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New record of parasitic infection among school children of Lower Dir Pakistan

Novo registro de infecção parasitária entre crianças em idade escolar de Lower Dir Paquistão

Abstract

Intestinal parasitic infections (IPIs) are a major cause of morbidity worldwide and have been described as an important public health problem. The present study aimed to determine the un usual parasitic infection and identification of risk factors among 4-12years old school age children residing in lower dir district, Pakistan from 2018- 2019. Of the 400 children studied in which the overall prevalence rate for intestinal parasitic infections was found to be 71.75%. Children infected with single parasite accounted for 67.94% and 32.05% were detected with poly-parasitism. Shistosoma japonicum (0.69%), Taxocara spp (0.69%) and cryptosporidium (0.69%), were identified in children living in studied areas. We conclude that there is a need for mass scale campaigns to create awareness regarding health and hygiene in children and the need for development of effective poverty control programmes.

Keywords:
new records; Cryptosporidium spp; Schistosoma spp; Toxocara spp; urban areas

Resumo

As infecções parasitárias intestinais (IPIs) são uma das principais causas de morbidade em todo o mundo e têm sido descritas como importante problema de saúde pública. O presente estudo teve como objetivo determinar a infecção parasitária incomum e a identificação de fatores de risco em crianças de 4 a 12 anos em idade escolar residentes no distrito de Lower Dir, Paquistão entre 2018-2019. Das 400 crianças estudadas em que a taxa de prevalência geral de parasitas intestinais infecções foi de 71,75%, as crianças infectadas com parasita único representaram 67,94%, e 32,05% foram detectadas com poliparasitismo. Shistosoma japonicum (0,69%), Taxocara spp (0,69%) e Cryptosporidium (0,69%) foram identificados em crianças residentes nas áreas estudadas. Concluímos que há uma necessidade de campanhas em grande escala para criar consciência sobre saúde e higiene em crianças e de desenvolvimento de programas eficazes de controle da pobreza.

Palavras-chave:
novos registros; Cryptosporidium spp; Schistosoma spp; Toxocara spp; áreas urbanas

1. Introduction

Intestinal protozoan and helminths are prevalent in those parts of the world where high temperature, poor cleanness, impure water, and imperfect and crowded accommodation exist.

Schistosome infection results from direct contact with fresh water contaminated by free-swimming larval forms of the parasite known as cercariae. Cercariae penetrate to human skin shed their tails, releasing schistosomula which enter to capillaries and lymphatic vessels then transfer to lungs. After several days, the male and female young worms migrate to the portal venous system, where they mature and unite. Adult worm meet then migrate to the veins of the intestines, in the case of Schistosoma mansoni and S.japonicum, or the bladder with S. haematobium. Eggs pass from the lumen of blood vessels into nearby tissues, and then pass to the intestinal or bladder mucosa and are shed with the faeces or urine. The life cycle is completed when the eggs hatch releasing miracidia which infect freshwater snails. After two asexual generations within the snail, mother followed by daughter sporocysts, cercariae are released (Gryseels et al., 2006GRYSEELS, B., POLMAN, K., CLERINX, J. and KESTENS, L., 2006. Human schistosomiasis. Lancet, vol. 368, no. 9541, pp. 1106-1118. http://dx.doi.org/10.1016/S0140-6736(06)69440-3. PMid:16997665.
http://dx.doi.org/10.1016/S0140-6736(06)...
).

Larval stages of Toxocara canis and Toxocara cati, common intestinal roundworms of dogs and cats, respectively, sometime infect humans. Toxocara eggs are passed unembryonated in the feces of these animals, become infectious in suitable environments, and can remain infective in the soil for many years .A condition known as covert toxocariasis may be the most common form of the disease and can include symptoms such as headache, cough, fever, and wheezing.

Cryptosporidium is a zoonotic intracellular spore forming protozoon parasite of the intestinal tract of humans as well as a number of domestic animals (Dozie et al., 2011DOZIE, I., NKEM, B. and CHUKWUOCHA, U., 2011. Cryptosporidiosis in Imo State, Nigeria. Journal of Rural and Tropical Public Health, vol. 10, pp. 106-110.). Potential sources of cryptosporidium are contaminated food and water, pet as well as farm animals.

