of parasites in migrants in southern Italy of 23.3% (13.9% for helminths and 14.7% for protozoa), similar to other studies conducted in Italy [7, 8, 24, 25].
However, it is not always easy to compare data on the prevalence of parasites in different areas/countries, due to a variety of confounding factors affecting the results of parasitological screenings, such as selection bias (i.e. mainly enrolled subjects attending hospitals, outpatient clinics) [7], as well as differences in diagnostic approaches (i.e. coprology, immunology, molecular biology), and laboratory protocols [26•].
We found a higher prevalence of intestinal parasites in migrants from African and Asian countries that are endemic for parasitic infections [27], although the prevalence registered in Italy is different (not only in terms of rate, but also in terms of parasite species) from the geographical regions of birth, as also reported by other authors [7, 28]. According to these authors, this may be due to the migration route which is sometimes very long and crosses many countries, and to the mixing of different ethnic groups which could affect the species of intestinal parasites in different migrant populations.
The most common helminths found in this study were hookworms (28.7%) and T. trichiura (19.5%). This is consistent with data from the WHO which indicated that STHs are among the most prevalent parasites worldwide, with approximately 1.5 billion people infected and 2.0 billion people at risk of disease by STH [3••]. Ascaris lumbricoides was not detected in any of the studied subjects, although it was previously found with a low prevalence (0.7–1.4%) in migrants in the Campania region [8, 19, 29]. Further studies could be interesting to understand how the parasitological scenario in migrants in this Italian region has changed over the years and in relation to the origin of migrants.
Among protozoa, E. coli (25.3%), E. nana (14.9%), and G. duodenalis (8.0%) showed a higher prevalence than in other studies [7, 30].
A significant association was found between the decreasing positivity to parasites and duration of stay in Italy (63.6% of migrants who tested positive for intestinal parasites had lived in Italy for less than 1 year). This could be due to the improvement in social conditions (i.e. stable accommodation, job opportunities, availability of health care, etc.) as reported by other authors [6, 7, 19].
Moreover, this paper provided interesting insights into the performance of copromicroscopic techniques. Most intestinal parasites do not give specific clinical signs and therefore can only be detected by laboratory diagnosis [3••]. As previously reported, FLOTAC and Mini-FLOTAC are highly sensitive, accurate, and precise techniques for the diagnosis of intestinal parasites in humans [15, 16, 19, 31,32,33,34,35,36,37,38,39]. The Mini-FLOTAC Kit 200 tests, validated for the first time in this study combines the performance of Mini-FLOTAC with the advantage of having a portable kit with all the components to perform the analysis anywhere, obtaining very similar results to the FLOTAC technique (FLOTAC: 52 positive stool samples vs Mini-FLOTAC Kit 200 tests: 49 stool samples) with a perfect agreement and high sensitivity (94.2%). The only three stool samples that were negative with Mini-FLOTAC had parasitic levels (4 EPG) below the detection limit of this technique (in this case, the analytic sensitivity is 10 EPG at a dilution factor of 1:20).
A rapid diagnosis is necessary for an appropriate strategy of intervention. A field technique such as the Mini-FLOTAC Kit 200 tests could be very useful to perform efficient, rapid, and reliable diagnosis directly upon on the arrival of migrants in our country, thus preventing chronic diseases and complications and ensuring public health [7]. The main limitation of on-site diagnosis with a portable microscope is that it is not able to achieve high magnification to enable the detection of protozoa. For this reason, we validated the Mini-FLOTAC Kit 200 test for helminths only.
The use of innovative AI-based tools, such as KFM, could be very important to complete and improve on-site diagnosis of intestinal parasites (i.e. for all helminths and protozoa) and overcome the gaps and limitations of quantitative techniques (i.e. human errors and time for analysis), increasing diagnostic efficiency. This tool has already been successfully used for the detection of gastrointestinal nematodes in cattle [18] and in companion animals [40]. In this study, the KFM was successfully used to count STH eggs, and no differences were observed between the total number of eggs counted using the Mini-FLOTAC at OM and the KFM (320 EPG vs 320 EPG), although only positive samples were used to assess the diagnostic accuracy of KFM. Further studies are needed for the validation of KFM, also using negative samples. In addition, the AI software was trained for the first time to detect STH eggs in stool samples, which yielded promising results. In the future, the KFM will be trained to detect other helminths and protozoa. Thanks to remote control via software using a smartphone, tablet, or PC, or via the Internet, it is possible to transmit the acquired images to other laboratories, which could be very useful to create a network or to support operators directly in the field.
