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Evidence that ectoparasites influence the hematological parameters of the host: a systematic review

Published online by Cambridge University Press:  02 August 2023

Bárbara Cristina Félix Nogueira
Affiliation:
Department of Veterinary Medicine, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
Elaine da Silva Soares
Affiliation:
Department of Veterinary Medicine, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
Andrés Mauricio Ortega Orozco
Affiliation:
Department of Veterinary Medicine, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
Leandro Abreu da Fonseca
Affiliation:
Department of Veterinary Medicine, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
Artur Kanadani Campos*
Affiliation:
Department of Veterinary Medicine, Federal University of Viçosa, Viçosa, Minas Gerais, Brazil
*
Corresponding author: Artur Kanadani Campos; Email: artur.kanadani@ufv.br

Abstract

Ectoparasites are important to the one health concept because their parasitism can result in the transmission of pathogens, allergic reactions, the release of toxins, morbidity, and even death of the host. Ectoparasites can affect host physiology, as reflected in immune defenses and body condition as well as hematological and biochemical parameters. Thus, evidence that ectoparasites influence host hematological parameters was systematically reviewed, and the methodological quality of these studies was analyzed. The Preferred Reporting Items for Systematic Reviews and Meta-Analysis guidelines were followed, and the studies included were limited to those that evaluated changes in hematological tests in ectoparasite-infested and non-infested animals, and bias and methodological quality were evaluated using the Animal Research: Reporting of In Vivo Experiments guideline. Thirty-four studies were selected and information about the host, ectoparasite infestation, blood collection, and analysis was collected and compared whenever possible. In this review, the presence of ectoparasites influenced both the red series and the white series of hematological parameters. Among the main parameters analyzed, hematocrit, red blood cells, hemoglobin, and lymphocytes showed reductions, probably due to ectoparasite blood-feeding, while including eosinophils, neutrophils, and basophils increased in infested animals due to the host immune response. However, methodologic improvements are needed to reduce the risk of bias, enhance the reproducibility of such studies, and ensure results aligned with the mechanisms that act in the ectoparasite-host relationship.

Type
Systematic Review
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

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References

Ajith, Y, Dimri, U, Madhesh, E, Gopalakrishnan, A, Verma, MR, Samad, HA, Reena, KK, Chaudhary, AK, Devi, G and Bosco, J (2020) Influence of weather patterns and air quality on ecological population dynamics of ectoparasites in goats. International Journal of Biometeorology 64, 17311742.CrossRefGoogle ScholarPubMed
Araujo, FR, Silva, MP, Lopes, AA, Ribeiro, OC, Pires, PP, Carvalho, CM, Balbuena, CB, Villas, AA and Ramos, JK (1998) Severe cat flea infestation of dairy calves in Brazil. Veterinary Parasitology 80, 8386.CrossRefGoogle ScholarPubMed
Barbosa, CG, Sanavria, A and Barbosa, MDPRC (2003) Alterações hematológicas em bovinos infestados experimentalmente com larvas de Dermatobia hominis (Diptera: Cuterebridae). Brazilian Journal of Veterinary Parasitology 12, 6167.Google Scholar
