Distribution and Prevalence of Coxiella burnetii in Animals, Humans, and Ticks in Nigeria: A Systematic Review
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search and Selection Criteria
2.2. Inclusion and Exclusion Criteria from the Study
2.3. Data Extraction and Analysis
3. Results
3.1. Outcome of the Literature Search
3.2. Characteristics of the Studies Included in the Systematic Review
3.3. Host-Vector Relationships
3.4. Vector-Pathogen Relationships
3.5. Diagnostic Assays Employed
4. Discussion
4.1. Diagnostic Techniques Employed So Far in Nigeria
4.2. Ticks as Vector of Coxiella burnetii
4.3. Coxiella burnetii in Domestic and Peri-Domestic Animals
4.4. Coxiella burnetii in Humans
4.5. Coxiella burnetii Infection in Northern Nigeria
4.6. Coxiella burnetii Infection in Southern Nigeria
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Angelakis, E.; Raoult, D. Q fever. Veter. Microbiol. 2010, 140, 297–309. [Google Scholar] [CrossRef] [PubMed]
- Abdel-Moein, K.A.; Hamza, D.A. The burden of Coxiella burnetii among aborted dairy animals in Egypt and its public health implications. Acta Trop. 2017, 166, 92–95. [Google Scholar] [CrossRef] [PubMed]
- Elelu, N.; Bankole, A.A.; Musa, R.J.; Odetokun, I.A.; Rabiu, M.; Biobaku, K.T.; Aremu, A.; Ahmed, A.O.; Ghali, M.I.; Raji, M.A.; et al. Serospatial epidemiology of zoonotic Coxiella burnetii in a cross section of cattle and small ruminants in northern Nigeria. PLoS ONE 2020, 15, e0240249. [Google Scholar] [CrossRef]
- Eldin, C.; Mélenotte, C.; Mediannikov, O.; Ghigo, E.; Million, M.; Edouard, S.; Mege, J.-L.; Maurin, M.; Raoult, D. From Q Fever to Coxiella burnetii Infection: A Paradigm Change. Clin. Microbiol. Rev. 2017, 30, 115–190. [Google Scholar] [CrossRef] [PubMed]
- Guatteo, R.; Seegers, H.; Taurel, A.-F.; Joly, A.; Beaudeau, F. Prevalence of Coxiella burnetii infection in domestic ruminants: A critical review. Veter. Microbiol. 2011, 149, 1–16. [Google Scholar] [CrossRef] [PubMed]
- Yessinou, R.E.; Katja, M.-S.; Heinrich, N.; Farougou, S. Prevalence of Coxiella-infections in ticks—Review and meta-analysis. Ticks Tick-Borne Dis. 2022, 13, 101926. [Google Scholar] [CrossRef]
- Lemtudo, A.P.; Mutai, B.K.; Mwamburi, L.; Waitumbi, J.N. Seroprevalence of Coxiella burnetii in patients presenting with acute febrile illness at Marigat District Hospital, Baringo County, Kenya. Veter. Med. Sci. 2021, 7, 2093–2099. [Google Scholar] [CrossRef] [PubMed]
- Rahravani, M.; Moravedji, M.; Mostafavi, E.; Mohammadi, M.; Seyfi, H.; Baseri, N.; Mozoun, M.M.; Latifian, M.; Esmaeili, S. The epidemiological survey of Coxiella burnetii in small ruminants and their ticks in western Iran. BMC Veter. Res. 2022, 18, 292. [Google Scholar] [CrossRef]
- Tissot-Dupont, H.; Vaillant, V.; Rey, S.; Raoult, D. Role of sex, age, previous valve lesion, and pregnancy in the clinical expression and outcome of Q fever after a large outbreak. Clin. Infect. Dis. 2007, 44, 232–237. [Google Scholar] [CrossRef]
- Gikas, A.; Kokkini, S.; Tsioutis, C. Q fever: Clinical manifestations and treatment. Expert Rev. Anti-Infect. Ther. 2010, 8, 529–539. [Google Scholar] [CrossRef]