Various studies have been published on intestinal parasites infecting different sectors of human population in the region as Khan et al. (2011KHAN, W., NOOR-UN-NISA and KHAN, A., 2011. An investigation of incidence of intestinal parasites in under and above 15 years age in farmers of Swat, Pakistan. Proceedings of Parasitology, vol. 52, pp. 43-53., 2012KHAN, W., NOOR-UN-NISA and KHAN, A., 2012. Endemicity of intestinal parasites with special reference to nematodes in individuals related to education (students, staff and teachers) in Swat, K.P.K, Pakistan. Pakistan Journal of Nematology, vol. 30, no. 1, pp. 77., 2014KHAN, W., NOOR-UN-NISA and KHAN, A., 2014. A case of Fasciola hepatica infection in Swat, Pakistan. Pakistan Journal of Zoology, vol. 46, no. 6, pp. 1789-1790., 2016KHAN, W., IMRAN and WAHAB, A., 2016. Intestinal obstruction by Ascaris lumbricoides in a 12 year old boy: a case report in Pakistan. Journal of Bacteriology & Parasitology, vol. 7, no. 1, pp. 262. http://dx.doi.org/10.4172/2155-9597.1000262.
http://dx.doi.org/10.4172/2155-9597.1000...
, 2017aKHAN, W., NOOR-UN-NISA and KHAN, A., 2017a. Prevalence and risk factors associated with intestinal parasitic infections among food handlers of Swat, Khyber Pakhtunkhwa, Pakistan. Journal of Food and Nutrition Research, vol. 5, no. 5, pp. 331-336. http://dx.doi.org/10.12691/jfnr-5-5-7.
http://dx.doi.org/10.12691/jfnr-5-5-7...
, bKHAN, W., NOOR-UN-NISA and KHAN, A., 2017b. Soil transmitted helminthiasis in different occupational groups in Swat, Khyber Pakhtunkhwa, Pakistan. Pakistan Journal of Pharmaceutical Sciences, vol. 30, no. 4, pp. 1345. PMid:29039336., 2018aKHAN, W., NOOR-UN-NISA and NAWAZ, M.A., 2018a. Prevalence of potentially important intestinal pathogenic protozoan parasitic infections in different occupational groups of Swat, Pakistan. Pakistan Journal of Zoology, vol. 50, no. 1, pp. 1-400. http://dx.doi.org/10.17582/journal.pjz/2018.50.1.123.129.
http://dx.doi.org/10.17582/journal.pjz/2...
, bKHAN, W., NOOR-UN-NISA. and NAWAZ, M.A., 2018b. Incidence of tapeworm infection in human population of Swat, Pakistan: an occupation based study. Pakistan Journal of Zoology, vol. 50, no. 2, pp. 639-639. http://dx.doi.org/10.17582/journal.pjz/2018.50.2.639.645.
http://dx.doi.org/10.17582/journal.pjz/2...
, 2019aKHAN, W., KHAN, J., KHAN, N., IQBAL, R., ULLAH, A., GHAFFAR, R., MEHMOOD, S.A., AHMAD, S., KHAN, S. and ULLAH, F., 2019a. Soil-transmitted helminth infections in school children of three districts of Malakand region, Khyber Pakhtunkhwa, Pakistan. Pakistan Journal of Pharmaceutical Sciences, vol. 32, no. 2, suppl., pp. 799-803. PMid:31103975., bKHAN, W., KHAN, N.I., BUKHARI, S.N.F. and BEGUM, N., 2019b. Prevalence of Intestinal Parasitic Infection among Drug Addicts in District Swat, Khyber Pakhtunkhwa, Pakistan. Iranian Journal of Parasitology, vol. 14, no. 2, pp. 359-361. PMid:31543928.), Arshad et al. (2019)ARSHAD, S., KHATOON, N., WARIND, J.A., KHAN, A., WAHEED, S. and KHAN, W., 2019. The prevalence of human intestinal protozoal and helminthic infection in Karachi. International Journal of Biology and Biotechnology, vol. 16, no. 2, pp. 319-323., Khan and Khan (2015)KHAN, W. and KHAN, A., 2015. Diversity