Batista, IFC, Ramos, OHP, Ventura, JS, Junquiera-de-Azevedo, ILM, Ho, PL and Chudzinski-Tavassi, AM (2010) A new factor Xa inhibitor from Amblyomma cajennense with a unique domain composition. Archives of Biochemistry and Biophysics 493, 151156.CrossRefGoogle ScholarPubMed
Birben, E, Sahiner, UM, Sackesen, C, Erzurum, S and Kalayci, O (2012) Oxidative stress and antioxidant defense. World Allergy Organization Journal 5, 919.CrossRefGoogle ScholarPubMed
Bray, GA, Kim, KK and Wilding, JPH (2017) Obesity: a chronic relapsing progressive disease process. A position statement of the World Obesity Federation. Obesity Reviews 18, 715723.CrossRefGoogle ScholarPubMed
Brommer, JE, Pitala, N, Siitari, H, Kluen, E and Gustafsson, L (2011) Body size and immune defense of Nestling Blue Tits (Cyanistes caeruleus) in response to manipulation of ectoparasites and food supply. The Auk 128, 556563.CrossRefGoogle Scholar
Carleton, RE (2008) Ectoparasites affect hemoglobin and percentages of immature erythrocytes but not hematocrit in nestling Eastern Bluebirds. The Wilson Journal of Ornithology 120, 565568.CrossRefGoogle Scholar
Carlson, JC (2017) Reactions to arthropod bites. In Freeman, T and Tracy, J (eds), Stinging Insect Allergy. Cham: Springer International Publishing, pp. 231246.CrossRefGoogle Scholar
Carvalho-Costa, TM, Mendes, MT, Silva, MV, Costa, TA, Tiburcio, MGS, Anhê, ACBM, Rodrigues, V Jr. and Oliveira, CJF (2015) Immunosuppressive effects of Amblyomma cajennense tick saliva on murine bone marrow-derived dendritic cells. Parasites & Vectors 8, 22.CrossRefGoogle ScholarPubMed
Cavalcante, RR, Pereira, MH and Gontijo, NF (2003) Anti-complement activity in the saliva of phlebotomine sand flies and other haematophagous insects. Parasitology 127, 8793.CrossRefGoogle ScholarPubMed
Chagas, WN, Moraes, APR, Lopes, CWG and Bittencourt, AJ (2011) Histopathologic and hemathologic changes in experimentally infested rabbits by Stomoxys calcitrans. Revista Brasileira de Medicina Veterinária 33, 165170.Google Scholar
Cray, C (2012) Acute phase proteins in animals. Progress in Molecular Biology and Translational Science 105, 113150.CrossRefGoogle ScholarPubMed
Daniel, TL and Kingsolver, JG (1983) Feeding strategy and the mechanics of blood sucking in insects. Journal of Theoretical Biology 105, 661677.CrossRefGoogle ScholarPubMed
Davis, DP and Williams, RE (1986) Influence of hog lice, Haematopinus suis, on blood components, behavior, weight gain and feed efficiency of pigs. Veterinary Parasitology 22, 307314.CrossRefGoogle ScholarPubMed
Dawson, L, Pike, AW, Houlihan, DF and McVicar, AH (1999) Changes in physiological parameters and feeding behaviour of Atlantic salmon Salmo salar infected with sea lice Lepeophtheirus salmonis. Diseases of Aquatic Organisms 35, 8999.CrossRefGoogle ScholarPubMed
De Bellocq, JG, Krasnov, BR, Khokhlova, IS, Ghazaryan, L and Pinshow, B (2006) Immunocompetence and flea parasitism of a desert rodent. Functional Ecology 20, 637646.CrossRefGoogle Scholar
De Coster, G, De Neve, L, Martín-Gálvez, D, Therry, L and Lens, L (2010) Variation in innate immunity in relation to ectoparasite load, age and season: a field experiment in great tits (Parus major). Journal of Experimental Biology 213, 30123018.CrossRefGoogle ScholarPubMed
de Oliveira, JCP, Reckziegel, GH, Ramos, CAN, Giannelli, A, Alves, LC, Carvalho, GA and Ramos, RAN (2020) Detection of Rickettsia felis in ectoparasites collected from domestic animals. Experimental & Applied Acarology 81, 255264.CrossRefGoogle ScholarPubMed
Devevey, G, Nirculita-Hirzel, H, Biollaz, F, Yvon, C, Chapuisat, M and Christe, P (2008) Developmental, metabolic and immunological costs of flea infestation in the common vole. Functional Ecology 22, 10911098.CrossRefGoogle Scholar
