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Acta Tropica | 2003

The emergence of Taenia solium cysticercosis in Eastern and Southern Africa as a serious agricultural problem and public health risk

Isaac K. Phiri; Helena A. Ngowi; Sónia Afonso; Elizabeth Matenga; M.E. Boa; S. Mukaratirwa; Sm Githigia; Margaret Saimo; Chummy Sikalizyo Sikasunge; N Maingi; George W. Lubega; A.A. Kassuku; Lm Michael; Seter Siziya; R.C. Krecek; Emilia Virginia Noormahomed; Manuela Vilhena; Pierre Dorny; A. Lee Willingham

Pig production has increased significantly in the Eastern and Southern Africa (ESA) region during the past decade, especially in rural, resource-poor, smallholder communities. Concurrent with the increase in smallholder pig keeping and pork consumption, there have been increasing reports of porcine cysticercosis in the ESA region. This article reviews the findings concerning the presence and impact of porcine cysticercosis in seven of the ESA countries. Most of the reported findings are based on surveys utilising lingual palpation and post-mortem examination, however, some also used serological assays. In Tanzania, community-based studies on porcine cysticercosis indicate a prevalence of 17.4% in the northern highlands district of Mbulu and a prevalence range of 5.1-16.9% in the southern highlands. In Kenya recent surveys in the southwestern part of the country where smallholder pig keeping is popular indicate that 10-14% of pigs are positive for cysticercosis by lingual examination. Uganda has the most pigs in Eastern Africa, most of which are kept under smallholder conditions. Preliminary surveys in 1998 and 1999 at slaughterhouses in Kampala indicated a prevalence of porcine cysticercosis between 0.12 and 1.2%, however, a rural survey in northern Uganda in 1999 indicated 34-45% of pigs slaughtered in selected villages were infected. Additionally, a new survey of 297 pigs slaughtered in Kampala in 2002 indicated that pigs from the central region of the country were negative for cysticercosis while 33.7% of the pigs coming from the rural Lira district in the north were positive. Interestingly 8 piglet foetuses removed from an infected slaughtered sow coming from Lira district were all found to harbour cysts of T. solium providing evidence of congenital transmission of porcine cysticercosis. In Mozambique, abattoir records indicate that porcine cysticercosis is present in all provinces of the country. A serological survey on pigs in rural Tete Province found 15% of pigs positive. In Zimbabwe, a retrospective study in official abattoirs around the country from 1994 to 2001 reported a mean prevalence of 0.34% which is in contrast to a post-mortem survey in 1999, which showed that the prevalence of porcine cysticercosis in rural west Zimbabwe where smallholder pig keeping is popular was 28.6%. In Zambia, abattoir records reported porcine cysticercosis in six of the nine provinces. Routine meat inspection of 1316 pigs at a slaughter slab in Lusaka showed that 20.6% of the pigs had cysticercosis whereas serological testing of 874 pigs at the same abattoir indicated that 56.6% were found to have circulating antigens of Taenia solium. Field surveys based on lingual palpation in Southern and Eastern Provinces of Zambia revealed prevalences of 8.2-28.4 and 5.2%, respectively. South Africa has the largest number of pigs in Southern Africa and cysticercosis has been recognised as a problem in the country for many decades. There is strong evidence supporting the high prevalence of neurocysticercosis infecting humans from resource-poor areas of the country where pigs are being raised under smallholder conditions. In spite of this community-based surveys on porcine cysticercosis have never been conducted in South Africa and the last slaughterhouse survey was conducted nearly 40 years ago. The prevalences of porcine cysticercosis found in these ESA countries rank among the highest in the world and the disease is emerging as an important constraint for the nutritional and economic well being of resource-poor smallholder farming communities. The current findings suggest the widespread presence of human tapeworm carriers and thus a high risk of human cysticercosis in both rural areas and urban centres in the ESA region. More research is required in the region to assess the extent and public health and economic impact of T. solium infection in order to determine whether and what prevention and control efforts are needed.


Veterinary Parasitology | 2008

Taenia solium porcine cysticercosis: viability of cysticerci and persistency of antibodies and cysticercal antigens after treatment with oxfendazole.