of intestinal parasites in male and female students and workers of Education Department of Swat, Pakistan. Pakistan Journal of Zoology, vol. 47, no. 2, pp. 565-568., Noor un Nisa et al. (2011)NOOR-UN-NISA, KHAN, W. and KHAN, A., 2011. A Prevalence of intestinal parasites in male and female shepherds of Swat, Pakistan. International Journal of Biology and Biotechnology, vol. 8, no. 4, pp. 597-603., Khan et al. (2020)KHAN, W., IQBAL, M. and DAD, O., 2020. Have we forgotten the threat posed by fascioliasis? A potential threat to public health. Iranian Journal of Public Health, vol. 49, no. 4, pp. 814-815. http://dx.doi.org/10.18502/ijph.v49i4.3194. PMid:32548067.
http://dx.doi.org/10.18502/ijph.v49i4.31...
, Iqbal et al. (2021)IQBAL, M., KHAN, W., KHAN, F. and KHAN, I., 2021. Albendazole and mebendazole in the treatment of ancylostomiasis in school children between the ages of 6-15 in Swat, Pakistan. Journal of the Pakistan Medical Association, vol. 71, no. 8, pp. 2058-2060. http://dx.doi.org/10.47391/JPMA.1055. PMid:34418029.
http://dx.doi.org/10.47391/JPMA.1055...
, Khan et al. (2022a)KHAN, W., ARSHAD, S., KHATOON, N., KHAN, I., AHMAD, N., KAMAL, M., ULHASSAN, H., KHAN, N., HAQ, A.U., ILYAS, M., ULLAH, S., ULLAH, I., MAHMOUD, A.H. and MOHAMMED, O.B., 2022a. Food handlers: an important reservoir of protozoans and helminth parasites of public health importance. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, p. e238891. http://dx.doi.org/10.1590/1519-6984.238891. PMid:34037080.
http://dx.doi.org/10.1590/1519-6984.2388...
, Khan et al. (2022b)KHAN, W., PANHWAR, W.A., MEHMOOD, S.A., AHMED, S., AHMED, M.S., KHAN, N., KHAN, M.M., AKRAM, W., ULLAH, S. and IMRAN., 2022b. Pinworm infection in school children of four districts of Malakand region, Khyber Pakhtunkhwa, Pakistan. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, p. e238769. http://dx.doi.org/10.1590/1519-6984.238769. PMid:34037078.
http://dx.doi.org/10.1590/1519-6984.2387...
, Khan et al. (2022c)KHAN, W., RAHMAN, H., RAFIQ, N., KABIR, M., AHMED, M.S. and ESCALANTE, P.D.L.R., 2022c. Risk factors associated with intestinal pathogenic parasites in schoolchildren. Saudi Journal of Biological Sciences, vol. 29, no. 4, pp. 2782-2786. http://dx.doi.org/10.1016/j.sjbs.2021.12.055. PMid:35531160.
http://dx.doi.org/10.1016/j.sjbs.2021.12...
, Ulhaq et al. (2022)ULHAQ, Z., KHAN, W., KHAN, M.F., KABIR, M., UJJAN, A.A., ULLAH, W., MASOOD, Z., KHAN, S. and ESCALANTE, P.R., 2022. Prevalence of intestinal parasitic diseases in school children of rural areas of district Lower Dir, Pakistan. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, p. e243150. http://dx.doi.org/10.1590/1519-6984.243150. PMid:34644727.
http://dx.doi.org/10.1590/1519-6984.2431...
and Rahman et al. (2022)RAHMAN, H.U., KHAN, W., MEHMOOD, S.A., AHMED, S., YASMIN, S., AHMAD, W., HAQ, Z.U., SHAH, M.I.A., KHAN, R., AHMAD, U., KHAN, A.A. and ESCALANTE, P.R., 2022. Prevalence of cestodes infection among school children of urban parts of Lower Dir district, Pakistan. Brazilian Journal of Biology = Revista Brasileira de Biologia, vol. 82, p. e242205. http://dx.doi.org/10.1590/1519-6984.242205. PMid:34644726.
http://dx.doi.org/10.1590/1519-6984.2422...
.