Dhumeaux, MP, Snead, ECR, Epp, TY, Taylor, SM, Carr, AP, Dickinson, RM and Leis, ML (2012) Effects of a standardized anesthetic protocol on hematologic variables in healthy cats. Journal of Feline Medicine and Surgery 14, 701705.CrossRefGoogle ScholarPubMed
Dusbábek, F, Uhliř, J and Borský, I (1994) Age-dependent immune response of chickens to feeding by Argas persicus larvae. Veterinary Parasitology 51, 307319.CrossRefGoogle ScholarPubMed
El Hadi, HM, El Bashir, S and El Jack, MH (1977) Haematological changes in fowls infested with black flies (Simulium griseicolle). Research in Veterinary Science 22, 361365.CrossRefGoogle ScholarPubMed
Elston, DM (2004) Prevention of arthropod-related disease. Journal of the American Academy of Dermatology 51, 947954.CrossRefGoogle ScholarPubMed
Esteves, E, Maruyama, SR, Kawahara, R, Fujita, A, Martins, LA, Righi, AA, Costa, FB, Palmisano, G, Labruna, MB, Sá-Nunes, A, Ribeiro, JMC and Fogaça, AC (2017) Analysis of the salivary gland transcriptome of unfed and partially fed Amblyomma sculptum ticks and descriptive proteome of the saliva. Frontiers in Cellular and Infection Microbiology 7, 476.CrossRefGoogle ScholarPubMed
Festing, S and Wilkinson, R (2007) The ethics of animal research. EMBO Reports 8, 526530.CrossRefGoogle ScholarPubMed
Fuller, C (2020) Dermatoses caused by arthropods. In Morrone, A, Hay, R and Naafs, B (eds), Skin Disorders in Migrants. Cham: Springer International Publishing, pp. 5557.CrossRefGoogle Scholar
Galay, RL, Umemiya-Shirafuji, R, Bacolod, ET, Maeda, H, Kusakisako, K, Koyama, J, Tsuji, N, Mochizuki, M, Fujisaki, K and Tanaka, T (2014) Two kinds of ferritin protect ixodid ticks from iron overload and consequent oxidative stress. PLoS One 9, e90661.CrossRefGoogle ScholarPubMed
Galvão, TF and Pereira, MG (2014) Revisões sistemáticas da literatura: passos para sua elaboração. Epidemiologia e serviços de saúde 23, 183184.CrossRefGoogle Scholar
Gauthier-Clerc, M, Mangin, S, Le Bohec, C, Gendner, J-P and Le Maho, Y (2003) Comparison of behaviour, body mass, haematocrit level, site fidelity and survival between infested and non-infested king penguin Aptenodytes patagonicus by ticks Ixodes uriae. Polar Biology 26, 379382.CrossRefGoogle Scholar
Gokçe, G and Kiziltepe, Ş (2013) Alterations in haematological and biochemical parameters in Morkaraman sheep with natural Psoroptes ovis infestation. Kafkas Universitesi Veteriner Fakultesi Dergisi 19, 975978.Google Scholar
Gonçalves, JM, Pereira, MCT, Evangelista, LG and Leite, ACR (2007) Expression of circulating leucocytes before, during and after myiasis by Dermatobia hominis in experimentally infected rats. Revista do Instituto de Medicina Tropical de São Paulo 49, 289292.CrossRefGoogle ScholarPubMed
Grab, KM, Hiller, BJ, Hurlbert, JH, Ingram, ME, Parker, AB, Pokutnaya, DY and Knutie, SA (2019) Host tolerance and resistance to parasitic nest flies differs between two wild bird species. Ecology and Evolution 9, 1214412155.CrossRefGoogle ScholarPubMed
Grisi, L, Leite, RC, Martins, JRS, Barros, ATM, Andreotti, R, Cançado, PHD, Léon, AAP, Pereira, JB and Villela, HS (2014) Reassessment of the potential economic impact of cattle parasites in Brazil. Revista Brasileira de Parasitologia Veterinária 23, 150156.CrossRefGoogle ScholarPubMed
Guo, S and DiPietro, LA (2010) Critical review in oral biology & medicine: factors affecting wound healing. Journal of Dental Research 89, 219229.CrossRefGoogle Scholar
Guyton, AC and Hall, JE (2006) Tratado de fisiologia médica. Rio de Janeiro: Elsevier Brasil.Google Scholar