- Duron, O.; Boumedine, K.S.; Rousset, E.; Moutailler, S.; Jourdain, F. The importance of ticks in Q fever transmission: What has (and has not) been demonstrated? Trends Parasitol. 2015, 31, 536–552. [Google Scholar] [CrossRef] [PubMed]
- Celina, S.S.; Cerný, J. Coxiella burnetii in ticks, livestock, pets and wildlife: A mini-review. Frontiers Veter. Sci. 2022, 9, 1068129. [Google Scholar] [CrossRef]
- Jourdain, E.; Duron, O.; Barry, S.; González-Acuña, D.; Sidi-Boumedine, K. Molecular methods routinely used to detect Coxiella burnetii in ticks cross-react with Coxiella-like bacteria. Infec. Ecol. Epidemiol. 2015, 5, 29230. [Google Scholar] [CrossRef] [PubMed]
- Reye, A.L.; Arinola, O.G.; Hübschen, J.M.; Muller, C.P. Pathogen prevalence in ticks collected from the vegetation and livestock in Nigeria. Appl. Environ. Microbiol. 2012, 78, 2562–2568. [Google Scholar] [CrossRef] [PubMed]
- Ogo, N.; de Mera, I.G.F.; Okubanjo, O.; de la Fuente, J. Genetic characterization of Coxiella burnetii in Amblyomma varigatum ticks from North-central Nigeria: Public health importance. Infection 2013, 5, 818–822. [Google Scholar] [CrossRef]
- Onyiche, T.E.; Răileanu, C.; Tauchmann, O.; Fischer, S.; Vasić, A.; Schäfer, M.; Silaghi, C. Prevalence and molecular characterization of ticks and tick-borne pathogens of one-humped camels (Camelus dromedarius) in Nigeria. Paras. Vect. 2020, 13, 428. [Google Scholar] [CrossRef]
- Fard, S.R.N.; Ghashghaei, O.O.; Khalili, M.; Sharifi, H. Tick diversity and detection of Coxiella burnetii in tick of small ruminants using nested Trans PCR in Southeast Iran. Trop. BioMed 2016, 33, 506–511. [Google Scholar]
- Körner, S.; Makert, G.R.; Ulbert, S.; Pfeffer, M.; Mertens-Scholz, K. The prevalence of Coxiella burnetii in hard ticks in Europe and their role in Q Fever transmission revisited—A systematic review. Front. Veter. Sci. 2021, 8, 655715. [Google Scholar] [CrossRef]
- Maurin, D.F. Raoult, Q fever. Clin. Microbial. Rev. 1999, 12, 518–553. [Google Scholar] [CrossRef]
- Raoult, D.; Marrie, T.; Mege, J. Natural history and pathophysiology of Q fever. Lancet Infect. Dis. 2005, 5, 219–226. [Google Scholar] [CrossRef]
- Vanderburg, S.; Rubach, M.P.; Halliday, J.E.B.; Cleaveland, S.; Reddy, E.A.; Crump, J.A. Epidemiology of Coxiella burnetii Infection in Africa: A OneHealth Systematic Review. PLoS Negl. Trop. Dis. 2014, 8, e2787. [Google Scholar] [CrossRef]
- Kamani, J.; Baneth, G.; Gutiérrez, R.; Nachum-Biala, Y.; Mumcuoglu, K.Y.; Harrus, S. Coxiella burnetii and Rickettsia conorii: Two zoonotic pathogens in peridomestic rodents and their ectoparasites in Nigeria. Ticks Tick-Borne Dis. 2018, 9, 86–92. [Google Scholar] [CrossRef]
- Blondeau, J.; Yates, L.; Martin, R.; Marrie, T.; Ukoli, P.; Thomas, A. Q fever in Sokoto, Nigeria. Ann. N. Y. Acad. Sci. 1990, 590, 281–282. [Google Scholar] [CrossRef]
- Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron, I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. Int. J. Surg. 2021, 88, 105906. [Google Scholar] [CrossRef] [PubMed]
- Nyifi, A.S.; Ardo, M.B.; Ja’afar, J.N.; Mbaya, P.Y. Detection of Coxiella burnetii antibodies among humans and slaughtered ruminants in Jalingo abattoir, Nigeria. Savannah Veter. J. 2018, 1, 14–18. [Google Scholar]