2. Material and Method

2.1. Location and boundary

Lower Dir is the inferior part of the old District Dir of Malakand division. The area of District Dir is 5,284 km2 and located in Hindu Kush range. These days it forms two districts of Pakistan Upper Dir and Lower Dir (1,585 km. About all of it connects in the valley of the Panjkora which elevated in the Hindu Kush at Lat. 35.45 and joins the Swat River close to Chakdara, where the district is typically entered, at Lat. 34.40.

2.2. Questionnaire survey

The questionnaire was organized to elicited information on the demographic data (age and gender) as well as socioeconomic profile of the inhabitants .On 1st day of record of survey, all students present was informed about the disadvantages of parasites which lives in digestive system particularly small intestine and then provided with empty fecal bottle, label with student name, class and age. Each student was called to carry back the bottle with a fresh fecal sample after that morning. Fecal samples was collected as of every of students on 2nd day, these fecal bottles was preserve in 10% formalin, and was shifted to, Laboratory of Parasitology, where the samples was examined with the help of light microscope by using direct smear technique in Lugol’s solution and usual salt solution (WHO, 2013WORLD HEALTH ORGANIZATION – WHO, 2013. Assessing the efficacy of anthelminthic drugs against schistosomiasis and soil –transmitted helminthiases. Geneva: WHO.). Those students who are positive for parasitizes was educated to please make contact with their existing specialist /physician to their parents/guardian, brother or either other warden.

2.3. Laboratory examination

Then a stool sample was taken to microscopic examination, with the help of wet-mount techniques (salt solution and Lugol’s iodine solutions). The formol-ether concentration was also used for the verification of negative cases to be positive. About 3 g of stool was emulsified in 3 drops of salt solution (0.9%) or Lugol’ siodine solution (WHO, 2013WORLD HEALTH ORGANIZATION – WHO, 2013. Assessing the efficacy of anthelminthic drugs against schistosomiasis and soil –transmitted helminthiases. Geneva: WHO.). One drop of the suspension was placed on the centre of the slide via wooden applicator and after that a cover-slip was sited. The slide with sample suspension was study with help of the light microscope first under low 10× and then high 40× power objectives. Salines direct smear was also used for the detection of tapeworm eggs. At the end of direct stool examination, one gram 125 of every stool sample was emulsified in 10% formalin solution and formol-ether concentration technique was perform as describe in another place in order to raise the possibility of detecting parasites (WHO, 2013WORLD HEALTH ORGANIZATION – WHO, 2013. Assessing the efficacy of anthelminthic drugs against schistosomiasis and soil –transmitted helminthiases. Geneva: WHO.).

2.4. Parasite identification

Intestinal parasite was examined under the microscope and was recognized based on morphological characteristics of eggs, larvas and adult stages through valid and standard keys.

2.5. Statistical analysis

The statistical measurement was made according to the result we was use the software (SPSS, Graph paid and Minitab) wherever applicable. P value when less than 0.05 will be measured statistically important.

3. Result

The overall prevalence of intestinal parasite was 71.75% (n=287/400). Multiple parasitic infections were identified in 32.05% (n=92/400) individuals. The most common prevalent parasite is taxocara, cryptosporidium (0.69%), Cryptosporidium spp (0.69%), and shistomasoma iapanicum (0.34%). The prevalence of intestinal parasites was at least a single infection was 195 (67.94%). Mixed infection was observed in 92 (30.05%) among school children who had intestinal parasitic infection. Of these, proportion 53 (18.46%) are double, 27 (8.36%) triple and 12 (4.18%) quadruple infections were noted (Tables 1 to 4).

Table 1
Proportion of mono-parasitism and di -parasitism of intestinal parasitic infections in school children of Lower Dir, Pakistan.
Table 2
Frequency distribution of intestinal parasites identified from school children stools.
Table 3
Prevalence of intestinal tapeworms, nematodes, trematodes and protozoan parasitic infections among school children in lower dir KP, Pakistan (January 2018 to December 2020).
Table 4
Association of socio-demographic factor with intestinal parasitic infection among school children urban areas of Lower Dir KP, Pakistan.