Harder, L and Boshkov, L (2010) The optimal hematocrit. Critical Care Clinics 26, 335354.CrossRefGoogle ScholarPubMed
Hernandez, EP, Kusakisako, K, Talactac, MR, Galay, RL, Hatta, T, Matsuo, T, Fujisaki, K, Tsuji, N and Tanaka, T (2018) Characterization and expression analysis of a newly identified glutathione S-transferase of the hard tick Haemaphysalis longicornis during blood-feeding. Parasites & Vectors 11, 91.CrossRefGoogle ScholarPubMed
Hernandez, EP, Talactac, MR, Fujisaki, K and Tanaka, T (2019) The case for oxidative stress molecule involvement in the tick-pathogen interactions -an omics approach. Developmental and Comparative Immunology 100, 103409.CrossRefGoogle ScholarPubMed
Heylen, DJA and Matthysen, E (2008) Effect of tick parasitism on the health status of a passerine bird. Functional Ecology 22, 10991107.CrossRefGoogle Scholar
Hiley, PJ, Byford, HL, Hallford, DM, Campbell, JW and Pehez-Egula, E (1995) Physiological responses of beef cattle to gulf coast tick (Acari: Ixodidae) infestations. Journal of Economic Entomology 88, 320325.CrossRefGoogle Scholar
Hurtado, OJB and Giraldo-Ríos, C (2019) Economic and health impact of the ticks in production animals. In Abubakar, M and Perera, PK (eds), Ticks and Tick-Borne Pathogens. IntechOpen. doi: 10.5772/intechopen.81167Google Scholar
Jakob, E, Sweten, T, Bennett, W and Jones, SRM (2013) Development of the salmon louse Lepeophtheirus salmonis and its effects on juvenile sockeye salmon Oncorhynchus nerka. Diseases of Aquatic Organisms 106, 217227.CrossRefGoogle ScholarPubMed
Johns, J and Heller, M (2021) Hematologic conditions of small ruminants. Veterinary Clinics of North America: Food Animal Practice 37, 183197.Google ScholarPubMed
Jones, D (1998) The neglected saliva: medically important toxins in the saliva of human lice. Parasitology 116, S73S81.CrossRefGoogle ScholarPubMed
Jones, CM and Grutter, AS (2005) Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. Journal of Fish Biology 66, 860864.CrossRefGoogle Scholar
Jones, CJ and Lloyd, JE (1987) Hypersensitivity reactions and hematologic changes in sheep exposed to mosquito (Diptera: Culicidae) feeding. Journal of Medical Entomology 24, 7176.CrossRefGoogle ScholarPubMed
Jonsson, N, Mayer, DG, Matschoss, AL, Green, PE and Ansell, J (1998) Production effects of cattle tick (Boophilus microplus) infestation of high yielding dairy cows. Veterinary Parasitology 78, 6577.CrossRefGoogle ScholarPubMed
Kelada, SNP, Aylor, DL, Peck, BCE, Ryan, JF, Tavarez, U, Buus, RJ, Miller, DR, Chesler, EJ, Threadgill, DW, Churchill, GA, Vilhena, FP-M and Collins, FS (2012) Genetic analysis of hematological parameters in incipient lines of the collaborative cross. Genes|Genomes|Genetics 2, 157165.CrossRefGoogle ScholarPubMed
Kilkenny, C, Browne, WJ, Cuthill, IC, Emerson, M and Altman, DG (2010) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLOS Biology 8, 6.CrossRefGoogle ScholarPubMed
Klein, SL and Flanagan, KL (2016) Sex differences in immune responses. Nature Reviews Immunology 16, 626638.CrossRefGoogle ScholarPubMed
Kotál, J, Langhansová, H, Lieskovská, J, Andersen, JF, Francischetti, IMB, Chavakis, T, Kopecký, J, Pedra, JHF, Kotsyfakis, M and Chmelar, J (2015) Modulation of host immunity by tick saliva. Journal of Proteomics 128, 5868.CrossRefGoogle ScholarPubMed
Latif, AA, Punyua, DK, Capstick, PB, Nokoe, S, Walker, AR and Fletcher, JD (1991) Histopathology of attachment sites of Amblyomma variegatum and Rhipicephalus appendiculatus on Zebu cattle of varying resistance to ticks. Veterinary Parasitology 38, 205213.CrossRefGoogle ScholarPubMed