Therefore, the combination of these innovative tools (i.e. Mini-FLOTAC Kit 200 tests and KFM) could be very important to improve the diagnosis of intestinal parasites, as well as to implement the parasitological assays provided in the “Italian guidelines on Health assessment for migrants and asylum seekers upon arrival and while hosted in reception centres” [11], towards a migrant-friendly health system.
Conclusion
The results of this study add data to the parasitological scenario of migrants arriving in southern Italy and provide important information on innovations in parasitological diagnosis, highlighting the importance of regular parasitological screening as soon as possible after their arrival.
These activities are in line with the mission statement of our WHO CC ITA-116 collaborating centre focused to improve public health worldwide and to achieve the main goals of the Neglected Tropical Diseases (NTD) 2021–2030 roadmap to validate and standardize innovative diagnostics for the control and elimination of intestinal parasites.
Data Availability
The data that support the findings of this study are available on request from the corresponding author.
References
Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance
Hasanović M, Šmigalović D, Fazlović M. Migration and acculturation: what we can expect in the future. Psychiatr Danub. 2020;32(Suppl 3):386–95.
Garcia MF, Birman D. Understanding the migration experience of unaccompanied youth: a review of the literature. Am J Orthopsychiatry. 2022;92(1):79–102. https://doi.org/10.1037/ort0000588.
WHO, 2022. Addressing the health challenges in immigration detention, and alternatives to detention. WHO, 2022, outlines current evidence, knowledge, and best practices relating to the health and health challenges of refugees and migrants in immigration detention, as well as the implementation of alternatives to detention.
Manfredi L, Sciannameo V, Destefanis C, Prisecaru M, Cossu G, Gnavi R, Macciotta A, Catalano A, Pepe RR, Sacerdote C, Ricceri F. Health status assessment of a population of asylum seekers in Northern Italy. Global Health. 2022;18(1):57. https://doi.org/10.1186/s12992-022-00846-0.
Pavli A, Maltezou H. Health problems of newly arrived migrants and refugees in Europe. J Travel Med. 2017;24(4). https://doi.org/10.1093/jtm/tax016.
Mazzitelli M, Torti C, Greco G, Strazzulla A, Costa C, Pisani V, Sorace C, Giancotti A, Lamberti A, Barreca GS, Quirino A, Liberto MC, Focà A, Matera G. Prevalence of parasitic infections in migrants: do official symptom-driven guidelines apply to the current situation? Infez Med. 2018;26(4):347–55.
FontanelliSulekova L, Ceccarelli G, Pombi M, Esvan R, Lopalco M, Vita S, Mattiucci S, Gabrielli S. Sanitary bureau of the asylum seekers center of Castelnuovo di Porto. Occurrence of intestinal parasites among asylum seekers in Italy: a cross-sectional study. Travel Med Infect Dis. 2019;27:46–52. https://doi.org/10.1016/j.tmaid.2018.10.006.
Gualdieri L, Piemonte M, Alfano S, Maffei R, Della Pepa ME, Rinaldi L, Galdiero M, Galdiero M, Cringoli G. Immigrants living in an urban milieu with sanitation in Southern Italy: persistence and transmission of intestinal parasites. Parasitol Res. 2016;115(3):1315–23. https://doi.org/10.1007/s00436-015-4868-2.
Buonfrate D, Gobbi F, Marchese V, Postiglione C, BadonaMonteiro G, Giorli G, Napoletano G, Bisoffi Z. Extended screening for infectious diseases among newly-arrived asylum seekers from Africa and Asia, Verona province, Italy, April 2014 to June 2015. Euro Surveill. 2018;23(16):17–00527. https://doi.org/10.2807/1560-7917.ES.2018.23.16.17-00527.