4. Discussion

In current study the prevalence of Toxocara spp is 0.69% (287) which is negligible as compare to other study 10% conducted in Prague, rural areas, and shelters of the Czech Republic through faecal microscopy (Dubná et al., 2007DUBNÁ, S., LANGROVÁ, I., JANKOVSKÁ, I., VADLEJCH, J., PEKÁR, S., NÁPRAVNÍK, J. and FECHTNER, J., 2007. Contamination of soil with Toxocara eggs in urban (Prague) and rural areas in the Czech Republic. Veterinary Parasitology, vol. 144, no. 1-2, pp. 81-86. http://dx.doi.org/10.1016/j.vetpar.2006.09.023. PMid:17049747.
http://dx.doi.org/10.1016/j.vetpar.2006....
), 9.25% conducted in Lahore (Farooqi et al., 2014FAROOQI, M.T., MAQBOOL, A., ASHRAF, K., & IMRAN, M., 2014. Canine zoonosis; its potential and association of soil-borne Helminthes from public parks and its gastro-intestinal helminthes in Lahore, Pakistan.Science International, vol. 26, no. 2, pp. 771-774.). The prevalence rate was higher 1.3% in different parts of the world than the present study. Taxocara spp reported 2.5% in Spain (Causapé et al., 1996CAUSAPÉ, A.C., QUILEZ, J., SANCHEZ-ACEDO, C. and DEL CACHO, E., 1996. Prevalence of intestinal parasites, including Cryptosporidium parvum, in dogs in Zaragoza city, Spain. Veterinary Parasitology, vol. 67, no. 3-4, pp. 161-167. http://dx.doi.org/10.1016/S0304-4017(96)01033-3. PMid:9017864.
http://dx.doi.org/10.1016/S0304-4017(96)...
). The soil of the kennels and public parks of the city is heavily contaminated with faeces of stray dogs. It is suggested to reduce the stray dogs in public parks and interference measures are necessarily to reduce the risk of transmission of parasites from dogs to humans.Cryptosporidium spp are intestinal protozoan parasites play important role in medical and veterinary science that infect humans and animals all over the world including Pakistan (Kotloff et al., 2013KOTLOFF, K.L., NATARO, J.P., BLACKWELDER, W.C., NASRIN, D., FARAG, T.H., PANCHALINGAM, S., WU, Y., SOW, S.O., SUR, D., BREIMAN, R.F., FARUQUE, A.S., ZAIDI, A.K., SAHA, D., ALONSO, P.L., TAMBOURA, B., SANOGO, D., ONWUCHEKWA, U., MANNA, B., RAMAMURTHY, T., KANUNGO, S., OCHIENG, J.B., OMORE, R., OUNDO, J.O., HOSSAIN, A., DAS, S.K., AHMED, S., QURESHI, S., QUADRI, F., ADEGBOLA, R.A., ANTONIO, M., HOSSAIN, M.J., AKINSOLA, A., MANDOMANDO, I., NHAMPOSSA, T., ACÁCIO, S., BISWAS, K., O’REILLY, C.E., MINTZ, E.D., BERKELEY, L.Y., MUHSEN, K., SOMMERFELT, H., ROBINS-BROWNE, R.M. and LEVINE, M.M., 2013. Burden and aetiology of diarrhoeal disease in infants and young children in developing countries (the Global Enteric Multicenter Study, GEMS): a prospective, case-control study. Lancet, vol. 382, no. 9888, pp. 209-222. http://dx.doi.org/10.1016/S0140-6736(13)60844-2. PMid:23680352.
http://dx.doi.org/10.1016/S0140-6736(13)...
). In humans there are about 20 Cryptosporidium species were observed, in which C. hominis and C. parvum are the most common species (Ryan and Xiao, 2014RYAN, U. and XIAO, L., 2014. Taxonomy and molecular taxonomy. In: S. CACCIÒ and G. WIDMER, eds. Cryptosporidium: parasite and disease. Vienna: Springer, pp. 3-41. http://dx.doi.org/10.1007/978-3-7091-1562-6_1.
http://dx.doi.org/10.1007/978-3-7091-156...