Little, SE, Davidson, WR, Rakich, PM, Nixon, TL, Bounous, DI and Nettles, VF (1998) Responses of red foxes to first and second infection with Sarcoptes scabiei. Journal of Wildlife Diseases 34, 600611.CrossRefGoogle ScholarPubMed
Louly, CCB, Soares, SF, Silveira, DN, Neto, OJS, Silva, AC and Borges, LMF (2009) Differences in the susceptibility of two breeds of dogs, English cocker spaniel and beagle, to Rhipicephalus sanguineus (Acari: Ixodidae). International Journal of Acarology 35, 2532.CrossRefGoogle Scholar
Mahajan, S, Panigrahi, PN, Dey, S, Dan, A, Kumar, A, Mahedran, K and Maurya, PS (2017) Circulating oxidative stress caused by Psoroptes natalensis infestation in Indian water buffaloes. Journal of Parasitic Diseases 41, 689692.CrossRefGoogle ScholarPubMed
Mays, AR, Brown, MA, von Tunglen, DL and Rosenkrans, CF Jr. (2014) Milk production traits of beef cows as affected by horn fly count and sire breed type1. Journal of Animal Science 92, 12081212.CrossRefGoogle Scholar
McKilligan, NG (1996) Field experiments on the effect of ticks on breeding success and chick health of cattle egrets. Austral Ecology 21, 442449.CrossRefGoogle Scholar
Moher, D, Liberati, A, Tetzlaff, J and Altman, DG (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Medicine 6, e1000097.CrossRefGoogle ScholarPubMed
Moonarmart, W, Tansakul, M, Kiewsiri, C, Watanaboonchai, R, Somrith, W, Yinharnmingmongkol, C and Tunhikorn, M (2018) Haematological response in the treatment of naturally acquired ectoparasite infestations in rabbits. World Rabbit Science 26, 313320.CrossRefGoogle Scholar
Moreira, HNS, Barcelos, RM, Vidigal, PMP, Klein, RC, Montadon, CE, Maciel, TEF, Carrizo, JFA, Lima, PHC, Soares, AC, Martins, MM and Magra, C (2017) A deep insight into the whole transcriptome of midguts, ovaries and salivary glands of the Amblyomma sculptum tick. Parasitology International 66, 6473.CrossRefGoogle ScholarPubMed
O'Brien, DJ, Robinson, AB, Gray, JS and O'Reilly, PF (1995) Haematology and blood biochemistry during the course of psoroptic scabies in sheep. Veterinary Research Communications 19, 3948.CrossRefGoogle ScholarPubMed
O'Brien, EL, Morrison, BL and Johnson, LS (2001) Assessing the effects of haematophagous ectoparasites on the health of nestling birds: haematocrit vs haemoglobin levels in House Wrens parasitized by blow fly larvae. Journal of Avian Biology 32, 7376.CrossRefGoogle Scholar
O'Connor, AM and Sargeant, JM (2014) An introduction to systematic reviews in animal health, animal welfare, and food safety. Animal Health Research Reviews 15, 313.CrossRefGoogle ScholarPubMed
O'Kelly, JC and Seifert, GW (1970) The effects of tick (Boophilus microplus) infestations on the blood composition of Shorthorn x Hereford cattle on high and low planes of nutrition. Australian Journal of Biological Science 23, 681690.CrossRefGoogle Scholar
Owen, JP, Delany, ME, Cardona, CJ, Bickford, AA and Mullens, BA (2009) Host inflammatory response governs fitness in an avian ectoparasite, the northern fowl mite (Ornithonyssus sylviarum). International Journal for Parasitology 39, 789799.CrossRefGoogle Scholar
Peña-Rehbein, P, Ruiz, K, Ortloff, A, Pizarro, MI and Navarrete, C (2013) Hematological changes in Eleginops maclovinus during an experimental Caligus rogercresseyi infestation. Revista Brasileira de Parasitologia Veterinária 22, 402406.CrossRefGoogle ScholarPubMed
Pérez de León, AA, Mitchell, RD and Watson, DW (2020) Ectoparasites of cattle. Veterinary Clinics of North America: Food Animal Practice 36, 173185.Google ScholarPubMed