Chummy Sikalizyo Sikasunge; Maria Vang Johansen; Arve Lee Willingham; Pall S. Leifsson; I.K. Phiri

The aim of this study was to assess the effect of treating Taenia solium infected pigs with oxfendazole (OFZ) on viability and clearance of cysticerci and the corresponding persistence of specific antibody isotypes (IgG(total), IgG1, IgG2 and IgA) and circulating cysticercal antigen (CCA). Antibody isotypes and CCA responses were measured by antibody-ELISA (Ab-ELISA) and antigen ELISA (Ag-ELISA), respectively. Correlations were made between antibodies, CCA and the total number of cysticerci enumerated at necropsy. Forty pigs with cysticercosis were randomly allocated into two groups: Treatment group (n=20) was treated with OFZ at 30 mg/kg orally while the treatment control group (n=20) was not treated. Five uninfected pigs served as negative controls. Pigs were killed at 1, 4, 8 and 26 weeks post-treatment (wkpt). Overall, the mean total cyst count in treated pigs was 2904+/-5397 (mean+/-S.D.) while in the controls it was 6235+/-6705. Mean cyst viability was 5+/-11% (mean+/-S.D.) and 97+/-4% in treated and control pigs, respectively. Results showed that OFZ killed muscular cysticerci over a period of 4 weeks but failed to kill cerebral cysticerci. Antibodies, CCA responses and clearance of dead cysts from the meat, depended on the cyst intensity of individual pigs at time of treatment since both antibody and CCA correlated with intensity of cysticerci at necropsy (r=0.441, P=0.005; r=0.654, P<0.001), respectively. IgG1 responses were the best indicator of treatment efficacy because they were predominant in both infected treated and control pigs and disappeared early after treatment. Both Ab/Ag-ELISA failed to detect cysts in the brain. Though dead cysticerci took some time (26 wkpt) to clear from the meat, treatment of porcine cysticercosis with OFZ should, in combination with other intervention measures be considered as an important, cost-effective measure in the control of taeniosis/cysticercosis.


Journal of Helminthology | 2006

Assessment of routine inspection methods for porcine cysticercosis in Zambian village pigs

Ik Phiri; Pierre Dorny; Sarah Gabriël; Al Willingham; Chummy Sikalizyo Sikasunge; Seter Siziya; Jozef Vercruysse

The value of tongue and meat inspection as diagnostic tools for porcine cysticercosis was assessed in 65 Zambian village pigs by comparing the results with carcass dissections. In addition, the intensity of infections, distribution and viability of cysts in infected pigs were measured. Five pigs (7.7%) were positive on tongue examination, while routine meat inspection showed 12 (18.5%) positives. However, carcass dissections detected cysticerci in 31 (47.7%) pigs. The range in number of cysticerci was 1 to 14,662 per carcass. Cysticerci were distributed throughout the carcass with the highest concentration in the heart, tongue and hind legs. In one animal 13 viable cysts were detected only in the brain. Fourteen pigs had more than 100 viable cysts, six between 2 and 100, and four had single cyst infections. Seven animals harboured only calcified cysts. These findings demonstrate the serious shortcomings of routine detection methods for porcine cysticercosis. While the specificity of tongue palpation and meat inspection was 100%, these tests failed to detect the infection in 83.9% and 61.3% of infected pigs, respectively.


Wiener Klinische Wochenschrift | 2009

Epilepsy and neurocysticercosis in sub-Saharan Africa

Andrea Sylvia Winkler; Arve Lee Willingham; Chummy Sikalizyo Sikasunge; Erich Schmutzhard