Asundi A, Beliavsky A, Liu XJ, Akaberi A, Schwarzer G, Bisoffi Z, Requena-Méndez A, Shrier I, Greenaway C. Prevalence of strongyloidiasis and schistosomiasis among migrants: a systematic review and meta-analysis. Lancet Glob Health. 2019;7(2):e236–48. https://doi.org/10.1016/S2214-109X(18)30490-X.
Baglio G, Marceca M, Tosti ME. I controlli alla frontiera La frontiera dei controlli. Controlli sanitari all’arrivo e percorsi di tutela per i migranti ospiti nei centri di accoglienza SNLG – Linee Guida Salute Migranti ed. 2017.
Suwansaksri J, Nithiuthai S, Wiwanitkit V, Soogarun S, Palatho P. The formol-ether concentration technique for intestinal parasites: comparing 0.1 N sodium hydroxide with normal saline preparations. Southeast Asian J Trop Med Public Health. 2002;33 Suppl 3:97–8.
Levecke B, Cools P, Albonico M, Ame S, Angebault C, Ayana M, Behnke JM, Bethony JM, Cringoli G, Dana D, Guillard B, Viet Hoa NT, Kang G, Kattula D, Keiser J, Kotze AC, Matoso LF, Maurelli MP, McCarthy JS, Mekonnen Z, Mirams G, Montresor A, Oliveira RC, Periago MV, Pinto SA, Rinaldi L, Sayasone S, Sumo L, Tchuem-Tchuenté LA, Cam Thach DT, Thomas E, Zeynudin A, Verweij JJ, Vlaminck J, Vercruysse J. Identifying thresholds for classifying moderate-to-heavy soil-transmitted helminth intensity infections for FECPAKG2, McMaster, Mini-FLOTAC and qPCR. PLoS Negl Trop Dis. 2020;14(7):e0008296. https://doi.org/10.1371/journal.pntd.0008296.
Levecke B, Behnke JM, Ajjampur SS, Albonico M, Ame SM, Charlier J, Geiger SM, Hoa NT, KamwaNgassam RI, Kotze AC, McCarthy JS, Montresor A, Periago MV, Roy S, TchuemTchuenté LA, Thach DT, Vercruysse J. A comparison of the sensitivity and fecal egg counts of the McMaster egg counting and Kato-Katz thick smear methods for soil-transmitted helminths. PLoS Negl Trop Dis. 2011;5(6):e1201. https://doi.org/10.1371/journal.pntd.0001201.
Cringoli G, Rinaldi L, Maurelli MP, Utzinger J. FLOTAC: new multivalent techniques for qualitative and quantitative copromicroscopic diagnosis of parasites in animals and humans. Nat Protoc. 2010;5(3):503–15. https://doi.org/10.1038/nprot.2009.235.
Cringoli G, Maurelli MP, Levecke B, Bosco A, Vercruysse J, Utzinger J, Rinaldi L. The Mini-FLOTAC technique for the diagnosis of helminth and protozoan infections in humans and animals. Nat Protoc. 2017;12(9):1723–32. https://doi.org/10.1038/nprot.2017.067.
Ayana M, Vlaminck J, Cools P, Ame S, Albonico M, Dana D, Keiser J, Manly H, Matoso LF, Mekonnen Z, Montresor A, Correa-Oliveira R, Rinaldi L, Sayasone S, Sowersby SJ, Tesfaye L, Vercruysse J, Mirams G, Levecke B. Modification and optimization of the FECPAKG2 protocol for the detection and quantification of soil-transmitted helminth eggs in human stool. PLoS Negl Trop Dis. 2018;12(10):e0006655. https://doi.org/10.1371/journal.pntd.0006655.
Cringoli G, Amadesi A, Maurelli MP, Celano B, Piantadosi G, Bosco A, Ciuca L, Cesarelli M, Bifulco P, Montresor A, Rinaldi L. The Kubic FLOTAC microscope (KFM): a new compact digital microscope for helminth egg counts. Parasitology. 2021;148(4):427–34. https://doi.org/10.1017/S003118202000219X.