- Adamu, G.; Kia, G.; Saidu, S.N.A.; Ejeh, F. Serosurvey and Risk Factors of Coxiella burnetii in Sheep and Goats in three agricultural zones of Borno State, Nigeria. Authorea 2022, preprints. [Google Scholar]
- Adamu, S.G.; Kabir, J.; Umoh, J.U.; Raji, M.A. Seroprevalence of brucellosis and Q fever (Coxiellosis) in cattle herds in Maigana and Birnin Gwari agro-ecological zone of Kaduna State, Nigeria. Trop. Anim. Health Prod. 2018, 50, 1583–1589. [Google Scholar] [CrossRef] [PubMed]
- Adamu, S.G.; Kabir, J.; Umoh, J.; Raji, M. Seroprevalence of Coxiellosis (Q fever) in Flocks of Goat in Birnin Gwari and Maigana Agro-Ecological Zone of Kaduna State, Nigeria. Sahel J. Veter. Sci. 2020, 17, 12–16. [Google Scholar] [CrossRef]
- Adamu, S.G.; Kabir, J.; Umoh, J.U.; Raji, M.A. Seroprevalence of Coxiella burnetii in sheep flocks in Kaduna State, Northwestern Nigeria. Acta Veter.- Hung. 2021, 69, 234–238. [Google Scholar] [CrossRef]
- Adamu, S.G.; Tijani, A.O.; Adamu, N.B.; Atsanda, N.N.; Dauda, J.; Lawan, F.A. Epidemiology of Q fever in flocks of sheep in Yobe State, Nigeria. J. Veter. Biomed. Sci. 2019, 2, 70–76. [Google Scholar] [CrossRef]
- Tukur, H.B.; Ajogi, I.; Kabir, J.; Umoh, J.U. Seroprevalence of Coxiella burnetii in cattle and its risk factors in Kaduna Metropolis, Kaduna State, Nigeria. IOSR J. Agric. Veter. Sci. 2014, 7, 1–5. [Google Scholar] [CrossRef]
- Cadmus, S.; Salam, S.P.; Adesokan, H.K.; Akporube, K.; Ola-Daniel, F.; Awosanya, E.J. Seroprevalence of brucellosis and Q fever infections amongst pastoralists and their cattle herds in Sokoto State, Nigeria. PLoS ONE 2021, 16, e0254530. [Google Scholar] [CrossRef]
- Cadmus, S.I.; Akporube, K.A.; Ola-Daniel, F.; Adelakun, O.D.; Akinseye, V.O. Seroprevalence and associated factors of brucellosis and Q-fever in cattle from Ibarapa area, Oyo state, south-western Nigeria. Pan Afr. Med. J. 2020, 36, 24925. [Google Scholar] [CrossRef] [PubMed]
- A Adesiyun, A.; Jagun, A.G.; Kwaga, J.K.; Tekdek, L.B. Shedding of Coxiella burnetii in milk by Nigerian dairy and dual purposes cows. Int. J. Zoonoses 1985, 12, 1–5. [Google Scholar]
- Pexara, A.; Solomakos, N.; Govaris, A. Q fever and seroprevalence of Coxiella burnetii in domestic ruminants. Veter. Ital. 2018, 54, 265–279. [Google Scholar]
- Kazar, J. Coxiella burnetii infection. Ann. N. Y. Acad. Sci. 2005, 1063, 105–114. [Google Scholar] [CrossRef] [PubMed]
- Koka, H.; Sang, R.; Kutima, H.L.; Musila, L. Coxiella burnetii detected in tick samples from pastoral communities in kenya. BioMed Res. Int. 2018, 2018, 8158102. [Google Scholar] [CrossRef] [PubMed]
- Mediannikov, O.; Diatta, G.; Fenollar, F.; Sokhna, C.; Trape, J.-F.; Raoult, D. Tick-borne rickettsioses, neglected emerging diseases in rural senegal. PLoS Negl. Trop. Dis. 2010, 4, e821. [Google Scholar] [CrossRef]
- Nimo-Paintsil, S.C.; Mosore, M.; Addo, S.O.; Lura, T.; Tagoe, J.; Ladzekpo, D.; Addae, C.; Bentil, R.E.; Behene, E.; Dafeamekpor, C.; et al. Ticks and prevalence of tick-borne pathogens from domestic animals in Ghana. Parasites Vectors 2022, 15, 86. [Google Scholar] [CrossRef] [PubMed]