Pfäffle, M, Petney, T, Elgas, M, Skuballa, J and Taraschewski, H (2009) Tick-induced blood loss leads to regenerative anaemia in the European hedgehog (Erinaceus europaeus). Parasitology 136, 443.CrossRefGoogle ScholarPubMed
Piagnerelli, M, Boudjeltia, KZ, Vanhaeverbeek, M and Vincent, J-L (2003) Red blood cell rheology in sepsis. Intensive Care Medicine 29, 10521061.CrossRefGoogle ScholarPubMed
Piper, EK, Jonsson, NN, Gondro, C, Vance, ME, Lew-Tabor, A and Jackson, LA (2017) Peripheral cellular and humoral responses to infestation with the cattle tick Rhipicephalus microplus in Santa Gertrudis cattle. Parasite Immunology 39, e12402.CrossRefGoogle ScholarPubMed
Pitala, N, Siitari, H, Gustafsson, L and Broomer, J (2009) Ectoparasites help to maintain variation in cell-mediated immunity in the Blue Tit–hen flea system. Evolutionary Ecology Research 11, 7994.Google Scholar
Pollock, NB, Vredevoe, LK and Taylor, EN (2012) How do host sex and reproductive state affect host preference and feeding duration of ticks? Parasitology Research 111, 897907.CrossRefGoogle ScholarPubMed
Potti, J, Moreno, J, Merino, S, Frías, O and Rodríguez, R (1999) Environmental and genetic variation in the haematocrit of fledgling pied flycatchers Ficedula hypoleuca. Oecologia 120, 18.CrossRefGoogle ScholarPubMed
Pritchard, MJ and Hwang, SW (2009) Severe anemia from bedbugs. Canadian Medical Association Journal 181, 287288.CrossRefGoogle ScholarPubMed
Pryor, LJE and Casto, JM (2015) Blood-feeding ectoparasites as developmental stressors: does corticosterone mediate effects of mite infestation on nestling growth, immunity and energy availability? Journal of Experimental Zoology Part A: Ecological Genetics and Physiology 323, 466477.CrossRefGoogle ScholarPubMed
Pryor, LJE and Casto, JM (2017) Ectoparasites as developmental stressors: effects on somatic and physiological development. Journal of Experimental Zoology Part A: Ecological and Integrative Physiology 327, 311321.CrossRefGoogle ScholarPubMed
Rashid, M, Rashid, MI, Akbar, H, Ahmad, L, Hassan, MA, Ashraf, K, Saeed, K and Gharbi, M (2019) A systematic review on modelling approaches for economic losses studies caused by parasites and their associated diseases in cattle. Parasitology 146, 129141.CrossRefGoogle ScholarPubMed
Ravikumar, S (2015) Image segmentation and classification of white blood cells with the extreme learning machine and the fast relevance vector machine. Artificial Cells, Nanomedicine, and Biotechnology 44, 15.CrossRefGoogle ScholarPubMed
Rechav, Y and Hay, L (1992) The effects of nutritional status of rabbits and sheep on their resistance to the ticks Rhipicephalus evertsi evertsi and R. appendiculatus. Experimental and Applied Acarology 15, 171179.CrossRefGoogle Scholar
Rechav, Y, Dauth, J and Els, D (1990) Resistance of Brahman and Simmentaler cattle to southern African ticks. Onderstepoort Journal of Veterinary Research 57, 712.Google ScholarPubMed
Reck, J Jr., Berger, M, Terra, RMS, Marks, FS, Vaz, IS Jr., Guimarães, JA and Termignoni, C (2009) Systemic alterations of bovine hemostasis due to Rhipicephalus (Boophilus) microplus infestation. Research in Veterinary Science 86, 5662.CrossRefGoogle ScholarPubMed
Rishniw, M and Pion, PD (2016) Evaluation of performance of veterinary in-clinic hematology analyzers. Veterinary Clinical Pathology 45, 604614.CrossRefGoogle ScholarPubMed
Rizzo, C, Ronca, R, Fiorentino, G, Verra, F, Mangano, V, Poinsignon, A, Sirima, SB, Nebie, I, Lombardo, F, Remoue, F, Coluzzi, M, Petrarca, V and Arca, DB (2011) Humoral response to the Anopheles gambiae salivary protein gSG6: a serological indicator of exposure to Afrotropical Malaria Vectors. PLoS One 6, e17980.CrossRefGoogle Scholar