Gualdieri L, Rinaldi L, Petrullo L, Morgoglione ME, Maurelli MP, Musella V, Piemonte M, Caravano L, Coppola MG, Cringoli G. Intestinal parasites in immigrants in the city of Naples (southern Italy). Acta Trop. 2011;117:196–201. https://doi.org/10.1016/j.actatropica.2010.12.003.
Maurelli MP, Alves LC, Aggarwal CS, Cociancic P, Levecke B, Cools P, Montresor A, Ianniello D, Gualdieri L, Cringoli G, Rinaldi L. Ascaris lumbricoides eggs or artefacts? A diagnostic conundrum Parasitology. 2021;148(13):1554–9. https://doi.org/10.1017/S0031182021001256.
Genchi M, Potters I, Kaminsky RG, Montresor A, Magnino S. Bench aids for the diagnosis of intestinal parasites, 2nd ed. World Health Organization. 2019;32 p.
Dendukuri N, Rahme E, Belisle P, Joseph L. Bayesian sample size determination for prevalence and diagnostic test studies in the absence of a gold standard test. Biometrics. 2004;60(2):388–97. https://doi.org/10.1111/j.0006-341X.2004.00183.x.
Thrusfield M. Veterinary epidemiology. 3rd ed. Oxford: Blackwell Science Ltd.; 2007.
Peruzzi S, Gorrini C, Piccolo G, Calderaro A, Dettori G, Chezzi C. Prevalence of intestinal parasites in the area of Parma during the year 2005. Acta Biomed. 2006;77(3):147–51.
Masucci L, Graffeo R, Bani S, Bugli F, Boccia S, Nicolotti N, Fiori B, Fadda G, Spanu T. Intestinal parasites isolated in a large teaching hospital, Italy, 1 May 2006 to 31 December 2008. Euro Surveill. 2011;16(24):19891. https://doi.org/10.2807/ese.16.24.19891-en.
Leméteil D, Gargala G, Razakandrainibe R, Ballet JJ, Favennec L, Costa D. Comparative evaluation of commercial concentration procedures for human intestinal parasite detection. Lab Med. 2019;50(3):243–8. https://doi.org/10.1093/labmed/lmy072. Lemeteil et al. discussed how differences in stool concentration methods may significantly affect the efficacy of parasite detection.
Al-Rifai RH, Loney T, Sheek-Hussein M, Zoughbor S, Ajab S, Olanda M, Al-Rasbi Z. Prevalence of, and factors associated with intestinal parasites in multinational expatriate workers in Al Ain City, United Arab Emirates: an occupational cross-sectional study. J Immigr Minor Health. 2020;22(2):359–74. https://doi.org/10.1007/s10903-019-00903-8.
Ceccarelli G, Sulekova LF, Milardi GL, Lopalco M, Vita S, Gabrielli S. Prevalence of intestinal parasitic infections among asylum seekers. Can Fam Physician. 2018;64(2):88.
Belli A, Coppola MG, Petrullo L, Lettieri G, Palumbo C, Dell’Isola C, Smeraglia R, Triassi M, Spada E, Amoroso P. The current spectrum and prevalence of intestinal parasitosis in Campania (region of southern Italy) and their relationship with migration from endemic countries. Int J Infect Dis. 2014;29:42–7. https://doi.org/10.1016/j.ijid.2014.04.021.
Müller F, Chandra S, Bogoch II, Rashid M, Redditt V. Intestinal parasites in stool testing among refugees at a primary care clinic in Toronto, Canada. BMC Infect Dis. 2022;22(1):249. https://doi.org/10.1186/s12879-022-07226-4.
Jeandron A, Rinaldi L, Abdyldaieva G, Usubalieva J, Steinmann P, Cringoli G, Utzinger J. Human infections with Dicrocoelium dendriticum in Kyrgyzstan: the tip of the iceberg? J Parasitol. 2011;97(6):1170–2. https://doi.org/10.1645/GE-2828.1.