- Knobel, D.L.; Maina, A.N.; Cutler, S.J.; Ogola, E.; Feikin, D.R.; Junghae, M.; Halliday, J.E.B.; Richards, A.L.; Breiman, R.F.; Cleaveland, S.; et al. Coxiella burnetii in humans, domestic ruminants, and ticks in rural western Kenya. Am. J. Trop. Med. Hyg. 2013, 88, 513–518. [Google Scholar] [CrossRef]
- Truong, A.-T.; Yun, B.-R.; Lim, J.; Min, S.; Yoo, M.-S.; Yoon, S.-S.; Yun, Y.-M.; Kim, J.-T.; Cho, Y.S. Real-time PCR biochip for on-site detection of Coxiella burnetii in ticks. Parasites Vectors 2021, 14, 239. [Google Scholar] [CrossRef] [PubMed]
- Kumsa, B.; Parola, P.; Almeras, L.; Raoult, D.; Socolovschi, C. Occurrence and Genotyping of Coxiella burnetii in Ixodid Ticks in Oromia, Ethiopia. Am. J. Trop. Med. Hyg. 2015, 93, 1074–1081. [Google Scholar] [CrossRef] [PubMed]
- Philip, C.B. Observations on Experimental Q Fever. J. Parasitol. 1948, 34, 457–464. [Google Scholar] [CrossRef] [PubMed]
- Rodolakis, A.; Berri, M.; Héchard, C.; Caudron, C.; Souriau, A.; Bodier, C.; Blanchard, B.; Camuset, P.; Devillechaise, P.; Natorp, J.; et al. Comparison of Coxiella burnetii shedding in milk of dairy bovine, caprine, and ovine herds. J. Dairy Sci. 2007, 90, 5352–5360. [Google Scholar] [CrossRef]
- Plummer, P.J.; McClure, J.; Menzies, P.; Morley, P.S.; Brom, R.V.D.; Van Metre, D.C. Management of Coxiella burnetii infection in livestock populations and the associated zoonotic risk: A consensus statement. J. Veter. Intern. Med. 2018, 32, 1481–1494. [Google Scholar] [CrossRef]
- Szymańska-Czerwińska, M.; Jodełko, A.; Zaręba-Marchewka, K.; Niemczuk, K. Shedding and genetic diversity of Coxiella burnetii in polish dairy cattle. PLoS ONE 2019, 14, e0210244. [Google Scholar] [CrossRef]
- Mobarez, A.M.; Mostafavi, E.; Khalili, M.; Esmaeili, S. Identification of Coxiella burnetii in Raw Milk of Livestock Animal in Iran. Int. J. Microbiol. 2021, 2021, 6632036. [Google Scholar] [CrossRef]
- Rabaza, A.; Fraga, M.; Corbellini, L.G.; Turner, K.M.; Riet-Correa, F.; Eisler, M.C. Molecular prevalence of Coxiella burnetii in bulk-tank milk from bovine dairy herds: Systematic review and meta-analysis. One Health 2020, 12, 100208. [Google Scholar] [CrossRef]
- Njeru, J.; Henning, K.; Pletz, M.W.; Heller, R.; Neubauer, H. Q fever is an old and neglected zoonotic disease in Kenya: A systematic review. BMC Public Health 2016, 16, 297. [Google Scholar] [CrossRef]
- Nahed, H.G.; Khaled, A.A.M. Seroprevalence of Coxiella burnetii antibodies among farm animals and human contacts in Egypt. J. Am. Sci. 2012, 8, 619–621. [Google Scholar]
- Schelling, E.; Diguimbaye, C.; Daoud, S.; Nicolet, J.; Boerlin, P.; Tanner, M.; Zinsstag, J. Brucellosis and Q-fever seroprevalences of nomadic pastoralists and their livestock in Chad. Prev. Veter. Med. 2003, 61, 279–293. [Google Scholar] [CrossRef]
- Chitanga, S.; Simulundu, E.; Simuunza, M.C.; Changula, K.; Qiu, Y.; Kajihara, M.; Nakao, R.; Syakalima, M.; Takada, A.; Mweene, A.S.; et al. First molecular detection and genetic characterization of Coxiella burnetii in Zambian dogs and rodents. Parasites Vectors 2018, 11, 40. [Google Scholar] [CrossRef] [PubMed]
- Liu, L.; Manxia, H.; Ming, L.; Chao, J.; Yingqun, F.; Yu, Y.; Jing, W.; Shasha, W.; Tianyu, G.; Baoliang, X.; et al. Coxiella burnetii in Rodents on Heixiazi Island at the Sino-Russian Border. Am. J. Trop. Med. Hyg. 2013, 88, 770–773. [Google Scholar] [CrossRef] [PubMed]