Rothwell, TLW, Pope, SE, Rajczyk, ZK and Collins, GH (1991) Haematological and pathological responses to experimental Trixacarus caviae infection in guinea pigs. Journal of Comparative Pathology 104, 179185.CrossRefGoogle ScholarPubMed
Rovirosa-Hernández, MJ, García-Orduña, F, Canales-Espinosa, D, Hermida-Lagunes, J and Torres-Pelayo, VR (2011) Blood parameters are little affected by time of sampling after the application of ketamine in black howler monkeys (Alouatta pigra). Journal of Medical Primatology 40, 294299.CrossRefGoogle ScholarPubMed
Ruane, NM, Nolan, DT, Rotllant, J, Costelloe, J and Wendelaar Bonga, SE (2000) Experimental exposure of rainbow trout Oncorhynchus mykiss (Walbaum) to the infective stages of the sea louse Lepeophtheirus salmonis (Krøyer) influences the physiological response to an acute stressor. Fish & Shellfish Immunology 10, 451463.CrossRefGoogle Scholar
Ruiz, JD, Gómez, V, Cadavid, AF and Baéz, P (2010) Evaluación de los efectos de dos protocolos anestésicos aplicados durante ovariohisterectomía sobre hemograma, creatinina, BUN, ALT y FA en hembras caninas. Revista CES Medicina Veterinaria y Zootecnia 5, 1023.Google Scholar
Sá Junior, PL, Câmara, DAD, Sciani, JM, Porcacchia, AS, Fonseca, PMM, Mendonça, RZ, Elifio-Esposito, S and Simons, SM (2019) Antiproliferative and antiangiogenic effect of Amblyomma sculptum (Acari: Ixodidae) crude saliva in endothelial cells in vitro. Biomedicine & Pharmacotherapy 110, 353361.CrossRefGoogle ScholarPubMed
Saleh, MA, Mahran, OM and Al-Salahy, MB (2011) Circulating oxidative stress status in dromedary camels infested with sarcoptic mange. Veterinary Research Communications 35, 3445.CrossRefGoogle ScholarPubMed
Santoro, P (2018) Manual methods vs automated hematology analyzers in veterinary hematology. Veterinary Clinical Pathology 47, 178178.CrossRefGoogle ScholarPubMed
Schleger, AV, Lincoln, DT, McKenna, RV, Kemp, DH and Roberts, JA (1976) Boophilus microplus: cellular responses to larval attachment and their relationship to host resistance. Australian Journal of Biological Science 29, 499512.CrossRefGoogle ScholarPubMed
Schoeler, GB and Wikel, SK (2001) Modulation of host immunity by haematophagous arthropods. Annals of Tropical Medicine and Parasitology 95, 755771.CrossRefGoogle ScholarPubMed
Shang, X, Wang, D, Miao, X, Wang, X, Li, J, Yang, Z and Pan, H (2014) The oxidative status and inflammatory level of the peripheral blood of rabbits infested with Psoroptes cuniculi. Parasites & Vectors 7, 124.CrossRefGoogle ScholarPubMed
Shieh, J-N and Rossignol, PA (1992) Opposite influences of host anaemia on blood feeding rate and fecundity of mosquitoes. Parasitology 105, 159163.CrossRefGoogle ScholarPubMed
Simon, A, Thomas, D, Blondel, J, Perret, P and Lambrechts, MM (2004) Physiological ecology of Mediterranean Blue Tits (Parus caeruleus L.): effects of ectoparasites (Protocalliphora spp.) and food abundance on metabolic capacity of nestlings. Physiological and Biochemical Zoology 77, 492501.CrossRefGoogle ScholarPubMed
Stockham, SL and Scott, MA (2011) Fundamentos de Patologia Clínica Veterinária. Rio de Janeiro: Guanabara Koogan.Google Scholar
Stoot, LJ, Cairns, NA, Cull, F, Taylor, JJ, Jeffrey, JD, Morin, F, Mandelman, JW, Clarck, TD and Cooke, SJ (2014) Use of portable blood physiology point-of-care devices for basic and applied research on vertebrates: a review. Conservation Physiology 2, cou011–cou01.CrossRefGoogle ScholarPubMed
Stromberg, PC and Guillot, DFS (1987) Hematology in the regressive phase of bovine Psoroptic scabies. Veterinary Pathology 24, 371377.CrossRefGoogle ScholarPubMed