Steinmann P, Cringoli G, Bruschi F, Matthys B, Lohourignon LK, Castagna B, Maurelli MP, Morgoglione ME, Utzinger J, Rinaldi L. FLOTAC for the diagnosis of Hymenolepis spp. infection: proof-of-concept and comparing diagnostic accuracy with other methods. Parasitol Res. 2012;111(2):749–54. https://doi.org/10.1007/s00436-012-2895-9.
Barda BD, Rinaldi L, Ianniello D, Zepherine H, Salvo F, Sadutshang T, Cringoli G, Clementi M, Albonico M. Mini-FLOTAC, an innovative direct diagnostic technique for intestinal parasitic infections: experience from the field. PLoS Negl Trop Dis. 2013;7(8):e2344. https://doi.org/10.1371/journal.pntd.0002344.
Barda B, Zepherine H, Rinaldi L, Cringoli G, Burioni R, Clementi M, Albonico M. Mini-FLOTAC and Kato-Katz: helminth eggs watching on the shore of Lake Victoria. Parasit Vectors. 2013;6(1):220. https://doi.org/10.1186/1756-3305-6-220.
Barda B, Cajal P, Villagran E, Cimino R, Juarez M, Krolewiecki A, Rinaldi L, Cringoli G, Burioni R, Albonico M. Mini-FLOTAC, Kato-Katz and McMaster: three methods, one goal; highlights from north Argentina. Parasit Vectors. 2014;7:271. https://doi.org/10.1186/1756-3305-7-271.
Knopp S, Salim N, Schindler T, KaragiannisVoules DA, Rothen J, Lweno O, Mohammed AS, Singo R, Benninghoff M, Nsojo AA, Genton B, Daubenberger C. Diagnostic accuracy of Kato-Katz, FLOTAC, Baermann, and PCR methods for the detection of light-intensity hookworm and Strongyloides stercoralis infections in Tanzania. Am J Trop Med Hyg. 2014;90(3):535–45. https://doi.org/10.4269/ajtmh.13-0268.
Hussein AH, Rashed SM, El-Hayawan IA, Aly NSM, AbouOuf EA, Ali AT. Intestinal parasite infections and accuracy of direct thin and thick smear, formol-ether sedimentation, centrifugal flotation, and mini-FLOTAC techniques among patients with gastrointestinal tract disorders from the greater Cairo Region. Egypt Am J Trop Med Hyg. 2017;96(3):589–94. https://doi.org/10.4269/ajtmh.16-0436.
Cociancic P, Rinaldi L, Zonta ML, Navone GT. Formalin-ethyl acetate concentration, FLOTAC Pellet and anal swab techniques for the diagnosis of intestinal parasites. Parasitol Res. 2018;117(11):3567–73. https://doi.org/10.1007/s00436-018-6054-9.
Allam AF, Farag HF, Lotfy W, Fawzy HH, Elhadad H, Shehab AY. Comparison among FLOTAC, Kato-Katz and formalin ether concentration techniques for diagnosis of intestinal parasitic infections in school children in an Egyptian rural setting. Parasitology. 2021;148(3):289–94. https://doi.org/10.1017/S0031182020001675.
Maurelli MP, Amadesi A, Sansone C, Marrone S, Gravina M, Bosco A, Celano B, Rinaldi L, Cringoli G. The Kubic Flotac microscope: a new tool for helminth eggs diagnosis in livestock and companion animals. 28th International Conference of the World Association for the Advancement of Veterinary Parasitology (WAAVP), 19–22 July 2021, Dublin, Ireland. pp. 362.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Human and Animal Rights and Informed Consent
This article does not contain any studies with human or animal subjects performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article is part of the Topical Collection on Tropical Medicine in the Mediterranean Region
Rights and permissions
Open Access This 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/.
About this article
Cite this article
Maurelli, M.P., Pepe, P., Gualdieri, L. et al. Improving Diagnosis of Intestinal Parasites Towards a Migrant-Friendly Health System. Curr Trop Med Rep 10, 17–25 (2023). https://doi.org/10.1007/s40475-022-00280-7
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40475-022-00280-7