- Meerburg, B.G.; Reusken, C.B.E.M. The role of wild rodents in spread and transmission of Coxiella burnetii needs further elucidation. Wildl. Res. 2011, 38, 617–625. [Google Scholar] [CrossRef]
- Corwin, A.; Olson, J.; Habib, M.; Watts, D.; Kleinosky, M.; Shope, R.; Lee, H.W.; Botros, B.; Kilpatrick, M.; Darwish, M.; et al. Community-based prevalence profile of arboviral, rickettsial, and hantaan-like viral antibody in the Nile river delta of Egypt. Am. J. Trop. Med. Hyg. 1993, 48, 776–783. [Google Scholar] [CrossRef] [PubMed]
- Julvez, J.; Michault, A.; Kerdelhue, C. Serological study of rickettsioses in Niamey, Niger/E’tude se’rologique des rickettsioses a Niamey, Niger. Med. Trop. 1997, 57, 153–156. [Google Scholar]
- Bwatota, S.F.; Shirima, G.M.; Hernandez-Castro, L.E.; Bronsvoort, B.M.d.C.; Wheelhouse, N.; Mengele, I.J.; Motto, S.K.; Komwihangilo, D.M.; Lyatuu, E.; Cook, E.A.J. Seroprevalence and Risk Factors for Q fever (Coxiella burnetii) Exposure in Smallholder Dairy Cattle in Tanzania. Veter. Sci. 2022, 9, 662. [Google Scholar] [CrossRef]
- Cetinkol, Y.; Enginyurt, Ö.; Celebi, B.; Yıldırım, A.A.; Cankaya, S.; Aktepe, O.C. Investigation of zoonotic infections in risk groups in Ordu University Hospital, Turkey. Niger. J. Clin. Prac. 2017, 20, 6–11. [Google Scholar] [CrossRef]
- Pouquet, M.; Bareille, N.; Guatteo, R.; Moret, L.; Beaudeau, F. Coxiella burnetii infection in humans: To what extent do cattle in infected areas free from small ruminants play a role? Epidemiol. Infec. 2020, 148, e232. [Google Scholar] [CrossRef]
- Mwololo, D.; Nthiwa, D.; Kitala, P.; Abuom, T.; Wainaina, M.; Kairu-Wanyoike, S.; Lindahl, J.F.; Ontiri, E.; Bukachi, S.; Njeru, I.; et al. Sero-epidemiological survey of Coxiella burnetii in livestock and humans in Tana River and Garissa counties in Kenya. PLoS Negl. Trop. Dis. 2022, 16, e0010214. [Google Scholar] [CrossRef]
- Wardrop, N.A.; Thomas, L.F.; Cook, E.A.; de Glanville, W.A.; Atkinson, P.M.; Wamae, C.N.; Fèvre, E.M. The sero-epidemiology of Coxiella burnetii in humans and cattle, Western Kenya: Evidence from a cross-sectional study. PLoS Negl. Trop. Dis. 2016, 10, e0005032. [Google Scholar] [CrossRef] [PubMed]
- Hussien, M.O.; Enan, K.A.; Alfaki, S.H.; Gafar, R.A.; Taha, K.M.; El Hussein, A.R.M. Seroprevalence of Coxiella burnetii in dairy cattle and camel in Sudan. Int. J. Infect. 2017, 4, 42945. [Google Scholar] [CrossRef]
- Deressa, F.B.; Kal, D.O.; Gelalcha, B.D.; Magalhães, R.J.S. Seroprevalence of and risk factors for Q fever in dairy and slaughterhouse cattle of Jimma town, South Western Ethiopia. BMC Veter. Res. 2020, 16, 385. [Google Scholar] [CrossRef] [PubMed]
- De Boni, L.; Mall, S.; Msimang, V.; de Voux, A.; Rossouw, J.; Frean, J. Exposure of South African Abattoir Workers to Coxiella burnetii. Trop. Med. Infect. Dis. 2022, 7, 28. [Google Scholar] [CrossRef]
Table Cont. | Reference ID | Study Design | Region (States) | Diagnostic Technique | Total AniSpecimen | Host Species (Prevalence) | Presence of Ticks (Infection Rate) | Tick Species |
---|---|---|---|---|---|---|---|---|