ZusammenfassungÜber die letzten Jahrzehnte hinweg konnten zahlreiche Studien belegen, dass Epilepsie in Subsahara-Afrika eine hochprävalente neurologische Erkrankung darstellt. Gründe hierfür sind mannigfaltig, Infektionen des zentralen Nervensystems spielen jedoch eine wichtige Rolle. Vor kurzem erst erkannte man Neurozystizerkose (NCC) als ernsthaftes Gesundheitsproblem mit steigender Tendenz in Subsahara-Afrika. Es wird geschätzt, dass NCC 30–50 % der erworbenen Epilepsien verursacht. NCC steht in unmittelbarem Zusammenhang mit der Schweinzystizerkose sowie der humanen Täniasis, erstere Erkrankung erreicht in einigen Schweinepopulationen Subsahara Afrikas fast 50%. In diesem Übersichtsartikel fassen wir zunächst die Prävalenz der Epilepsie in Subsahara-Afrika zusammen und zeigen einige Besonderheiten dieser Erkrankung im afrikanischen Kontext auf. Dann konzentrieren wir uns auf die Prävalenz der NCC, ihre klinischen Ausprägungen und gängige Diagnosekriterien für die NCC bezogen auf Afrika. Es schließt sich ein Abschnitt über die neuesten Entwicklungen in der serologischen Diagnostik der Zystizerkose und ein weiterer über therapeutische Aspekte an. NCC stellt einen häufigen Risikofaktor für Epilepsie dar; korrekte Diagnose und konsequente Behandlung der NCC könnte Epilepsie von Millionen von Menschen in Subsahara-Afrika heilen.SummaryOver the last decades, studies in sub-Saharan Africa have indicated that epilepsy is a highly prevalent neurological disorder. Causes may be varied with infections of the central nervous system playing an important role. Neurocysticercosis (NCC) has recently been recognised as an emerging public health problem and a growing concern throughout sub-Saharan Africa and has been estimated to be responsible for 30–50% of acquired epilepsy. NCC is closely linked with porcine cysticercosis and human taeniosis, the former reaching a prevalence of almost 50% in some pig populations. In this review, we first summarize prevalence data on epilepsy and highlight some special aspects of the disorder within sub-Saharan Africa. We then focus on the prevalence of NCC, clinical signs and symptoms and diagnostic criteria for NCC with special reference to sub-Saharan Africa. This is followed by a section on the latest developments regarding serodiagnosis of cysticercosis and a section on care management of people infected with NCC. NCC clearly represents a major risk factor of epilepsy, thus detecting and treating NCC may help cure epilepsy in millions of people in sub-Saharan Africa.


Veterinary Parasitology | 2013

Prevalence of porcine cysticercosis and associated risk factors in smallholder pig production systems in Mbeya region, southern highlands of Tanzania

Erick V.G. Komba; Eliakunda Casmir Kimbi; Helena A. Ngowi; Sharadhuli I. Kimera; James Mlangwa; Faustin Lekule; Chummy Sikalizyo Sikasunge; Arve Lee Willingham; Maria Vang Johansen; Stig M. Thamsborg

Porcine cysticercosis (PC) caused by the larval stage of a zoonotic tapeworm Taenia solium, is known to pose serious economic losses and public health risk among smallholder pig production communities. The present study was conducted to determine prevalence and associated risk factors for PC in smallholder pig production systems in Mbeya region, the major pig rearing region of Tanzania. A cross-sectional survey employing a random sample of 300 pig keepers from 30 villages of Mbozi and Mbeya Rural districts, Mbeya region were used to evaluate pig production systems and practices. Concurrently, 600 male and female pigs of different age categories were randomly selected and examined for PC using lingual examination method and antigen enzyme-linked immunosorbent assay (Ag-ELISA). The overall pig level PC prevalence in Mbozi district was 11.7% (95% CI=8.5-15.8%) and 32% (95% CI: 27-37.5%) based on lingual examination and Ag-ELISA, respectively. In Mbeya Rural district, the prevalences were 6% (95% CI: 3.8-9.3%) and 30.7% (95% CI: 25.8-36.1%) by lingual examination and Ag-ELISA, respectively. In Mbozi district 46% of the households were found infected (one or more infected pigs) and the corresponding figure was 45% for Mbeya Rural district. The agreement between lingual examination and Ag-ELISA was poor (κ<0.40). There were no significant differences in the prevalence of PC in different sex categories of pigs. Significant risk factors associated with PC prevalence were free roaming of pigs (OR=2.1; 95% CI=1.3-3.6; p=0.006), past experience of porcine cysticercosis in the household (OR=2.6; 95% CI=1.5-4.8; p=0.002), increased age of pig (OR=1.9; 95% CI=1.2-3.0), slatted raised floor in pig pen (OR=8.4; 95% CI=1.0-70.0), in-house origin of the pig (OR=1.6; 95% CI=1.1-2.5) and sourcing of water from rivers (OR=3.1; 95% CI=1.6-6.3; p<0.001) and ponds (OR=5.0; 95% CI=1.2-21.7; p=0.031). This study has clearly revealed a high sero-prevalence of PC in the study area, which imposes a major economical and public health burden to the smallholder pig farmers. The study also points to a number of important risk factors in smallholder pig management that may be addressed (e.g. confinement, quality of pens and water sources) in future interventions and educational campaigns for control of T. solium.