). It has major public health problems because infection can result from exposure to low doses of Cryptosporidium oocysts (Gatei et al., 2006GATEI, W., WAMAE, C. N., MBAE, C., WARURU, A., MULINGE, E., WAITHERA, T., GATIKA, S.M., KAMWATI, S.K., REVATHI, G. and HART, C. A., 2006. Cryptosporidiosis: prevalence, genotype analysis, and symptoms associated with infections in children in Kenya.American Journal of Tropical Medicine and Hygiene, 75(1), 78-82.). Each of them have different sources of infection, transmission routes and pathogencity (Cama et al., 2007CAMA, V.A., ROSS, J.M., CRAWFORD, S., KAWAI, V., CHAVEZ-VALDEZ, R., VARGAS, D., VIVAR, A., TICONA, E., NAVINCOPA, M., WILLIAMSON, J., ORTEGA, Y., GILMAN, R.H., BERN, C. and XIAO, L., 2007. Differences in clinical manifestations among Cryptosporidium species and subtypes in HIV-infected persons. The Journal of Infectious Diseases, vol. 196, no. 5, pp. 684-691. http://dx.doi.org/10.1086/519842. PMid:17674309.
http://dx.doi.org/10.1086/519842...
). In healthy individuals, cryptosporidium infection causes a self-limiting diarrheal disease (Hunter et al., 2004HUNTER, P.R., HUGHES, S., WOODHOUSE, S., NICHOLAS, R., SYED, Q., CHALMERS, R.M., VERLANDER, N.Q. and GOODACRE, J., 2004. Health sequelae of human cryptosporidiosis in immunocompetent patients. Clinical Infectious Diseases, vol. 39, no. 4, pp. 504-510. http://dx.doi.org/10.1086/422649. PMid:15356813.
http://dx.doi.org/10.1086/422649...
). Cryptosporidium oocysts were identified in 2 school children (0.69%), but there is no data recorded which is lower than the rate of infection in current 0.69% data . In the present study the presence of C. parvum in young children (aged 5-12years) was addressed in geographic regions of District lower Dir by examining both asymptomatic and symptomatic school children. This prevalence rate is lower than the previous studies 83.8%, reported from Peshawar (Mumtaz et al., 2010MUMTAZ, S., AHMED, J. and ALI, L., 2010. Frequency of cryptosporidium infection in children under five years of age having diarrhea in the North West of Pakistan. African Journal of Biotechnology, vol. 9, no. 8, pp. 1230-1235. http://dx.doi.org/10.5897/AJB09.1278.
http://dx.doi.org/10.5897/AJB09.1278...
) 15.99% in Lahore (Khan et al., 2017KHAN, W., MUMTAZ, G., BIBI, S. and AFZAL, S., 2017. Parasitic contamination of fresh vegetables sold at upper and lower Dir Districts, Khyber Pakhtunkhwa, Pakistan. Pakistan Journal of Zoology, vol. 49, no. 3, pp. 1115-1118. http://dx.doi.org/10.17582/journal.pjz/2017.49.3.sc3.
http://dx.doi.org/10.17582/journal.pjz/2...
) 14.66% in Peshawar (Akbar et al., 2015AKBAR, N., AYAZ, S., KHAN, M. A., RAHMAN, S., KHAN, S., KHAN, S.N., WAQAR, M., RAZA, F., SHAGUFTA, B.I., ALI, S., SAEED, S., ZAREEN, S., ALAM, M.S., KHAN, I., & KHAN, S.A., 2015. Molecular detection of Cryptosporidium parvum in different water sources of District Peshawar, Pakistan.Advances in Biological Research,9(5), pp. 344-349.). Schistosoma japonicum (Oriental blood Fluke. The parasitic worms have a complex developmental cycle that involves infection of freshwater intermediate molluscan hosts and the blood stream of mammals. Schistosoma japonicum is the rare prevalent i.e 0.34% (287) in urban region District Lower Dir which is lower than other studies conducted in different areas of Pakistan.School children infected with the ingestion of eggs, cysts or oocysts with help of infected food or water, hands, inhalation of dirty air, and penetration of larvae to the skin (Lee et al., 2010LEE, A.C., MONTGOMERY, S.P., THEIS, J.H., BLAGBURN, B.L. and EBERHARD, M.L., 2010. Public health issues concerning the widespread distribution of canine heartworm disease. Trends in Parasitology, vol. 26, no. 4, pp. 168-173. http://dx.doi.org/10.1016/j.pt.2010.01.003. PMid:20181530.
http://dx.doi.org/10.1016/j.pt.2010.01.0...
).

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Publication Dates

  • Publication in this collection
    29 Aug 2022
  • Date of issue
    2022

History

  • Received
    20 Oct 2020
  • Accepted
    01 Mar 2021
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