Sulbi, IM, Jawad, RA, Mousa, RF, Jameel, YJ and Abd-Al-Hussain, AF (2019) Study of hematological changes in the experimentally infected sheep with ticks Hyalomma spp. Indian Journal of Public Health Research & Development 10, 551.CrossRefGoogle Scholar
Szabó, MPJ and Bechara, GH (1999) Sequential histopathology at the Rhipicephalus sanguineus tick feeding site on dogs and guinea pigs. Experimental and Applied Acarology 23, 915928.CrossRefGoogle ScholarPubMed
Szabó, K, Szalmás, A, Liker, A and Barta, Z (2002) Effects of haematophagous mites on nestling house sparrows (Passer domesticus). Acta Parasitologica 47, 318322.Google Scholar
Szabó, MPJ, Aoki, VL, Sanches, FPS, Aquino, LPTCT, Garcia, MV, Machado, RZ and Bechara, GH (2003) Antibody and blood leukocyte response in Rhipicephalus sanguineus (Latreille, 1806) tick-infested dogs and guinea pigs. Veterinary Parasitology 115, 4959.CrossRefGoogle ScholarPubMed
Tavares-Dias, M, de Moraes, FR, Onaka, EM and Rezende, PCB (2007) Changes in blood parameters of hybrid tambacu fish parasitized by Dolops carvalhoi (Crustacea, Branchiura), a fish louse. Veterinarski Arhiv 77, 355363.Google Scholar
Tefferi, A, Hanson, CA and Inwards, DJ (2005) How to interpret and pursue an abnormal complete blood cell count in adults. Mayo Clinic Proceedings 80, 923936.CrossRefGoogle ScholarPubMed
Thongsahuan, S, Fonghoi, L, Kaewfai, S and Srinoun, K (2020) Precision and accuracy of the Mindray BC-5000Vet hematology analyzer for canine and feline blood. Veterinary Clinical Pathology 49, 207216.CrossRefGoogle ScholarPubMed
Thrall, MA (2015) Hematologia e Bioquímica Clínica Veterinária. São Paulo: Rocca.Google Scholar
Triki, Z, Grutter, AS, Bshary, R and Ros, AFH (2016) Effects of short-term exposure to ectoparasites on fish cortisol and hematocrit levels. Marine Biology 163, 187.CrossRefGoogle Scholar
Veitch, JSM, Bowman, J, Mastromonaco, G and Schulte-Hostedde, AI (2021) Corticosterone response by Peromyscus mice to parasites, reproductive season, and age. General and Comparative Endocrinology 300, 113640.CrossRefGoogle ScholarPubMed
Vogt, L, Reichlin, TS, Nathues, C and Wurbel, H (2016) Authorization of animal experiments is based on confidence rather than evidence of scientific rigor. PLOS Biology 14, e2000598.CrossRefGoogle ScholarPubMed
Vriezen, R, Sargeant, JM, Vriezen, E, Reist, M, Winder, CB and O'Connor, AM (2019) Systematic reviews and meta-analyses in animal health, performance, and on-farm food safety: a scoping review. Animal Health Research Reviews 2, 116127.CrossRefGoogle Scholar
Wagner, GN, Fast, MD and Johnson, SC (2008) Physiology and immunology of Lepeophtheirus salmonis infections of salmonids. Trends in Parasitology 24, 176183.CrossRefGoogle ScholarPubMed
Webster, KN, Hill, NJ, Burnett, L and Deane, EM (2014) Ectoparasite infestation patterns, haematology and serum biochemistry of urban-dwelling common brushtail possums. Wildlife Biology 20, 206216.CrossRefGoogle Scholar
Weiss, DJ and Wardrop, KJ (2010) Schalm's Veterinary Hematology, 6th Edn. Ames: Wiley-Blackwell.Google Scholar
Wilkerson, MJ, Bagladi-Swanson, M, Wheeler, DW, Floyd-Hawkins, K, Craig, C, Lee, KW and Dryden, M (2004) The immunopathogenesis of flea allergy dermatitis in dogs, an experimental study. Veterinary Immunology and Immunopathology 99, 179192.CrossRefGoogle ScholarPubMed
Williams, RE, Hair, JA and McNew, RW (1978) Effects of gulf coast ticks on blood composition and weights of pastured Herefords teers. Journal of Parasitology 64, 336342.CrossRefGoogle Scholar
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