1 | Elelu et al. [3] | Cross-sectional | North (Kwara, Plateau and Borno) | ELISA | 538 | Cattle (28/268; (10.44%) Sheep (1/26; 3.8%) Goat (5/158; 3.16%) | - | - |
2 | Onyiche et al. [16] | Cross-sectional | North (Kano, Jigawa and Sokoto) | PCR | 176 | Camel | Yes (17/593; 2.9%) | Hyalomma truncatum, Amblyomma variegatum, Rh. evertsi evertsi, Hyalomma. dromedarii, Hy. rufipes, Hy. impeltatum, Hy. Impressum |
3 | Kamani et al. [22] | Cross-sectional | North (Plateau) | PCR | 194 | Rodent; 4/194 (2.2%) | NA | - |
4 | Adamu et al. [27] | Cross-sectional | North (Kaduna) | ELISA | 400 | Cattle (25/400; 6.2%) | NA | - |
5 | Adamu et al. [28] | Cross-sectional | North (Kaduna) | indirect enzyme-linked immunosorbent assay ELISA | 400 | Goats (35/400; 8.7%) | NA | - |
6 | Adamu et al. [26] | Cross-sectional | North (Borno) | ELISA | 768 | Sheep (46/384; 11.9%) Goats (42/384; 10.9%) | NA | - |
7 | Reye et al. [14] | Cross-sectional | South (Oyo) | PCR | 836 | - | YES (19/136; 14%) | Amblyomma variegatum, Rh. (Boophilus) annulatus, Hyalomma impeltatum, Rhipicephalus evertsi |
8 | Ogo et al. [15] | Cross-sectional | North (Plateau and Nasarrawa) | PCR | 40 | - | YES (10/40; 25%) | Amblyomma. Variegatum |
9 | Tukur et al. [31] | Cross sectional | North (Kaduna) | ELISA | 539 | Cattle: 78/539; (14.5%) | NA | - |
10 | Cadmus et al. [32] | Cross-sectional | North (Sokoto) | ELISA | 503 | Human: 84/137; (61.31%) Cattle: 9/366; (2.45%) | NA | - |
11 | Nyifi et al. [25] | Cross-sectional | North (Taraba) | ELISA | 350 | Human (6/50; 12%) Goat (10/100; 10%) Sheep (9/100; 9.0%) Cattle (13/100; 13%) | NA | - |
12 | Blondeau et al. [23] | Case control | North (Sokoto) | Microimmunofluorescence test | 75 | Human (33/75; 44%) | NA | - |
13 | Adamu et al. [29] | Cross-sectional | North (Kaduna) | ELISA | 400 | Sheep (32/400; 8%) | NA | - |
14 | Cadmus et al. [33] | Cross-sectional | South (Oyo) | ELISA AND RBPT | 149 | Cattle (35/149; 23.5%) | NA | - |
15 | Adamu et al. [30] | Cross-sectional | North (Yobe) | ELISA | 420 | Sheep (49/420; 11.7%) | NA | |
Study on Milk Samples | ||||||||
S/N | Reference ID | Study Design | Region (States) | Diagnostic Technique | Total Animals Screened | Host Species (Prevalence) | Infection rate | |
1 | Adesiyun et al. [34] | Cross-sectional | North (Kaduna) | Capillary Agglutination Test (CAT) | 169 | Cow milk (41/169; 24.2%) | NA |
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Muhammad, K.A.; Gadzama, U.N.; Onyiche, T.E. Distribution and Prevalence of Coxiella burnetii in Animals, Humans, and Ticks in Nigeria: A Systematic Review. Infect. Dis. Rep. 2023, 15, 576-588. https://doi.org/10.3390/idr15050056
Muhammad KA, Gadzama UN, Onyiche TE. Distribution and Prevalence of Coxiella burnetii in Animals, Humans, and Ticks in Nigeria: A Systematic Review. Infectious Disease Reports. 2023; 15(5):576-588. https://doi.org/10.3390/idr15050056
Chicago/Turabian StyleMuhammad, Kaka A., Usman N. Gadzama, and ThankGod E. Onyiche. 2023. "Distribution and Prevalence of Coxiella burnetii in Animals, Humans, and Ticks in Nigeria: A Systematic Review" Infectious Disease Reports 15, no. 5: 576-588. https://doi.org/10.3390/idr15050056