Journal of Parasitology Research | 2009

Porcine Cysticercosis in Southeast Uganda: Seroprevalence in Kamuli and Kaliro Districts

Charles Waiswa; Eric M. Fèvre; Zachary Nsadha; Chummy Sikalizyo Sikasunge; Arve Lee Willingham

The recent recognition of neurocysticercosis as a major cause of epilepsy in Uganda and changes in pig demography have lead to a need to better understand the basic epidemiology of Taenia solium infections in pigs and humans. Human exposure is a function of the size of the animal reservoir of this zoonosis. This is the first field survey for porcine cysticercosis to investigate the prevalence of antigen-positive pigs across an entire rural district of south-east Uganda. In our field surveys, 8.6% of 480 pigs screened were seropositive for the parasite by B158/B60 Ag-ELISA. In addition, of the 528 homesteads surveyed 138 (26%) did not have pit latrines indicating a high probability of pigs having access to human faeces and thus T. solium eggs. This study thus indicates the need for better data on this neglected zoonotic disease in Uganda, with a particular emphasis on the risk factors for infection in both pigs and humans. In this regard, further surveys of pigs, seroprevalence surveys in humans and an understanding of cysticercosis-related epilepsy are required, together with risk-factor studies for human and porcine infections.


Veterinary Parasitology | 2009

The immune response in Taenia solium neurocysticercosis in pigs is associated with astrogliosis, axonal degeneration and altered blood–brain barrier permeability

Chummy Sikalizyo Sikasunge; Maria Vang Johansen; I.K. Phiri; Arve Lee Willingham; Pall S. Leifsson

Immunohistochemistry was used to examine the immuno-pathological changes and the extent of neuronal damage caused by either viable or dead Taenia solium cysticerci during porcine neurocysticercosis. Thirty pig brains with cerebral cysticercosis and 5 brains from T. solium free pigs were used in this study. Results revealed extensive astrogliosis, neuronal and mostly axonal damage in both early (grade I) and late (grades III and V) lesions as evidenced by an increased expression of glial fibrillary acidic protein (GFAP) and neurofilament protein (NFP). In many late lesions, astrocyte end-feet formed glial scars that surrounded the dead parasite. Rapid angiogenesis resulted in blood vessels lacking astrocyte end-feet suggesting loss of blood-brain barrier (BBB) hence allowing an influx of peripheral blood immune cells such as eosinophils, macrophages, CD3+ T cells, B lymphocytes and plasma cells into lesions. This study showed that porcine NCC was associated with severe nervous tissue damage, the host response of which is a collaborative effort between the local and peripheral immune responses comparable to that observed in human NCC. Results further implied that porcine NCC could be a useful model for understanding the course of NCC in human as well as provide useful information for therapeutic and/or immune strategies.


Acta Tropica | 2013

Efficacy of ivermectin and oxfendazole against Taenia solium cysticercosis and other parasitoses in naturally infected pigs.

Ernatus Martin Mkupasi; Helena A. Ngowi; Chummy Sikalizyo Sikasunge; Pall S. Leifsson; Maria Vang Johansen

Smallholder semi-confined pig production is a fast growing practice in sub-Saharan Africa with an unfortunate outcome of high prevalence of Taenia solium cysticercosis and other parasitoses. The widely used anthelmintic for control of endo and ecto-parasites in pigs in the area is ivermectin at a recommended dose of 0.3mg/kg. This study was conducted to evaluate the efficacy and safety in pigs after subcutaneous injection of ivermectin (IVM, 0.3mg/kg) and orally administration of oxfendazole (OFZ, 30mg/kg) in treatment of porcine cysticercosis and other parasitoses in naturally infected pigs. A total of 61 pigs with T. solium cysticercosis (38 males and 23 females) as identified by tongue palpation with age ranging from 3 to 24 months were recruited. The pigs were stratified based on sex, age and number of cysts on the tongue and randomly allocated to IVM, OFZ and control groups. Three days before treatment and two weeks after treatment faecal samples and skin scrapings were taken to establish the burden of endo- and ectoparasites, respectively and the effect of the treatment. No adverse effect was observed in any of the treatment groups throughout the study period. Half of the pigs from each group were slaughtered at week four and the remaining half at week twelve post treatment. The IVM treatment group had no significant effect (p=0.224) on T. solium cysts viability in comparison to the control group. Significant effect on cysts viability was observed in the OFZ treated group (p<0.001) compared to IVM and control groups in all muscle tissues. Regarding to brain cysts, neither of the drugs was efficacious. Ivermectin and OFZ treatments significantly reduced (p<0.001) the faecal egg count of Ascaris suum, strongyles and Trichuris suis two weeks after treatment. At slaughter, Oesophagostomum dentatum, Ascarops strongylina and Physocephalus sexalatus were recovered from pigs in the IVM treated and in the control groups. Ivermectin was 100% effective in control of Sarcoptes scabiei. In conclusion, IVM at a single dose of 0.3mg/kg was efficacious against ectoparasites but did not effectively cure pigs from T. solium cysticercosis or nematodes. Oxfendazole, on the other hand, killed all nematodes and muscle cysts, but did not have any effect on ectoparasites. A combination of the two drugs would be a most useful treatment option for control of pig parasitoses in sub-Saharan Africa.


Parasitology | 2008

Host-cell apoptosis in Taenia solium-induced brain granulomas in naturally infected pigs

Chummy Sikalizyo Sikasunge; I.K. Phiri; Maria Vang Johansen; Arve Lee Willingham; Pall S. Leifsson

To assess whether apoptosis occurs in pig brain granulomas due to Taenia solium cysticerci, brain tissues from 30 pigs naturally infected with T. solium cysticercosis were evaluated by terminal deoxynucleotidyl transferase-end labelling (TUNEL) staining. In addition, tissues were stained with CD3 marker to identify T lymphocytes. Examination of TUNEL-stained tissues showed apoptotic cells in early lesions that contained viable cysticerci. Apoptotic cells were primarily found interspersed with normal cell types, and were mostly located in the inflammatory infiltrate. Late or advanced granulomas with disintegrated scolices did not show TUNEL-positive cells. CD3+ cells were found in both early and advanced lesions and apoptosis mainly co-localized with CD3+ T lymphocytes. This suggests that these cells are constantly undergoing apoptosis and thus die as soon as they arrive at the site of infection. Apoptosis indeed may be one way by which T. solium cysticerci down-regulate the hosts cellular immune response in early cysticercosis. Therefore, further research is needed to establish if other cells besides T-lymphocytes are also a target for destruction by cysticerci in early cysticercosis as well as studies to assess if cysteine protease is expressed by viable cysticerci in situ.


Acta Tropica | 2017

Control of Taenia solium taeniasis/cysticercosis: The best way forward for sub-Saharan Africa?

Sarah Gabriël; Pierre Dorny; Kabemba E. Mwape; Chiara Trevisan; Uffe Christian Braae; Pascal Magnussen; Sarah Thys; C Bulaya; I.K. Phiri; Chummy Sikalizyo Sikasunge; Chitwambi Makungu; Sónia Afonso; Q Nicolau; Maria Vang Johansen

Taenia solium taeniasis/cysticercosis is a neglected parasitic zoonosis with significant economic and public health impacts. Control measures can be broadly grouped into community health education, improvements in hygiene and sanitary conditions, proper meat handling at household and community level, improved standards of meat inspection, pig management, treatment of individual patients and possibly human populations, and treatment and/or vaccination of porcine populations. This manuscript looks critically into currently existing control options and provides suggestions on which (combination of) tools would be most effective in the control of T. solium taeniasis/cysticercosis in sub-Saharan Africa. Field data and disease transmission simulations suggest that implementation of a single intervention control strategy will not lead to a satisfactory reduction of disease morbidity or transmission. A feasible strategy to combat T. solium taeniasis/cysticercosis would include a combination of approaches focussing on both human (health education and treatment) and animal host (management, treatment and vaccination), which can vary for different communities and different geographical locations. Selection of the specific strategy depends on cost-effectiveness analyses based on solid field data, currently unavailable, though urgently needed; as well as on health priorities and resources of the country. A One Health approach involving medical, veterinary, environmental and social sectors is essential for T. solium to be controlled and eventually eliminated. Finally the success of any intervention is largely dependent on the level of societal and political acceptance, commitment and engagement.

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Arve Lee Willingham

Ross University School of Veterinary Medicine

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Sónia Afonso

Eduardo Mondlane University

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